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AIMS Neuroscience

2019, Volume 6, Issue 3: 146-174. doi: 10.3934/Neuroscience.2019.3.146
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A review of the actions of Nitric Oxide in development and neuronal function in major invertebrate model systems

  • Associate professor of pharmacy, Wingate University School of Pharmacy, Wingate, NC28174, USA
  • Received: 23 June 2019 Accepted: 24 July 2019 Published: 19 August 2019

  • Ever since the late-eighties when endothelium-derived relaxing factor was found to be the gas nitric oxide, endogenous nitric oxide production has been observed in virtually all animal groups tested and additionally in plants, diatoms, slime molds and bacteria. The fact that this new messenger was actually a gas and therefore didn’t obey the established rules of neurotransmission made it even more intriguing. In just 30 years there is now too much information for useful comprehensive reviews even if limited to animals alone. Therefore this review attempts to survey the actions of nitric oxide on development and neuronal function in selected major invertebrate models only so allowing some detailed discussion but still covering most of the primary references. Invertebrate model systems have some very useful advantages over more expensive and demanding animal models such as large, easily identifiable neurons and simple circuits in tissues that are typically far easier to keep viable. A table summarizing this information along with the major relevant references has been included for convenience.

    Citation: Nicholas J. D. Wright. A review of the actions of Nitric Oxide in development and neuronal function in major invertebrate model systems[J]. AIMS Neuroscience, 2019, 6(3): 146-174. doi: 10.3934/Neuroscience.2019.3.146

    Related Papers:

  • Ever since the late-eighties when endothelium-derived relaxing factor was found to be the gas nitric oxide, endogenous nitric oxide production has been observed in virtually all animal groups tested and additionally in plants, diatoms, slime molds and bacteria. The fact that this new messenger was actually a gas and therefore didn’t obey the established rules of neurotransmission made it even more intriguing. In just 30 years there is now too much information for useful comprehensive reviews even if limited to animals alone. Therefore this review attempts to survey the actions of nitric oxide on development and neuronal function in selected major invertebrate models only so allowing some detailed discussion but still covering most of the primary references. Invertebrate model systems have some very useful advantages over more expensive and demanding animal models such as large, easily identifiable neurons and simple circuits in tissues that are typically far easier to keep viable. A table summarizing this information along with the major relevant references has been included for convenience.


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    Conflict of interest


    The author declares no conflict of interest.

    [1] Ignarro LJ, Buga GM, Wood KS, et al. (1987) Endothelium-derived relaxing factor produced and released from artery and vein is nitric oxide. Proc Natl Acad Sci USA 84: 9265–9269. doi: 10.1073/pnas.84.24.9265
    [2] Moncada S, Palmer RM, Higgs EA (1991) Nitric oxide: Physiology, pathophysiology, and pharmacology. Pharmacol Rev 43: 109–142.
    [3] Palmer RM, Ferrige AG, Moncada S (1987) Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor. Nature 327: 524–526. doi: 10.1038/327524a0
    [4] Moroz LL (2000) On the origin and early evolution of neuronal nitric oxide signaling: A comparative analysis. In: Kalsner S, editor. Nitric Oxide and Free Radicals in Peripheral Neurotransmission. Boston, MA: Birkhäuser Boston, 1–34.
    [5] Moroz LL, Kohn AB (2007) On the comparative biology of Nitric Oxide (NO) synthetic pathways: Parallel evolution of NO–mediated signaling. Adv Exp Biol 1: 1–44. doi: 10.1016/S1872-2423(07)01001-0
    [6] Zumft WG (1993) The biological role of nitric oxide in bacteria. Arch Microbiol 160: 253–264. doi: 10.1007/BF00292074
    [7] Zumft WG (2005) Nitric oxide reductases of prokaryotes with emphasis on the respiratory, heme-copper oxidase type. J Inorg Biochem 99: 194–215. doi: 10.1016/j.jinorgbio.2004.09.024
    [8] Moroz LL (2015) Gaseous transmission across time and species. Am Zool 41: 304–320.
    [9] Moroz LL, Kohn AB (2011) Parallel evolution of nitric oxide signaling: Diversity of synthesis and memory pathways. Front Biosci (Landmark Ed) 16: 2008–2051. doi: 10.2741/3837
    [10] Brandes JA, Boctor NZ, Cody GD, et al. (1998) Abiotic nitrogen reduction on the early Earth. Nature 395: 365–367. doi: 10.1038/26450
    [11] Kasting JF (1992) Bolide impacts and the oxidation state of carbon in the Earth's early atmosphere. Orig Life Evol Biosph 20: 199–231.
    [12] Martin RS, Mather TA, Pyle DM (2007) Volcanic emissions and the early Earth atmosphere. Geochim Cosmochim Ac 71: 3673–3685. doi: 10.1016/j.gca.2007.04.035
    [13] Nna Mvondo D, Navarro-Gonzalez R, McKay CP, et al. (2001) Production of nitrogen oxides by lightning and coronae discharges in simulated early Earth, Venus and Mars environments. Adv Space Res 27: 217–223. doi: 10.1016/S0273-1177(01)00050-3
    [14] Nna-Mvondo D, Navarro-Gonzalez R, Raulin F, et al. (2005) Nitrogen fixation by corona discharge on the early precambrian Earth. Orig Life Evol Biosph 35: 401–409. doi: 10.1007/s11084-005-1972-9
    [15] Summers DP, Chang S (1993) Prebiotic ammonia from reduction of nitrite by iron (II) on the early Earth. Nature 365: 630–633. doi: 10.1038/365630a0
    [16] Flores-Santana W, Switzer C, Ridnour LA, et al. (2009) Comparing the chemical biology of NO and HNO. Arch Pharm Res 32: 1139–1153. doi: 10.1007/s12272-009-1805-x
    [17] Fukuto JM, Cho JY, Switzer CH (2000) Chapter 2-The chemical properties of Nitric Oxide and related nitrogen oxides. In: Ignarro LJ, editor. Nitric Oxide. San Diego: Academic Press, 23–40.
    [18] Gladwin MT, Schechter AN, Kim-Shapiro DB, et al. (2005) The emerging biology of the nitrite anion. Nat Chem Biol 1: 308–314. doi: 10.1038/nchembio1105-308
    [19] Stamler JS, Singel DJ, Loscalzo J (1992) Biochemistry of nitric oxide and its redox-activated forms. Science 258: 1898–1902. doi: 10.1126/science.1281928
    [20] Lancaster Jr JR (1994) Simulation of the diffusion and reaction of endogenously produced nitric oxide. Proc Natl Acad Sci USA 91: 8137–8141. doi: 10.1073/pnas.91.17.8137
    [21] Lancaster Jr JR (1996) Diffusion of free nitric oxide. Methods Enzymol 268: 31–50. doi: 10.1016/S0076-6879(96)68007-0
    [22] Lancaster Jr JR (1997) A tutorial on the diffusibility and reactivity of free nitric oxide. Nitric Oxide 1: 18–30. doi: 10.1006/niox.1996.0112
    [23] Thomas DD, Liu X, Kantrow SP, et al. (2001) The biological lifetime of nitric oxide: Implications for the perivascular dynamics of NO and O2. Proc Natl Acad Sci USA 98: 355–360. doi: 10.1073/pnas.98.1.355
    [24] Wood J, Garthwaite J (1994) Models of the diffusional spread of nitric oxide: implications for neural nitric oxide signalling and its pharmacological properties. Neuropharmacology 33: 1235–1244. doi: 10.1016/0028-3908(94)90022-1
    [25] Bryan NS, Rassaf T, Maloney RE, et al. (2004) Cellular targets and mechanisms of nitros(yl)ation: An insight into their nature and kinetics in vivo. Proc Natl Acad Sci USA 101: 4308–4313. doi: 10.1073/pnas.0306706101
    [26] Nathan C (2004) The moving frontier in nitric oxide-dependent signaling. Sci STKE 2004: pe52.
    [27] Benamar A, Rolletschek H, Borisjuk L, et al. (2008) Nitrite-nitric oxide control of mitochondrial respiration at the frontier of anoxia. Biochim Biophys Acta 1777: 1268–1275. doi: 10.1016/j.bbabio.2008.06.002
    [28] Hendgen-Cotta UB, Merx MW, Shiva S, et al. (2008) Nitrite reductase activity of myoglobin regulates respiration and cellular viability in myocardial ischemia-reperfusion injury. Proc Natl Acad Sci USA 105: 10256–10261. doi: 10.1073/pnas.0801336105
    [29] Hill BG, Darley-Usmar VM (2008) S–nitrosation and thiol switching in the mitochondrion: A new paradigm for cardioprotection in ischaemic preconditioning. Biochem J 412: e11–13. doi: 10.1042/BJ20080716
    [30] Lopez-Lluch G, Irusta PM, Navas P, et al. (2008) Mitochondrial biogenesis and healthy aging. Exp Gerontol 43: 813–819. doi: 10.1016/j.exger.2008.06.014
    [31] Moncada S, Bolanos JP (2006) Nitric oxide, cell bioenergetics and neurodegeneration. J Neurochem 97: 1676–1689. doi: 10.1111/j.1471-4159.2006.03988.x
    [32] Navarro A (2008) Mitochondrial nitric oxide synthase and the regulation of heart rate. Am J Hypertens 21: 485. doi: 10.1038/ajh.2008.22
    [33] Nisoli E, Falcone S, Tonello C, et al. (2004) Mitochondrial biogenesis by NO yields functionally active mitochondria in mammals. Proc Natl Acad Sci USA 101: 16507–16512. doi: 10.1073/pnas.0405432101
    [34] Nisoli E, Tonello C, Cardile A, et al. (2005) Calorie restriction promotes mitochondrial biogenesis by inducing the expression of eNOS. Science 310: 314–317. doi: 10.1126/science.1117728
    [35] Quintero M, Colombo SL, Godfrey A, et al. (2006) Mitochondria as signaling organelles in the vascular endothelium. Proc Natl Acad Sci USA 103: 5379–5384. doi: 10.1073/pnas.0601026103
    [36] Valdez LB, Boveris A (2007) Mitochondrial nitric oxide synthase, a voltage-dependent enzyme, is responsible for nitric oxide diffusion to cytosol. Front Biosci 12: 1210–1219. doi: 10.2741/2139
    [37] Abe S, Nakabayashi S, Murayama J, et al. (2010) Development of a novel fluorometric assay for nitric oxide utilizing sesamol and its application to analysis of nitric oxide-releasing drugs. Luminescence 25: 456–462. doi: 10.1002/bio.1180
    [38] Boudko DY, Cooper BY, Harvey WR, et al. (2002) High-resolution microanalysis of nitrite and nitrate in neuronal tissues by capillary electrophoresis with conductivity detection. J Chromatogr B Analyt Technol Biomed Life Sci 774: 97–104. doi: 10.1016/S1570-0232(02)00219-2
    [39] Chang JYH, Chow LW, Dismuke WM, et al. (2017) Peptide-Functionalized Fluorescent Particles for In Situ Detection of Nitric Oxide via Peroxynitrite-Mediated Nitration. Adv Healthc Mater 6.
    [40] Cruz L, Moroz LL, Gillette R, et al. (1997) Nitrite and nitrate levels in individual molluscan neurons: Single-cell capillary electrophoresis analysis. J Neurochem 69: 110–115.
    [41] Davies IR, Zhang X (2008) Nitric oxide selective electrodes. Methods Enzymol 436: 63–95. doi: 10.1016/S0076-6879(08)36005-4
    [42] Fuller RR, Moroz LL, Gillette R, et al. (1998) Single neuron analysis by capillary electrophoresis with fluorescence spectroscopy. Neuron 20: 173–181. doi: 10.1016/S0896-6273(00)80446-8
    [43] Ghafourifar P, Parihar MS, Nazarewicz R, et al. (2008) Detection assays for determination of mitochondrial nitric oxide synthase activity; advantages and limitations. Methods Enzymol 440: 317–334. doi: 10.1016/S0076-6879(07)00821-X
    [44] Ha Y, Sim J, Lee Y, et al. (2016) Insertable fast-response amperometric NO/CO dual microsensor: Study of neurovascular coupling during acutely induced seizures of rat brain cortex. Anal Chem 88: 2563–2569. doi: 10.1021/acs.analchem.5b04288
    [45] Li H, Wan A (2015) Fluorescent probes for real–time measurement of nitric oxide in living cells. Analyst 140: 7129–7141. doi: 10.1039/C5AN01628B
    [46] Likhtenshtein GI (2009) Novel fluorescent methods for biotechnological and biomedical sensoring: Assessing antioxidants, reactive radicals, NO dynamics, immunoassay, and biomembranes fluidity. Appl Biochem Biotechnol 152: 135–155. doi: 10.1007/s12010-008-8219-y
    [47] Moroz LL, Dahlgren RL, Boudko D, et al. (2005) Direct single cell determination of nitric oxide synthase related metabolites in identified nitrergic neurons. J Inorg Biochem 99: 929–939. doi: 10.1016/j.jinorgbio.2005.01.013
    [48] Moroz LL, Gillette R, Sweedler JV (1999) Single-cell analyses of nitrergic neurons in simple nervous systems. J Exp Biol 202: 333–341.
    [49] Moroz LL, Radbourne S, Winlow W (1995) The use of NO-sensitive microelectrodes for direct detection of nitric oxide (NO) production in molluscs. Acta Biol Hung 46: 155–167.
    [50] Nagano T (1999) Practical methods for detection of nitric oxide. Luminescence 14: 283–290. doi: 10.1002/(SICI)1522-7243(199911/12)14:6<283::AID-BIO572>3.0.CO;2-G
    [51] Nagano T (2009) Bioimaging probes for reactive oxygen species and reactive nitrogen species. J Clin Biochem Nutr 45: 111–124. doi: 10.3164/jcbn.R09-66
    [52] Teng X, Scott Isbell T, Crawford JH, et al. (2008) Novel method for measuring S–nitrosothiols using hydrogen sulfide. Methods Enzymol 441: 161–172. doi: 10.1016/S0076-6879(08)01209-3
    [53] Vanin A, Poltorakov A (2009) NO spin trapping in biological systems. Front Biosci (Landmark Ed) 14: 4427–4435.
    [54] Ye X, Rubakhin SS, Sweedler JV (2008) Detection of nitric oxide in single cells. Analyst 133: 423–433. doi: 10.1039/b716174c
    [55] Zhou X, He P (2011) Improved measurements of intracellular nitric oxide in intact microvessels using 4,5-diaminofluorescein diacetate. Am J Physiol Heart Circ Physiol 301: H108–114. doi: 10.1152/ajpheart.00195.2011
    [56] Elofsson R, Carlberg M, Moroz L, et al. (1993) Is nitric oxide (NO) produced by invertebrate neurones? Neuroreport 4: 279–282. doi: 10.1097/00001756-199303000-00013
    [57] Lukowiak K, Moroz LL, Bulloch AGM, et al. (1993) Putative NO-synthesizing neurons of lymnaea in vivo and in vitro. Neth J Zool 44: 535–549. doi: 10.1163/156854293X00601
    [58] Moroz LL (2000) Giant identified NO-releasing neurons and comparative histochemistry of putative nitrergic systems in gastropod molluscs. Microsc Res Tech 49: 557–569. doi: 10.1002/1097-0029(20000615)49:6<557::AID-JEMT6>3.0.CO;2-S
    [59] Moroz LL, Gillette R (1995) From polyplacophora to cephalopoda: Comparative analysis of nitric oxide signalling in mollusca. Acta Biol Hung 46: 169–182.
    [60] Bredt DS, Hwang PM, Snyder SH (1990) Localization of nitric oxide synthase indicating a neural role for nitric oxide. Nature 347: 768–770. doi: 10.1038/347768a0
    [61] Bredt DS, Snyder SH (1990) Isolation of nitric oxide synthetase, a calmodulin-requiring enzyme. Proc Natl Acad Sci USA 87: 682–685. doi: 10.1073/pnas.87.2.682
    [62] Ghosh DK, Salerno JC (2003) Nitric oxide synthases: Domain structure and alignment in enzyme function and control. Front Biosci 8: d193–209. doi: 10.2741/959
    [63] Griffith OW, Stuehr DJ (1995) Nitric oxide synthases: Properties and catalytic mechanism. Annu Rev Physiol 57: 707–736. doi: 10.1146/annurev.ph.57.030195.003423
    [64] Zemojtel T, Wade RC, Dandekar T (2003) In search of the prototype of nitric oxide synthase. FEBS Lett 554: 1–5. doi: 10.1016/S0014-5793(03)01081-0
    [65] Angelo M, Hausladen A, Singel DJ, et al. (2008) Interactions of NO with hemoglobin: From microbes to man. Methods Enzymol 436: 131–168. doi: 10.1016/S0076-6879(08)36008-X
    [66] Basu S, Azarova NA, Font MD, et al. (2008) Nitrite reductase activity of cytochrome c. J Biol Chem 283: 32590–32597. doi: 10.1074/jbc.M806934200
    [67] Cosby K, Partovi KS, Crawford JH, et al. (2003) Nitrite reduction to nitric oxide by deoxyhemoglobin vasodilates the human circulation. Nat Med 9: 1498–1505. doi: 10.1038/nm954
    [68] Huang Z, Shiva S, Kim-Shapiro DB, et al. (2005) Enzymatic function of hemoglobin as a nitrite reductase that produces NO under allosteric control. J Clin Invest 115: 2099–2107. doi: 10.1172/JCI24650
    [69] Kollau A, Beretta M, Russwurm M, et al. (2009) Mitochondrial nitrite reduction coupled to soluble guanylate cyclase activation: Lack of evidence for a role in the bioactivation of nitroglycerin. Nitric Oxide 20: 53–60. doi: 10.1016/j.niox.2008.09.003
    [70] Nohl H, Staniek K, Kozlov AV (2005) The existence and significance of a mitochondrial nitrite reductase. Redox Rep 10: 281–286. doi: 10.1179/135100005X83707
    [71] Philippot L (2002) Denitrifying genes in bacterial and Archaeal genomes. Biochim Biophys Acta 1577: 355–376. doi: 10.1016/S0167-4781(02)00420-7
    [72] Reutov VP (2002) Nitric oxide cycle in mammals and the cyclicity principle. Biochemistry (Mosc) 67: 293–311. doi: 10.1023/A:1014832416073
    [73] Shiva S, Huang Z, Grubina R, et al. (2007) Deoxymyoglobin is a nitrite reductase that generates nitric oxide and regulates mitochondrial respiration. Circ Res 100: 654–661. doi: 10.1161/01.RES.0000260171.52224.6b
    [74] Bredt DS, Hwang PM, Glatt CE, et al. (1991) Cloned and expressed nitric oxide synthase structurally resembles cytochrome P-450 reductase. Nature 351: 714–718. doi: 10.1038/351714a0
    [75] Lowenstein CJ, Glatt CS, Bredt DS, et al. (1992) Cloned and expressed macrophage nitric oxide synthase contrasts with the brain enzyme. Proc Natl Acad Sci USA 89: 6711–6715. doi: 10.1073/pnas.89.15.6711
    [76] Lyons CR, Orloff GJ, Cunningham JM (1992) Molecular cloning and functional expression of an inducible nitric oxide synthase from a murine macrophage cell line. J Biol Chem 267: 6370–6374.
    [77] Xie QW, Cho HJ, Calaycay J, et al. (1992) Cloning and characterization of inducible nitric oxide synthase from mouse macrophages. Science 256: 225–228. doi: 10.1126/science.1373522
    [78] Janssens SP, Shimouchi A, Quertermous T, et al. (1992) Cloning and expression of a cDNA encoding human endothelium-derived relaxing factor/nitric oxide synthase. J Biol Chem 267: 14519–14522.
    [79] Lamas S, Marsden PA, Li GK, et al. (1992) Endothelial nitric oxide synthase: Molecular cloning and characterization of a distinct constitutive enzyme isoform. Proc Natl Acad Sci USA 89: 6348–6352. doi: 10.1073/pnas.89.14.6348
    [80] Marsden PA, Schappert KT, Chen HS, et al. (1992) Molecular cloning and characterization of human endothelial nitric oxide synthase. FEBS Lett 307: 287–293. doi: 10.1016/0014-5793(92)80697-F
    [81] Nishida K, Harrison DG, Navas JP, et al. (1992) Molecular cloning and characterization of the constitutive bovine aortic endothelial cell nitric oxide synthase. J Clin Invest 90: 2092–2096. doi: 10.1172/JCI116092
    [82] Sessa WC, Harrison JK, Barber CM, et al. (1992) Molecular cloning and expression of a cDNA encoding endothelial cell nitric oxide synthase. J Biol Chem 267: 15274–15276.
    [83] Knowles RG, Moncada S (1994) Nitric oxide synthases in mammals. Biochem J 298 (Pt 2): 249–258.
    [84] Zhou L, Zhu DY (2009) Neuronal nitric oxide synthase: Structure, subcellular localization, regulation, and clinical implications. Nitric Oxide 20: 223–230. doi: 10.1016/j.niox.2009.03.001
    [85] Radomski MW, Martin JF, Moncada S (1991) Synthesis of Nitric Oxide by the haemocytes of the American horseshoe crab (Limulus polyphemus). Philos T R Soc B 334: 129–133. doi: 10.1098/rstb.1991.0102
    [86] Garthwaite J (2019) NO as a multimodal transmitter in the brain: Discovery and current status. Br J Pharmacol 176: 197–211. doi: 10.1111/bph.14532
    [87] Russwurm M, Wittau N, Koesling D (2001) Guanylyl cyclase/PSD-95 interaction: Targeting of the nitric oxide-sensitive alpha2beta1 guanylyl cyclase to synaptic membranes. J Biol Chem 276: 44647–44652. doi: 10.1074/jbc.M105587200
    [88] Schulz S, Chinkers M, Garbers DL (1989) The guanylate cyclase/receptor family of proteins. Faseb J 3: 2026–2035. doi: 10.1096/fasebj.3.9.2568301
    [89] Arnold WP, Mittal CK, Katsuki S, et al. (1977) Nitric oxide activates guanylate cyclase and increases guanosine 3':5'-cyclic monophosphate levels in various tissue preparations. Proc Natl Acad Sci USA 74: 3203–3207. doi: 10.1073/pnas.74.8.3203
    [90] Francis SH, Busch JL, Corbin JD, et al. (2010) cGMP-dependent protein kinases and cGMP phosphodiesterases in nitric oxide and cGMP action. Pharmacol Rev 62: 525–563. doi: 10.1124/pr.110.002907
    [91] Foster MW, Hess DT, Stamler JS (2009) Protein S-nitrosylation in health and disease: A current perspective. Trends Mol Med 15: 391–404. doi: 10.1016/j.molmed.2009.06.007
    [92] Hara MR, Agrawal N, Kim SF, et al. (2005) S-nitrosylated GAPDH initiates apoptotic cell death by nuclear translocation following Siah1 binding. Nat Cell Biol 7: 665–674. doi: 10.1038/ncb1268
    [93] Hess DT, Matsumoto A, Kim SO, et al. (2005) Protein S-nitrosylation: Purview and parameters. Nat Rev Mol Cell Biol 6: 150–166. doi: 10.1038/nrm1569
    [94] Kim WK, Choi YB, Rayudu PV, et al. (1999) Attenuation of NMDA receptor activity and neurotoxicity by nitroxyl anion, NO. Neuron 24: 461–469. doi: 10.1016/S0896-6273(00)80859-4
    [95] Lipton SA, Choi YB, Pan ZH, et al. (1993) A redox-based mechanism for the neuroprotective and neurodestructive effects of nitric oxide and related nitroso-compounds. Nature 364: 626–632. doi: 10.1038/364626a0
    [96] Lipton SA, Choi YB, Takahashi H, et al. (2002) Cysteine regulation of protein function-as exemplified by NMDA-receptor modulation. Trends Neurosci 25: 474–480. doi: 10.1016/S0166-2236(02)02245-2
    [97] Mannick JB, Hausladen A, Liu L, et al. (1999) Fas-induced caspase denitrosylation. Science 284: 651–654. doi: 10.1126/science.284.5414.651
    [98] Sen N, Hara MR, Ahmad AS, et al. (2009) GOSPEL: A neuroprotective protein that binds to GAPDH upon S-nitrosylation. Neuron 63: 81–91. doi: 10.1016/j.neuron.2009.05.024
    [99] Uehara T, Nakamura T, Yao D, et al. (2006) S-nitrosylated protein-disulphide isomerase links protein misfolding to neurodegeneration. Nature 441: 513–517. doi: 10.1038/nature04782
    [100] Ball EE, Truman JW (1998) Developing grasshopper neurons show variable levels of guanylyl cyclase activity on arrival at their targets. J Comp Neurol 394: 1–13. doi: 10.1002/(SICI)1096-9861(19980427)394:1<1::AID-CNE1>3.0.CO;2-4
    [101] Haase A, Bicker G (2003) Nitric oxide and cyclic nucleotides are regulators of neuronal migration in an insect embryo. Development 130: 3977–3987. doi: 10.1242/dev.00612
    [102] Herbert Z, Rauser S, Williams L, et al. (2010) Developmental expression of neuromodulators in the central complex of the grasshopper Schistocerca gregaria. J Morphol 271: 1509–1526. doi: 10.1002/jmor.10895
    [103] Knipp S, Bicker G (2009) A developmental study of enteric neuron migration in the grasshopper using immunological probes. Dev Dyn 238: 2837–2849. doi: 10.1002/dvdy.22115
    [104] Knipp S, Bicker G (2009) Regulation of enteric neuron migration by the gaseous messenger molecules CO and NO. Development 136: 85–93. doi: 10.1242/dev.026716
    [105] Seidel C, Bicker G (2000) Nitric oxide and cGMP influence axonogenesis of antennal pioneer neurons. Development 127: 4541–4549.
    [106] Seidel C, Bicker G (2002) Developmental expression of nitric oxide/cyclic GMP signaling pathways in the brain of the embryonic grasshopper. Brain Res Dev Brain Res 138: 71–79. doi: 10.1016/S0165-3806(02)00466-2
    [107] Stern M, Bicker G (2008) Nitric oxide regulates axonal regeneration in an insect embryonic CNS. Dev Neurobiol 68: 295–308. doi: 10.1002/dneu.20585
    [108] Stern M, Bicker G (2010) Nitric oxide as a regulator of neuronal motility and regeneration in the locust embryo. J Insect Physiol 56: 958–965. doi: 10.1016/j.jinsphys.2010.03.031
    [109] Stern M, Boger N, Eickhoff R, et al. (2010) Development of nitrergic neurons in the nervous system of the locust embryo. J Comp Neurol 518: 1157–1175.
    [110] Truman JW, De Vente J, Ball EE (1996) Nitric oxide–sensitive guanylate cyclase activity is associated with the maturational phase of neuronal development in insects. Development 122: 3949–3958.
    [111] Enikolopov G, Banerji J, Kuzin B (1999) Nitric oxide and Drosophila development. Cell Death Differ 6: 956–963. doi: 10.1038/sj.cdd.4400577
    [112] Gibbs SM, Becker A, Hardy RW, et al. (2001) Soluble guanylate cyclase is required during development for visual system function in Drosophila. J Neurosci 21: 7705–7714. doi: 10.1523/JNEUROSCI.21-19-07705.2001
    [113] Gibbs SM, Truman JW (1998) Nitric oxide and cyclic GMP regulate retinal patterning in the optic lobe of Drosophila. Neuron 20: 83–93. doi: 10.1016/S0896-6273(00)80436-5
    [114] Kanao T, Sawada T, Davies SA, et al. (2012) The nitric oxide-cyclic GMP pathway regulates FoxO and alters dopaminergic neuron survival in Drosophila. PLoS One 7: e30958. doi: 10.1371/journal.pone.0030958
    [115] Kuzin B, Regulski M, Stasiv Y, et al. (2000) Nitric oxide interacts with the retinoblastoma pathway to control eye development in Drosophila. Curr Biol 10: 459–462. doi: 10.1016/S0960-9822(00)00443-7
    [116] Kuzin B, Roberts I, Peunova N, et al. (1996) Nitric oxide regulates cell proliferation during Drosophila development. Cell 87: 639–649. doi: 10.1016/S0092-8674(00)81384-7
    [117] Lacin H, Rusch J, Yeh RT, et al. (2014) Genome-wide identification of Drosophila Hb9 targets reveals a pivotal role in directing the transcriptome within eight neuronal lineages, including activation of nitric oxide synthase and Fd59a/Fox-D. Dev Biol 388: 117–133. doi: 10.1016/j.ydbio.2014.01.029
    [118] Rabinovich D, Yaniv SP, Alyagor I, et al. (2016) Nitric Oxide as a switching mechanism between axon degeneration and regrowth during developmental remodeling. Cell 164: 170–182. doi: 10.1016/j.cell.2015.11.047
    [119] Regulski M, Stasiv Y, Tully T, et al. (2004) Essential function of nitric oxide synthase in Drosophila. Curr Biol 14: R881–882. doi: 10.1016/j.cub.2004.09.068
    [120] Regulski M, Tully T (1995) Molecular and biochemical characterization of dNOS: A Drosophila Ca2+/calmodulin-dependent nitric oxide synthase. Proc Natl Acad Sci USA 92: 9072–9076. doi: 10.1073/pnas.92.20.9072
    [121] Shakiryanova D, Levitan ES (2008) Prolonged presynaptic posttetanic cyclic GMP signaling in Drosophila motoneurons. Proc Natl Acad Sci USA 105: 13610–13613. doi: 10.1073/pnas.0802131105
    [122] Van Wagenen S, Rehder V (1999) Regulation of neuronal growth cone filopodia by nitric oxide. J Neurobiol 39: 168–185. doi: 10.1002/(SICI)1097-4695(199905)39:2<168::AID-NEU2>3.0.CO;2-F
    [123] Wildemann B, Bicker G (1999) Developmental expression of nitric oxide/cyclic GMP synthesizing cells in the nervous system of Drosophila melanogaster. J Neurobiol 38: 1–15. doi: 10.1002/(SICI)1097-4695(199901)38:1<1::AID-NEU1>3.0.CO;2-L
    [124] Wingrove JA, O'Farrell PH (1999) Nitric oxide contributes to behavioral, cellular, and developmental responses to low oxygen in Drosophila. Cell 98: 105–114. doi: 10.1016/S0092-8674(00)80610-8
    [125] Champlin DT, Truman JW (2000) Ecdysteroid coordinates optic lobe neurogenesis via a nitric oxide signaling pathway. Development 127: 3543–3551.
    [126] Gibson NJ, Nighorn A (2000) Expression of nitric oxide synthase and soluble guanylyl cyclase in the developing olfactory system of Manduca sexta. J Comp Neurol 422: 191–205. doi: 10.1002/(SICI)1096-9861(20000626)422:2<191::AID-CNE4>3.0.CO;2-C
    [127] Gibson NJ, Rossler W, Nighorn AJ, et al. (2001) Neuron-glia communication via nitric oxide is essential in establishing antennal-lobe structure in Manduca sexta. Dev Biol 240: 326–339. doi: 10.1006/dbio.2001.0463
    [128] Grueber WB, Truman JW (1999) Development and organization of a nitric-oxide-sensitive peripheral neural plexus in larvae of the moth, Manduca sexta. J Comp Neurol 404: 127–141. doi: 10.1002/(SICI)1096-9861(19990201)404:1<127::AID-CNE10>3.0.CO;2-M
    [129] Qazi S, Trimmer BA (1999) The role of nitric oxide in motoneuron spike activity and muscarinic-evoked changes in cGMP in the CNS of larval Manduca sexta. J Comp Physiol A 185: 539–550. doi: 10.1007/s003590050414
    [130] Schachtner J, Homberg U, Truman JW (1999) Regulation of cyclic GMP elevation in the developing antennal lobe of the Sphinx moth, Manduca sexta. J Neurobiol 41: 359–375. doi: 10.1002/(SICI)1097-4695(19991115)41:3<359::AID-NEU5>3.0.CO;2-B
    [131] Wright JW, Schwinof KM, Snyder MA, et al. (1998) A delayed role for nitric oxide-sensitive guanylate cyclases in a migratory population of embryonic neurons. Dev Biol 204: 15–33. doi: 10.1006/dbio.1998.9066
    [132] Zayas RM, Qazi S, Morton DB, et al. (2000) Neurons involved in nitric oxide-mediated cGMP signaling in the tobacco hornworm, Manduca sexta. J Comp Neurol 419: 422–438. doi: 10.1002/(SICI)1096-9861(20000417)419:4<422::AID-CNE2>3.0.CO;2-S
    [133] Cayre M, Malaterre J, Scotto-Lomassese S, et al. (2005) A role for nitric oxide in sensory-induced neurogenesis in an adult insect brain. Eur J Neurosci 21: 2893–2902. doi: 10.1111/j.1460-9568.2005.04153.x
    [134] Bicker G (1996) Transmitter-induced calcium signalling in cultured neurons of the insect brain. J Neurosci Methods 69: 33–41. doi: 10.1016/S0165-0270(96)00018-0
    [135] Dacher M, Gauthier M (2008) Involvement of NO-synthase and nicotinic receptors in learning in the honey bee. Physiol Behav 95: 200–207. doi: 10.1016/j.physbeh.2008.05.019
    [136] Hosler JS, Buxton KL, Smith BH (2000) Impairment of olfactory discrimination by blockade of GABA and nitric oxide activity in the honey bee antennal lobes. Behav Neurosci 114: 514–525. doi: 10.1037/0735-7044.114.3.514
    [137] Menzel R, Muller U (1996) Learning and memory in honeybees: From behavior to neural substrates. Annu Rev Neurosci 19: 379–404. doi: 10.1146/annurev.ne.19.030196.002115
    [138] Muller U, Hildebrandt H (2002) Nitric oxide/cGMP-mediated protein kinase A activation in the antennal lobes plays an important role in appetitive reflex habituation in the honeybee. J Neurosci 22: 8739–8747. doi: 10.1523/JNEUROSCI.22-19-08739.2002
    [139] Muller U (1996) Inhibition of nitric oxide synthase impairs a distinct form of long-term memory in the honeybee, Apis mellifera. Neuron 16: 541–549. doi: 10.1016/S0896-6273(00)80073-2
    [140] Armstrong GA, Rodgers CI, Money TG, et al. (2009) Suppression of spreading depression-like events in locusts by inhibition of the NO/cGMP/PKG pathway. J Neurosci 29: 8225–8235. doi: 10.1523/JNEUROSCI.1652-09.2009
    [141] Bicker G, Schmachtenberg O (1997) Cytochemical evidence for nitric oxide/cyclic GMP signal transmission in the visual system of the locust. Eur J Neurosci 9: 189–193. doi: 10.1111/j.1460-9568.1997.tb01366.x
    [142] Bullerjahn A, Mentel T, Pfluger HJ, et al. (2006) Nitric oxide: A co-modulator of efferent peptidergic neurosecretory cells including a unique octopaminergic neurone innervating locust heart. Cell Tissue Res 325: 345–360. doi: 10.1007/s00441-006-0188-2
    [143] Homberg U (2002) Neurotransmitters and neuropeptides in the brain of the locust. Microsc Res Tech 56: 189–209. doi: 10.1002/jemt.10024
    [144] Kurylas AE, Ott SR, Schachtner J, et al. (2005) Localization of nitric oxide synthase in the central complex and surrounding midbrain neuropils of the locust Schistocerca gregaria. J Comp Neurol 484: 206–223. doi: 10.1002/cne.20467
    [145] Muller U, Bicker G (1994) Calcium-activated release of nitric oxide and cellular distribution of nitric oxide-synthesizing neurons in the nervous system of the locust. J Neurosci 14: 7521–7528. doi: 10.1523/JNEUROSCI.14-12-07521.1994
    [146] Munch D, Ott SR, Pfluger HJ (2010) Three-dimensional distribution of NO sources in a primary mechanosensory integration center in the locust and its implications for volume signaling. J Comp Neurol 518: 2903–2916. doi: 10.1002/cne.22396
    [147] Newland PL, Yates P (2008) Nitric oxide modulates salt and sugar responses via different signaling pathways. Chem Senses 33: 347–356. doi: 10.1093/chemse/bjm094
    [148] Ott SR, Delago A, Elphick MR (2004) An evolutionarily conserved mechanism for sensitization of soluble guanylyl cyclase reveals extensive nitric oxide-mediated upregulation of cyclic GMP in insect brain. Eur J Neurosci 20: 1231–1244. doi: 10.1111/j.1460-9568.2004.03588.x
    [149] Ott SR, Jones IW, Burrows M, et al. (2000) Sensory afferents and motor neurons as targets for nitric oxide in the locust. J Comp Neurol 422: 521–532. doi: 10.1002/1096-9861(20000710)422:4<521::AID-CNE4>3.0.CO;2-H
    [150] Ott SR, Philippides A, Elphick MR, et al. (2007) Enhanced fidelity of diffusive nitric oxide signalling by the spatial segregation of source and target neurones in the memory centre of an insect brain. Eur J Neurosci 25: 181–190. doi: 10.1111/j.1460-9568.2006.05271.x
    [151] Rast GF (2001) Nitric oxide induces centrally generated motor patterns in the locust suboesophageal ganglion. J Exp Biol 204: 3789–3801.
    [152] Schuppe H, Cuttle M, Newland PL (2007) Nitric oxide modulates sodium taste via a cGMP–independent pathway. Dev Neurobiol 67: 219–232. doi: 10.1002/dneu.20343
    [153] Schuppe H, Newland PL (2011) Differential effects of nitric oxide on the responsiveness of tactile hairs. Invert Neurosci 11: 85–90. doi: 10.1007/s10158-011-0119-0
    [154] Seidel C, Bicker G (1997) Colocalization of NADPH–diaphorase and GABA-immunoreactivity in the olfactory and visual system of the locust. Brain Res 769: 273–280. doi: 10.1016/S0006-8993(97)00716-6
    [155] Siegl T, Schachtner J, Holstein GR, et al. (2009) NO/cGMP signalling: L-citrulline and cGMP immunostaining in the central complex of the desert locust Schistocerca gregaria. Cell Tissue Res 337: 327–340. doi: 10.1007/s00441-009-0820-z
    [156] Collmann C, Carlsson MA, Hansson BS, et al. (2004) Odorant-evoked nitric oxide signals in the antennal lobe of Manduca sexta. J Neurosci 24: 6070–6077. doi: 10.1523/JNEUROSCI.0710-04.2004
    [157] Gage SL, Daly KC, Nighorn A (2013) Nitric oxide affects short-term olfactory memory in the antennal lobe of Manduca sexta. J Exp Biol 216: 3294–3300. doi: 10.1242/jeb.086694
    [158] Higgins M, Miller M, Nighorn A (2012) Nitric oxide has differential effects on currents in different subsets of Manduca sexta antennal lobe neurons. PLoS One 7: e42556. doi: 10.1371/journal.pone.0042556
    [159] Nighorn A, Gibson NJ, Rivers DM, et al. (1998) The nitric oxide-cGMP pathway may mediate communication between sensory afferents and projection neurons in the antennal lobe of Manduca sexta. J Neurosci 18: 7244–7255. doi: 10.1523/JNEUROSCI.18-18-07244.1998
    [160] Seki Y, Aonuma H, Kanzaki R (2005) Pheromone processing center in the protocerebrum of Bombyx mori revealed by nitric oxide-induced anti-cGMP immunocytochemistry. J Comp Neurol 481: 340–351. doi: 10.1002/cne.20392
    [161] Simpson PJ, Nighorn A, Morton DB (1999) Identification of a novel guanylyl cyclase that is related to receptor guanylyl cyclases, but lacks extracellular and transmembrane domains. J Biol Chem 274: 4440–4446. doi: 10.1074/jbc.274.7.4440
    [162] Wilson CH, Christensen TA, Nighorn AJ (2007) Inhibition of nitric oxide and soluble guanylyl cyclase signaling affects olfactory neuron activity in the moth, Manduca sexta. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 193: 715–728. doi: 10.1007/s00359-007-0227-9
    [163] Zayas RM, Qazi S, Morton DB, et al. (2002) Nicotinic-acetylcholine receptors are functionally coupled to the nitric oxide/cGMP-pathway in insect neurons. J Neurochem 83: 421–431. doi: 10.1046/j.1471-4159.2002.01147.x
    [164] Zayas RM, Trimmer BA (2007) Characterization of NO/cGMP-mediated responses in identified motoneurons. Cell Mol Neurobiol 27: 191–209. doi: 10.1007/s10571-006-9091-3
    [165] Duan J, Li W, Yuan D, et al. (2012) Nitric oxide signaling modulates cholinergic synaptic input to projection neurons in Drosophila antennal lobes. Neuroscience 219: 1–9. doi: 10.1016/j.neuroscience.2012.05.068
    [166] Morton DB (2004) Atypical soluble guanylyl cyclases in Drosophila can function as molecular oxygen sensors. J Biol Chem 279: 50651–50653. doi: 10.1074/jbc.C400461200
    [167] Ray SS, Sengupta R, Tiso M, et al. (2007) Reductase domain of Drosophila melanogaster nitric-oxide synthase: Redox transformations, regulation, and similarity to mammalian homologues. Biochemistry 46: 11865–11873. doi: 10.1021/bi700805x
    [168] Wildemann B, Bicker G (1999) Nitric oxide and cyclic GMP induce vesicle release at Drosophila neuromuscular junction. J Neurobiol 39: 337–346. doi: 10.1002/(SICI)1097-4695(19990605)39:3<337::AID-NEU1>3.0.CO;2-9
    [169] Greenfield MD (2001) Missing link in firefly bioluminescence revealed: NO regulation of photocyte respiration. Bioessays 23: 992–995. doi: 10.1002/bies.1144
    [170] Murata Y, Mashiko M, Ozaki M, et al. (2004) Intrinsic nitric oxide regulates the taste response of the sugar receptor cell in the blowfly, Phormia regina. Chem Senses 29: 75–81. doi: 10.1093/chemse/bjh007
    [171] Nakamura T, Murata Y, Mashiko M, et al. (2005) The nitric oxide–cyclic GMP cascade in sugar receptor cells of the blowfly, Phormia regina. Chem Senses 30 Suppl 1: i281–282.
    [172] Wasserman SL, Itagaki H (2003) The olfactory responses of the antenna and maxillary palp of the fleshfly, Neobellieria bullata (Diptera: Sarcophagidae), and their sensitivity to blockage of nitric oxide synthase. J Insect Physiol 49: 271–280. doi: 10.1016/S0022-1910(02)00288-3
    [173] Kunst M, Pfortner R, Aschenbrenner K, et al. (2011) Neurochemical architecture of the central complex related to its function in the control of grasshopper acoustic communication. PLoS One 6: e25613. doi: 10.1371/journal.pone.0025613
    [174] Weinrich A, Kunst M, Wirmer A, et al. (2008) Suppression of grasshopper sound production by nitric oxide-releasing neurons of the central complex. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 194: 763–776. doi: 10.1007/s00359-008-0347-x
    [175] Wenzel B, Kunst M, Gunther C, et al. (2005) Nitric oxide/cyclic guanosine monophosphate signaling in the central complex of the grasshopper brain inhibits singing behavior. J Comp Neurol 488: 129–139. doi: 10.1002/cne.20600
    [176] Wirmer A, Heinrich R (2011) Nitric oxide/cGMP signaling in the corpora allata of female grasshoppers. J Insect Physiol 57: 94–107. doi: 10.1016/j.jinsphys.2010.09.010
    [177] Muller U (2000) Prolonged activation of cAMP–dependent protein kinase during conditioning induces long-term memory in honeybees. Neuron 27: 159–168. doi: 10.1016/S0896-6273(00)00017-9
    [178] Aonuma H, Kitamura Y, Niwa K, et al. (2008) Nitric oxide-cyclic guanosine monophosphate signaling in the local circuit of the cricket abdominal nervous system. Neuroscience 157: 749–761. doi: 10.1016/j.neuroscience.2008.09.032
    [179] Aonuma H, Niwa K (2004) Nitric oxide regulates the levels of cGMP accumulation in the cricket brain. Acta Biol Hung 55: 65–70. doi: 10.1556/ABiol.55.2004.1-4.8
    [180] Cayre M, Malaterre J, Scotto-Lomassese S, et al. (2005) Hormonal and sensory inputs regulate distinct neuroblast cell cycle properties in adult cricket brain. J Neurosci Res 82: 659–664. doi: 10.1002/jnr.20672
    [181] Kosakai K, Tsujiuchi Y, Yoshino M (2015) Nitric oxide augments single Ca(2+) channel currents via cGMP-dependent protein kinase in Kenyon cells isolated from the mushroom body of the cricket brain. J Insect Physiol 78: 26–32. doi: 10.1016/j.jinsphys.2015.04.009
    [182] Matsumoto Y, Hatano A, Unoki S, et al. (2009) Stimulation of the cAMP system by the nitric oxide-cGMP system underlying the formation of long-term memory in an insect. Neurosci Lett 467: 81–85. doi: 10.1016/j.neulet.2009.10.008
    [183] Stevenson PA, Schildberger K (2013) Mechanisms of experience dependent control of aggression in crickets. Curr Opin Neurobiol 23: 318–323. doi: 10.1016/j.conb.2013.03.002
    [184] Mannai S, Bitri L, Thany SH (2016) cGMP/cGMP-dependent protein kinase pathway modulates nicotine-induced currents through the activation of alpha-bungarotoxin-insensitive nicotinic acetylcholine receptors from insect neurosecretory cells. J Neurochem 137: 931–938. doi: 10.1111/jnc.13633
    [185] Matsumoto CS, Kuramochi T, Matsumoto Y, et al. (2013) Participation of NO signaling in formation of long-term memory in salivary conditioning of the cockroach. Neurosci Lett 541: 4–8. doi: 10.1016/j.neulet.2013.01.010
    [186] Nieto-Fernandez FE, Ianuzzi F, Ruiz A, et al. (2004) Estradiol-stimulated nitric oxide release in nervous tissue, vasculature, and gonads of the giant cockroach Blaberus craniifer. Acta Biol Hung 55: 143–148. doi: 10.1556/ABiol.55.2004.1-4.17
    [187] Ott SR, Elphick MR (2002) Nitric oxide synthase histochemistry in insect nervous systems: Methanol/formalin fixation reveals the neuroarchitecture of formaldehyde-sensitive NADPH diaphorase in the cockroach Periplaneta americana. J Comp Neurol 448: 165–185. doi: 10.1002/cne.10235
    [188] Wicher D, Messutat S, Lavialle C, et al. (2004) A new regulation of non-capacitative calcium entry in insect pacemaker neurosecretory neurons. Involvement of arachidonic acid, no-guanylyl cyclase/cGMP, and cAMP. J Biol Chem 279: 50410–50419.
    [189] Cooke RM, Mistry R, Challiss RA, et al. (2013) Nitric oxide synthesis and cGMP production is important for neurite growth and synapse remodeling after axotomy. J Neurosci 33: 5626–5637. doi: 10.1523/JNEUROSCI.3659-12.2013
    [190] Park JH, Straub VA, O'Shea M (1998) Anterograde signaling by nitric oxide: Characterization and in vitro reconstitution of an identified nitrergic synapse. J Neurosci 18: 5463–5476. doi: 10.1523/JNEUROSCI.18-14-05463.1998
    [191] Serfozo Z, Elekes K (2002) Nitric oxide level regulates the embryonic development of the pond snail Lymnaea stagnalis: Pharmacological, behavioral, and ultrastructural studies. Cell Tissue Res 310: 119–130. doi: 10.1007/s00441-002-0589-9
    [192] Artinian L, Tornieri K, Zhong L, et al. (2010) Nitric oxide acts as a volume transmitter to modulate electrical properties of spontaneously firing neurons via apamin-sensitive potassium channels. J Neurosci 30: 1699–1711. doi: 10.1523/JNEUROSCI.4511-09.2010
    [193] Cole AG, Mashkournia A, Parries SC, et al. (2002) Regulation of early embryonic behavior by nitric oxide in the pond snail Helisoma trivolvis. J Exp Biol 205: 3143–3152.
    [194] Estes S, Artinian L, Rehder V (2017) Modulation of growth cone filopodial length by carbon monoxide. Dev Neurobiol 77: 677–690. doi: 10.1002/dneu.22430
    [195] Estes S, Zhong LR, Artinian L, et al. (2015) The role of action potentials in determining neuron-type-specific responses to nitric oxide. Dev Neurobiol 75: 435–451. doi: 10.1002/dneu.22233
    [196] Tornieri K, Rehder V (2007) Nitric oxide release from a single cell affects filopodial motility on growth cones of neighboring neurons. Dev Neurobiol 67: 1932–1943. doi: 10.1002/dneu.20572
    [197] Trimm KR, Rehder V (2004) Nitric oxide acts as a slow-down and search signal in developing neurites. Eur J Neurosci 19: 809–818. doi: 10.1111/j.0953-816X.2004.03182.x
    [198] Van Wagenen S, Cheng S, Rehder V (1999) Stimulation-induced changes in filopodial dynamics determine the action radius of growth cones in the snail Helisoma trivolvis. Cell Motil Cytoskeleton 44: 248–262. doi: 10.1002/(SICI)1097-0169(199912)44:4<248::AID-CM3>3.0.CO;2-Z
    [199] Van Wagenen S, Rehder V (2001) Regulation of neuronal growth cone filopodia by nitric oxide depends on soluble guanylyl cyclase. J Neurobiol 46: 206–219. doi: 10.1002/1097-4695(20010215)46:3<206::AID-NEU1003>3.0.CO;2-S
    [200] Welshhans K, Rehder V (2005) Local activation of the nitric oxide/cyclic guanosine monophosphate pathway in growth cones regulates filopodial length via protein kinase G, cyclic ADP ribose and intracellular Ca2+ release. Eur J Neurosci 22: 3006–3016. doi: 10.1111/j.1460-9568.2005.04490.x
    [201] Welshhans K, Rehder V (2007) Nitric oxide regulates growth cone filopodial dynamics via ryanodine receptor-mediated calcium release. Eur J Neurosci 26: 1537–1547. doi: 10.1111/j.1460-9568.2007.05768.x
    [202] Gifondorwa DJ, Leise EM (2006) Programmed cell death in the apical ganglion during larval metamorphosis of the marine mollusc Ilyanassa obsoleta. Biol Bull 210: 109–120. doi: 10.2307/4134600
    [203] Leise EM, Kempf SC, Durham NR, et al. (2004) Induction of metamorphosis in the marine gastropod Ilyanassa obsoleta: 5HT, NO and programmed cell death. Acta Biol Hung 55: 293–300. doi: 10.1556/ABiol.55.2004.1-4.35
    [204] Kerkut GA, Lambert JD, Gayton RJ, et al. (1975) Mapping of nerve cells in the suboesophageal ganglia of Helix aspersa. Comp Biochem Physiol A Comp Physiol 50: 1–25. doi: 10.1016/S0010-406X(75)80194-0
    [205] Pisu MB, Conforti E, Fenoglio C, et al. (1999) Nitric oxide-containing neurons in the nervous ganglia of Helix aspersa during rest and activity: Immunocytochemical and enzyme histochemical detection. J Comp Neurol 409: 274–284. doi: 10.1002/(SICI)1096-9861(19990628)409:2<274::AID-CNE8>3.0.CO;2-E
    [206] Sanchez-Alvarez M, Leon–Olea M, Talavera E, et al. (1994) Distribution of NADPH-diaphorase in the perioesophageal ganglia of the snail, Helix aspersa. Neurosci Lett 169: 51–55. doi: 10.1016/0304-3940(94)90354-9
    [207] D'Yakonova TL (2000) NO-producing compounds transform neuron responses to glutamate. Neurosci Behav Physiol 30: 153–159. doi: 10.1007/BF02463153
    [208] D'Yakonova TL (2002) Interaction between serotonin and nitric oxide (NO) in the activation of the serotoninergic system in the common snail. Neurosci Behav Physiol 32: 275–282. doi: 10.1023/A:1015062324019
    [209] D'Yakonova TL, Reutov VP (2000) The effects of nitrite on the excitability of brain neurons in the common snail. Neurosci Behav Physiol 30: 179–186. doi: 10.1007/BF02463156
    [210] Huang S, Kerschbaum HH, Hermann A (1998) Nitric oxide-mediated cGMP synthesis in Helix neural ganglia. Brain Res 780: 329–336. doi: 10.1016/S0006-8993(97)01147-5
    [211] Kavaliers M, Choleris E, Prato FS, et al. (1998) Evidence for the involvement of nitric oxide and nitric oxide synthase in the modulation of opioid-induced antinociception and the inhibitory effects of exposure to 60-Hz magnetic fields in the land snail. Brain Res 809: 50–57. doi: 10.1016/S0006-8993(98)00844-0
    [212] Kavaliers M, Prato FS (1999) Light-dependent effects of magnetic fields on nitric oxide activation in the land snail. Neuroreport 10: 1863–1867. doi: 10.1097/00001756-199906230-00012
    [213] Korshunova TA, Balaban PM (2014) Nitric oxide is necessary for long-term facilitation of synaptic responses and for development of context memory in terrestrial snails. Neuroscience 266: 127–135. doi: 10.1016/j.neuroscience.2014.02.004
    [214] Malyshev AY, Balaban PM (1999) Synaptic facilitation in Helix neurons depends upon postsynaptic calcium and nitric oxide. Neurosci Lett 261: 65–68. doi: 10.1016/S0304-3940(98)01010-6
    [215] Nacsa K, Elekes K, Serfozo Z (2015) Ultrastructural localization of NADPH diaphorase and nitric oxide synthase in the neuropils of the snail CNS. Micron 75: 58–66. doi: 10.1016/j.micron.2015.04.015
    [216] Pedder SM, Muneoka Y, Walker RJ (1998) Evidence for the involvement of nitric oxide in the inhibitory effect of GSPYFVamide on Helix aspersa central neurones. Regul Pept 74: 121–127. doi: 10.1016/S0167-0115(98)00031-7
    [217] Pivovarov AS, Egido-Villareal W (1996) NO synthase and guanylate cyclase inhibitors block modulation of the plasticity of common snail cholinoreceptors by 15-hydroxy-eicosatetraenoic acid. Neurosci Behav Physiol 26: 428–434. doi: 10.1007/BF02359403
    [218] Rigon P, de Castilhos J, Molina CG, et al. (2010) Distribution of NADPH-diaphorase activity in the central nervous system of the young and adult land snail Megalobulimus abbreviatus. Tissue Cell 42: 307–313. doi: 10.1016/j.tice.2010.07.005
    [219] Rigon P, de Castilhos J, Saur L, et al. (2009) NADPH-diaphorase activity in the nociceptive pathways of land snail Megalobulimus abbreviatus: The involvement of pedal ganglia. Invert Neurosci 9: 155–165. doi: 10.1007/s10158-009-0094-x
    [220] Roszer T, Jenei Z, Gall T, et al. (2004) A possible stimulatory effect of FMRFamide on neural nitric oxide production in the central nervous system of Helix lucorum L. Brain Behav Evol 63: 23–33. doi: 10.1159/000073757
    [221] Roszer T, Kiss-Toth E, Rozsa D, et al. (2010) Hypothermia translocates nitric oxide synthase from cytosol to membrane in snail neurons. Cell Tissue Res 342: 191–203. doi: 10.1007/s00441-010-1063-8
    [222] Schrofner S, Zsombok A, Hermann A, et al. (2004) Nitric oxide decreases a calcium-activated potassium current via activation of phosphodiesterase 2 in Helix U-cells. Brain Res 999: 98–105. doi: 10.1016/j.brainres.2003.11.038
    [223] Serfozo Z, Nacsa K, Vereb Z, et al. (2017) Nitric oxide-coupled signaling in odor elicited molecular events in the olfactory center of the terrestrial snail, Helix pomatia. Cell Signal 30: 67–81. doi: 10.1016/j.cellsig.2016.11.017
    [224] Serfozo Z, Szentmiklosi AJ, Elekes K (2008) Characterization of nitric oxidergic neurons in the alimentary tract of the snail Helix pomatia L.: Histochemical and physiological study. J Comp Neurol 506: 801–821.
    [225] Wright NJ, Sides LJ, Walling K (2015) Initial studies on the direct and modulatory effects of nitric oxide on an identified central Helix aspersa neuron. Invert Neurosci 15: 175. doi: 10.1007/s10158-014-0175-3
    [226] Xie M, Hermann A, Richter K, et al. (2001) Nitric oxide up-regulates ferritin mRNA level in snail neurons. Eur J Neurosci 13: 1479–1486. doi: 10.1046/j.0953-816x.2001.01526.x
    [227] Zsombok A, Schrofner S, Hermann A, et al. (2000) Nitric oxide increases excitability by depressing a calcium activated potassium current in snail neurons. Neurosci Lett 295: 85–88. doi: 10.1016/S0304-3940(00)01606-2
    [228] Fujie S, Yamamoto T, Murakami J, et al. (2005) Nitric oxide synthase and soluble guanylyl cyclase underlying the modulation of electrical oscillations in a central olfactory organ. J Neurobiol 62: 14–30. doi: 10.1002/neu.20046
    [229] Gelperin A (1994) Nitric oxide mediates network oscillations of olfactory interneurons in a terrestrial mollusc. Nature 369: 61–63. doi: 10.1038/369061a0
    [230] Gelperin A, Flores J, Raccuia-Behling F, et al. (2000) Nitric oxide and carbon monoxide modulate oscillations of olfactory interneurons in a terrestrial mollusk. J Neurophysiol 83: 116–127. doi: 10.1152/jn.2000.83.1.116
    [231] Inoue T, Watanabe S, Kirino Y (2001) Serotonin and NO complementarily regulate generation of oscillatory activity in the olfactory CNS of a terrestrial mollusk. J Neurophysiol 85: 2634–2638. doi: 10.1152/jn.2001.85.6.2634
    [232] Matsuo R, Ito E (2009) A novel nitric oxide synthase expressed specifically in the olfactory center. Biochem Biophys Res Commun 386: 724–728. doi: 10.1016/j.bbrc.2009.06.112
    [233] Watanabe S, Hirono M (2016) Phase-dependent modulation of oscillatory phase and synchrony by long-lasting depolarizing inputs in central neurons. eNeuro 3.
    [234] Watanabe S, Kirino Y, Gelperin A (2008) Neural and molecular mechanisms of microcognition in Limax. Learn Mem 15: 633–642. doi: 10.1101/lm920908
    [235] Watanabe S, Takanashi F, Ishida K, et al. (2015) Nitric oxide-mediated modulation of central network dynamics during olfactory perception. PLoS One 10: e0136846. doi: 10.1371/journal.pone.0136846
    [236] Artinian L, Zhong L, Yang H, et al. (2012) Nitric oxide as intracellular modulator: Internal production of NO increases neuronal excitability via modulation of several ionic conductances. Eur J Neurosci 36: 3333–3343. doi: 10.1111/j.1460-9568.2012.08260.x
    [237] D'Yakonova TL, D'Yakonova VE (2008) Modification of the effects of glutamate by nitric oxide (NO) in a pattern-generating network. Neurosci Behav Physiol 38: 407–413. doi: 10.1007/s11055-008-0058-3
    [238] Dyakonova TL, Dyakonova VE (2008) Electrical activity of no-producing neuron depends on NO level. Bull Exp Biol Med 145: 665–668. doi: 10.1007/s10517-008-0180-9
    [239] Dyakonova VE, Dyakonova TL (2010) Coordination of rhythm-generating units via NO and extrasynaptic neurotransmitter release. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 196: 529–541. doi: 10.1007/s00359-010-0541-5
    [240] Elliott CJ, Vehovszky A (2000) Comparative pharmacology of feeding in molluscs. Acta Biol Hung 51: 153–163.
    [241] Elphick MR, Kemenes G, Staras K, et al. (1995) Behavioral role for nitric oxide in chemosensory activation of feeding in a mollusc. J Neurosci 15: 7653–7664. doi: 10.1523/JNEUROSCI.15-11-07653.1995
    [242] Erokhova LA, Brazhe NA, Maksimov GV, et al. (2005) Analysis of conformational changes in neuronal carotenoids under the influence of neuromediator. Dokl Biochem Biophys 402: 233–235. doi: 10.1007/s10628-005-0079-6
    [243] Kobayashi S, Ogawa H, Fujito Y, et al. (2000) Nitric oxide suppresses fictive feeding response in Lymnaea stagnalis. Neurosci Lett 285: 209–212. doi: 10.1016/S0304-3940(00)01079-X
    [244] Kobayashi S, Sadamoto H, Ogawa H, et al. (2000) Nitric oxide generation around buccal ganglia accompanying feeding behavior in the pond snail, Lymnaea stagnalis. Neurosci Res 38: 27–34. doi: 10.1016/S0168-0102(00)00136-X
    [245] Korneev SA, Kemenes I, Straub V, et al. (2002) Suppression of nitric oxide (NO)-dependent behavior by double-stranded RNA-mediated silencing of a neuronal NO synthase gene. J Neurosci 22: Rc227. doi: 10.1523/JNEUROSCI.22-11-j0003.2002
    [246] Korneev SA, Straub V, Kemenes I, et al. (2005) Timed and targeted differential regulation of nitric oxide synthase (NOS) and anti-NOS genes by reward conditioning leading to long-term memory formation. J Neurosci 25: 1188–1192. doi: 10.1523/JNEUROSCI.4671-04.2005
    [247] Lukowiak K, Martens K, Orr M, et al. (2006) Modulation of aerial respiratory behaviour in a pond snail. Respir Physiol Neurobiol 154: 61–72. doi: 10.1016/j.resp.2006.02.009
    [248] Moghadam HF, Winlow W, Moroz LL (1995) Effects of hydrogen peroxide and nitric oxide (NO) on neuronal discharges and intracellular calcium concentration in the molluscan CNS. Acta Biol Hung 46: 145–153.
    [249] Moroz LL, Park JH, Winlow W (1993) Nitric oxide activates buccal motor patterns in Lymnaea stagnalis. Neuroreport 4: 643–646. doi: 10.1097/00001756-199306000-00010
    [250] Patel BA, Arundell M, Parker KH, et al. (2006) Detection of nitric oxide release from single neurons in the pond snail, Lymnaea stagnalis. Anal Chem 78: 7643–7648. doi: 10.1021/ac060863w
    [251] Peruzzi E, Fontana G, Sonetti D (2004) Presence and role of nitric oxide in the central nervous system of the freshwater snail Planorbarius corneus: Possible implication in neuron-microglia communication. Brain Res 1005: 9–20. doi: 10.1016/j.brainres.2003.12.042
    [252] Ribeiro M, Straub VA, Schofield M, et al. (2008) Characterization of NO-sensitive guanylyl cyclase: Expression in an identified interneuron involved in NO-cGMP-dependent memory formation. Eur J Neurosci 28: 1157–1165. doi: 10.1111/j.1460-9568.2008.06416.x
    [253] Sidorov AV, Kazakevich VB, Moroz LL (1999) Nitric oxide selectively enhances cAMP levels and electrical coupling between identified RPaD2/VD1 neurons in the CNS of Lymnaea stagnalis (L.). Acta Biol Hung 50: 229–233.
    [254] Sonetti D, Ottaviani E, Stefano GB (1997) Opiate signaling regulates microglia activities in the invertebrate nervous system. Gen Pharmacol 29: 39–47. doi: 10.1016/S0306-3623(96)00523-X
    [255] Straub VA, Grant J, O'Shea M, et al. (2007) Modulation of serotonergic neurotransmission by nitric oxide. J Neurophysiol 97: 1088–1099. doi: 10.1152/jn.01048.2006
    [256] Wyeth RC, Croll RP (2011) Peripheral sensory cells in the cephalic sensory organs of Lymnaea stagnalis. J Comp Neurol 519: 1894–1913. doi: 10.1002/cne.22607
    [257] Zhong LR, Estes S, Artinian L, et al. (2013) Nitric oxide regulates neuronal activity via calcium–activated potassium channels. PLoS One 8: e78727. doi: 10.1371/journal.pone.0078727
    [258] Zhong LR, Estes S, Artinian L, et al. (2015) Cell-specific regulation of neuronal activity by endogenous production of nitric oxide. Eur J Neurosci 41: 1013–1024. doi: 10.1111/ejn.12875
    [259] Cioni C, Di Patti MC, Venturini G, et al. (2012) Cellular, biochemical, and molecular characterization of nitric oxide synthase expressed in the nervous system of the prosobranch Stramonita haemastoma (Gastropoda, Neogastropoda). J Comp Neurol 520: 364–383. doi: 10.1002/cne.22729
    [260] Toni M, De Angelis F, di Patti MC, et al. (2015) Nitric Oxide synthase in the central nervous system and peripheral organs of Stramonita haemastoma: Protein distribution and gene expression in response to thermal stress. Mar Drugs 13: 6636–6664. doi: 10.3390/md13116636
    [261] Cadet P (2004) Nitric oxide modulates the physiological control of ciliary activity in the marine mussel Mytilus edulis via morphine: Novel mu opiate receptor splice variants. Neuro Endocrinol Lett 25: 184–190.
    [262] Cheng J, Zhang C, Han JS, et al. (2007) TENS stimulates constitutive nitric oxide release via opiate signaling in invertebrate neural tissues. Med Sci Monit 13: Br163–167.
    [263] Gomez MP, Nasi E (2000) Light transduction in invertebrate hyperpolarizing photoreceptors: Possible involvement of a Go-regulated guanylate cyclase. J Neurosci 20: 5254–5263. doi: 10.1523/JNEUROSCI.20-14-05254.2000
    [264] Kotsyuba EP, Vaschenko MA (2010) Neuroplastic and neuropathological changes in the central nervous system of the Gray mussel Crenomytilus grayanus (Dunker) under environmental stress. Invert Neurosci 10: 35–46. doi: 10.1007/s10158-010-0103-0
    [265] Stefano GB, Salzet B, Rialas CM, et al. (1997) Morphine- and anandamide-stimulated nitric oxide production inhibits presynaptic dopamine release. Brain Res 763: 63–68. doi: 10.1016/S0006-8993(97)00403-4
    [266] Vaschenko MA, Kotsyuba EP (2008) NADPH-diaphorase activity in the central nervous system of the Gray mussel Crenomytilus grayanus (Dunker) under stress conditions: A histochemical study. Mar Environ Res 66: 249–258. doi: 10.1016/j.marenvres.2008.03.001
    [267] Antonov I, Ha T, Antonova I, et al. (2007) Role of nitric oxide in classical conditioning of siphon withdrawal in Aplysia. J Neurosci 27: 10993–11002. doi: 10.1523/JNEUROSCI.2357-07.2007
    [268] Hatcher NG, Sudlow LC, Moroz LL, et al. (2006) Nitric oxide potentiates cAMP-gated cation current in feeding neurons of Pleurobranchaea californica independent of cAMP and cGMP signaling pathways. J Neurophysiol 95: 3219–3227. doi: 10.1152/jn.00815.2005
    [269] Jacklet JW, Tieman DG (2004) Nitric oxide and histamine induce neuronal excitability by blocking background currents in neuron MCC of Aplysia. J Neurophysiol 91: 656–665. doi: 10.1152/jn.00409.2003
    [270] Katzoff A, Miller N, Susswein AJ (2010) Nitric oxide and histamine signal attempts to swallow: A component of learning that food is inedible in Aplysia. Learn Mem 17: 50–62. doi: 10.1101/lm.1624610
    [271] Koh HY, Jacklet JW (1999) Nitric oxide stimulates cGMP production and mimics synaptic responses in metacerebral neurons of Aplysia. J Neurosci 19: 3818–3826. doi: 10.1523/JNEUROSCI.19-10-03818.1999
    [272] Koh HY, Jacklet JW (2001) Nitric oxide induces cGMP immunoreactivity and modulates membrane conductance in identified central neurons of Aplysia. Eur J Neurosci 13: 553–560. doi: 10.1046/j.0953-816x.2000.01416.x
    [273] Lewin MR, Walters ET (1999) Cyclic GMP pathway is critical for inducing long-term sensitization of nociceptive sensory neurons. Nat Neurosci 2: 18–23. doi: 10.1038/4520
    [274] Meulemans A, Mothet JP, Schirar A, et al. (1995) A nitric oxide synthase activity is involved in the modulation of acetylcholine release in Aplysia ganglion neurons: A histological, voltammetric and electrophysiological study. Neuroscience 69: 985–995. doi: 10.1016/0306-4522(95)00316-B
    [275] Miller N, Katzoff A, Susswein AJ (2008) Nitric oxide induces aspects of egg-laying behavior in Aplysia. J Exp Biol 211: 2388–2396. doi: 10.1242/jeb.015040
    [276] Miller N, Saada R, Fishman S, et al. (2011) Neurons controlling Aplysia feeding inhibit themselves by continuous NO production. PLoS One 6: e17779. doi: 10.1371/journal.pone.0017779
    [277] Moroz LL (2006) Localization of putative nitrergic neurons in peripheral chemosensory areas and the central nervous system of Aplysia californica. J Comp Neurol 495: 10–20. doi: 10.1002/cne.20842
    [278] Moroz LL, Chen D, Gillette MU, et al. (1996) Nitric oxide synthase activity in the molluscan CNS. J Neurochem 66: 873–876.
    [279] Mothet JP, Fossier P, Tauc L, et al. (1996) Opposite actions of nitric oxide on cholinergic synapses: Which pathways? Proc Natl Acad Sci USA 93: 8721–8726. doi: 10.1073/pnas.93.16.8721
    [280] Potgieter K, Hatcher NG, Gillette R, et al. (2010) Nitric oxide potentiates cAMP-gated cation current by intracellular acidification in feeding neurons of pleurobranchaea. J Neurophysiol 104: 742–745. doi: 10.1152/jn.00021.2010
    [281] Sawada M, Ichinose M (1996) Nitric oxide donor sodium nitroprusside inhibits the acetylcholine-induced K+ current in identified Aplysia neurons. J Neurosci Res 44: 21–26. doi: 10.1002/(SICI)1097-4547(19960401)44:1<21::AID-JNR3>3.0.CO;2-K
    [282] Sawada M, Ichinose M, Anraku M (1998) Nitric oxide donors inhibit the acetylcholine-induced Cl– current in identified Onchidium neurons. J Neurobiol 35: 388–394. doi: 10.1002/(SICI)1097-4695(19980615)35:4<388::AID-NEU6>3.0.CO;2-V
    [283] Sawada M, Ichinose M, Anraku M (2000) Inhibition of the glutamate-induced K(+) current in identified Onchidium neurons by nitric oxide donors. J Neurosci Res 60: 642–648. doi: 10.1002/(SICI)1097-4547(20000601)60:5<642::AID-JNR9>3.0.CO;2-#
    [284] Sawada M, Ichinose M, Hara N (1995) Nitric oxide induces an increased Na+ conductance in identified neurons of Aplysia. Brain Res 670: 248–256. doi: 10.1016/0006-8993(94)01284-O
    [285] Sawada M, Ichinose M, Stefano GB (1996) Inhibition of the Met-enkephalin-induced K+ current in B-cluster neurons of Aplysia by nitric oxide donor. Brain Res 740: 124–130. doi: 10.1016/S0006-8993(96)00853-0
    [286] Sawada M, Ichinose M, Stefano GB (1997) Nitric oxide inhibits the dopamine-induced K+ current via guanylate cyclase in Aplysia neurons. J Neurosci Res 50: 450–456. doi: 10.1002/(SICI)1097-4547(19971101)50:3<450::AID-JNR11>3.0.CO;2-A
    [287] Sung YJ, Walters ET, Ambron RT (2004) A neuronal isoform of protein kinase G couples mitogen-activated protein kinase nuclear import to axotomy-induced long-term hyperexcitability in Aplysia sensory neurons. J Neurosci 24: 7583–7595. doi: 10.1523/JNEUROSCI.1445-04.2004
    [288] Susswein AJ, Chiel HJ (2012) Nitric oxide as a regulator of behavior: New ideas from Aplysia feeding. Prog Neurobiol 97: 304–317. doi: 10.1016/j.pneurobio.2012.03.004
    [289] Ye X, Kim WS, Rubakhin SS, et al. (2007) Ubiquitous presence of argininosuccinate at millimolar levels in the central nervous system of Aplysia californica. J Neurochem 101: 632–640.
    [290] Benton JL, Sandeman DC, Beltz BS (2007) Nitric oxide in the crustacean brain: Regulation of neurogenesis and morphogenesis in the developing olfactory pathway. Dev Dyn 236: 3047–3060. doi: 10.1002/dvdy.21340
    [291] Scholz NL, Chang ES, Graubard K, et al. (1998) The NO/cGMP pathway and the development of neural networks in postembryonic lobsters. J Neurobiol 34: 208–226. doi: 10.1002/(SICI)1097-4695(19980215)34:3<208::AID-NEU2>3.0.CO;2-6
    [292] Dickinson PS, Calkins A, Stevens JS (2015) Related neuropeptides use different balances of unitary mechanisms to modulate the cardiac neuromuscular system in the American lobster, Homarus americanus. J Neurophysiol 113: 856–870. doi: 10.1152/jn.00585.2014
    [293] Goy MF (2005) Nitric oxide: An inhibitory retrograde modulator in the crustacean heart. Comp Biochem Physiol A Mol Integr Physiol 142: 151–163. doi: 10.1016/j.cbpb.2005.05.050
    [294] Mahadevan A, Lappe J, Rhyne RT, et al. (2004) Nitric oxide inhibits the rate and strength of cardiac contractions in the lobster Homarus americanus by acting on the cardiac ganglion. J Neurosci 24: 2813–2824. doi: 10.1523/JNEUROSCI.3779-03.2004
    [295] McGrath LL, Vollmer SV, Kaluziak ST, et al. (2016) De novo transcriptome assembly for the lobster Homarus americanus and characterization of differential gene expression across nervous system tissues. BMC Genomics 17: 63. doi: 10.1186/s12864-016-2373-3
    [296] Dyuizen IV, Kotsyuba EP, Lamash NE (2012) Changes in the nitric oxide system in the shore crab Hemigrapsus sanguineus (Crustacea, Decapoda) CNS induced by a nociceptive stimulus. J Exp Biol 215: 2668–2676. doi: 10.1242/jeb.066845
    [297] Filgueira Dde M, Guterres LP, Votto AP, et al. (2010) Nitric oxide-dependent pigment migration induced by ultraviolet radiation in retinal pigment cells of the crab Neohelice granulata. Photochem Photobiol 86: 1278–1284. doi: 10.1111/j.1751-1097.2010.00787.x
    [298] Scholz NL, de Vente J, Truman JW, et al. (2001) Neural network partitioning by NO and cGMP. J Neurosci 21: 1610–1618. doi: 10.1523/JNEUROSCI.21-05-01610.2001
    [299] Scholz NL, Goy MF, Truman JW, et al. (1996) Nitric oxide and peptide neurohormones activate cGMP synthesis in the crab stomatogastric nervous system. J Neurosci 16: 1614–1622. doi: 10.1523/JNEUROSCI.16-05-01614.1996
    [300] Scholz NL, Labenia JS, de Vente J, et al. (2002) Expression of nitric oxide synthase and nitric oxide-sensitive guanylate cyclase in the crustacean cardiac ganglion. J Comp Neurol 454: 158–167. doi: 10.1002/cne.10442
    [301] Stein W, Eberle CC, Hedrich UB (2005) Motor pattern selection by nitric oxide in the stomatogastric nervous system of the crab. Eur J Neurosci 21: 2767–2781. doi: 10.1111/j.1460-9568.2005.04117.x
    [302] Aonuma H, Nagayama T, Takahata M (2000) Modulatory effects of nitric oxide on synaptic depression in the crayfish neuromuscular system. J Exp Biol 203: 3595–3602.
    [303] Aonuma H, Newland PL (2001) Opposing actions of nitric oxide on synaptic inputs of identified interneurones in the central nervous system of the crayfish. J Exp Biol 204: 1319–1332.
    [304] Aonuma H, Newland PL (2002) Synaptic inputs onto spiking local interneurons in crayfish are depressed by nitric oxide. J Neurobiol 52: 144–155. doi: 10.1002/neu.10081
    [305] Araki M, Schuppe H, Fujimoto S, et al. (2004) Nitric oxide modulates local reflexes of the tailfan of the crayfish. J Neurobiol 60: 176–186. doi: 10.1002/neu.20007
    [306] Christie AE, Edwards JM, Cherny E, et al. (2003) Immunocytochemical evidence for nitric oxide- and carbon monoxide-producing neurons in the stomatogastric nervous system of the crayfish Cherax quadricarinatus. J Comp Neurol 467: 293–306. doi: 10.1002/cne.10926
    [307] Johansson KU, Mellon Jr D (1998) Nitric oxide as a putative messenger molecule in the crayfish olfactory midbrain. Brain Res 807: 237–242. doi: 10.1016/S0006-8993(98)00826-9
    [308] Kovaleva VD, Uzdensky AB (2016) Photodynamic therapy-induced nitric oxide production in neuronal and glial cells. J Biomed Opt 21: 105005. doi: 10.1117/1.JBO.21.10.105005
    [309] Mita A, Yoshida M, Nagayama T (2014) Nitric oxide modulates a swimmeret beating rhythm in the crayfish. J Exp Biol 217: 4423–4431. doi: 10.1242/jeb.110551
    [310] Ott SR, Aonuma H, Newland PL, et al. (2007) Nitric oxide synthase in crayfish walking leg ganglia: Segmental differences in chemo-tactile centers argue against a generic role in sensory integration. J Comp Neurol 501: 381–399. doi: 10.1002/cne.21242
    [311] Schuppe H, Araki M, Aonuma H, et al. (2004) Effects of nitric oxide on proprioceptive signaling. Zoolog Sci 21: 1–5. doi: 10.2108/0289-0003(2004)21[1:EONOOP]2.0.CO;2
    [312] Schuppe H, Newland PL (2004) Nitric oxide modulates presynaptic afferent depolarization of mechanosensory neurons. J Neurobiol 59: 331–342. doi: 10.1002/neu.10333
    [313] Uzdensky A, Berezhnaya E, Khaitin A, et al. (2015) Protection of the Crayfish Mechanoreceptor Neuron and Glial Cells from Photooxidative Injury by Modulators of Diverse Signal Transduction Pathways. Mol Neurobiol 52: 811–825. doi: 10.1007/s12035-015-9237-8
    [314] Christie AE, Fontanilla TM, Roncalli V, et al. (2014) Diffusible gas transmitter signaling in the copepod crustacean Calanus finmarchicus: Identification of the biosynthetic enzymes of nitric oxide (NO), carbon monoxide (CO) and hydrogen sulfide (H2S) using a de novo assembled transcriptome. Gen Comp Endocrinol 202: 76–86. doi: 10.1016/j.ygcen.2014.04.003
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