Search Advanced

AIMS Molecular Science

2018, Volume 5, Issue 1: 117-130. doi: 10.3934/molsci.2018.1.117
Previous Article Next Article
Review

Steroid hormones as interkingdom signaling molecules: Innate immune function and microbial colonization modulation

  • Department of Microbiology and Immunology, Midwestern University, Downers Grove, IL 60515, USA
  • Received: 03 January 2018 Accepted: 23 March 2018 Published: 27 March 2018

  • Steroid hormones e.g., estrogen, progesterone, testosterone and dehydroepiandosterone, act as inter-kingdom quorum chemical signaling compounds. All steroids examined exhibit a steroid concentration specific bi-functionality. At one end of the spectrum, the steroids enhance expression of virulence-associated behaviors, most specifically, increased rate of replication and adherence to surfaces. In contrast, the hormones also function as innate immune system compounds providing first-line protection against essential pathogen behaviors e.g., biofilm formation, which plays a role in initiation of the vast majority of infectious processes, especially chronic infections. Mechanistically, this protection is mediated by both direct effects of steroids on microbes, as well as indirect actions which result in expression of nitric oxide at levels reported to inhibit proper biofilm formation and cause return of sessile cells to a planktonic state.

    Citation: Michael W Patt, Lisa Conte, Mary Blaha, Balbina J Plotkin. Steroid hormones as interkingdom signaling molecules: Innate immune function and microbial colonization modulation[J]. AIMS Molecular Science, 2018, 5(1): 117-130. doi: 10.3934/molsci.2018.1.117

    Related Papers:

  • Steroid hormones e.g., estrogen, progesterone, testosterone and dehydroepiandosterone, act as inter-kingdom quorum chemical signaling compounds. All steroids examined exhibit a steroid concentration specific bi-functionality. At one end of the spectrum, the steroids enhance expression of virulence-associated behaviors, most specifically, increased rate of replication and adherence to surfaces. In contrast, the hormones also function as innate immune system compounds providing first-line protection against essential pathogen behaviors e.g., biofilm formation, which plays a role in initiation of the vast majority of infectious processes, especially chronic infections. Mechanistically, this protection is mediated by both direct effects of steroids on microbes, as well as indirect actions which result in expression of nitric oxide at levels reported to inhibit proper biofilm formation and cause return of sessile cells to a planktonic state.


    加载中
    [1] Miller MB, Bassler BL (2001) Quorum sensing in bacteria. Annu Rev Microbiol 55: 165–199. doi: 10.1146/annurev.micro.55.1.165
    [2] Hastings JW, Greenberg EP (1999) Quorum sensing: The explanation of a curious phenomenon reveals a common characteristic of bacteria. J Bacteriol 181: 2667–2668.
    [3] Horswill A, Stoodley P, Stewart PS, et al. (2007) The effect of the chemical, biological, and physical environment on quorum sensing in structured microbial communities. Anal Bioanal Chem 387: 371–380. doi: 10.1007/s00216-006-0720-y
    [4] Miller M, Bassler B (2001) Quorum sensing in bacteria. Annu Rev Microbiol 55: 165–199. doi: 10.1146/annurev.micro.55.1.165
    [5] Reading N, Sperandio V (2006) Quorum sensing: The many languages of bacteria. FEMS Microbiol Lett 254: 1–11. doi: 10.1111/j.1574-6968.2005.00001.x
    [6] Plotkin BJ, Viselli SM (2000) Effect of insulin on microbial growth. Curr Microbiol 41: 60–64. doi: 10.1007/s002840010092
    [7] Plotkin B, Wu Z, Ward K, et al. (2014) Effect of human insulin on the formation of catheter-associated E. coli biofilms. Open J Urol 4: 49–56.
    [8] Sperandio V, Torres AG, Jarvis B, et al. (2003) Bacteria-host communication: The language of hormones. Proc Natl Acad Sci U.S.A 100: 8951–8956. doi: 10.1073/pnas.1537100100
    [9] Bjarnsholt T (2013) The role of bacterial biofilms in chronic infections. Apmis 121: 1–58.
    [10] Bryers J (2008) Medical biofilms. Biotechnol Bioeng 100: 1–18. doi: 10.1002/bit.21838
    [11] Burmølle M, Hansen L, Sørensen S (2007) Establishment and early succession of a multispecies biofilm composed of soil bacteria. Microb Ecol 54: 352–362. doi: 10.1007/s00248-007-9222-5
    [12] Costerton J, Stewart P, Greenberg E (1999) Bacterial biofilms: A common cause of persistent infections. Science 284: 1318–1322. doi: 10.1126/science.284.5418.1318
    [13] Donlan R (2001) Biofilm formation: A clinically relevant microbiological process. Clin Infect Dis 33: 1387–1392. doi: 10.1086/322972
    [14] Martinotti MG, Savoia D (1985) Effect of some steroid hormones on the growth of Trichomonas vaginalis. G Batteriol Virol Immunol 78: 52–59.
    [15] Sugarman B, Mummaw N (1988) The effect of hormones on Trichomonas vaginalis. J Gen Microbiol 134: 1623–1628.
    [16] Drutz DJ, Huppert M, Sun SH, et al. (1981) Human sex hormones stimulate the growth and maturation of Coccidioides immitis. Infect Immun 32: 897–907.
    [17] Elsherif S, Refai M (1976) Studies on the fungistatic action of hormones on dermatophytes. E Rodenwaldt-Archiv 3: 101–108.
    [18] Hall-Stoodley L, Costerton JW, Stoodley P (2004) Bacterial biofilms: From the natural environment to infectious diseases. Nat Rev Microbiol 2: 95–108. doi: 10.1038/nrmicro821
    [19] Zhang X, Essmann M, Burt ET, et al. (2000) Estrogen effects on Candida albicans: A potential virulence-regulating mechanism. J Infect Dis 181: 1441–1446. doi: 10.1086/315406
    [20] Cheng G, Yeater KM, Hoyer LL (2006) Cellular and molecular biology of Candida albicans estrogen response. Eukaryotic cell 5: 180–191. doi: 10.1128/EC.5.1.180-191.2006
    [21] Kinsman OS, Pitblado K, Coulson CJ (2010) Effect of mammalian steroid hormones and luteinizing hormone on the germination of Candida albicans and implications for vaginal candidosis. Mycoses 31: 617–626.
    [22] White S, Larsen B (1997) Candida albicans morphogenesis is influenced by estrogen. Cell Mol Life Sci CMLS 53: 744–749. doi: 10.1007/s000180050094
    [23] White T, Silver P (2005) Regulation of sterol metabolism in Candida albicans by the UPC2 gene. Biochem Soc Trans 33: 1215–1218.
    [24] Tarry W, Fisher M, Shen S, et al. (2005) Candida albicans: The estrogen target for vaginal colonization. J Surg Res 129: 278–282. doi: 10.1016/j.jss.2005.05.019
    [25] Fidel PL, Cutright J, Steele C (2000) Effects of reproductive hormones on experimental vaginal candidiasis. Infect Immun 68: 651–657. doi: 10.1128/IAI.68.2.651-657.2000
    [26] Micheli Md, Bille J, Schueller C, et al. (2002) A common drug-responsive element mediates the upregulation of the Candida albicans ABC transports CDR1 and CDR2, two genes involved in antifunal drug resistance. Mol Microbiol 43: 1197–1214. doi: 10.1046/j.1365-2958.2002.02814.x
    [27] Karnani N, Gaur NA, Jha S, et al. (2004) SRE1 and SRE2 are two specific steroid-responsive modules of Candida drug resistance gene 1 (CDR1) promoter. Yeast 21: 219–239. doi: 10.1002/yea.1067
    [28] Krishnamurthy S, Gupta V, Prasad R, et al. (1998) Expression of CDR1, a multidrug resistance gene of Candida albicans: Transcriptional activation by heat shock, drugs and human steroid hormones. FEMS Microbiol Lett 160: 191–197. doi: 10.1111/j.1574-6968.1998.tb12910.x
    [29] Kornman KS, Loesche WJ (1982) Effects of estradiol and progesterone on Bacteroides melaninogenicus and Bacteroides gingivalis. Infect Immun 35: 256–263.
    [30] Chotirmall SH, Smith SG, Gunaratnam C, et al. (2012) Effect of estrogen on pseudomonas mucoidy and exacerbations in cystic fibrosis. N Engl J Med 366: 1978–1986. doi: 10.1056/NEJMoa1106126
    [31] Lyczak JB, Cannon CL, Pier GB (2002) Lung Infections Associated with Cystic Fibrosis. Clin Microbiol Rev 15: 194–222. doi: 10.1128/CMR.15.2.194-222.2002
    [32] Mihai MM, Holban AM, Giurcaneanu C, et al. (2015) Microbial biofilms: Impact on the pathogenesis of periodontitis, cystic fibrosis, chronic wounds and medical device-related infections. Curr Top Med Chem 15: 1552–1576. doi: 10.2174/1568026615666150414123800
    [33] Rowland SS, Falkler WA, Bashirelahi N (1992) Identification of an estrogen-binding protein in Pseudomonas aeruginosa. J Steroid Biochem Mol Biol 42: 721–727. doi: 10.1016/0960-0760(92)90113-W
    [34] Amirshahi A, Wan C, Beagley K, et al. (2011) Modulation of the Chlamydia trachomatis in vitro transcriptome response by the sex hormones estradiol and progesterone. BMC Microbiol 11: 150. doi: 10.1186/1471-2180-11-150
    [35] Edwards JL (2010) Neisseria gonorrhoeae survival during primary human cervical epithelial cell infection requires nitric oxide and is augmented by progesterone. Infect Immun 78: 1202–1213. doi: 10.1128/IAI.01085-09
    [36] Yamaguchi H, Kamiya S, Uruma T, et al. (2008) Chlamydia pneumoniae Growth Inhibition in Cells by the Steroid Receptor Antagonist RU486 (Mifepristone). Antimicrob Agents Chemother 52: 1991–1998. doi: 10.1128/AAC.01416-07
    [37] Ishida K, Yamazaki T, Motohashi K, et al. (2012) Effect of the steroid receptor antagonist RU486 (mifepristone) on an IFNγ-induced persistent Chlamydophila pneumoniae infection model in epithelial HEp-2 cells. J Infect Chemother 19: 22–29.
    [38] Hahn DL, Mcdonald R (1998) Can acute Chlamydia pneumoniae respiratory tract infection initiate chronic asthma? Ann Allergy Asthma Immunol 81: 339–344. doi: 10.1016/S1081-1206(10)63126-2
    [39] Renee MD, Morehead MS (2001) Mifepristone. Ann Pharmacother 35: 707–719. doi: 10.1345/aph.10397
    [40] Farr S, Banks W, Uezu K, et al. (2004) DHEAS improves learning and memory in aged SAMP8 mice but not in diabetic mice. Life Sci 75: 2775–2785. doi: 10.1016/j.lfs.2004.05.026
    [41] Nippoldt T (1998) Dehydroepiandrosterone supplements: Bringing sense to sensational claims. Endocr Pract 4: 106–111. doi: 10.4158/EP.4.2.106
    [42] Straub R, Konecna L, Hrach S, et al. (1998) Serum dehydroepiandrosterone (DHEA) and DHEA sulfate are negatively correlated with serum interleukin-6 (IL-6), and DHEA inhibits IL-6 secretion from mononuclear cells in man in vitro: Possible link between endocrinsensecence and immunosenescence. J Clin Endocrinol Metab 83: 2012–2017. doi: 10.1210/jcem.83.6.4876
    [43] Yotis W, Waner J (1968) Antimicrobial properties of testosterone and its intermediates. Antonie van Leeuwenhoek 34: 275–286. doi: 10.1007/BF02046449
    [44] Plotkin BJ, Konakieva MI (2017) Attenuation of antimicrobial activity by the human steroid hormones. Steroids 128: 120–127. doi: 10.1016/j.steroids.2017.09.007
    [45] Plotkin B, Erickson Q, Roose R, et al. (2003) Effect of androgens and glucocorticoids on microbial growth and antimicrobial susceptibility. Curr Microbiol 47: 514–520.
    [46] Plotkin B, Konaklieva M (2007) Possible role of sarA in dehydroepiandosterone (DHEA)-mediated increase in Staphylococcus aureus resistance to vancomycin. Chemotherapy 53: 181–184. doi: 10.1159/000100863
    [47] Proctor R, Peters G (1998) Small colony variants in staphylococcal infections: Diagnostic and therapeutic implications. Clin Infect Dis 27: 419–422. doi: 10.1086/514706
    [48] Wong SS, Ho PL, Woo PC, et al. (1999) Bacteremia caused by staphylococci with inducible vancomycin heteroresistance. Clin Infect Dis 29: 760–767. doi: 10.1086/520429
    [49] Donlan RM (2002) Biofilms: Microbial Life on Surfaces. Emerging Infect Dis 8: 881–890. doi: 10.3201/eid0809.020063
    [50] Plotkin B, Morejon A, Laddaga R, et al. (2005) Induction of increased resistance to vancomycin in Staphylococcus aureus clinical isolates (MSSA, MRSA) by dehydroepiandosterone (DHEA). Lett Appl Microbiol 40: 249–254. doi: 10.1111/j.1472-765X.2005.01665.x
    [51] Hiramatsu K, Dick JD, Perl TM (1998) Vancomycin resistance in staphylococci. Drug Resist Updates 1: 135–150. doi: 10.1016/S1368-7646(98)80029-0
    [52] Howe R, Wootton M, Walsh T, et al. (1999) Expression and detection of hetero-vancomycin resistance in Staphylococcus aureus. J Antimicrob Chemother 44: 675–678. doi: 10.1093/jac/44.5.675
    [53] Moise PA, Schentag JJ (2000) Vancomycin treatment failures in Staphylococcus aureus lower respiratory tract infections. Int J Antimicrob Agents 16: 31–34.
    [54] Martinotti MG, Savoia D (1985) Effect of some steroid hormones on the growth of Trichomonas vaginalis. G Batteriol Virol Immunol 78: 52–59.
    [55] Yotis WW, Fitzgerald T (1974) Hormonally induced alterations in Staphylococcus aureus. Ann N Y Acad Sci 236: 187–202. doi: 10.1111/j.1749-6632.1974.tb41491.x
    [56] Reiss F (1947) The effect of hormones on the growth of Trichophyton purpureum and Trichophyton gypseum. J Invest Dermatol 8: 245–250. doi: 10.1038/jid.1947.35
    [57] Lysko PG, Morse SA (1980) Effects of steroid hormones on Neisseria gonorrhoeae. Antimicrob Agents Chemother 18: 281–288. doi: 10.1128/AAC.18.2.281
    [58] Morse SA, Fitzgerald TJ (1974) Effect of progesterone on Neisseria gonorrhoeae. Infect Immun 10: 1370–1377.
    [59] Yotis WW, Savov ZT (1970) Reduction of the cytolytic action of staphylococcal alpha toxin by progesterone. Yale J Biol Med 42: 411.
    [60] Haam VE, Rosenfeld I (1942) The effect of the various sex hormones upon experimental pneumococcus infections in mice. J Infect Dis 70: 243–247. doi: 10.1093/infdis/70.3.243
    [61] Yotis W, Fitzgerald T (1968) Responses of staphylococci to androgens. Appl Microbiol 16: 1512–1517.
    [62] Li J, Niu J, Ou S, et al. (2012) Effects of SCR-3 on the immunosuppression accompanied with the systemic inflammatory response syndrome. Mol Cell Biochem 364: 29–37. doi: 10.1007/s11010-011-1201-y
    [63] Yu C, York B, Wang S, et al. (2007) An essential function of the SRC-3 coactivator in suppression of cytokine mRNA translation and inflammatory response. Mol Cell 25: 765–778. doi: 10.1016/j.molcel.2007.01.025
    [64] Chen CY, Hofmann CS, Cottrell BJ, et al. (2013) Phenotypic and genotypic characterization of biofilm forming capabilities in non-O157 Shiga toxin-producing Escherichia coli strains. PloS One 8: e84863. doi: 10.1371/journal.pone.0084863
    [65] Bäumler AJ, Sperandio V (2016) Interactions between the microbiota and pathogenic bacteria in the gut. Nature 535: 85–93. doi: 10.1038/nature18849
    [66] Mittler R, Vanderauwera S, Suzuki N, et al. (2011) ROS signaling: The new wave? Trends plant Sci 16: 300–309. doi: 10.1016/j.tplants.2011.03.007
    [67] Lushchak VI (2011) Adaptive response to oxidative stress: Bacteria, fungi, plants and animals. Comp Biochem Physiol Toxicol Pharmacol Cbp 153: 175–190. doi: 10.1016/j.cbpc.2010.10.004
    [68] Tanaka H, Ishibashi J, Fujita K, et al. (2008) A genome-wide analysis of genes and gene families involved in innate immunity of Bombyx mori. Insect Biochem Mol Biol 38: 1087–1110. doi: 10.1016/j.ibmb.2008.09.001
    [69] Daiber A, Steven S, Weber A, et al. (2017) Targeting vascular (endothelial) dysfunction. Br J Pharmacol 174: 1591–1619. doi: 10.1111/bph.13517
    [70] Jankovic A, Korac A, Buzadzic B, et al. (2017) Targeting the NO/superoxide ratio in adipose tissue: Relevance to obesity and diabetes management. Br J Pharmacol 174: 1570–1590. doi: 10.1111/bph.13498
    [71] Vergadi E, Ieronymaki E, Lyroni K, et al. (2017) Akt signaling pathway in macrophage activation and M1/M2 polarization. J Immun 198: 1006–1014. doi: 10.4049/jimmunol.1601515
    [72] Wink DA, Mitchell JB (1998) Chemical biology of nitric oxide: Insights into regulatory, cytotoxic, and cytoprotective mechanisms of nitric oxide. Free Radical Biol Med 25: 434–456. doi: 10.1016/S0891-5849(98)00092-6
    [73] Knowles RG, Moncada S (1994) Nitric oxide synthases in mammals. Biochem J 298: 249–258. doi: 10.1042/bj2980249
    [74] Alderton WK, Cooper CE, Knowles RG (2001) Nitric oxide synthases: Structure, function and inhibition. Biochem J 357: 593. doi: 10.1042/bj3570593
    [75] Laubach VE, Foley PL, Shockey KS, et al. (1998) Protective roles of nitric oxide and testosterone in endotoxemia: Evidence from NOS-2-deficient mice. Am J Physiol 275: 2211–2218.
    [76] Yin F, Kang J, Han N, et al. (2015) Effect of dehydroepiandrosterone treatment on hormone levels and antioxidant parameters in aged rats. Genet Mol Res 14: 11300–11311. doi: 10.4238/2015.September.22.24
    [77] Alagöl H, Erdem E, Sancak B, et al. (1999) Nitric oxide biosynthesis and malondialdehyde levels in advanced breast cancer. Aust N Z J Surg 69: 647–650. doi: 10.1046/j.1440-1622.1999.01656.x
    [78] Karpuzoglu E, Ahmed SA (2006) Estrogen regulation of nitric oxide and inducible nitric oxide synthase (iNOS) in immune cells: Implications for immunity, autoimmune diseases, and apoptosis. Nitric Oxide 15: 177–186. doi: 10.1016/j.niox.2006.03.009
    [79] Straub RH (2007) The Complex Role of Estrogens in Inflammation. Endocr Rev 28: 521–574. doi: 10.1210/er.2007-0001
    [80] Tomaszewska A, Guevara I, Wilczok T, et al. (2003) 17β-estradiol- and lipopolysaccharide-induced changes in nitric oxide, tumor necrosis factor-α and vascular endothelial growth factor release from RAW 264.7 macrophages. Gynecol Obstet Invest 56: 152–159. doi: 10.1159/000073775
    [81] Shimizu T, Szalay L, Choudhry MA, et al. (2005) Mechanism of salutary effects of androstenediol on hepatic function after trauma-hemorrhage: Role of endothelial and inducible nitric oxide synthase. Am J Physiol Gastrointest Liver Physiol 288: G244–G250. doi: 10.1152/ajpgi.00387.2004
    [82] Cattaneo MG, Vanetti C, Decimo I, et al. (2017) Sex-specific eNOS activity and function in human endothelial cells. Sci Rep 7: 9612. doi: 10.1038/s41598-017-10139-x
    [83] Osol G, Ko NL, Mandalà M (2017) Altered endothelial nitric oxide signaling as a paradigm for maternal vascular maladaptation in preeclampsia. Curr Hypertens Rep 19: 82. doi: 10.1007/s11906-017-0774-6
    [84] Chen R, Tu Y, Lin J, et al. (2010) The nongenomic effects of progesterone in repressing iNOS activation through P38MAPK pathways in gonococci-infected polymorphonuclear leukocytes and the clinical significance. J Huazhong Univ Sci Technol Med Sci 30: 119–125. doi: 10.1007/s11596-010-0122-4
    [85] Sulemankhil I, Ganopolsky JG, Dieni CA, et al. (2012) Prevention and treatment of virulent bacterial biofilms with an enzymatic nitric oxide-releasing dressing. Antimicrob Agents Chemother 56: 6095–6103. doi: 10.1128/AAC.01173-12
    [86] Braeken K, Debkumari B, Fauvart M, et al. (2008) Living on a surface: Swarming and biofilm formation. Trends Microbiol 16: 496. doi: 10.1016/j.tim.2008.07.004
    [87] Costerton J, Lewandowski Z, Caldwell D, et al. (1995) Microbial biofilms. Annu Rev Microbiol 49: 711–745. doi: 10.1146/annurev.mi.49.100195.003431
    [88] Barraud N, Schleheck D, Klebensberger J, et al. (2009) Nitric oxide signaling in Pseudomonas aeruginosa biofilms mediates phosphodiesterase activity, decreased cyclic di-GMP levels, and enhanced dispersal. J Bacteriol 191: 7333–7342. doi: 10.1128/JB.00975-09
    [89] Barraud N, Storey MV, Moore ZP, et al. (2009) Nitric oxide-mediated dispersal in single- and multi-species biofilms of clinically and industrially relevant microorganisms. Microb Biotechnol 2: 370–378. doi: 10.1111/j.1751-7915.2009.00098.x
    [90] Povolotsky TL, Hengge R (2012) "Life-style" control networks in Escherichia coli: Signaling by the second messenger c-di-GMP. J Biotechnol 160: 10–16. doi: 10.1016/j.jbiotec.2011.12.024
    [91] Sancheztorres V, Hu H, Wood TK (2011) GGDEF Proteins YeaI, YedQ, and YfiN Reduce Early Biofilm Formation and Swimming Motility in Escherichia coli. Appl Microbiol Biotechnol 90: 651–658. doi: 10.1007/s00253-010-3074-5
    [92] Van Oss CJ (1978) Phagocytosis as a Surface Phenomenon. Annu Rev Microbiol 32: 19–39. doi: 10.1146/annurev.mi.32.100178.000315
    [93] Hallstoodley L, Costerton JW, Stoodley P (2004) Bacterial biofilms: From the natural environment to infectious diseases. Nat Rev Microbiol 2: 95–108. doi: 10.1038/nrmicro821
    [94] Barraud N, Hassett DJ, Hwang SH, et al. (2006) Involvement of nitric oxide in biofilm dispersal of Pseudomonas aeruginosa. J Bacteriol 188: 7344–7353. doi: 10.1128/JB.00779-06
    [95] Barraud N, Storey MV, Moore ZP, et al. (2009) Nitric oxide-mediated dispersal in single- and multi-species biofilms of clinically and industrially relevant microorganisms. Microb Biotechnol 2: 370–378. doi: 10.1111/j.1751-7915.2009.00098.x
    [96] Scarpin KM, Graham JD, Mote PA, et al. (2009) Progesterone action in human tissues: regulation by progesterone receptor (PR) isoform expression, nuclear positioning and coregulator expression. Nucl Recept Signaling 7: e009.
    [97] Falsetta ML, Bair TB, Ku SC, et al. (2009) Transcriptional profiling identifies the metabolic phenotype of gonococcal biofilms. Infect Immun 77: 3522–3532. doi: 10.1128/IAI.00036-09
    [98] Zaitseva J, Granik V, Belik A, et al. (2009) Effect of nitrofurans and NO generators on biofilm formation by Pseudomonas aeruginosa PAO1 and Burkholderia cenocepacia 370. Res Microbiol 160: 353–357. doi: 10.1016/j.resmic.2009.04.007
    [99] Arora DP, Hossain S, Xu Y, et al. (2015) Nitric Oxide Regulation of Bacterial Biofilms. Biochemistry 54: 3717–3728. doi: 10.1021/bi501476n
    [100] Beckman JS, Beckman TW, Chen J, et al. (1990) Apparent hydroxyl radical production by peroxynitrite: Implications for endothelial injury from nitric oxide and superoxide. Proc Natl Acad Sci U.S.A 87: 1620–1624. doi: 10.1073/pnas.87.4.1620
    [101] Ghaffari A, Miller CC, Mcmullin B, et al. (2006) Potential application of gaseous nitric oxide as a topical antimicrobial agent. Nitric Oxide 14: 21–29.
    [102] Anstey NM, Weinberg JB, Hassanali MY, et al. (1996) Nitric oxide in Tanzanian children with malaria: Inverse relationship between malaria severity and nitric oxide production/nitric oxide synthase type 2 expression. J Exp Med 184: 557. doi: 10.1084/jem.184.2.557
    [103] Schmidt I, Steenbakkers PJM, Camp HJMOD, et al. (2004) Physiologic and Proteomic Evidence for a Role of Nitric Oxide in Biofilm Formation by Nitrosomonas europaea and Other Ammonia Oxidizers. J Bacteriol 186: 2781–2788. doi: 10.1128/JB.186.9.2781-2788.2004
    [104] Yoon MY, Lee KM, Park Y, et al. (2011) Contribution of Cell Elongation to the Biofilm Formation of Pseudomonas aeruginosa during Anaerobic Respiration. PLoS One 6: e16105. doi: 10.1371/journal.pone.0016105
    [105] Yoon SS, Hennigan RF, Hilliard GM, et al. (2002) Pseudomonas aeruginosa anaerobic respiration in biofilms: Relationships to cystic fibrosis pathogenesis. Dev Cell 3: 593–603. doi: 10.1016/S1534-5807(02)00295-2
    [106] Casillo A, Papa R, Ricciardelli A, et al. (2017) Anti-Biofilm Activity of a Long-Chain Fatty Aldehyde from Antarctic Pseudoalteromonas haloplanktis TAC125 against Staphylococcus epidermidis Biofilm. Front Cell Infect Microbiol 7: 46.
    [107] Parrilli E, Papa R, Carillo S, et al. (2015) Anti-biofilm activity of pseudoalteromonas haloplanktis tac125 against staphylococcus epidermidis biofilm: Evidence of a signal molecule involvement? Int J Immunopathol Pharmacol 28: 104–113. doi: 10.1177/0394632015572751
  • Reader Comments
  • © 2018 the Author(s), licensee AIMS Press. This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0)
通讯作者: 陈斌, bchen63@163.com
  • 1. 

    沈阳化工大学材料科学与工程学院 沈阳 110142

  1. 本站搜索
  2. 百度学术搜索
  3. 万方数据库搜索
  4. CNKI搜索
AIMS Molecular Science
0.7

Metrics

Article views(6848) PDF downloads(2360) Cited by(6)

Preview PDF
Download XML
Export Citation
Article outline

Figures and Tables

Figures(3)

Other Articles By Authors

Related pages

Tools

/

DownLoad:  Full-Size Img  PowerPoint
Return
Return

Catalog