Research article

Prosopis africana exerts neuroprotective activity against quaternary metal mixture-induced memory impairment mediated by oxido-inflammatory response via Nrf2 pathway

  • Received: 19 February 2024 Revised: 04 April 2024 Accepted: 12 April 2024 Published: 22 April 2024
  • The beneficial effects of Prosopis africana (PA) on human health have been demonstrated; however, its protective effects against heavy metals (HM) are not yet understood. This study evaluated the potential neuroprotective effects of PA in the cerebral cortex and cerebellum. To accomplish this, we divided 35 albino Sprague Dawley rats into five groups. Group I did not receive either heavy metal mixture (HMM) or PA. Group II received a HMM of PbCl2 (20 mg/kg), CdCl2 (1.61 mg/kg), HgCl2 (0.40 mg/kg), and NaAsO3 (10 mg/kg) orally for a period of two months. Groups III, IV, and V received HMM along with PA at doses of 500, 1000, and 1500 mg/kg, respectively. PA caused decreased levels of HM accumulation in the cerebral cortex and cerebellum and improved performance in the Barnes maze and rotarod tests. PA significantly reduced levels of IL-6 and TNF-α. PA increased concentrations of SOD, CAT, GSH, and Hmox-1 and decreased the activities of AChE and Nrf2. In addition, levels of MDA and NO decreased in groups III, IV, and V, along with an increase in the number of live neurons. In conclusion, PA demonstrates a complex neuroprotective effect with the potential to alleviate various aspects of HM-induced neurotoxicity.

    Citation: Orish E. Orisakwe, Evelyn Utomoibor Ikpeama, Chinna N. Orish, Anthonet N. Ezejiofor, Kenneth O. Okolo, Aleksandar Cirovic, Ana Cirovic, Ify L. Nwaogazie, Chinekwu Samson Onoyima. Prosopis africana exerts neuroprotective activity against quaternary metal mixture-induced memory impairment mediated by oxido-inflammatory response via Nrf2 pathway[J]. AIMS Neuroscience, 2024, 11(2): 118-143. doi: 10.3934/Neuroscience.2024008

    Related Papers:

  • The beneficial effects of Prosopis africana (PA) on human health have been demonstrated; however, its protective effects against heavy metals (HM) are not yet understood. This study evaluated the potential neuroprotective effects of PA in the cerebral cortex and cerebellum. To accomplish this, we divided 35 albino Sprague Dawley rats into five groups. Group I did not receive either heavy metal mixture (HMM) or PA. Group II received a HMM of PbCl2 (20 mg/kg), CdCl2 (1.61 mg/kg), HgCl2 (0.40 mg/kg), and NaAsO3 (10 mg/kg) orally for a period of two months. Groups III, IV, and V received HMM along with PA at doses of 500, 1000, and 1500 mg/kg, respectively. PA caused decreased levels of HM accumulation in the cerebral cortex and cerebellum and improved performance in the Barnes maze and rotarod tests. PA significantly reduced levels of IL-6 and TNF-α. PA increased concentrations of SOD, CAT, GSH, and Hmox-1 and decreased the activities of AChE and Nrf2. In addition, levels of MDA and NO decreased in groups III, IV, and V, along with an increase in the number of live neurons. In conclusion, PA demonstrates a complex neuroprotective effect with the potential to alleviate various aspects of HM-induced neurotoxicity.



    加载中

    Acknowledgments



    None.

    Ethical approval



    All procedures involving animals and the experimental protocol followed guidelines for the safe use of animals in research and were approved by the University of Port Harcourt animal research committee (UPH/CEREMAD/REC/MM73/014).

    Consent to Publish



    All authors have given their consent for publication.

    Funding



    None.

    Conflicts of interests



    Authors confirm that there was no conflict of interest.

    Availability of data and materials



    All data have been provided.

    [1] Bjørklund G, Chartrand MS, Aaseth J (2017) Manganese exposure and neurotoxic effects in children. Environ Res 155: 380-384. https://doi.org/10.1016/j.envres.2017.03.003
    [2] Mason LH, Harp JP, Han DY (2014) Pb neurotoxicity: neuropsychological effects of lead toxicity. Biomed Res Int 2014: 840547. https://doi.org/10.1155/2014/840547
    [3] Florea AM, Büsselberg D (2006) Occurrence, use and potential toxic effects of metals and metal compounds. Biometals 19: 419-427. https://doi.org/10.1007/s10534-005-4451-x
    [4] Jaishankar M, Tseten T, Anbalagan N, et al. (2014) Toxicity, mechanism and health effects of some heavy metals. Interdiscip Toxicol 7: 60-72. https://doi.org/10.2478/intox-2014-0009
    [5] Aherrera A, Olmedo P, Grau-Perez M, et al. (2017) The association of e-cigarette use with exposure to nickel and chromium: A preliminary study of non-invasive biomarkers. Environ Res 159: 313-320. https://doi.org/10.1016/j.envres.2017.08.014
    [6] Olmedo P, Goessler W, Tanda S, et al. (2018) Metal Concentrations in e-Cigarette Liquid and Aerosol Samples: The Contribution of Metallic Coils. Environ Health Perspect 126: 027010. https://doi.org/10.1289/EHP2175
    [7] Zhao D, Navas-Acien A, Ilievski V, et al. (2019) Metal concentrations in electronic cigarette aerosol: Effect of open-system and closed-system devices and power settings. Environ Res 174: 125-134. https://doi.org/10.1016/j.envres.2019.04.003
    [8] Gade M, Comfort N, Re DB (2021) Sex-specific neurotoxic effects of heavy metal pollutants: Epidemiological, experimental evidence and candidate mechanisms. Environ Res 201: 111558. https://doi.org/10.1016/j.envres.2021.111558
    [9] Zheng W, Aschner M, Ghersi-Egea JF (2003) Brain barrier systems: a new frontier in metal neurotoxicological research. Toxicol Appl Pharmacol 192: 1-11. https://doi.org/10.1016/S0041-008X(03)00251-5
    [10] Singh G, Singh V, Sobolewski M, et al. (2018) Sex-Dependent Effects of Developmental Lead Exposure on the Brain. Front Genet 9: 89. https://doi.org/10.3389/fgene.2018.00089
    [11] Lidsky TI, Schneider JS (2003) Lead neurotoxicity in children: basic mechanisms and clinical correlates. Brain 126: 5-19. https://doi.org/10.1093/brain/awg014
    [12] Aliomrani M, Sahraian MA, Shirkhanloo H, et al. (2017) Correlation between heavy metal exposure and GSTM1 polymorphism in Iranian multiple sclerosis patients. Neurol Sci 38: 1271-1278. https://doi.org/10.1007/s10072-017-2934-5
    [13] Tyler CR, Allan AM (2014) The Effects of Arsenic Exposure on Neurological and Cognitive Dysfunction in Human and Rodent Studies: A Review. Curr Environ Health Rep 1: 132-147. https://doi.org/10.1007/s40572-014-0012-1
    [14] Amin-Zaki L, Elhassani S, Majeed MA, et al. (1974) Intra-uterine methylmercury poisoning in Iraq. Pediatrics 54: 587-595. https://doi.org/10.1542/peds.54.5.587
    [15] Fløtre CH, Varsi K, Helm T, et al. Predictors of mercury, lead, cadmium and antimony status in Norwegian never-pregnant women of fertile age (2017)12: e0189169. https://doi.org/10.1371/journal.pone.0189169
    [16] Zheng G, Zhong H, Guo Z, et al. (2014) Levels of heavy metals and trace elements in umbilical cord blood and the risk of adverse pregnancy outcomes: a population-based study. Biol Trace Elem Res 160: 437-444. https://doi.org/10.1007/s12011-014-0057-x
    [17] Okoye EA, Bocca B, Ruggieri F, et al. (2021) Metal pollution of soil, plants, feed and food in the Niger Delta, Nigeria: Health risk assessment through meat and fish consumption. Environ Res 198: 111273. https://doi.org/10.1016/j.envres.2021.111273
    [18] Okoye EA, Bocca B, Ruggieri F, et al. (2022) Arsenic and toxic metals in meat and fish consumed in Niger delta, Nigeria: Employing the margin of exposure approach in human health risk assessment. Food Chem Toxicol 159: 112767. https://doi.org/10.1016/j.fct.2021.112767
    [19] Abbaoui A, Chatoui H, El Hiba O, et al. (2017) Neuroprotective effect of curcumin-I in copper-induced dopaminergic neurotoxicity in rats: A possible link with Parkinson's disease. Neurosci Lett 660: 103-108. https://doi.org/10.1016/j.neulet.2017.09.032
    [20] Albarracin SL, Stab B, Casas Z, et al. (2012) Effects of natural antioxidants in neurodegenerative disease. Nutr Neurosci 15: 1-9. https://doi.org/10.1179/1476830511Y.0000000028
    [21] Moosmann B, Behl C (2000) Dietary phenols: antioxidants for the brain?. Nutr Neurosci 3: 1-10. https://doi.org/10.1080/1028415X.2000.11747298
    [22] Li H-w, Lan T-j, Yun C-x, et al. (2020) Mangiferin exerts neuroprotective activity against lead-induced toxicity and oxidative stress via Nrf2 pathway. Chin Herb Med 12: 36-46. https://doi.org/10.1016/j.chmed.2019.12.002
    [23] Falade KO, Akeem SA (2020) Physicochemical properties, protein digestibility and thermal stability of processed African mesquite bean (Prosopis africana) flours and protein isolates. J Food Meas Charact 14: 1481-1496. https://doi.org/10.1007/s11694-020-00398-0
    [24] Aremu M, Awala E, Opaluwa O, et al. (2015) Effect of processing on nutritional composition of African locust bean (Parkia biglobosa) and mesquite bean (Prosopis africana) seeds. Commun Appl Sci 3.
    [25] Aremu M, Olonisakin A, Atolaye B, et al. (2007) Some nutritional composition and functional properties of Prosopis africana. Bangladesh J Sci Ind Res 42: 269-280. https://doi.org/10.3329/bjsir.v42i3.665
    [26] Keay R (1989) Trees of Nigeria. Clarendon. Oxford: Oxford University) Press.
    [27] Ozoani H, Ezejiofor AN, Okolo KO, et al. (2024) Ameliorative Effects of Zn and Se Supplementation on Heavy Metal Mixture Burden via Increased Renal Metal Excretion and Restoration of Redoxo-Inflammatory Alterations. Biol Trace Elem Res 202: 643-658. https://doi.org/10.1007/s12011-023-03709-w
    [28] Murakami A (2022) Novel mechanisms underlying bioactivities of polyphenols via hormesis. Curr Opinion Toxicol 30: 100337. https://doi.org/10.1016/j.cotox.2022.02.010
    [29] Murakami A (2024) Impact of hormesis to deepen our understanding of the mechanisms underlying the bioactivities of polyphenols. Curr Opinion Biotechnol 86: 103074. https://doi.org/10.1016/j.copbio.2024.103074
    [30] Hannan MA, Dash R, Sohag AAM, et al. (2020) Neuroprotection Against Oxidative Stress: Phytochemicals Targeting TrkB Signaling and the Nrf2-ARE Antioxidant System. Front Mol Neurosci 13: 116. https://doi.org/10.3389/fnmol.2020.00116
    [31] Ezike AC, Akah PA, Okoli CO, et al. (2010) Medicinal Plants Used in Wound Care: A Study of Prosopis africana (Fabaceae) Stem Bark. Indian J Pharm Sci 72: 334-339. https://doi.org/10.4103/0250-474X.70479
    [32] Anyanwu BO, Orish CN, Ezejiofor AN, et al. (2020) Neuroprotective effect of Costus afer on low dose heavy metal mixture (lead, cadmium and mercury) induced neurotoxicity via antioxidant, anti-inflammatory activities. Toxicol Rep 7: 1032-1038. https://doi.org/10.1016/j.toxrep.2020.08.008
    [33] Messarah M, Klibet F, Boumendjel A, et al. (2012) Hepatoprotective role and antioxidant capacity of selenium on arsenic-induced liver injury in rats. Exp Toxicol Pathol 64: 167-174. https://doi.org/10.1016/j.etp.2010.08.002
    [34] Tarantino LM, Gould TJ, Druhan JP, et al. (2000) Behavior and mutagenesis screens: the importance of baseline analysis of inbred strains. Mamm Genome 11: 555-564. https://doi.org/10.1007/s003350010107
    [35] Popović N, Madrid JA, Rol MÁ, et al. (2010) Barnes maze performance of Octodon degus is gender dependent. Behav Brain Res 212: 159-167. https://doi.org/10.1016/j.bbr.2010.04.005
    [36] Popović N, Baño-Otalora B, Rol MÁ, et al. (2023) Effects of long-term individual housing of middle-aged female Octodon degus on spatial learning and memory in the Barnes maze task. Front Behav Neurosci 17: 1221090. https://doi.org/10.3389/fnbeh.2023.1221090
    [37] van den Berg R, Laman JD, van Meurs M, et al. (2016) Rotarod motor performance and advanced spinal cord lesion image analysis refine assessment of neurodegeneration in experimental autoimmune encephalomyelitis. J Neurosci Meth 262: 66-76. https://doi.org/10.1016/j.jneumeth.2016.01.013
    [38] Pritchett K, Mulder GB (2003) The rotarod. J Am Assoc Lab Anim 42: 49-49.
    [39] Eddie-Amadi BF, Ezejiofor AN, Orish CN, et al. (2023) Zn and Se abrogate heavy metal mixture induced ovarian and thyroid oxido-inflammatory effects mediated by activation of NRF2-HMOX-1 in female albino rats. Curr Res Toxicol 4: 100098. https://doi.org/10.1016/j.crtox.2022.100098
    [40] Eddie-Amadi BF, Ezejiofor AN, Orish CN, et al. (2022) Zinc and selenium mitigated heavy metals mixture (Pb, Al, Hg and Mn) mediated hepatic-nephropathy via modulation of oxido-inflammatory status and NF‑kB signaling in female albino rats. Toxicology 481: 153350. https://doi.org/10.1016/j.tox.2022.153350
    [41] Paglia DE, Valentine WN (1967) Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J Lab Clin Med 70: 158-169.
    [42] Jollow D, Mitchell J, Zampaglione Na, et al. (1974) Bromobenzene-induced liver necrosis. Protective role of glutathione and evidence for 3, 4-bromobenzene oxide as the hepatotoxic metabolite. Pharmacology 11: 151-169. https://doi.org/10.1159/000136485
    [43] Wh H (1974) Glutathione S-transferase. J Biol Chem 249: 7130-7139. https://doi.org/10.1016/S0021-9258(19)42083-8
    [44] Marklund S, Marklund G (1974) Involvement of the superoxide anion radical in the autoxidation of pyrogallol and a convenient assay for superoxide dismutase. Eur J Biochem 47: 469-474. https://doi.org/10.1111/j.1432-1033.1974.tb03714.x
    [45] Bergmeyer HU, Bernt E (1974) UV-assay with pyruvate and NADH. Methods of enzymatic analysis.Elsevier pp. 574-579. https://doi.org/10.1016/B978-0-12-091302-2.50010-4
    [46] Esterbauer H, Cheeseman KH (1990) [42] Determination of aldehydic lipid peroxidation products: malonaldehyde and 4-hydroxynonenal. Methods in enzymology.Elsevier pp. 407-421. https://doi.org/10.1016/0076-6879(90)86134-H
    [47] Sosroseno W, Sugiatno E, Samsudin AR, et al. (2008) The role of nitric oxide on the proliferation of a human osteoblast cell line stimulated with hydroxyapatite. Jb Oral Implantol 34: 196-202. https://doi.org/10.1563/0.910.1
    [48] Ikpeama EU, Orish CN, Ezejiofor AN, et al. (2023) Essential Trace Elements Prevent the Impairment in the Retention Memory, Cerebral Cortex, and Cerebellum Damage in Male Rats Exposed to Quaternary Metal Mixture by Up-regulation, of Heme Oxygynase-1 and Down-regulation of Nuclear Factor Erythroid 2-related Factor 2-NOs Signaling Pathways. Neuroscience 512: 70-84. https://doi.org/10.1016/j.neuroscience.2023.01.002
    [49] Okoye EA, Ezejiofor AN, Nwaogazie IL, et al. (2022) Heavy metals and arsenic in soil and vegetation of Niger Delta, Nigeria: Ecological risk assessment. Case Studies in Chemical and Environmental Engineering 6: 100222. https://doi.org/10.1016/j.cscee.2022.100222
    [50] Doungue HT, Kengne APN, Kuate D (2018) Neuroprotective effect and antioxidant activity of Passiflora edulis fruit flavonoid fraction, aqueous extract, and juice in aluminum chloride-induced Alzheimer's disease rats. Nutrire 43: 1-12. https://doi.org/10.1186/s41110-018-0082-1
    [51] Trott O, Olson AJ (2010) AutoDock Vina: improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading. J Comput Chem 31: 455-461. https://doi.org/10.1002/jcc.21334
    [52] Ahmed MQ, Alenazi FS, Fazaludeen MF, et al. (2018) Pathology and Management of Alzheimer's disease: A review. Int J Pharm Res Alli 7.
    [53] Colizzi C (2019) The protective effects of polyphenols on Alzheimer's disease: a systematic review. Alzh Dement-TRCI 5: 184-196. https://doi.org/10.1016/j.trci.2018.09.002
    [54] Qu Z, Zhang J, Yang H, et al. (2016) Protective effect of tetrahydropalmatine against d-galactose induced memory impairment in rat. Physiol Behav 154: 114-125. https://doi.org/10.1016/j.physbeh.2015.11.016
    [55] Mattson MP (2004) Pathways towards and away from Alzheimer's disease. Nature 430: 631-639. https://doi.org/10.1038/nature02621
    [56] Afzal S, Abdul Manap AS, Attiq A, et al. (2023) From imbalance to impairment: the central role of reactive oxygen species in oxidative stress-induced disorders and therapeutic exploration. Front Pharmacol 14: 1269581. https://doi.org/10.3389/fphar.2023.1269581
    [57] Hu B, Ouyang Y, Zhao T, et al. (2024) Antioxidant Hydrogels: Antioxidant Mechanisms, Design Strategies, and Applications in the Treatment of Oxidative Stress-Related Diseases. Adv Healthc Mater 2303817. https://doi.org/10.1002/adhm.202303817
    [58] Oluwafemi R, Agubosi O, Alagbe J (2021) Proximate, minerals, vitamins and amino acid composition of Prosopis africana (African mesquite) seed oil. Asian J Adv Res 4: 1011-1017.
    [59] Alagbe JO, Agubosi OC, Oluwafemi RA (2023) Histopathology of broiler chickens fed diets supplemented with Prosopis africana (African mesquite) essential oil. Brazilian J Sci 2: 49-59. https://doi.org/10.14295/bjs.v2i9.385
    [60] Hu H-C, Lei Y-H, Zhang W-H, et al. (2022) Antioxidant and Anti-inflammatory Properties of Resveratrol in Diabetic Nephropathy: A Systematic Review and Meta-analysis of Animal Studies. Front Pharmacol 13. https://doi.org/10.3389/fphar.2022.841818
    [61] Musial C, Kuban-Jankowska A, Gorska-Ponikowska M (2020) Beneficial Properties of Green Tea Catechins. Int J Mol Sci 21. https://doi.org/10.3390/ijms21051744
    [62] Tvrda E, Straka P, Galbavy D, et al. (2019) Epicatechin Provides Antioxidant Protection to Bovine Spermatozoa Subjected to Induced Oxidative Stress. Molecules 24. https://doi.org/10.3390/molecules24183226
    [63] Qu Z, Liu A, Li P, et al. (2021) Advances in physiological functions and mechanisms of (−)-epicatechin. Crit Rev Food Sci 61: 211-233. https://doi.org/10.1080/10408398.2020.1723057
    [64] Auti ST, Kulkarni YA (2019) Neuroprotective Effect of Cardamom Oil Against Aluminum Induced Neurotoxicity in Rats. Front Neurol 10: 399. https://doi.org/10.3389/fneur.2019.00399
    [65] El-Hawary SS, Sobeh M, Badr WK, et al. (2020) HPLC-PDA-MS/MS profiling of secondary metabolites from Opuntia ficus-indica cladode, peel and fruit pulp extracts and their antioxidant, neuroprotective effect in rats with aluminum chloride induced neurotoxicity. Saudi J Biol Sci 27: 2829-2838. https://doi.org/10.1016/j.sjbs.2020.07.003
    [66] Elsawi SA, Aly HF, Elbatanony MM, et al. (2018) Phytochemical evaluation of Lagerstroemia indica (L.) Pers leaves as anti-Alzheimer's. J Mater Environ Sci 9: 2575-2586.
    [67] Olennikov DN, Kashchenko NI, Chirikova NK, et al. (2017) Isorhamnetin and quercetin derivatives as anti-acetylcholinesterase principles of marigold (Calendula officinalis) flowers and preparations. Int J Mol Sci 18: 1685. https://doi.org/10.3390/ijms18081685
    [68] Anwar HM, Georgy GS, Hamad SR, et al. (2021) A leaf extract of harrisonia abyssinica ameliorates neurobehavioral, histological and biochemical changes in the hippocampus of rats with aluminum chloride-induced alzheimer's disease. Antioxidants 10: 947. https://doi.org/10.3390/antiox10060947
    [69] Taïr K, Kharoubi O, Taïr OA, et al. (2016) Aluminium-induced acute neurotoxicity in rats: Treatment with aqueous extract of Arthrophytum (Hammada scoparia). J Acute Dis 5: 470-482. https://doi.org/10.1016/j.joad.2016.08.028
    [70] El-Hawary S, Abd El-Kader E, Rabeh M, et al. (2020) Eliciting callus culture for production of hepatoprotective flavonoids and phenolics from Sequoia sempervirens (D. Don Endl). Nat Prod Res 34: 3125-3129. https://doi.org/10.1080/14786419.2019.1607334
    [71] Amri Z, Ghorbel A, Turki M, et al. (2017) Effect of pomegranate extracts on brain antioxidant markers and cholinesterase activity in high fat-high fructose diet induced obesity in rat model. BMC Complement Altern Med 17: 339. https://doi.org/10.1186/s12906-017-1842-9
    [72] Kujawska M, Jourdes M (2020) Neuroprotective Effects of Pomegranate Juice against Parkinson's Disease and Presence of Ellagitannins-Derived Metabolite-Urolithin A-In the Brain. Int J Mol Sci 21: 202. https://doi.org/10.3390/ijms21010202
    [73] Zhang H, Wei M, Lu X, et al. (2020) Aluminum trichloride caused hippocampal neural cells death and subsequent depression-like behavior in rats via the activation of IL-1β/JNK signaling pathway. Sci Total Environ 715: 136942. https://doi.org/10.1016/j.scitotenv.2020.136942
    [74] Yaseen AA, Al-Okbi SY, Hussein AM, et al. (2019) Potential protection from Alzheimer's disease by wheat germ and rice bran nano-form in rat model. J Appl Pharm Sci 9: 067-076. https://doi.org/10.7324/JAPS.2019.S108
    [75] Lu T-H, Tseng T-J, Su C-C, et al. (2014) Arsenic induces reactive oxygen species-caused neuronal cell apoptosis through JNK/ERK-mediated mitochondria-dependent and GRP 78/CHOP-regulated pathways. Toxicol Lett 224: 130-140. https://doi.org/10.1016/j.toxlet.2013.10.013
    [76] Chakraborti D, Singh SK, Rahman MM, et al. (2018) Groundwater arsenic contamination in the Ganga River Basin: a future health danger. Int J Env Res Pub He 15: 180. https://doi.org/10.3390/ijerph15020180
    [77] Firdaus F, Zafeer MF, Anis E, et al. (2018) Ellagic acid attenuates arsenic induced neuro-inflammation and mitochondrial dysfunction associated apoptosis. Toxicol Rep 5: 411-417. https://doi.org/10.1016/j.toxrep.2018.02.017
    [78] Jahan-Abad AJ, Morteza-Zadeh P, Negah SS, et al. (2017) Curcumin attenuates harmful effects of arsenic on neural stem/progenitor cells. Avicenna J Phytomedi 7: 376.
    [79] Essa AF, Teleb M, El-Kersh DM, et al. (2023) Natural acylated flavonoids: Their chemistry and biological merits in context to molecular docking studies. Phytochem Rev 22: 1469-1508. https://doi.org/10.1007/s11101-022-09840-1
    [80] Naoi M, Inaba-Hasegawa K, Shamoto-Nagai M, et al. (2017) Neurotrophic function of phytochemicals for neuroprotection in aging and neurodegenerative disorders: modulation of intracellular signaling and gene expression. J Neural Transm 124: 1515-1527. https://doi.org/10.1007/s00702-017-1797-5
    [81] Hannan MA, Sohag AAM, Dash R, et al. (2020) Phytosterols of marine algae: Insights into the potential health benefits and molecular pharmacology. Phytomedicine 69: 153201. https://doi.org/10.1016/j.phymed.2020.153201
    [82] Gao Y, Xu X, Chang S, et al. (2015) Totarol prevents neuronal injury in vitro and ameliorates brain ischemic stroke: Potential roles of Akt activation and HO-1 induction. Toxicol Appl Pharmacol 289: 142-154. https://doi.org/10.1016/j.taap.2015.10.001
    [83] Fang J, Wang H, Zhou J, et al. (2018) Baicalin provides neuroprotection in traumatic brain injury mice model through Akt/Nrf2 pathway. Drug Des Devel Ther 12: 2497-2508. https://doi.org/10.2147/DDDT.S163951
    [84] Cui HY, Zhang XJ, Yang Y, et al. (2018) Rosmarinic acid elicits neuroprotection in ischemic stroke via Nrf2 and heme oxygenase 1 signaling. Neural Regen Res 13: 2119-2128. https://doi.org/10.4103/1673-5374.241463
    [85] Hui Y, Chengyong T, Cheng L, et al. (2018) Resveratrol Attenuates the Cytotoxicity Induced by Amyloid-β(1-42) in PC12 Cells by Upregulating Heme Oxygenase-1 via the PI3K/Akt/Nrf2 Pathway. Neurochem Res 43: 297-305. https://doi.org/10.1007/s11064-017-2421-7
    [86] Dinkova-Kostova AT, Kostov RV, Kazantsev AG (2018) The role of Nrf2 signaling in counteracting neurodegenerative diseases. Febs J 285: 3576-3590. https://doi.org/10.1111/febs.14379
    [87] Joshi G, Johnson JA (2012) The Nrf2-ARE pathway: a valuable therapeutic target for the treatment of neurodegenerative diseases. Recent Pat CNS Drug Discov 7: 218-229. https://doi.org/10.2174/157488912803252023
    [88] Cuadrado A, Rojo AI (2008) Heme oxygenase-1 as a therapeutic target in neurodegenerative diseases and brain infections. Curr Pharm Des 14: 429-442. https://doi.org/10.2174/138161208783597407
    [89] Schipper HM (2004) Heme oxygenase expression in human central nervous system disorders. Free Radical Bio Med 37: 1995-2011. https://doi.org/10.1016/j.freeradbiomed.2004.09.015
  • Reader Comments
  • © 2024 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

Metrics

Article views(326) PDF downloads(46) Cited by(0)

Article outline

Figures and Tables

Figures(3)  /  Tables(11)

/

DownLoad:  Full-Size Img  PowerPoint
Return
Return

Catalog