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Role of Nitric Oxide and Hydrogen Sulfide in Neuronal and Glial Cell Death in Neurodegenerative Processes

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Biochemistry (Moscow), Supplement Series A: Membrane and Cell Biology Aims and scope

Abstract

Neurodegeneration is a complex progressive pathological process leading to the neuronal death, which is induced by various external and internal factors. Neurodegenerative diseases, injuries of the central and peripheral nervous system, mental disorders, and a number of other pathological conditions, accompanied by functional and structural degradation of neurons and their death, is a serious problem in the global healthcare system, as due to these diseases millions of people around the world become disabled or die every year. The situation is complicated by the lack of selective, clinically effective neuroprotective drugs. It has been shown that nitric oxide (NO) and hydrogen sulfide (H2S) are actively involved in neurodegeneration and cell death of neurons and glia, but their role is not completely clear. This review considers NO- and H2S-dependent signaling mechanisms underlying the pathogenesis of neurodegenerative processes. The prospects for further studies of the role of NO and H2S in the nervous tissue under conditions of pathological conditions associated with neurodegeneration are considered.

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REFERENCES

  1. Przedborski S., Vila M., Jackson-Lewis V. 2003. Series introduction neurodegeneration what is it and where are we? J. Clin. Invest. 111, 3–10.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  2. Pérez-Neri I., Ramírez-Bermúdez J., Montes S., Ríos C. 2006. Possible mechanisms of neurodegeneration in schizophrenia. Neurochem. Res. 31, 1279–1294.

    Article  PubMed  Google Scholar 

  3. Dzreyan V., Rodkin S., Nikul V., Pitinova M., Uzdensky A. 2021. The expression of E2F1, p53, and caspase 3 in the rat dorsal root ganglia after sciatic nerve transection. J. Mol. Neurosci. 71, 826–835.

    Article  PubMed  CAS  Google Scholar 

  4. Dreßler J., Hanisch U., Kuhlisch E., Geiger K. 2007. Neuronal and glial apoptosis in human traumatic brain injury. Int. J. Legal Med. 121, 365–375.

    Article  PubMed  Google Scholar 

  5. Rodkin S.V., Dzreyan V.A., Demyanenko S.V., Uzdensky V.B. 2021. The role of p53-dependent signaling pathways in survival and death of neurons and glial cells in peripheral nerve injury. Biochemistry (Moscow), Suppl. Series A: Membr. Cell Biol. 15, 334–347.

    CAS  Google Scholar 

  6. Flores G., Morales-Medina J., Diaz A. 2016. Neuronal and brain morphological changes in animal models of schizophrenia. Behav. Brain Res. 301, 190–203.

    Article  PubMed  CAS  Google Scholar 

  7. Nakamura T., Lipton S. 2017. ‘SNO’-storms compromise protein activity and mitochondrial metabolism in neurodegenerative disorders. Trends Endocrinol. Metab. 28, 879–892.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  8. Muchowski P., Wacker J. 2005. Modulation of neurodegeneration by molecular chaperones. Nat. Rev. Neurosci. 6, 11–22.

    Article  PubMed  CAS  Google Scholar 

  9. Giovinazzo D., Bursac B., Sbodio J., Nalluru S., Vignane T., Snowman A., Albacarys L., Sedlak T., Torregrossa R., Whiteman M., Filipovic M., Snyder S., Paul D. 2021. Hydrogen sulfide is neuroprotective in Alzheimer’s disease by sulfhydrating GSK3β and inhibiting Tau hyperphosphorylation. Proc. Natl. Acad. Sci. USA. 118, e2017225118.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  10. Stewart V., Heales S. 2003. Nitric oxide-induced mitochondrial dysfunction implications for neurodegeneration. Free Radic. Biol. Med. 34, 287–303.

    Article  PubMed  CAS  Google Scholar 

  11. Chen K., Northington F., Martin L. 2010. Inducible nitric oxide synthase is present in motor neuron mitochondria and Schwann cells and contributes to disease mechanisms in ALS mice. Brain Struct. Funct. 214, 219–234.

    Article  PubMed  CAS  Google Scholar 

  12. Jung J., Jeong N. 2014. Hydrogen sulfide controls peripheral nerve degeneration and regeneration a novel therapeutic strategy for peripheral demyelinating disorders or nerve degenerative diseases. Neural. Regen. Res. 9, 2119.

    Article  PubMed  PubMed Central  Google Scholar 

  13. Caviedes A., Varas-Godoy M., Lafourcade C., Sandoval S., Bravo-Alegria J., Kaehne T., Massmann A., Figueroa J., Nualart F., Wyneken U. 2017. Endothelial nitric oxide synthase is present in dendritic spines of neurons in primary cultures. Front. Cell. Neurosci. 11, 180.

    Article  PubMed  PubMed Central  Google Scholar 

  14. Lin Y., Liang H., Xu K., Ni H., Dong J., Xiao H., Chang L., Wu H., Li F., Zhu D., Luo C. 2018. Dissociation of nNOS from PSD-95 promotes functional recovery after cerebral ischaemia in mice through reducing excessive tonic GABA release from reactive astrocytes. J. Pathol. 244, 176–188.

    Article  PubMed  CAS  Google Scholar 

  15. Hou X., Hu Z., Zhang D., Lu W., Zhou J., Wu P., Guan X., Han Q., Deng S., Zhang H., Chen J., Wang F. 2017. Rapid antidepressant effect of hydrogen sulfide evidence for activation of mTORC1-TrkB-AMPA receptor pathways. Antioxid. Redox Signal. 27, 472–488.

    Article  PubMed  CAS  Google Scholar 

  16. Wang Y., Hong F., Yang S. 2022. Roles of nitric oxide in brain ischemia and reperfusion. Int. J. Mol. Sci. 23, 4243.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  17. Ghanbari F., Khaksari M., Vaezi G., Hojati V., Shiravi A. 2019. Hydrogen sulfide protects hippocampal neurons against methamphetamine neurotoxicity via inhibition of apoptosis and neuroinflammation. J. Mol. Neurosci. 67, 133–141.

    Article  PubMed  CAS  Google Scholar 

  18. Park K., Lee Y., Park S., Lee S., Hong Y., Kil S., Hong Y. 2010. Synergistic effect of melatonin on exercise-induced neuronal reconstruction and functional recovery in a spinal cord injury animal model. J. Pineal Res. 48, 270–281.

    Article  PubMed  CAS  Google Scholar 

  19. Zhang J., Zhang S., Shan H., Zhang M. 2020. Biologic effect of hydrogen sulfide and its role in traumatic brain injury. Oxid. Med. Cell. Longev. 2020, 7301615.

    Article  PubMed  PubMed Central  Google Scholar 

  20. Qu W., Cheng Y., Peng W., Wu Y., Rui T., Luo C., Zhang J. 2022. Targeting iNOS alleviates early brain injury after experimental subarachnoid hemorrhage via promoting ferroptosis of M1 microglia and reducing neuroinflammation. Mol. Neurobiol. 59, 3124–3139.

    Article  PubMed  CAS  Google Scholar 

  21. Jin R., Yang R., Cui C., Zhang H., Cai J., Geng B., Chen Z. 2022. Ferroptosis due to cystathionine γ lyase/hydrogen sulfide downregulation under high hydrostatic pressure exacerbates VSMC dysfunction. Front. Cell Dev. Biol. 10, 829316.

    Article  PubMed  PubMed Central  Google Scholar 

  22. Xu X., Shi R., Fu Y., Wang J., Tong X., Zhang S., Wang N., Li M., Tong Y., Wang W., He M., Liu B., Chen G., Guo F. 2023. Neuronal nitric oxide synthase/reactive oxygen species pathway is involved in apoptosis and pyroptosis in epilepsy. Neural Regen. Res. 18, 1277.

    Article  PubMed  Google Scholar 

  23. Yang K., Li W., Liu Y., Wei Y., Ren Y., Mai C., Zhang S., Zuo Y., Sun Z., Li D., Yang C. 2022. Hydrogen sulfide attenuates neuroinflammation by inhibiting the NLRP3/Caspase-1/GSDMD pathway in retina or brain neuron following rat ischemia/reperfusion. Brain Sci. 12, 1245.

    Article  PubMed  PubMed Central  Google Scholar 

  24. Chen Y., Chen Y., Chiu H., Ko Y., Wang R., Wang W., Chuang Y., Huang C., Lu T. 2021. Cell-penetrating delivery of nitric oxide by biocompatible dinitrosyl iron complex and its dermato-physiological implications. Int. J. Mol. Sci. 22, 10101.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  25. Goshi E., Zhou G., He Q. 2019. Nitric oxide detection methods in vitro and in vivo. Med. Gas Res. 9, 192–207.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  26. Hall C., Garthwaite J. 2009. What is the real physiological NO concentration in vivo? Nitric Oxide. 21, 92–103.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  27. Forstermann U., Sessa W. 2012. Nitric oxide synthases regulation and function. Eur. Heart J. 33, 829–837.

    Article  PubMed  Google Scholar 

  28. Lvova O.A., Orlova A.E., Gusev V.V., Kovtun O.P., Chegodaev D.A. 2010. To the question of the role of nitric oxide in norm and pathology of the nervous system. System Integral Healthcare. 4, 20–35.

    Google Scholar 

  29. Kone B. 2001. Molecular biology of natriuretic peptides and nitric oxide synthases. Cardiovasc. Res. 51, 429–441.

    Article  PubMed  CAS  Google Scholar 

  30. Gusakova S.V., Kovalev I.V., Smaglii L.V., Birulina Y.G., Nosarev A.V., Petrova I.V., Medvedev M.A., Orlov S.N., Reutov V.P. 2015. Gas signaling in mammalian cells. Uspekhi fiziol. nauk. (Rus.). 46, 53–73.

  31. Keszler A., Lindemer B., Hogg N., Weihrauch D., Lohr N. 2018. Wavelength-dependence of vasodilation and NO release from S-nitrosothiols and dinitrosyl iron complexes by far red/near infrared light. Arch. Biochem. Biophys. 649, 47–52.

    Article  PubMed  CAS  Google Scholar 

  32. Vincent S. 2010. Nitric oxide neurons and neurotransmission. Prog. Neurobiol. 90, 246–255.

    Article  PubMed  CAS  Google Scholar 

  33. Yang G., Chen G., Ebner T., Iadecola C. 1999. Nitric oxide is the predominant mediator of cerebellar hyperemia during somatosensory activation in rats. Am. J. Physiol. Integr. Comp. Physiol. 277, R1760–R1770.

    Article  CAS  Google Scholar 

  34. Kodama T., Koyama Y. 2006. Nitric oxide from the laterodorsal tegmental neurons its possible retrograde modulation on norepinephrine release from the axon terminal of the locus coeruleus neurons. Neuroscience. 138, 245–256.

    Article  PubMed  CAS  Google Scholar 

  35. Vincent S. 2000. The ascending reticular activating system – from aminergic neurons to nitric oxide. J. Chem. Neuroanat. 18, 23–30.

    Article  PubMed  CAS  Google Scholar 

  36. Lin D., Fretier P., Jiang C., Vincent S. 2010. Nitric oxide signaling via cGMP-stimulated phosphodiesterase in striatal neurons. Synapse. 64, 460–466.

    Article  PubMed  CAS  Google Scholar 

  37. Yakovleva O.V., Shafigullin M.U., Sitdikova G.F. 2013. The role of nitric oxide in the regulation of mediator secretion and processes of exo- and endocytosis of synaptic vesicles in mouse motor nerve endings. Neurochem J. 7, 103–110.

    Article  CAS  Google Scholar 

  38. Garthwaite J. 2019. NO as a multimodal transmitter in the brain discovery and current status. Br. J. Pharmacol. 176, 197–211.

    Article  PubMed  CAS  Google Scholar 

  39. Gallo E., Iadecola C. 2011. Neuronal nitric oxide contributes to neuroplasticity-associated protein expression through cGMP protein kinase g and extracellular signal-regulated kinase. J. Neurosci. 31, 6947–6955.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  40. Bradley S., Steinert J. 2016. Nitric oxide-mediated posttranslational modifications impacts at the synapse. Oxid. Med. Cell. Longev. 2016, 5681036.

    Article  PubMed  Google Scholar 

  41. Selvakumar B., Jenkins M., Hussain N., Huganir R., Traynelis S., Snyder S. 2013. S-nitrosylation of AMPA receptor GluA1 regulates phosphorylation single-channel conductance and endocytosis. Proc. Natl. Acad. Sci. USA. 110,1077–1082.

    Article  PubMed  CAS  Google Scholar 

  42. Schafe G., Bauer E., Rosis S., Farb C., Rodrigues S., LeDoux J. 2005. Memory consolidation of Pavlovian fear conditioning requires nitric oxide signaling in the lateral amygdala. Eur. J. Neurosci. 22, 201–211.

    Article  PubMed  Google Scholar 

  43. Sudorgina P.V., Saulskaya N.B. 2015. Sound danger signals activate the nitrergic system of the medial prefrontal cortex. Neurosci. Behav. Physiol. 46, 1017–1023.

    Article  Google Scholar 

  44. Balaban P.M., Roshchin M.V., Korshunova T.A. 2011. Two-faced nitric oxide is necessary for both memory erasure and memory formation. Neurosci. Behav. Physiol. 42, 895–900.

    Article  Google Scholar 

  45. Ill-Raga G., Tajes M., Busquets-García A., Ramos-Fernández E., Vargas L., Bosch-Morató M., Guivernau B., Valls-Comamala V., Eraso-Pichot A., Guix F., Fandos C., Rosen M., Rabinowitz M., Maldonado R., Alvarez A., Ozaita A., Muñoz F. 2015. Physiological control of nitric oxide in neuronal BACE1 translation by heme-regulated eIF2α kinase HRI induces synaptogenesis. Antioxid. Redox Signal. 22, 1295–1307.

    Article  PubMed  CAS  Google Scholar 

  46. Ill-Raga G., Köhler C., Radiske A., Lima R., Rosen M., Muñoz F., Cammarota M. 2013. Consolidation of object recognition memory requires HRI kinase-dependent phosphorylation of eIF2α in the hippocampus. Hippocampus. 23, 431–436.

    Article  PubMed  CAS  Google Scholar 

  47. Bel E., Del Guimarães F., Bermũdez-Echeverry M., Gomes M., Schiaveto-de-Souza A., Padovan-Neto F., Tumas V., Barion-Cavalcanti A., Lazzarini M., Nucci-da-Silva L., de Paula-Souza D. 2005. Role of nitric oxide on motor behavior. Cell. Mol. Neurobiol. 25, 371–392.

    Article  PubMed  Google Scholar 

  48. Contestabile A. 2012. Role of nitric oxide in cerebellar development and function focus on granule neurons. Cerebellum. 11, 50–61.

    Article  PubMed  CAS  Google Scholar 

  49. Xiao Q., Ying J., Xiang L., Zhang C. 2018. The biologic effect of hydrogen sulfide and its function in various diseases. Medicine (Baltimore). 97, e13065.

    Article  PubMed  Google Scholar 

  50. Kolesnikov S., Vlasov B., Kolesnikova L. 2015. Hydrogen as a third essential gas molecule in living tissues. Ann. Russ. Acad. Med. Sci. 70, 237–241.

    Article  Google Scholar 

  51. Lu D., Wang L., Liu G., Wang S., Wang Y., Wu Y., Wang J., Sun X. 2022. Role of hydrogen sulfide in subarachnoid hemorrhage. CNS Neurosci. Ther. 28, 805–817.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  52. Kimura H., Shibuya N., Kimura Y. 2012. Hydrogen sulfide is a signaling molecule and a cytoprotectant. Antioxid. Redox Signal. 17, 45–57.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  53. Furne J., Saeed A., Levitt M.D. 2008. Whole tissue hydrogen sulfide concentrations are orders of magnitude lower than presently accepted values. Am. J. Physiol. Regul. Integr. Comp. Physiol. 295, R1479–R1485.

    Article  PubMed  CAS  Google Scholar 

  54. Rodkin S., Nwosu C., Sannikov A., Tyurin A., Chulkov V., Raevskaya M., Ermakov A., Kirichenko E., Gasanov M. 2023. The role of gasotransmitter-dependent signaling mechanisms in apoptotic cell death in cardiovascular rheumatic kidney and neurodegenerative diseases and mental disorders. Int. J. Mol. Sci. 24, 6014.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  55. Sen N. 2017. Functional and molecular insights of hydrogen sulfide signaling and protein sulfhydration. J. Mol. Biol. 429, 543–561.

    Article  PubMed  CAS  Google Scholar 

  56. Zhu H., Blake S., Chan K., Pearson R., Kang J. 2018. Cystathionine β -synthase in physiology and cancer. Biomed. Res. Int. 11, 3205125.

    Google Scholar 

  57. Zuhra K., Augsburger F., Majtan T., Szabo C. 2020. Cystathionine-β-synthase molecular regulation and pharmacological inhibition. Biomolecules. 10, 697.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  58. Jurkowska H., Kaczor-Kamińska M., Bronowicka-Adamska P., Wróbel M. 2014. Cystathionine γ-lyase. Postepy Hig. Med. Dosw. 68, 1–9.

    Article  Google Scholar 

  59. Sharif A., Iqbal M., Manhoosh B., Gholampoor N., Ma D., Marwah M., Sanchez-Aranguren L. 2023. Hydrogen sulphide-based therapeutics for neurological conditions perspectives and challenges. Neurochem. Res. 48, 1981–1996

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  60. Lupoli R., Di Minno A., Spadarella G., Franchini M., Sorrentino R., Cirino G., Di Minno G. 2015. Methylation reactions the redox balance and atherothrombosis the search for a link with hydrogen sulfide. Semin. Thromb. Hemost. 41, 423–432.

    Article  PubMed  CAS  Google Scholar 

  61. Yakovlev A., Kurmasheva E., Ishchenko Y., Giniatullin R., Sitdikova G. 2017. Age-dependent subunit specific action of hydrogen sulfide on GluN1/2A and GluN1/2B NMDA receptors. Front. Cell. Neurosci. 11, 375.

    Article  PubMed  PubMed Central  Google Scholar 

  62. Munaron L., Avanzato D., Moccia F., Mancardi D. 2013. Hydrogen sulfide as a regulator of calcium channels. Cell Calcium. 53, 77–84.

    Article  PubMed  CAS  Google Scholar 

  63. Liu D., Wang Z., Zhan J., Zhang Q., Wang J., Zhang Q., Xian X., Luan Q., Hao A. 2014. Hydrogen sulfide promotes proliferation and neuronal differentiation of neural stem cells and protects hypoxia-induced decrease in hippocampal neurogenesis. Pharmacol. Biochem. Behav. 116, 55–63.

    Article  PubMed  CAS  Google Scholar 

  64. Kamat P., Kalani A. 2015. Abstract T P87 hydrogen sulfide enhances neurogenesis through the IRAK-1/GSK3β/AKT signaling pathways after ischemic stroke. Stroke. 46, ATP87-ATP87.

    Article  Google Scholar 

  65. Pomierny B., Krzyżanowska W., Jurczyk J., Skórkowska A., Strach B., Szafarz M., Przejczowska-Pomierny K., Torregrossa R., Whiteman M., Marcinkowska M., Pera J., Budziszewska B. 2021.The slow-releasing and mitochondria-targeted hydrogen sulfide (H2S) Delivery molecule AP39 induces brain tolerance to ischemia. Int. J. Mol. Sci. 22, 7816.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  66. Mohseni F., Bagheri F., Rafaiee R., Norozi P., Khaksari M. 2020. Hydrogen sulfide improves spatial memory impairment via increases of BDNF expression and hippocampal neurogenesis following early postnatal alcohol exposure. Physiol. Behav. 215, 112784.

    Article  PubMed  CAS  Google Scholar 

  67. Varaksin A.A., Pushchina E.V. 2012. Significance of hydrogen sulfide in the regulation of organ functions. Tikhookeanskii med. zhurnal. (Rus.). 2, 27–36.

  68. Yakovlev A.V., Sitdikova G.F. 2014. Physiological role of hydrogen sulfide in the nervous system. Genes & Cells. 9, 34–40.

    Google Scholar 

  69. Wang M., Zhu J., Pan Y., Dong J., Zhang L., Zhang X., Zhang L. 2015. Hydrogen sulfide functions as a neuromodulator to regulate striatal neurotransmission in a mouse model of Parkinson’s disease. J. Neurosci. Res. 93, 487–494.

    Article  PubMed  CAS  Google Scholar 

  70. Ali R., Pal H., Hameed R., Nazir A., Verma S. 2019. Controlled release of hydrogen sulfide significantly reduces ROS stress and increases dopamine levels in transgenic C. elegans. Chem. Commun. 55, 10142–10145.

    Article  CAS  Google Scholar 

  71. Sitdikova G.F., Yakovlev A.V., Odnoshivkina Y.G., Zefirov A.L. 2011. Effect of hydrogen sulfide on the processes of exo- and endocytosis of synaptic vesicles in the frog motor nerve ending. Neurochem. J. 28, 280–286.

    Google Scholar 

  72. Gerasimova E., Lebedeva J., Yakovlev A., Zefirov A., Giniatullin R., Sitdikova G. 2015. Mechanisms of hydrogen sulfide (H2S) action on synaptic transmission at the mouse neuromuscular junction. Neuroscience. 303, 577–585.

    Article  PubMed  CAS  Google Scholar 

  73. Wang Y., Jia J., Ao G., Hu L., Liu H., Xiao Y., Du H., Alkayed N., Liu C., Cheng J. 2014. Hydrogen sulfide protects blood-brain barrier integrity following cerebral ischemia. J. Neurochem. 129, 827–838.

    Article  PubMed  CAS  Google Scholar 

  74. Campolo M., Esposito E., Ahmad A., Di Paola R., Paterniti I., Cordaro M., Bruschetta G., Wallace J., Cuzzocrea S. 2014. Hydrogen sulfide-releasing cyclooxygenase inhibitor ATB-346 enhances motor function and reduces cortical lesion volume following traumatic brain injury in mice. J. Neuroinflammation. 11, 196.

    Article  PubMed  PubMed Central  Google Scholar 

  75. Tabassum R., Jeong N. 2019. Potential for therapeutic use of hydrogen sulfide in oxidative stress-induced neurodegenerative diseases. Int. J. Med. Sci. 16, 1386–1396.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  76. Zhang M., Shan H., Wang T., Liu W., Wang Y., Wang L., Zhang L., Chang P., Dong W., Chen X., Tao L. 2013. Dynamic change of hydrogen sulfide after traumatic brain injury and its effect in mice. Neurochem. Res. 38, 714–725.

    Article  PubMed  CAS  Google Scholar 

  77. Ide M., Ohnishi T., Toyoshima M., Balan S., Maekawa M., Shimamoto-Mitsuyama C., Iwayama Y., Ohba H., Watanabe A., Ishii T., Shibuya N., Kimura Y., Hisano Y., Murata Y., Hara T., Morikawa M., Hashimoto K., Nozaki Y., Toyota T., Wada Y., Yoshikawa T. 2019. Excess hydrogen sulfide and polysulfides production underlies a schizophrenia pathophysiology. EMBO Mol. Med. 11, e10695.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  78. Gopalakrishnan P., Shrestha B., Kaskas A., Green J., Alexander J., Pattillo C. 2019. Hydrogen sulfide therapeutic or injurious in ischemic stroke? Pathophysiology. 26, 1–10.

    Article  PubMed  CAS  Google Scholar 

  79. DiSabato D., Quan N., Godbout J. 2016. Neuroinflammation: The devil is in the details. J. Neurochem. 139, 136–153.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  80. Woodburn S., Bollinger J., Wohleb E. 2021. The semantics of microglia activation neuroinflammation homeostasis and stress. J. Neuroinflammation. 18, 258.

    Article  PubMed  PubMed Central  Google Scholar 

  81. Liao R., Wood T., Nance E. 2020. Nanotherapeutic modulation of excitotoxicity and oxidative stress in acute brain injury. Nanobiomedicine. 7, 184954352097081.

    Article  Google Scholar 

  82. Hirsch E., Vyas S., Hunot S. 2012. Neuroinflammation in Parkinson’s disease. Parkinsonism Relat. Disord. 18, S210–S212.

    Article  PubMed  Google Scholar 

  83. Kummer M., Hermes M., Delekarte A., Hammerschmidt T., Kumar S., Terwel D., Walter J., Pape H., König S., Roeber S., Jessen F., Klockgether T., Korte M., Heneka M. 2011. Nitration of tyrosine 10 critically enhances amyloid β aggregation and plaque formation. Neuron. 71, 833–844.

    Article  PubMed  CAS  Google Scholar 

  84. Evonuk K., Doyle R., Moseley C., Thornell I., Adler K., Bingaman A., Bevensee M., Weaver C., Min B., DeSilva T. 2020. Reduction of AMPA receptor activity on mature oligodendrocytes attenuates loss of myelinated axons in autoimmune neuroinflammation. Sci. Adv. 6, eaax5936.

  85. Alawieh A., Langley E., Weber S., Adkins D., Tomlinson S. 2018. Identifying the role of complement in triggering neuroinflammation after traumatic brain injury. J. Neurosci. 38, 2519–2532.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  86. Picca A., Calvani R., Coelho-Junior H., Landi F., Bernabei R., Marzetti E. 2020. Mitochondrial dysfunction oxidative stress and neuroinflammation intertwined roads to neurodegeneration. Antioxidants. 9, 647.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  87. Gao F., Lucke-Wold B., Li X., Logsdon A., Xu L., Xu S., LaPenna K., Wang H., Talukder M., Siedlecki C., Huber J., Rosen C., He P. 2018. Reduction of endothelial nitric oxide increases the adhesiveness of constitutive endothelial membrane ICAM-1 through src-mediated phosphorylation. Front. Physiol. 8, 1124.

    Article  PubMed  PubMed Central  Google Scholar 

  88. Fukumura D., Gohongi T., Kadambi A., Izumi Y., Ang J., Yun C., Buerk D., Huang P., Jain R. 2001. Predominant role of endothelial nitric oxide synthase in vascular endothelial growth factor-induced angiogenesis and vascular permeability. Proc. Natl. Acad. Sci. USA. 98, 2604–2609.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  89. Hollenberg S., Guglielmi M., Parrillo J. 2007. Discordance between microvascular permeability and leukocyte dynamics in septic inducible nitric oxide synthase deficient mice. Crit. Care. 11, R125.

    Article  PubMed  PubMed Central  Google Scholar 

  90. Chen Z., Mou R., Feng D., Wang Z., Chen G. 2017. The role of nitric oxide in stroke. Med. Gas Res. 7, 194.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  91. Oh G., Pae H., Lee B., Kim B., Kim J., Kim H., Jeon S., Jeon W., Chae H., Chung H. 2006. Hydrogen sulfide inhibits nitric oxide production and nuclear factor-κB via heme oxygenase-1 expression in RAW264.7 macrophages stimulated with lipopolysaccharide. Free Radic. Biol. Med. 41, 106–119.

    Article  PubMed  CAS  Google Scholar 

  92. Kondo K., Bhushan S., King A., Prabhu S., Hamid T., Koenig S., Murohara T., Predmore B., Gojon G., Gojon G., Wang R., Karusula N., Nicholson C., Calvert J., Lefer D. 2013. H2S protects against pressure overload–induced heart failure via upregulation of endothelial nitric oxide synthase. Circulation. 127, 1116–1127.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  93. Liy P., Puzi N., Jose S., Vidyadaran S. 2021. Nitric oxide modulation in neuroinflammation and the role of mesenchymal stem cells. Exp. Biol. Med. 246, 2399–2406.

    Article  CAS  Google Scholar 

  94. Pandareesh M., Anand T. 2014. Neuroprotective and anti-apoptotic propensity of bacopa monniera extract against sodium nitroprusside induced activation of inos heat shock proteins and apoptotic markers in PC12 cells. Neurochem. Res. 39, 800–814.

    Article  PubMed  CAS  Google Scholar 

  95. Radi E., Formichi P., Battisti C., Federico A. 2014. Apoptosis and oxidative stress in neurodegenerative diseases. J. Alzheimers Dis. 42, S125–S152.

    Article  PubMed  Google Scholar 

  96. Xie Z., Liu Y., Bian J. 2016. Hydrogen sulfide and cellular redox homeostasis. Oxid. Med. Cell. Longev. 2016, 6043038.

    Article  PubMed  PubMed Central  Google Scholar 

  97. Corsello T., Komaravelli N., Casola A. 2018. Role of hydrogen sulfide in NRF2- and sirtuin-dependent maintenance of cellular redox balance. Antioxidants. 7, 129.

    Article  PubMed  PubMed Central  Google Scholar 

  98. Bruce King S. 2013. Potential biological chemistry of hydrogen sulfide (H2S) with the nitrogen oxides. Free Radic. Biol. Med. 55, 1–7.

    Article  PubMed  CAS  Google Scholar 

  99. Austin S., Santhanam A., Hinton D., Choi D., Katusic Z. 2013. Endothelial nitric oxide deficiency promotes Alzheimer’s disease pathology. J. Neurochem. 127, 691–700.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  100. Lundberg J., Weitzberg E. 2022. Nitric oxide signaling in health and disease. Cell. 185, 2853–2878.

    Article  PubMed  CAS  Google Scholar 

  101. Tieu K., Ischiropoulos H., Przedborski S. 2003. Nitric oxide and reactive oxygen species in parkinson’s disease. IUBMB Life. 55, 329–335.

    Article  PubMed  CAS  Google Scholar 

  102. He X., Yan N., Chen X., Qi Y., Yan Y., Cai Z. 2016. Hydrogen sulfide down-regulates BACE1 and PS1 via activating PI3K/Akt pathway in the brain of APP/PS1 transgenic mouse. Pharmacol. Reports. 68, 975–982.

    Article  CAS  Google Scholar 

  103. Tyagi N., Moshal K., Sen U., Vacek T., Kumar M., Hughes W., Kundu S., Tyagi S. 2009. H2S protects against methionine–induced oxidative stress in brain endothelial cells. Antioxid. Redox Signal. 11, 25–33.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  104. Kesherwani V., Nelson K., Agrawal S. 2013. Effect of sodium hydrosulphide after acute compression injury of spinal cord. Brain Res. 1527, 222–229.

    Article  PubMed  CAS  Google Scholar 

  105. Logsdon A., Schindler A., Meabon J., Yagi M., H-erbert M., Banks W., Raskind M. Marshall D., Keene C., Perl D., Peskind E., Cook D. 2020. Nitric oxide synthase mediates cerebellar dysfunction in mice exposed to repetitive blast-induced mild traumatic brain injury. Sci. Rep. 10, 9420.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  106. Rodkin S., Kovaleva V., Berezhnaya E., Neginskaya M., Uzdensky A. 2019. Ca2+- and NF-κB-dependent generation of NO in the photosensitized neurons and satellite glial cells. J. Photochem. Photobiol. B. 199, 111603.

    Article  PubMed  CAS  Google Scholar 

  107. Dobson C. 2003. Protein folding and misfolding. Nature. 426, 884–890.

    Article  PubMed  CAS  Google Scholar 

  108. Morán Luengo T., Mayer M., Rüdiger S. 2019. The Hsp70–Hsp90 chaperone cascade in protein folding. Trends Cell Biol. 29, 164–177.

    Article  PubMed  Google Scholar 

  109. Naeem A., Fazili N. 2011. Defective protein folding and aggregation as the basis of neurodegenerative diseases the darker aspect of proteins. Cell Biochem. Biophys. 61, 237–250.

    Article  PubMed  CAS  Google Scholar 

  110. Zheng Q., Huang T., Zhang L., Zhou Y., Luo H., Xu H., Wang X. 2016. Dysregulation of ubiquitin-proteasome system in neurodegenerative diseases. Front. Aging Neurosci. 8, 303.

    Article  PubMed  PubMed Central  Google Scholar 

  111. Meng F., Yao D., Shi Y., Kabakoff J., Wu W., Reicher J., Ma Y., Moosmann B., Masliah E., Lipton S., Gu, Z. 2011. Oxidation of the cysteine-rich regions of parkin perturbs its E3 ligase activity and contributes to protein aggregation. Mol. Neurodegener. 6, 34.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  112. Chen X., Guan T, Li C., Shang H., Cui L., Li X., Kong J. 2012. SOD1 aggregation in astrocytes following ischemia/reperfusion injury a role of NO-mediated S-nitrosylation of protein disulfide isomerase (PDI). J. Neuroinflammation. 9, 237.

    Article  PubMed  PubMed Central  Google Scholar 

  113. Xu B., Jin C., Deng Y., Liu W., Yang T., Feng S., Xu Z. 2014. Alpha-synuclein oligomerization in manganese-induced nerve cell injury in brain slices a role of NO-mediated s-nitrosylation of protein disulfide isomerase. Mol. Neurobiol. 50, 1098–1110.

    Article  PubMed  CAS  Google Scholar 

  114. Wang H., Shi X., Qiu M., Lv S., Liu H. 2020. Hydrogen Sulfide plays an important protective role through influencing endoplasmic reticulum stress in diseases. Int. J. Biol. Sci. 16, 264–271.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  115. Vandiver M., Paul B., Xu R., Karuppagounder S., Rao F., Snowman A., Seok Ko H., Il Lee Y., Dawson V., Dawson T., Sen N., Snyder S. 2013. Sulfhydration mediates neuroprotective actions of parkin. Nat. Commun. 4, 1626.

    Article  PubMed  Google Scholar 

  116. Tapias V. 2019. Editorial mitochondrial dysfunction and neurodegeneration. Front. Neurosci. 13, 1372.

    Article  PubMed  PubMed Central  Google Scholar 

  117. Rachek L., Grishko V., LeDoux S., Wilson G. 2006. Role of nitric oxide-induced mtDNA damage in mitochondrial dysfunction and apoptosis. Free Radic. Biol. Med. 40, 754–762.

    Article  PubMed  CAS  Google Scholar 

  118. Luo Y., Yang X., Zhao S., Wei C., Yin Y., Liu T., Jiang S., Xie J., Wan X., Mao M., Wu J. 2013. Hydrogen sulfide prevents OGD/R-induced apoptosis via improving mitochondrial dysfunction and suppressing an ROS-mediated caspase-3 pathway in cortical neurons. Neurochem. Int. 63, 826–831.

    Article  PubMed  CAS  Google Scholar 

  119. Guo W., Kan J., Cheng Z., Chen J., Shen Y., Xu J., Wu D., Zhu Y. 2012. Hydrogen sulfide as an endogenous modulator in mitochondria and mitochondria dysfunction. Oxid. Med. Cell. Longev. 9, 878052.

    Google Scholar 

  120. Wang J., Medress Z., Barres B. 2012. Axon degeneration molecular mechanisms of a self-destruction pathway. J. Cell Biol. 196, 7–18.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  121. Koeberle P., Ball A. 1999. Nitric oxide synthase inhibition delays axonal degeneration and promotes the survival of axotomized retinal ganglion cells. Exp. Neurol. 158, 366–381.

    Article  PubMed  CAS  Google Scholar 

  122. Tang X., Lan M., Zhang M., Yao Z. 2017.Effect of nitric oxide to axonal degeneration in multiple sclerosis via downregulating monocarboxylate transporter 1 in oligodendrocytes. Nitric Oxide. 67, 75–80.

    Article  PubMed  CAS  Google Scholar 

  123. Smith K., Kapoor R., Hall S. 2001. Electrically active axons degenerate when exposed to nitric oxide. Ann Neurol. 49, 470–476.

    Article  PubMed  CAS  Google Scholar 

  124. Liñares D., Taconis M., Maña P., Correcha M., Fordham S., Staykova M., Willenborg D. 2006. neuronal nitric oxide synthase plays a key role in CNS demyelination. J. Neurosci. 26, 12 672–12 681.

    Article  Google Scholar 

  125. Keswani S., Bosch-Marcé M., Reed N., Fischer A, Semenza G., Höke A. 2011. Nitric oxide prevents axonal degeneration by inducing HIF-1–dependent expression of erythropoietin. Proc. Natl. Acad. Sci. USA. 108, 4986–4990.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  126. Cooke R., Mistry R., Challiss R., Straub V. 2013. Nitric oxide synthesis and cGMP production is important for neurite growth and synapse remodeling after axotomy. J. Neurosci. 33, 5626–5637.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  127. Xu K., Wu F, Xu K., Li Z., Wei X., Lu Q., Jiang T., Wu F., Xu X., Xiao J., Chen D., Zhang H. 2018. NaHS restores mitochondrial function and inhibits autophagy by activating the PI3K/Akt/mTOR signalling pathway to improve functional recovery after traumatic brain injury. Chem. Biol. Interact. 286, 96–105.

    Article  PubMed  CAS  Google Scholar 

  128. Pchitskaya E., Bezprozvanny I. 2020. Dendritic spines shape analysis-classification or clusterization? Perspective. Front. Synaptic Neurosci. 12, 31.

    Article  PubMed  PubMed Central  Google Scholar 

  129. Luo C., Lin Y., Qian X., Tang Y., Zhou H., Jin X., Ni H., Zhang F., Qin C., Li F., Zhang Y., Wu H., Chang L., Zhu D. 2014. Interaction of nNOS with PSD-95 negatively controls regenerative repair after stroke. J. Neurosci. 34, 13535–13548.

    Article  PubMed  PubMed Central  Google Scholar 

  130. Zhang Y., Zhu Z., Liang H., Zhang L., Zhou Q., Ni H., Luo C., Zhu D. 2018. nNOS-CAPON interaction mediates amyloid-β-induced neurotoxicity especially in the early stages. Aging Cell. 17, e12754.

    Article  PubMed  PubMed Central  Google Scholar 

  131. Mir S., Sen T., Sen N. 2014. Cytokine-induced GAPDH sulfhydration affects PSD95 degradation and memory. Mol. Cell. 56, 786–795.

    Article  PubMed  CAS  Google Scholar 

  132. Sen T., Saha P., Jiang T., Sen N. 2020. Sulfhydration of AKT triggers Tau-phosphorylation by activating glycogen synthase kinase 3β in Alzheimer’s disease. Proc. Natl. Acad. Sci. USA. 117, 4418–4427.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  133. Wang X., Du J., Cui H. 2014. Sulfur dioxide a double-faced molecule in mammals. Life Sci. 98, 63–67.

    Article  PubMed  CAS  Google Scholar 

  134. Rodkin S., Dzreyan V., Bibov M., Ermakov A., Derezina T., Kirichenko E. 2022. NO-dependent mechanisms of p53 expression and cell death in rat’s dorsal root ganglia after sciatic-nerve transection. Biomedicines. 10, 1664.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  135. Nakaya N., Lowe S., Taya Y., Chenchik A., Enikolopov G. 2000. Specific pattern of p53 phosphorylation during nitric oxide-induced cell cycle arrest. Oncogene. 19, 6369–6375.

    Article  PubMed  CAS  Google Scholar 

  136. Wang X., Zalcenstein A., Oren M. 2003. Nitric oxide promotes p53 nuclear retention and sensitizes neuroblastoma cells to apoptosis by ionizing radiation. Cell Death Differ. 10, 468–476.

    Article  PubMed  CAS  Google Scholar 

  137. Sun J., Li X., Gu X., Du H., Zhang G., Wu J., Wang F. 2021. Neuroprotective effect of hydrogen sulfide against glutamate-induced oxidative stress is mediated via the p53/glutaminase 2 pathway after traumatic brain injury. Aging. 13, 7180–7189.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  138. Luo Q., Wu X., Chang W., Zhao P., Nan Y., Zhu X., Katz J., Su D., Liu Z. 2020. ARID1A prevents squamous cell carcinoma initiation and chemoresistance by antagonizing pRb/E2F1/c-Myc-mediated cancer stemness. Cell Death Differ. 27, 1981–1997.

    Article  PubMed  CAS  Google Scholar 

  139. Cui X., Zhang J., Ma P., Myers D., Goldberg I., Sittle-r K., Barb J., Munson P., del Pilar Cintron A., McCoy J., Wang S., Danner R. 2005. cGMP-independent nitric oxide signaling and regulation of the cell cycle. BMC Genomics. 6, 151.

    Article  PubMed  PubMed Central  Google Scholar 

  140. Cai Z., Guo H., Wang C., Wei M., Cheng C., Yang Z., Chen Y., Le W., Li S. 2016. Double-edged roles of nitric oxide signaling on APP processing and amyloid-β production in vitro preliminary evidence from sodium nitroprusside. Neurotox. Res. 29, 21–34.

    Article  PubMed  CAS  Google Scholar 

  141. Kobayashi S., Sasaki T., Katayama T., Hasegawa T., Nagano A., Sato K. 2010. Temporal–spatial expression of presenilin 1 and the production of amyloid-β after acute spinal cord injury in adult rat. Neurochem. Int. 56, 387–393.

    Article  PubMed  CAS  Google Scholar 

  142. Ayton S., Lei P., Hare D.J., Duce J.A., George J.L., Adlard P.A., McLean C., Rogers J.T., Cherny R.A., Finkelstein D.I., Bush A.I. 2015 Parkinson’s disease iron deposition caused by nitric oxide-induced loss of β-amyloid precursor protein. J. Neurosci. 35, 3591–3597.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  143. Tejedo J., Bernabé J., Ramírez R., Sobrino F. 1999. NO induces a cGMP-independent release of cytochrome c from mitochondria which precedes caspase 3 activation in insulin producing RINm5F cells. FEBS Lett. 459, 238–243.

    Article  PubMed  CAS  Google Scholar 

  144. Huang Z., Pinto J., Deng H., Richie J. 2008. Inhibition of caspase-3 activity and activation by protein glutathionylation. Biochem. Pharmacol. 75, 2234–2244.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  145. Xu C., Zhang M., Zhang G., Yan S., Yan W. 2021. Hydrogen sulfide improves functional recovery in rat traumatic spinal cord injury model by inducing nuclear translocation of NF-E2-related factor 2. Biol. Pharm. Bull. 44, b21-00259.

    Article  Google Scholar 

  146. Ye X., Li Y., Lv B., Qiu B., Zhang S., Peng H., Kong W., Tang C., Huang Y., Du J., Jin H. 2022. Endogenous hydrogen sulfide persulfidates caspase-3 at cysteine 163 to inhibit doxorubicin-induced cardiomyocyte apoptosis. Oxid. Med. Cell. Longev. 20, 6153772.

    Google Scholar 

  147. Wu J., Lipinski M. 2019. Autophagy in neurotrauma good bad or dysregulated. Cells. 8, 693.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  148. Sarkar S., Korolchuk V., Renna M., Imarisio S., Fleming A., Williams A., Garcia-Arencibia M., Rose C., Luo S., Underwood B., Kroemer G., O’Kane C., Rubinsztein D. 2011. Complex inhibitory effects of nitric oxide on autophagy. Mol. Cell. 43, 19–32.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  149. Cervia D., Perrotta C., Moscheni C., De Palma C. 2013. Nitric oxide and sphingolipids control apoptosis and autophagy with a significant impact on Alzheimer’s disease. J. Biol. Regul. Homeost. Agents. 27, 11–22.

    PubMed  CAS  Google Scholar 

  150. Li L., Jiang H., Li Y., Guo Y. 2015. Hydrogen sulfide protects spinal cord and induces autophagy via miR-30c in a rat model of spinal cord ischemia-reperfusion injury. J. Biomed. Sci. 22, 50.

    Article  PubMed  PubMed Central  Google Scholar 

  151. Zhou J., Jin Y., Lei Y., Liu T., Wan Z., Meng H., Wang H. 2020. Ferroptosis is regulated by mitochondria in neurodegenerative diseases. Neurodegener. Dis. 20, 20–34.

    Article  PubMed  CAS  Google Scholar 

  152. Feng Z., Min L., Chen H., Deng W., Tan M., Liu H., Hou J. 2021. Iron overload in the motor cortex induces neuronal ferroptosis following spinal cord injury. Redox Biol. 43, 101984.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  153. Yu Y., Li X., Wu X., Li X., Wei J., Chen X., Sun Z., Zhang Q. 2023. Sodium hydrosulfide inhibits hemin-induced ferroptosis and lipid peroxidation in BV2 cells via the CBS/H2S system. Cell. Signal. 104, 110594.

    Article  PubMed  CAS  Google Scholar 

  154. Hu X., Chen H., Xu H., Wu Y., Wu C., Jia C., Li Y., Sheng S., Xu C., Xu H., Ni W., Zhou, K. 2020. Role of pyroptosis in traumatic brain and spinal cord injuries. Int. J. Biol. Sci. 16, 2042–2050.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  155. Chen X., Huang X., Liu C., Li S., Yang Z., Zhang F., Chen X., Shan H., Tao L., Zhang M. 2022. Surface-fill H2S-releasing silk fibroin hydrogel for brain repair through the repression of neuronal pyroptosis. Acta Biomater. 154, 259–274.

    Article  PubMed  CAS  Google Scholar 

  156. Godínez-Rubí M., Rojas-Mayorquín A., Ortuño-Sahagún D. 2013. Nitric oxide donors as neuroprotective agents after an ischemic stroke-related inflammatory reaction. Oxid. Med. Cell. Longev. 16, 297357.

    Google Scholar 

  157. Fernandez P., Pozo-Rodrigalvarez A., Serrano J., Martinez-Murillo R. 2010. Nitric oxide target for therapeutic strategies in alzheimers disease. Curr. Pharm. Des. 16, 2837–2850.

    Article  PubMed  CAS  Google Scholar 

  158. Singh S., Das T., Ravindran A. Chaturvedi R.K. Shukla Y. Agarwal A.K. Dikshit M. 2005. Involvement of nitric oxide in neurodegeneration a study on the experimental models of Parkinson’s disease. Redox Rep. 10, 103–109.

    Article  PubMed  CAS  Google Scholar 

  159. Lu D., Mahmood A., Zhang R., Li Y. 2003. Chopp M. Upregulation of neurogenesis and reduction in functional deficits following administration of DETA/NONOate a nitric oxide donor after traumatic brain injury in rats. J. Neurosurg. 99, 351–361.

    Article  PubMed  CAS  Google Scholar 

  160. Khan M., Im Y., Shunmugavel A., Gilg A., Dhindsa R., Singh A., Singh I. 2009. Administration of S-nitrosoglutathione after traumatic brain injury protects the neurovascular unit and reduces secondary injury in a rat model of controlled cortical impact. J. Neuroinflammation. 6, 32.

    Article  PubMed  PubMed Central  Google Scholar 

  161. Pannu R., Singh I. 2006. Pharmacological strategies for the regulation of inducible nitric oxide synthase neurodegenerative versus neuroprotective mechanisms. Neurochem. Int. 49, 170–182.

    Article  PubMed  CAS  Google Scholar 

  162. Lai Y., Tian Y., You X., Du J., Huang J. 2022. Effects of sphingolipid metabolism disorders on endothelial cells. Lipids Health Dis. 21, 101.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  163. Pannu R., Won J., Khan M., Singh A., Singh I. 2004. A novel role of lactosylceramide in the regulation of lipopolysaccharide/interferon-γ-mediated inducible nitric oxide synthase gene expression implications for neuroinflammatory diseases. J. Neurosci. 24, 5942–5954.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  164. Jia J., Xiao Y., Wang W., Qing L., Xu Y., Song H., Zhen X., Ao G., Alkayed N., Cheng J. 2013. Differential mechanisms underlying neuroprotection of hydrogen sulfide donors against oxidative stress. Neurochem. Int. 62, 1072–1078.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  165. Wang R., Wu X., Tian Z., Hu T., Cai C., Wu G., Jian-g G., Liu B. 2023. Sustained release of hydrogen sulfide from anisotropic ferrofluid hydrogel for the repair of spinal cord injury. Bioact. Mater. 23, 118–128.

    PubMed  Google Scholar 

  166. Liu Y., Pan L., Jiang A., Yin M. 2018. Hydrogen sulfide upregulated lncRNA CasC7 to reduce neuronal cell apoptosis in spinal cord ischemia-reperfusion injury rat. Biomed. Pharmacother. 98, 856–862.

    Article  PubMed  CAS  Google Scholar 

  167. Asimakopoulou A., Panopoulos P., Chasapis C., Coletta C., Zhou Z., Cirino G, Giannis A., Szabo C., Spyroulias G., Papapetropoulos A. 2013. Selectivity of commonly used pharmacological inhibitors for cystathionine β synthase (CBS) and cystathionine γ lyase (CSE). Br. J. Pharmacol. 169, 922–932.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  168. Wang F., Zhou H., Zhang X. 2022. SAM a cystathionine beta-synthase activator promotes hydrogen sulfide to promote neural repair resulting from massive cerebral infarction induced by middle cerebral artery occlusion. Metab. Brain Dis. 37, 1641–1654.

    Article  PubMed  CAS  Google Scholar 

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Rodkin, S.V., Nwosu, C.D. Role of Nitric Oxide and Hydrogen Sulfide in Neuronal and Glial Cell Death in Neurodegenerative Processes. Biochem. Moscow Suppl. Ser. A 17, 223–242 (2023). https://doi.org/10.1134/S1990747823050069

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