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Biological Effects of Hydrogen Sulfide and Its Protective Role in Intracerebral Hemorrhage

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Abstract

Intracerebral hemorrhage (ICH) has extremely high morbidity and mortality, substantially impacting public health. Studying the pathophysiological mechanisms of ICH is a complicated undertaking, and there remains a lack of effective medical treatment for improving ICH survival rates and promoting recovery. This review describes the preclinical studies of intracerebral hemorrhage that have been performed to date in detail, including different methods used to establish animal models and identify the cellular mechanisms involved after ICH. Recently, it was reported that the endogenous hydrogen sulfide (H2S) pathway is downregulated in the brain after ICH. Thus, exogenous H2S may have therapeutic potential by rescuing the decreased levels of endogenous H2S level after injury. Furthermore, we also discuss the molecular mechanisms involved in the protective effects of H2S and how these effects may have therapeutic use to treat and prevent ICH-induced neuronal injury.

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References

  • Abe K, Kimura H (1996) The possible role of hydrogen sulfide as an endogenous neuromodulator. J Neurosci 16:1066–1071. https://doi.org/10.1523/JNEUROSCI.16-03-01066.1996

  • Afonina IS, Zhong Z, Karin M, Beyaert R (2017) Limiting inflammation-the negative regulation of NF-kappaB and the NLRP3 inflammasome Nat Immunol 18:861-869 doi:https://doi.org/10.1038/ni.3772

  • Alharbi BM, Tso MK, Macdonald RL (2016) Animal models of spontaneous intracerebral hemorrhage. Neurological Research 38:448–455. https://doi.org/10.1080/01616412.2016.1144671

  • An SJ, Kim TJ, Yoon BW (2017) Epidemiology, Risk factors, and clinical features of intracerebral hemorrhage: an update J Stroke 19:3–10 doi:https://doi.org/10.5853/jos.2016.00864

  • Bhatia K, Hepburn M, Ziu E, Siddiq F, Qureshi AI (2018) Modern approaches to evacuating intracerebral hemorrhage. Curr Cardiol Rep 20:132. https://doi.org/10.1007/s11886-018-1078-4

  • Cao X, Ding L, Xie ZZ, Yang Y, Whiteman M, Moore PK, Bian JS (2019) A review of hydrogen sulfide synthesis, metabolism, and measurement: is modulation of hydrogen sulfide a novel therapeutic for cancer? Antioxid Redox Signal 31:1–38. https://doi.org/10.1089/ars.2017.7058

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chunyu Z, Junbao D, Dingfang B, Hui Y, Xiuying T, Chaoshu T (2003) The regulatory effect of hydrogen sulfide on hypoxic pulmonary hypertension in rats Biochemical and Biophysical Research Communications 302:810–816 doi:https://doi.org/10.1016/s0006-291x(03)00256-0

  • Dou Y, Wang Z, Chen G (2016) The role of hydrogen sulfide in stroke Med Gas Res 6:79–84. https://doi.org/10.4103/2045-9912.184717

  • Duan X, Wen Z, Shen H, Shen M, Chen G (2016) Intracerebral hemorrhage, oxidative stress, and antioxidant therapy. Oxid Med Cell Longev 2016:1203285. https://doi.org/10.1155/2016/1203285

  • Duan XC et al (2017) Roles of autophagy and endoplasmic reticulum stress in intracerebral hemorrhage-induced secondary brain injury in rats. CNS Neurosci Ther 23:554–566. https://doi.org/10.1111/cns.12703

  • Enokido Y, Suzuki E, Iwasawa K, Namekata K, Okazawa H, Kimura H (2005) Cystathionine beta-synthase, a key enzyme for homocysteine metabolism, is preferentially expressed in the radial glia/astrocyte lineage of developing mouse CNS FASEB journal : official publication of the Federation of American Societies for Experimental Biology 19:1854-1856 doi:https://doi.org/10.1096/fj.05-3724fje

  • Eto K, Kimura H (2002) The production of hydrogen sulfide is regulated by testosterone and S-adenosyl-L-methionine in mouse brain. J Neurochem 83:80–86. https://doi.org/10.1046/j.1471-4159.2002.01097.x

  • Eto K, Kimura H (2005) The production of hydrogen sulfide is regulated by testosterone and S-adenosyl-L-methionine in mouse brain. J Neurochem 93:1633. https://doi.org/10.1111/j.1471-4159.2005.03283.x

  • Fiorucci S, Distrutti E, Cirino G, Wallace JL (2006) The emerging roles of hydrogen sulfide in the gastrointestinal tract and liver Gastroenterology 131:259–271 doi:https://doi.org/10.1053/j.gastro.2006.02.033

  • Furne J, Saeed A, Levitt MD (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. https://doi.org/10.1152/ajpregu.90566.2008

  • Furne J, Springfield J, Koenig T, DeMaster E, Levitt MD (2001) Oxidation of hydrogen sulfide and methanethiol to thiosulfate by rat tissues: a specialized function of the colonic mucosa Biochem Pharmacol 62:255–259 doi:https://doi.org/10.1016/s0006-2952(01)00657-8

  • Gao C et al. (2018) Neuroprotective effects of hydrogen sulfide on sodium azide-induced oxidative stress in PC12 cells Int J Mol Med 41:242-250 doi:https://doi.org/10.3892/ijmm.2017.3227

  • Guo W, Cheng ZY, Zhu YZ (2013) Hydrogen sulfide and translational medicine Acta Pharmacol Sin 34:1284–1291 doi:https://doi.org/10.1038/aps.2013.127

  • Hughes MN, Centelles MN, Moore KP (2009) Making and working with hydrogen sulfide: the chemistry and generation of hydrogen sulfide in vitro and its measurement in vivo: a review Free Radic Biol Med 47:1346–1353. https://doi.org/10.1016/j.freeradbiomed.2009.09.018

  • Hui Y, Du J, Tang C, Bin G, Jiang H (2003) Changes in arterial hydrogen sulfide (H(2)S) content during septic shock and endotoxin shock in rats J Infect 47:155-160 doi:https://doi.org/10.1016/s0163-4453(03)00043-4

  • Ishigami M, Hiraki K, Umemura K, Ogasawara Y, Ishii K, Kimura H (2009) A source of hydrogen sulfide and a mechanism of its release in the brain Antioxid Redox Signal 11:205–214 doi:https://doi.org/10.1089/ARS.2008.2132

  • Jia G, Yu S, Sun W, Yang J, Wang Y, Qi Y, Chen Y (2020) Hydrogen sulfide attenuates particulate matter-induced emphysema and airway inflammation through Nrf2-dependent manner front Pharmacol 11:29 doi:https://doi.org/10.3389/fphar.2020.00029

  • Kamat PK, Kalani A, Tyagi N (2015) Role of hydrogen sulfide in brain synaptic remodeling Methods Enzymol 555:207–229. https://doi.org/10.1016/bs.mie.2014.11.025

  • Kar S, Shahshahan HR, Hackfort BT, Yadav SK, Yadav R, Kambis TN, Lefer DJ, Mishra PK (2019) Exercise training promotes cardiac hydrogen sulfide biosynthesis and mitigates pyroptosis to prevent high-fat diet-induced diabetic cardiomyopathy. Antioxidants (Basel) 8. https://doi.org/10.3390/antiox8120638

  • Kim B, Lee J, Jang J, Han D, Kim KH (2011) Prediction on the seasonal behavior of hydrogen sulfide using a neural network model ScientificWorldJournal 11:992–1004 doi:https://doi.org/10.1100/tsw.2011.95

  • Klebe D, Iniaghe L, Burchell S, Reis C, Akyol O, Tang J, Zhang JH (2018) Intracerebral Hemorrhage in Mice. In: Intracerebral hemorrhage in mice. Traumatic and Ischemic Injury. Methods in Molecular Biology, In, pp 83–91. https://doi.org/10.1007/978-1-4939-7526-6_7

    Chapter  Google Scholar 

  • Lan X, Han X, Li Q, Yang QW, Wang J (2017) Modulators of microglial activation and polarization after intracerebral haemorrhage Nat Rev Neurol 13:420–433 doi:https://doi.org/10.1038/nrneurol.2017.69

  • Lee M, Schwab C, Yu S, McGeer E, McGeer PL (2009) Astrocytes produce the antiinflammatory and neuroprotective agent hydrogen sulfide Neurobiol Aging 30:1523–1534 doi:https://doi.org/10.1016/j.neurobiolaging.2009.06.001

  • Levitt MD, Abdel-Rehim MS, Furne J (2011) Free and acid-labile hydrogen sulfide concentrations in mouse tissues: anomalously high free hydrogen sulfide in aortic tissue Antioxid Redox Signal 15:373–378. https://doi.org/10.1089/ars.2010.3525

  • Levitt MD, Furne J, Springfield J, Suarez F, DeMaster E (1999) Detoxification of hydrogen sulfide and methanethiol in the cecal mucosa. J Clin Invest 104:1107–1114. https://doi.org/10.1172/JCI7712

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li Q, Han X, Lan X, Gao Y, Wan J, Durham F, Cheng T, Yang J, Wang Z, Jiang C, Ying M, Koehler RC, Stockwell BR, Wang J (2017) Inhibition of neuronal ferroptosis protects hemorrhagic brain. JCI Insight 2. https://doi.org/10.1172/jci.insight.90777

  • Li Z, Polhemus DJ, Lefer DJ (2018) Evolution of hydrogen sulfide therapeutics to treat cardiovascular disease. Circ Res 123:590–600. https://doi.org/10.1161/CIRCRESAHA.118.311134

  • Li J et al (2020a) Ferroptosis: past, present and future. Cell Death Dis 11:88. https://doi.org/10.1038/s41419-020-2298-2

  • Li X, Zhuang YY, Wu L, Xie M, Gu HF, Wang B, Tang XQ (2020b) Hydrogen sulfide ameliorates cognitive dysfunction in formaldehyde-exposed rats: involvement in the upregulation of brain-derived neurotrophic factor. Neuropsychobiology 79:119–130. https://doi.org/10.1159/000501294

  • Liu H, Wang Y, Xiao Y, Hua Z, Cheng J, Jia J (2016) Hydrogen sulfide attenuates tissue plasminogen activator-induced cerebral hemorrhage following experimental stroke. Translational Stroke Research 7:209–219. https://doi.org/10.1007/s12975-016-0459-5

  • Madangarli N, Bonsack F, Dasari R, Sukumari-Ramesh S (2019) Intracerebral hemorrhage: blood components and neurotoxicity brain. Sci 9. https://doi.org/10.3390/brainsci9110316

  • Manaenko A, Chen H, Zhang JH, Tang J (2011) Comparison of different preclinical models of intracerebral hemorrhage Acta Neurochir Suppl 111:9–14 doi:https://doi.org/10.1007/978-3-7091-0693-8_2

  • Mitchell TW, Savage JC, Gould DH (1993) High-performance liquid chromatography detection of sulfide in tissues from sulfide-treated mice. J Appl Toxicol 13:389–394. https://doi.org/10.1002/jat.2550130605

    Article  CAS  PubMed  Google Scholar 

  • Mok YY, Atan MS, Yoke Ping C, Zhong Jing W, Bhatia M, Moochhala S, Moore PK (2004) Role of hydrogen sulphide in haemorrhagic shock in the rat: protective effect of inhibitors of hydrogen sulphide biosynthesis Br J Pharmacol 143:881–889 doi:https://doi.org/10.1038/sj.bjp.0706014

  • Ogasawara Y, Isoda S, Tanabe S (1994) Tissue and subcellular distribution of bound and acid-labile sulfur, and the enzymic capacity for sulfide production in the rat Biol Pharm Bull 17:1535-1542 doi:https://doi.org/10.1248/bpb.17.1535

  • Olson KR, Deleon ER, Gao Y, Hurley K, Sadauskas V, Batz C, Stoy GF (2013) Thiosulfate: a readily accessible source of hydrogen sulfide in oxygen sensing Am J Physiol Regul Integr Comp Physiol 305:R592–R603 doi:https://doi.org/10.1152/ajpregu.00421.2012

  • Omura T, Sadano H, Hasegawa T, Yoshida Y, Kominami S (1984) Hemoprotein H-450 identified as a form of cytochrome P-450 having an endogenous ligand at the 6th coordination position of the heme. Journal of Biochemistry 96:1491–1500. https://doi.org/10.1093/oxfordjournals.jbchem.a134978

  • Panthi S, Chung HJ, Jung J, Jeong NY (2016) Physiological importance of hydrogen sulfide: emerging potent neuroprotector and neuromodulator. Oxid Med Cell Longev 2016:9049782. https://doi.org/10.1155/2016/9049782.

  • Ravanan P, Srikumar IF, Talwar P (2017) Autophagy: the spotlight for cellular stress responses Life Sci 188:53–67. https://doi.org/10.1016/j.lfs.2017.08.029

  • Robert K, Vialard F, Thiery E, Toyama K, Sinet PM, Janel N, London J (2003) Expression of the cystathionine beta synthase (CBS) gene during mouse development and immunolocalization in adult brain. J Histochem Cytochem 51:363–371. https://doi.org/10.1177/002215540305100311

    Article  CAS  PubMed  Google Scholar 

  • Scimemi A (2018) Astrocytes and the warning signs of intracerebral hemorrhagic stroke. Neural Plast 2018:7301623. https://doi.org/10.1155/2018/7301623

  • Shan H et al. (2019a) Exogenous hydrogen sulfide offers neuroprotection on Intracerebral hemorrhage injury through modulating endogenous H2S metabolism in mice Frontiers in Cellular Neuroscience 13 doi:https://doi.org/10.3389/fncel.2019.00349

  • Shan H et al. (2019b) Exogenous hydrogen sulfide offers neuroprotection on intracerebral hemorrhage injury through modulating endogenous H2S metabolism in mice front cell Neurosci 13:349 doi:https://doi.org/10.3389/fncel.2019.00349

  • Shao A, Zhu Z, Li L, Zhang S, Zhang J (2019) Emerging therapeutic targets associated with the immune system in patients with intracerebral haemorrhage (ICH): from mechanisms to translation EBioMedicine 45:615-623 doi:https://doi.org/10.1016/j.ebiom.2019.06.012

  • Shen F, Zhao CS, Shen MF, Wang Z, Chen G (2019) The role of hydrogen sulfide in gastric mucosal damage Med Gas Res 9:88–92 doi:https://doi.org/10.4103/2045-9912.260650

  • Shen X, Pattillo CB, Pardue S, Bir SC, Wang R, Kevil CG (2011) Measurement of plasma hydrogen sulfide in vivo and in vitro Free Radic Biol Med 50:1021–1031 doi:https://doi.org/10.1016/j.freeradbiomed.2011.01.025

  • Shibuya N, Tanaka M, Yoshida M, Ogasawara Y, Togawa T, Ishii K, Kimura H (2009) 3-Mercaptopyruvate sulfurtransferase produces hydrogen sulfide and bound sulfane sulfur in the brain Antioxid Redox Signal 11:703-714 doi:https://doi.org/10.1089/ARS.2008.2253

  • Sulpizio M, Falone S, Amicarelli F, Marchisio M, di Giuseppe F, Eleuterio E, di Ilio C, Angelucci S (2011) Molecular basis underlying the biological effects elicited by extremely low-frequency magnetic field (ELF-MF) on neuroblastoma cells. J Cell Biochem 112:3797–3806. https://doi.org/10.1002/jcb.23310

    Article  CAS  PubMed  Google Scholar 

  • Szabo C (2007) Hydrogen sulphide and its therapeutic potential Nat Rev Drug Discov 6:917-935 doi:https://doi.org/10.1038/nrd2425

  • Tan B, Jin S, Sun J, Gu Z, Sun X, Zhu Y, Huo K, Cao Z, Yang P, Xin X, Liu X, Pan L, Qiu F, Jiang J, Jia Y, Ye F, Xie Y, Zhu YZ (2017) New method for quantification of gasotransmitter hydrogen sulfide in biological matrices by LC-MS/MS. New method for quantification of gasotransmitter hydrogen sulfide in biological matrices by LC-MS/MS Sci Rep 7:46278. https://doi.org/10.1038/srep46278

    Article  CAS  PubMed  Google Scholar 

  • Tschoe C, Bushnell CD, Duncan PW, Alexander-Miller MA, Wolfe SQ (2020) Neuroinflammation after intracerebral hemorrhage and potential therapeutic targets J Stroke 22:29–46. https://doi.org/10.5853/jos.2019.02236

  • Wang L, Cai H, Hu Y, Liu F, Huang S, Zhou Y, Yu J, Xu J, Wu F (2018) A pharmacological probe identifies cystathionine beta-synthase as a new negative regulator for ferroptosis. Cell Death Dis 9:1005. https://doi.org/10.1038/s41419-018-1063-2

  • Wang R (2012) Physiological implications of hydrogen sulfide: a whiff exploration that blossomed Physiol Rev 92:791-896 doi:https://doi.org/10.1152/physrev.00017.2011

  • Whiteman M, Armstrong JS, Chu SH, Jia-Ling S, Wong BS, Cheung NS, Halliwell B, Moore PK (2004) The novel neuromodulator hydrogen sulfide: an endogenous peroxynitrite ‘scavenger’? J Neurochem 90:765–768. https://doi.org/10.1111/j.1471-4159.2004.02617.x

    Article  CAS  PubMed  Google Scholar 

  • Whiteman M, Moore PK (2009) Hydrogen sulfide and the vasculature: a novel vasculoprotective entity and regulator of nitric oxide bioavailability? J Cell Mol Med 13:488–507. https://doi.org/10.1111/j.1582-4934.2009.00645.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wilkinson DA, Pandey AS, Thompson BG, Keep RF, Hua Y, Xi G (2018) Injury mechanisms in acute intracerebral hemorrhage Neuropharmacology 134:240–248 doi:https://doi.org/10.1016/j.neuropharm.2017.09.033

  • Wu B, Ma Q, Khatibi N, Chen W, Sozen T, Cheng O, Tang J (2010) Ac-YVAD-CMK decreases blood-brain barrier degradation by inhibiting caspase-1 activation of interleukin-1beta in Intracerebral hemorrhage mouse model. Transl Stroke Res 1:57-64. https://doi.org/10.1007/s12975-009-0002-z

  • Wu D, Hu Q, Zhu D (2018a) An update on hydrogen sulfide and nitric oxide interactions in the cardiovascular system. Oxid Med Cell Longev 2018:4579140. https://doi.org/10.1155/2018/4579140

  • Wu D, Wang H, Teng T, Duan S, Ji A, Li Y (2018b) Hydrogen sulfide and autophagy: a double edged sword. Pharmacol Res 131:120–127. https://doi.org/10.1016/j.phrs.2018.03.002

  • Wu C, Yan X, Liao Y, Liao L, Huang S, Zuo Q, Zhou L, Gao L, Wang Y, Lin J, Li S, Wang K, Ge X, Song H, Yang R, Lu F (2019) Increased perihematomal neuron autophagy and plasma thrombin-antithrombin levels in patients with intracerebral hemorrhage: an observational study. Medicine (Baltimore) 98:e17130. https://doi.org/10.1097/MD.0000000000017130

  • Yu YP, Chi XL, Liu LJ (2014) A hypothesis: hydrogen sulfide might be neuroprotective against subarachnoid hemorrhage induced brain injury ScientificWorldJournal 2014:432318.https://doi.org/10.1155/2014/432318

  • Zhang J et al. (2019) Hydrogen sulfide protects against cell damage through modulation of PI3K/Akt/Nrf2 signaling Int J Biochem Cell Biol 117:105636 doi:https://doi.org/10.1016/j.biocel.2019.105636

  • Zhang JY, Ding YP, Wang Z, Kong Y, Gao R, Chen G (2017a) Hydrogen sulfide therapy in brain diseases: from bench to bedside Med Gas Res 7:113–119 doi:https://doi.org/10.4103/2045-9912.208517

  • Zhang M, Shan H, Wang Y, Wang T, Liu W, Wang L, Zhang L, Chang P, Dong W, Chen X, Tao L (2013) The expression changes of cystathionine-beta-synthase in brain cortex after traumatic brain injury. J Mol Neurosci 51:57–67. https://doi.org/10.1007/s12031-012-9948-5

    Article  CAS  PubMed  Google Scholar 

  • Zhang M et al. (2017b) The cystathionine beta-synthase/hydrogen sulfide pathway contributes to microglia-mediated neuroinflammation following cerebral ischemia Brain Behav Immun 66:332-346 doi:https://doi.org/10.1016/j.bbi.2017.07.156

  • Zhang Z et al. (2018) Glutathione peroxidase 4 participates in secondary brain injury through mediating ferroptosis in a rat model of intracerebral hemorrhage Brain Res 1701:112-125 doi:https://doi.org/10.1016/j.brainres.2018.09.012

  • Zhao H et al. (2017) Endogenous hydrogen sulphide attenuates NLRP3 inflammasome-mediated neuroinflammation by suppressing the P2X7 receptor after intracerebral haemorrhage in rats J Neuroinflammation 14:163 doi:https://doi.org/10.1186/s12974-017-0940-4

  • Zhao H et al. (2018) Taurine supplementation reduces neuroinflammation and protects against white matter injury after intracerebral hemorrhage in rats Amino Acids 50:439-451 doi:https://doi.org/10.1007/s00726-017-2529-8

  • Zheng F et al. (2018) Cystathionine beta synthase-hydrogen sulfide system in paraventricular nucleus reduced high fatty diet induced obesity and insulin resistance by brain-adipose axis Biochim Biophys Acta Mol Basis Dis 1864:3281-3291 doi:https://doi.org/10.1016/j.bbadis.2018.07.014

  • Zhong WX et al (2012) Lanthionine synthetase C-like protein 1 interacts with and inhibits cystathionine beta-synthase: a TARGET FOR NEURONAL ANTIOXIDANT DEFENSE The Journal of biological chemistry 287:34189-34201. https://doi.org/10.1074/jbc.M112.383646

  • Zhou Y, Wang Y, Wang J, Anne Stetler R, Yang QW (2014) Inflammation in intracerebral hemorrhage: from mechanisms to clinical translation Prog Neurobiol 115:25–44 doi:https://doi.org/10.1016/j.pneurobio.2013.11.003

  • Zhu W, Gao Y, Chang CF, Wan JR, Zhu SS, Wang J (2014) Mouse models of intracerebral hemorrhage in ventricle, cortex, and hippocampus by injections of autologous blood or collagenase PLoS One 9:e97423 doi:https://doi.org/10.1371/journal.pone.0097423

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Funding

This study was funded by grants from the National Natural Science Foundation of China (No. 81601306, No. 81301039, and No. 81530062); the China Postdoctoral Science Foundation Funded Project (No. 2015 M570476); the Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD); the Jiangsu Talent Youth Medical Program (QNRC2016245); the Shanghai Key Lab of Forensic Medicine (KF1801); and the Suzhou Science and Technology Development Project (SYS2018082).

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  1. Jiaxin Zhang and Haiyan Shan contributed equally to this work.

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  1. Shanghai Key Laboratory of Forensic Medicine (Academy of Forensic Science), Shanghai, 200063, China

    Jiaxin Zhang & Mingyang Zhang

  2. Institute of Forensic Sciences, Soochow University, Suzhou, 215123, Jiangsu, China

    Jiaxin Zhang, Luyang Tao & Mingyang Zhang

  3. Department of Obstetrics and Gynecology, The Affiliated Suzhou Hospital of Nanjing Medical University, Suzhou, 215000, China

    Haiyan Shan

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  1. Jiaxin Zhang
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Zhang, J., Shan, H., Tao, L. et al. Biological Effects of Hydrogen Sulfide and Its Protective Role in Intracerebral Hemorrhage. J Mol Neurosci 70, 2020–2030 (2020). https://doi.org/10.1007/s12031-020-01608-6

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