Skip to main content
SpringerLink
Log in

Role of hydrogen sulfide in cerebrovascular alteration during aging

  • Review
  • Published:
Archives of Pharmacal Research Aims and scope Submit manuscript

Abstract

Hydrogen sulfide (H2S), a gasotransmitter molecule, has attracted attention as an endogenous signaling molecule because of its various pathological and physiological effects, including pathologies related to aging. In this review, we aimed to discuss the morphological changes in each vessel following aging, and to evaluate the possible role of H2S in the cerebrovascular alteration, such as arterial stiffness, microvessel loss, and blood–brain barrier disruption, with advancing age. Additionally, the review outlines the therapeutic efficacy of the H2S-releasing compounds on the cerebrovasculature. In the central nervous system, cerebrovascular aging can lead to the loss of blood–brain integrity, which causes cognitive impairment. The findings discussed in this review strongly support the notion that H2S has a potential therapeutic role in cerebrovascular alteration in aging.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Abbott NJ, Patabendige AA, Dolman DE, Yusof SR, Begley DJ (2010) Structure and function of the blood-brain barrier. Neurobiol Dis 37:13–25

    Article  CAS  PubMed  Google Scholar 

  • Ahmad A, Sattar MA, Azam M, Abdulla MH, Khan SA, Hashmi F, Abdullah NA, Johns EJ (2016) Cystathione gamma lyase/hydrogen sulphide pathway up regulation enhances the responsiveness of α1A and α1B-adrenoreceptors in the kidney of rats with left ventricular hypertrophy. PLoS ONE 11:e0154995

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Asai K, Kudej RK, Shen YT, Yang GP, Takagi G, Kudej AB, Geng YJ, Sato N, Nazareno JB, Vatner DE, Natividad F, Bishop SP, Vatner SF (2000) Peripheral vascular endothelial dysfunction and apoptosis in old monkeys. Arterioscler Thromb Vasc Biol 20:1493–1499

    Article  CAS  PubMed  Google Scholar 

  • Bełtowski J (2015) Hydrogen sulfide in pharmacology and medicine: an update. Pharmacol Rep 67:647–658

    Article  CAS  PubMed  Google Scholar 

  • Briones AM, Aras-López R, Alonso MJ, Salaices M (2014) Small artery remodeling in obesity and insulin resistance. Curr Vasc Pharmacol 12:427–437

    Article  CAS  PubMed  Google Scholar 

  • Burns EM, Kruckeberg TW, Gaetano PK (1981) Changes with age in cerebral capillary morphology. Neurobiol Aging 2:283–291

    Article  CAS  PubMed  Google Scholar 

  • Candela J, Velmurugan GV, White C (2016) Hydrogen sulfide depletion contributes to microvascular remodeling in obesity. Am J Physiol Heart Circ Physiol 310:H1071–H1080

    Article  PubMed  Google Scholar 

  • Chang EI, Loh SA, Ceradini DJ, Chang EI, Lin SE, Bastidas N, Aarabi S, Chan DA, Freedman ML, Giaccia AJ, Gurtner GC (2007) Age decreases endothelial progenitor cell recruitment through decreases in hypoxia-inducible factor 1α stabilization during ischemia. Circulation 116:2818–2829

    Article  CAS  PubMed  Google Scholar 

  • Chen YH, Yao WZ, Geng B, Ding YL, Lu M, Zhao MW, Tang CS (2005) Endogenous hydrogen sulfide in patients with COPD. Chest 128:3205–3211

    Article  CAS  PubMed  Google Scholar 

  • Chen Y, Zhao J, Du J, Xu G, Tang C, Geng B (2012) Hydrogen sulfide regulates cardiac sarcoplasmic reticulum Ca2 + uptake via KATP channel and PI3K/Akt pathway. Life Sci 91:271–278

    Article  CAS  PubMed  Google Scholar 

  • Chen X, Pang S, Lin J, Xia J, Wang Y (2016) Allicin prevents oxidized low-density lipoprotein-induced endothelial cell injury by inhibiting apoptosis and oxidative stress pathway. BMC Complement Altern Med 16:133

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheung SH, Kwok WK, To KF, Lau JY (2014) Anti-atherogenic effect of hydrogen sulfide by over-expression of cystathionine gamma-lyase (CSE) gene. PLoS ONE 9:e113038

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chinta SJ, Woods G, Rane A, Demaria M, Campisi J, Andersen JK (2015) Cellular senescence and the aging brain. Exp Gerontol 68:3–7

    Article  CAS  PubMed  Google Scholar 

  • Choi SY, Oh BH, Bae Park J, Choi DJ, Rhee MY, Park S (2013) Age-associated increase in arterial stiffness measured according to the cardio-ankle vascular index without blood pressure changes in healthy adults. J Atheroscler Thromb 20:911–923

    Article  CAS  PubMed  Google Scholar 

  • Christensen K, Doblhammer G, Rau R, Vaupel JW (2009) Ageing populations: the challenges ahead. Lancet 374:1196–1208

    Article  PubMed  PubMed Central  Google Scholar 

  • Csiszar A, Labinskyy N, Orosz Z, Xiangmin Z, Buffenstein R, Ungvari Z (2007) Vascular aging in the longest-living rodent, the naked mole rat. Am J Physiol Heart Circ Physiol 293:H919–H927

    Article  CAS  PubMed  Google Scholar 

  • Das A, Huang GX, Bonkowski MS, Longchamp A, Li C, Schultz MB, Kim LJ, Osborne B, Joshi S, Lu Y, Treviño-Villarreal JH, Kang MJ, Hung TT, Lee B, Williams EO, Igarashi M, Mitchell JR, Wu LE, Turner N, Arany Z, Guarente L, Sinclair DA (2018) Impairment of an endothelial NAD + -H2S signaling network is a reversible cause of vascular aging. Cell 173:74–89

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Du C, Lin X, Xu W, Zheng F, Cai J, Yang J, Cui Q, Tang C, Cai J, Xu G, Geng B (2018) Sulfhydrated sirtuin-1 increasing its deacetylation activity is an essential epigenetics mechanism of anti-atherogenesis by hydrogen sulfide. Antioxid Redox Signal. https://doi.org/10.1089/ars.2017.7195

    Article  PubMed  Google Scholar 

  • Duca L, Blaise S, Romier B, Laffargue M, Gayral S, El Btaouri H, Kawecki C, Guillot A, Martiny L, Debelle L, Maurice P (2016) Matrix ageing and vascular impacts: focus on elastin fragmentation. Cardiovasc Res 110:298–308

    Article  CAS  PubMed  Google Scholar 

  • Elahy M, Jackaman C, Mamo JC, Lam V, Dhaliwal SS, Giles C, Nelson D, Takechi R (2015) Blood-brain barrier dysfunction developed during normal aging is associated with inflammation and loss of tight junctions but not with leukocyte recruitment. Immun Ageing 12:2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Farrall AJ, Wardlaw JM (2009) Blood-brain barrier: ageing and microvascular disease–systematic review and meta-analysis. Neurobiol Aging 30:337–352

    Article  CAS  PubMed  Google Scholar 

  • Frohman EM, Frohman TC, Gupta S, de Fougerolles A, van den Noort S (1991) Expression of intercellular adhesion molecule 1 (ICAM-1) in Alzheimer’s disease. J Neurol Sci 106:105–111

    Article  CAS  PubMed  Google Scholar 

  • Gao L, Cheng C, Sparatore A, Zhang H, Wang C (2014) Hydrogen sulfide inhibits human platelet aggregation in vitro in part by interfering gap junction channels: effects of ACS14, a hydrogen sulfide-releasing aspirin. Heart Lung Circ 24:77–85

    Article  PubMed  Google Scholar 

  • Geng Y, Li E, Mu Q, Zhang Y, Wei X, Li H, Cheng L, Zhang B (2015) Hydrogen sulfide inhalation decreases early blood-brain barrier permeability and brain edema induced by cardiac arrest and resuscitation. J Cereb Blood Flow Metab 35:494–500

    Article  CAS  PubMed  Google Scholar 

  • Giustarini D, Del Soldato P, Sparatore A, Rossi R (2010) Modulation of thiol homeostasis induced by H2S-releasing aspirin. Free Radic Biol Med 48:1263–1272

    Article  CAS  PubMed  Google Scholar 

  • Grambow E, Mueller-Graf F, Delyagina E, Frank M, Kuhla A, Vollmar B (2014) Effect of the hydrogen sulfide donor GYY4137 on platelet activation and microvascular thrombus formation in mice. Platelets 25:166–174

    Article  CAS  PubMed  Google Scholar 

  • Grambow E, Leppin C, Leppin K, Kundt G, Klar E, Frank M, Vollmar B (2017) The effects of hydrogen sulfide on platelet-leukocyte aggregation and microvascular thrombolysis. Platelets 28:509–517

    Article  CAS  PubMed  Google Scholar 

  • Harman D (1956) Aging: a theory based on free radical and radiation chemistry. J Gerontol 11:298–300

    Article  CAS  PubMed  Google Scholar 

  • Hiramatsu K, Tsuneyoshi T, Ogawa T, Morihara N (2016) Aged garlic extract enhances heme oxygenase-1 and glutamate-cysteine ligase modifier subunit expression via the nuclear factor erythroid 2-related factor 2-antioxidant response element signaling pathway in human endothelial cells. Nutr Res 36:143–149

    Article  CAS  PubMed  Google Scholar 

  • Hongfang J, Cong B, Zhao B, Zhang C, Liu X, Zhou W, Shi Y, Tang C, Junbao D (2006) Effects of hydrogen sulfide on hypoxic pulmonary vascular structural remodeling. Life Sci 78:1299–1309

    Article  CAS  PubMed  Google Scholar 

  • Hu Y, Li R, Yang H, Luo H, Chen Z (2015) Sirtuin 6 is essential for sodium sulfide-mediated cytoprotective effect in ischemia/reperfusion-stimulated brain endothelial cells. J Stroke Cerebrovasc Dis 24:601–609

    Article  PubMed  Google Scholar 

  • Huang Q, Sparatore A, Del Soldato P, Wu L, Desai K (2014) Hydrogen sulfide releasing aspirin, ACS14, attenuates high glucose-induced increased methylglyoxal and oxidative stress in cultured vascular smooth muscle cells. PLoS ONE 9:e97315

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jiang Z, Li C, Manuel ML, Yuan S, Kevil CG, McCarter KD, Lu W, Sun H (2015) Role of hydrogen sulfide in early blood-brain barrier disruption following transient focal cerebral ischemia. PLoS ONE 10:e0117982

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kamat PK, Kyles P, Kalani A, Tyagi N (2016) Hydrogen sulfide ameliorates homocysteine-induced alzheimer’s disease-like pathology, blood-brain barrier disruption, and synaptic disorder. Mol Neurobiol 53:2451–2467

    Article  CAS  PubMed  Google Scholar 

  • Kan J, Guo W, Huang C, Bao G, Zhu Y, Zhu YZ (2014) S-propargyl-cysteine, a novel water-soluble modulator of endogenous hydrogen sulfide, promotes angiogenesis through activation of signal transducer and activator of transcription 3. Antioxid Redox Signal 20:2303–2316

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kang HM, Sohn I, Jung J, Jeong JW, Park C (2016) Age-related changes in pial arterial structure and blood flow in mice. Neurobiol Aging 37:161–170

    Article  PubMed  Google Scholar 

  • Kawahara TL, Michishita E, Adler AS, Damian M, Berber E, Lin M, McCord RA, Ongaigui KC, Boxer LD, Chang HY, Chua KF (2009) SIRT6 links histone H3 lysine 9 deacetylation to NF-kappaB-dependent gene expression and organismal life span. Cell 136:62–74

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kimura H (2014) Hydrogen sulfide and polysulfides as biological mediators. Molecules 19:16146–16157

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kimura Y, Kimura H (2004) Hydrogen sulfide protects neurons from oxidative stress. FASEB J 18:1165–1167

    Article  CAS  PubMed  Google Scholar 

  • Kimura H, Nagai Y, Umemura K, Kimura Y (2005) Physiological roles of hydrogen sulfide: synaptic modulation, neuroprotection, and smooth muscle relaxation. Antioxid Redox Signal 7:795–803

    Article  CAS  PubMed  Google Scholar 

  • Kimura Y, Goto Y, Kimura H (2010) Hydrogen sulfide increases glutathione production and suppresses oxidative stress in mitochondria. Antioxid Redox Signal 12:1–13

    Article  CAS  PubMed  Google Scholar 

  • Latorre E, Torregrossa R, Wood ME, Whiteman M, Harries LW (2018) Mitochondria-targeted hydrogen sulfide attenuates endothelial senescence by selective induction of splicing factors HNRNPD and SRSF2. Aging (Albany NY) 10:1666–1681

    Article  Google Scholar 

  • Le Couteur DG, Lakatta EG (2010) A vascular theory of aging. J Gerontol A Biol Sci Med Sci 65:1025–1027

    Article  PubMed  Google Scholar 

  • Li XH, Xue WL, Wang MJ, Zhou Y, Zhang CC, Sun C, Zhu L, Liang K, Chen Y, Tao BB, Tan B, Yu B, Zhu YC (2017) H2S regulates endothelial nitric oxide synthase protein stability by promoting microRNA-455-3p expression. Sci Rep 7:44807

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li H, Zhu L, Feng J, Hu X, Li C, Zhang B (2018) Hydrogen sulfide decreases blood-brain barrier damage via regulating protein kinase C and tight junction after cardiac arrest in rats. Cell Physiol Biochem 47:994–1006

    Article  CAS  PubMed  Google Scholar 

  • Liu Z, Han Y, Li L, Lu H, Meng G, Li X, Shirhan M, Peh MT, Xie L, Zhou S, Wang X, Chen Q, Dai W, Tan CH, Pan S, Moore PK, Ji Y (2013) The hydrogen sulfide donor, GYY4137, exhibits anti-atherosclerotic activity in high fat fed apolipoprotein E(−/−) mice. Br J Pharmacol 169:1795–1809

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mani S, Li H, Untereiner A, Wu L, Yang G, Austin RC, Dickhout JG, Lhoták Š, Meng QH, Wang R (2013) Decreased endogenous production of hydrogen sulfide accelerates atherosclerosis. Circulation 127:2523–2534

    Article  CAS  PubMed  Google Scholar 

  • Mao Z, Hine C, Tian X, Van Meter M, Au M, Vaidya A, Seluanov A, Gorbunova V (2011) SIRT6 promotes DNA repair under stress by activating PARP1. Science 332:1443–1446

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miller DL, Roth MB (2007) Hydrogen sulfide increases thermotolerance and lifespan in Caenorhabditis elegans. Proc Natl Acad Sci USA 104:20618–20622

    Article  PubMed  PubMed Central  Google Scholar 

  • Mitchell GF, Parise H, Benjamin EJ, Larson MG, Keyes MJ, Vita JA, Vasan RS, Levy D (2004) Changes in arterial stiffness and wave reflection with advancing age in healthy men and women: the Framingham Heart Study. Hypertension 43:1239–1245

    Article  CAS  PubMed  Google Scholar 

  • Mori T, Kawara S, Shinozaki M, Hayashi N, Kakinuma T, Igarashi A, Takigawa M, Nakanishi T, Takehara K (1999) Role and interaction of connective tissue growth factor with transforming growth factor-β in persistent fibrosis: a mouse fibrosis model. J Cell Physiol 181:153–159

    Article  CAS  PubMed  Google Scholar 

  • Muller M, Grobbee DE, Aleman A, Bots M, van der Schouw YT (2007) Cardiovascular disease and cognitive performance in middle-aged and elderly men. Atherosclerosis 190:143–149

    Article  CAS  PubMed  Google Scholar 

  • Mustafa AK, Sikka G, Gazi SK, Steppan J, Jung SM, Bhunia AK, Barodka VM, Gazi FK, Barrow RK, Wang R, Amzel LM, Berkowitz DE, Snyder SH (2011) Hydrogen sulfide as endothelium-derived hyperpolarizing factor sulfhydrates potassium channels. Circ Res 109:1259–1268

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Olas B (2015) Hydrogen sulfide in signaling pathways. Clin Chim Acta 439:212–218

    Article  CAS  PubMed  Google Scholar 

  • Pan LL, Liu XH, Zheng HM, Yang HB, Gong QH, Zhu YZ (2012) S-propargyl-cysteine, a novel hydrogen sulfide-modulated agent, attenuated tumor necrosis factor-α-induced inflammatory signaling and dysfunction in endothelial cells. Int J Cardiol 155:327–332

    Article  PubMed  Google Scholar 

  • Pezzoli D, Di Paolo J, Kumra H, Fois G, Candiani G, Reinhardt DP, Mantovani D (2018) Fibronectin promotes elastin deposition, elasticity and mechanical strength in cellularised collagen-based scaffolds. Biomaterials 180:130–142

    Article  CAS  PubMed  Google Scholar 

  • Pircher J, Fochler F, Czermak T, Mannell H, Kraemer BF, Wörnle M, Sparatore A, Del Soldato P, Pohl U, Krötz F (2012) Hydrogen sulfide-releasing aspirin derivative ACS14 exerts strong antithrombotic effects in vitro and in vivo. Arterioscler Thromb Vasc Biol 32:2884–2891

    Article  CAS  PubMed  Google Scholar 

  • Popov D (2013) An outlook on vascular hydrogen sulphide effects, signalling, and therapeutic potential. Arch Physiol Biochem 119:189–194

    Article  CAS  PubMed  Google Scholar 

  • Qabazard B, Li L, Gruber J, Peh MT, Ng LF, Kumar SD, Rose P, Tan CH, Dymock BW, Wei F, Swain SC, Halliwell B, Stürzenbaum SR, Moore PK (2014) Hydrogen sulfide is an endogenous regulator of aging in Caenorhabditis elegans. Antiox Redox Signal 20:2621–2630

    Article  CAS  Google Scholar 

  • Riddle DR, Sonntag WE, Lichtenwalner RJ (2003) Microvascular plasticity in aging. Ageing Res Rev 2:149–168

    Article  PubMed  Google Scholar 

  • Roggendorf W, Cervós-Navarro J (1977) Ultrastructure of arterioles in the cat brain. Cell Tissue Res 178:495–515

    Article  CAS  PubMed  Google Scholar 

  • Ruitenberg A, den Heijer T, Bakker SL, van Swieten JC, Koudstaal PJ, Hofman A, Breteler MM (2005) Cerebral hypoperfusion and clinical onset of dementia: the Rotterdam Study. Ann Neurol 57:789–794

    Article  PubMed  Google Scholar 

  • Saha S, Chakraborty PK, Xiong X, Dwivedi SK, Mustafi SB, Leigh NR, Ramchandran R, Mukherjee P, Bhattacharya R (2016) Cystathionine β-synthase regulates endothelial function via protein S-sulfhydration. FASEB J 30:441–456

    Article  CAS  PubMed  Google Scholar 

  • Semba RD, Sun K, Schwartz AV, Varadhan R, Harris TB, Satterfield S, Garcia M, Ferrucci L, Newman AB (2015) Serum carboxymethyl-lysine, an advanced glycation end product, is associated with arterial stiffness in older adults. J Hypertens 33:797–803

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shao WH, Li C, Chen L, Qiu X, Zhang W, Huang CX, Xia L, Kong JM, Tang Y (2010) Stereological investigation of age-related changes of the capillaries in white matter. Anat Rec (Hoboken) 293:1400–1407

    Article  Google Scholar 

  • Shirai K, Song M, Suzuki J, Kurosu T, Oyama T, Nagayama D, Miyashita Y, Yamamura S, Takahashi M (2011) Contradictory effects of β1- and α1- aderenergic receptor blockers on cardio-ankle vascular stiffness index (CAVI)–CAVI independent of blood pressure. J Atheroscler Thromb 18:49–55

    Article  CAS  PubMed  Google Scholar 

  • Shuang T, Fu M, Yang G, Wu L, Wang R (2018) The interaction of IGF-1/IGF-1R and hydrogen sulfide on the proliferation of mouse primary vascular smooth muscle cells. Biochem Pharmacol 149:143–152

    Article  CAS  PubMed  Google Scholar 

  • Spinetti G, Wang M, Monticone R, Zhang J, Zhao D, Lakatta EG (2004) Rat aortic MCP-1 and its receptor CCR2 increase with age and alter vascular smooth muscle cell function. Arterioscler Thromb Vasc Biol 24:1397–1402

    Article  CAS  PubMed  Google Scholar 

  • Vaitkevicius PV, Fleg JL, Engel JH, O’Connor FC, Wright JG, Lakatta LE, Yin FC, Lakatta EG (1993) Effects of age and aerobic capacity on arterial stiffness in healthy adults. Circulation 88:1456–1462

    Article  CAS  PubMed  Google Scholar 

  • Vicente JB, Malagrinò F, Arese M, Forte E, Sarti P, Giuffrè A (2016) Bioenergetic relevance of hydrogen sulfide and the interplay between gasotransmitters at human cystathionine β-synthase. Biochim Biophys Acta 1857:1127–1138

    Article  CAS  PubMed  Google Scholar 

  • Wang R (2011) Signaling pathways for the vascular effects of hydrogen sulfide. Curr Opin Nephrol Hypertens 20:107–112

    Article  CAS  PubMed  Google Scholar 

  • Wu JS, Chen XC, Chen H, Shi YQ (2006) A study on blood-brain barrier ultrastructural changes induced by cerebral hypoperfusion of different stages. Neurol Res 28:50–58

    Article  PubMed  Google Scholar 

  • Wu W, Hou CL, Mu XP, Sun C, Zhu YC, Wang MJ, Lv QZ (2017) H2S donor NaHS changes the production of endogenous H2S and NO in d-galactose-induced accelerated ageing. Oxid Med Cell Longev 2017:5707830

    PubMed  PubMed Central  Google Scholar 

  • Xu X, Wang B, Ren C, Hu J, Greenberg DA, Chen T, Xie L, Jin K (2017) Age-related impairment of vascular structure and functions. Aging Dis 8:590–610

    Article  PubMed  PubMed Central  Google Scholar 

  • 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  CAS  PubMed  Google Scholar 

  • Yang G, Li H, Tang G, Wu L, Zhao K, Cao Q, Xu C, Wang R (2012) Increased neointimal formation in cystathionine gamma-lyase deficient mice: role of hydrogen sulfide in α5β1-integrin and matrix metalloproteinase-2 expression in smooth muscle cells. J Mol Cell Cardiol 52:677–688

    Article  CAS  PubMed  Google Scholar 

  • Yang T, Sun Y, Lu Z, Leak RK, Zhang F (2017) The impact of cerebrovascular aging on vascular cognitive impairment and dementia. Ageing Res Rev 34:15–29

    Article  PubMed  Google Scholar 

  • Zhang ET, Inman CB, Weller RO (1990) Interrelationships of the pia mater and the perivascular (Virchow-Robin) spaces in the human cerebrum. J Anat 170:111–123

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang H, Guo C, Zhang A, Fan Y, Gu T, Wu D (2012a) Effect of S-aspirin, a novel hydrogen-sulfide-releasing aspirin (ACS14), on atherosclerosis in apoE-deficient mice. Eur J Pharmacol 697:106–116

    Article  CAS  PubMed  Google Scholar 

  • Zhang R, Kadar T, Sirimanne E, MacGibbon A, Guan J (2012b) Age-related memory decline is associated with vascular and microglial degeneration in aged rats. Behav Brain Res 235:210–217

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang M, Pan H, Xu Y, Wang X, Qiu Z, Jiang L (2017b) Allicin decreases lipopolysaccharide-induced oxidative stress and inflammation in human umbilical vein endothelial cells through suppression of mitochondrial dysfunction and activation of Nrf2. Cell Physiol Biochem 41:2255–2267

    Article  CAS  PubMed  Google Scholar 

  • Zhao W, Zhang J, Lu Y, Wang R (2001) The vasorelaxant effect of H2S as a novel endogenous gaseous KATP channel opener. EMBO J 20:6008–6016

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao X, Zhang LK, Zhang CY, Zeng XJ, Yan H, Jin HF, Tang CS, Du JB (2008) Regulatory effect of hydrogen sulfide on vascular collagen content in spontaneously hypertensive rats. Hypertens Res 31:1619–1630

    Article  CAS  PubMed  Google Scholar 

  • Zheng M, Qiao W, Cui J, Liu L, Liu H, Wang Z, Yan C (2014) Hydrogen sulfide delays nicotinamide-induced premature senescence via upregulation of SIRT1 in human umbilical vein endothelial cells. Mol Cell Biochem 393:59–67

    Article  CAS  PubMed  Google Scholar 

  • Zhuo JM, Wang H, Praticò D (2011) Is hyperhomocysteinemia an Alzheimer’s disease (AD) risk factor, an AD marker, or neither? Trends Pharmacol Sci 32:562–571

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was supported by grants from the National Research Foundation of Korea (NRF-2016R1A2B4011607).

Author information

Authors and Affiliations

  1. Department of Anatomy and Neurobiology, Graduate School, School of Medicine, Biomedical Science Institute, Kyung Hee University, Seoul, 02447, Republic of Korea

    Juyeon Mun & Chan Park

  2. Department of Anatomy and Neurobiology, Biomedical Science Institute, College of Medicine, Kyung Hee University, 26, Kyungheedae-ro, Dongdaemun-gu, Seoul, 02447, Republic of Korea

    Juyeon Mun, Hye-Min Kang, Junyang Jung & Chan Park

Authors
  1. Juyeon Mun
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hye-Min Kang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Junyang Jung
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Chan Park
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Chan Park.

Ethics declarations

Conflict of interest

The authors have no conflict of interest to declare.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mun, J., Kang, HM., Jung, J. et al. Role of hydrogen sulfide in cerebrovascular alteration during aging. Arch. Pharm. Res. 42, 446–454 (2019). https://doi.org/10.1007/s12272-019-01135-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12272-019-01135-y

Keywords

Search

Navigation