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The hydrogen sulfide signaling system: changes during aging and the benefits of caloric restriction

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Abstract

Hydrogen sulfide gas (H2S) is a putative signaling molecule that causes diverse effects in mammalian tissues including relaxation of blood vessels and regulation of perfusion in the liver, but the effects of aging on H2S signaling are unknown. Aging has negative impacts on the cardiovascular system. However, the liver is more resilient with age. Caloric restriction (CR) attenuates affects of age in many tissues. We hypothesized that the H2S signaling system is negatively affected by age in the vasculature but not in the liver, which is typically more resilient to age, and that a CR diet minimizes the age affect in the vasculature. To investigate this, we determined protein and mRNA expression of the H2S-producing enzymes cystathionine γ-lyase (CSE) and cystathionine β-synthase (CBS), H2S production rates in the aorta and liver, and the contractile response of aortic rings to exogenous H2S. Tissue was collected from Fisher 344 × Brown Norway rats from 8–38 months of age, which had been maintained on an ad libitum (AL) or CR diet. The results demonstrate that age and diet have differential effects on the H2S signaling system in aorta and liver. The aorta showed a sizeable effect of both age and diet, whereas the liver only showed a sizeable effect of diet. Aortic rings showed increased contractile sensitivity to H2S and increased protein expression of CSE and CBS with age, consistent with a decrease in H2S concentration with age. CR appears to benefit CSE and CBS protein in both aorta and liver, potentially by reducing oxidative stress and ameliorating the negative effect of age on H2S concentration. Therefore, CR may help maintain the H2S signaling system during aging.

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References

  • Abe K, Kimura H (1996) The possible role of hydrogen sulfide as an endogenous neuromodulator. J Neurosci 16(3):1066–1071

    CAS  PubMed  Google Scholar 

  • Ali MY, Ping CY, Mok YY, Ling L, Whiteman M, Bhatia M, Moore PK (2006) Regulation of vascular nitric oxide in vitro and in vivo; a new role for endogenous hydrogen sulphide? Br J Pharmacol 146:625–634

    Article  Google Scholar 

  • Anantharaju A, Feller A, Chedid A (2002) Aging liver. A review. Gerontology 48(6):343–353

    Article  CAS  PubMed  Google Scholar 

  • Anderson RM, Weindruch R (2010) Metabolic reprogramming, caloric restriction and aging. Trends Endocrinol Metab 21(3):134–141

    Article  CAS  PubMed  Google Scholar 

  • Aspnes LE, Lee CM, Weindruch R, Chung SS, Roecker EB, Aiken JM (1997) Caloric restriction reduces fiber loss and mitochondrial abnormalities in aged rat muscle. FASEB J 11(7):573–581

    CAS  PubMed  Google Scholar 

  • Barja G (2002) Endogenous oxidative stress: relationship to aging, longevity and caloric restriction. Ageing Res Rev 1(3):397–411

    Article  CAS  PubMed  Google Scholar 

  • Beauchamp RO, Bus JS, Popp JS, Boreiko CJ, Andjelkovich DA (1984) A critical review of the literature on hydrogen sulfide toxicity. CRC Crit Rev Toxicol 13:25–97

    Article  CAS  Google Scholar 

  • Calvert JW, Jha S, Gundewar S, Elrod JW, Ramachandran A, Pattillo CB, Kevil CG, Lefer DJ (2009) Hydrogen sulfide mediates cardioprotection through Nrf2 signaling. Circ Res 105(4):365–374

    Article  CAS  PubMed  Google Scholar 

  • Carter CS, Leeuwenburgh C, Daniels M, Foster TC (2009) Influence of calorie restriction on measures of age-related cognitive decline: role of increased physical activity. J Gerontol A Biol Sci Med Sci 64(8):850–859

    PubMed  Google Scholar 

  • Castello L, Froio T, Cavallini G, Biasi F, Sapino A, Leonarduzzi G, Bergamini E, Poli G, Chiarpotto E (2005) Calorie restriction protects against age-related rat aorta sclerosis. FASEB J 19(13):1863–1865

    CAS  PubMed  Google Scholar 

  • Cernadas MR, Sanchez de Miguel L, Garcia-Duran M, Gonzalez-Fernandez F, Millas I, Monton M, Rodrigo J, Rico L, Fernandez P, de Frutos T, Rodriguez-Feo JA, Guerra J, Caramelo C, Casado S, Lopez F (1998) Expression of constitutive and inducible nitric oxide synthases in the vascular wall of young and aging rats. Circ Res 83(3):279–286

    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(5):3205–3211

    Article  CAS  PubMed  Google Scholar 

  • Dombkowski RA, Russell MJ, Schulman AA, Doellman MM, Olson KR (2005) Vertebrate phylogeny of hydrogen sulfide vasoactivity. Am J Physiol Regul Integr Comp Physiol 288(1):R243–R252

    CAS  PubMed  Google Scholar 

  • Dombkowski RA, Doellman MM, Head SK, Olson KR (2006) Hydrogen sulfide mediates hypoxia-induced relaxation of trout urinary bladder smooth muscle. J Exp Biol 209(Pt 16):3234–3240

    Article  PubMed  Google Scholar 

  • Ebrahimkhani MR, Mani AR, Moore K (2005) Hydrogen sulphide and the hyperdynamic circulation in cirrhosis: a hypothesis. Gut 54(12):1668–1671

    Article  CAS  PubMed  Google Scholar 

  • Fiorucci S, Antonelli E, Distrutti E, Rizzo G, Mencarelli A, Orlandi S, Zanardo R, Renga B, Di Sante M, Morelli A, Cirino G, Wallace JL (2005a) Inhibition of hydrogen sulfide generation contributes to gastric injury caused by anti-inflammatory nonsteroidal drugs. Gastroenterology 129(4):1210–1224

    Article  CAS  Google Scholar 

  • Fiorucci S, Antonelli E, Mencarelli A, Orlandi S, Renga B, Rizzo G, Distrutti E, Shah V, Morelli A (2005b) The third gas: H2S regulates perfusion pressure in both the isolated and perfused normal rat liver and in cirrhosis. Hepatology 42(3):539–548

    Article  CAS  Google Scholar 

  • Fujii K, Sakuragawa T, Kashiba M, Sugiura Y, Kondo M, Maruyama K, Goda N, Nimura Y, Suematsu M (2005) Hydrogen sulfide as an endogenous modulator of biliary bicarbonate excretion in the rat liver. Antioxid Redox Signal 7(5–6):788–794

    Article  CAS  PubMed  Google Scholar 

  • Gainey LF Jr, Greenberg MJ (2005) Hydrogen sulfide is synthesized in the gills of the clam Mercenaria mercenaria and acts seasonally to modulate branchial muscle contraction. Biol Bull 209(1):11–20

    Article  CAS  PubMed  Google Scholar 

  • Geng B, Chang L, Pan C, Qi Y, Zhao J, Pang Y, Du J, Tang C (2004a) Endogenous hydrogen sulfide regulation of myocardial injury induced by isoproterenol. Biochem Biophys Res Commun 318(3):756–763

    Article  CAS  Google Scholar 

  • Geng B, Yang J, Qi Y, Zhao J, Pang Y, Du J, Tang C (2004b) H2S generated by heart in rat and its effects on cardiac function. Biochem Biophys Res Commun 313(2):362–368

    Article  CAS  Google Scholar 

  • Gilboa-Garber N (1971) Direct spectrophotometric determination of inorganic sulfide in biological materials and in other complex mixtures. Anal Biochem 43:129–133

    Article  CAS  PubMed  Google Scholar 

  • Goettsch W, Lattmann T, Amann K, Szibor M, Morawietz H, Munter K, Muller SP, Shaw S, Barton M (2001) Increased expression of endothelin-1 and inducible nitric oxide synthase isoform II in aging arteries in vivo: implications for atherosclerosis. Biochem Biophys Res Commun 280(3):908–913

    Article  CAS  PubMed  Google Scholar 

  • Goodwin LR, Francom D, Dieken FP, Taylor JD, Warenycia MW, Reiffenstein RJ, Dowling G (1989) Determination of sulfide in brain tissue by gas dialysis/ion chromatography: postmortem studies and two case reports. J Anal Toxicol 13(2):105–109

    CAS  PubMed  Google Scholar 

  • Gredilla R, Sanz A, Lopez-Torres M, Barja G (2001) Caloric restriction decreases mitochondrial free radical generation at complex I and lowers oxidative damage to mitochondrial DNA in the rat heart. FASEB J 15(9):1589–1591

    CAS  PubMed  Google Scholar 

  • Gredilla R, Phaneuf S, Selman C, Kendaiah S, Leeuwenburgh C, Barja G (2004) Short-term caloric restriction and sites of oxygen radical generation in kidney and skeletal muscle mitochondria. Ann N Y Acad Sci 1019:333–342

    Article  CAS  PubMed  Google Scholar 

  • Gygi SP, Rochon Y, Franza BR, Aebersold R (1999) Correlation between protein and mRNA abundance in yeast. Mol Cell Biol 19(3):1720–1730

    CAS  PubMed  Google Scholar 

  • Hofer T, Servais S, Seo AY, Marzetti E, Hiona A, Upadhyay SJ, Wohlgemuth SE, Leeuwenburgh C (2009) Bioenergetics and permeability transition pore opening in heart subsarcolemmal and interfibrillar mitochondria: effects of aging and lifelong calorie restriction. Mech Ageing Dev 130(5):297–307

    Article  CAS  PubMed  Google Scholar 

  • Hosoki R, Matsuki N, Kimura H (1997) The possible role of hydrogen sulfide as an endogenous smooth muscle relaxant in synergy with nitric oxide. Biochem Biophys Res Commun 237(3):527–531

    Article  CAS  PubMed  Google Scholar 

  • Julian D, Statile JL, Wohlgemuth SE, Arp AJ (2002) Enzymatic hydrogen sulfide production in marine invertebrate tissues. Comp Biochem Physiol A Mol Integr Physiol 133(1):105–115

    Article  PubMed  Google Scholar 

  • Julian D, Statile J, Roepke TA, Arp AJ (2005) Sodium nitroprusside potentiates hydrogen-sulfide-induced contractions in body wall muscle from a marine worm. Biol Bull 209(1):6–10

    Article  CAS  PubMed  Google Scholar 

  • Kimura H (2000) Hydrogen sulfide induces cyclic AMP and modulates the NMDA receptor. Biochem Biophys Res Commun 267(1):129–133

    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(5–6):795–803

    Article  CAS  PubMed  Google Scholar 

  • Kitani K (1991) Aging of the liver: facts and theories. Arch Gerontol Geriatr 12(2–3):133–154

    Article  CAS  PubMed  Google Scholar 

  • Kitani K (1994) Aging and the liver: functional aspects. Arch Gerontol Geriatr 19(2):145–158

    Article  CAS  PubMed  Google Scholar 

  • Koenitzer JR, Isbell TS, Patel HD, Benavides GA, Dickinson DA, Patel RP, Darley-Usmar VM, Lancaster JR Jr, Doeller JE, Kraus DW (2007) Hydrogen sulfide mediates vasoactivity in an O2-dependent manner. Am J Physiol Heart Circ Physiol 292(4):H1953–H1960

    Article  CAS  PubMed  Google Scholar 

  • Kubo S, Doe I, Kurokawa Y, Nishikawa H, Kawabata A (2007) Direct inhibition of endothelial nitric oxide synthase by hydrogen sulfide: contribution to dual modulation of vascular tension. Toxicology 232(1–2):138–146

    Article  CAS  PubMed  Google Scholar 

  • Labinskyy N, Csiszar A, Veress G, Stef G, Pacher P, Oroszi G, Wu J, Ungvari Z (2006) Vascular dysfunction in aging: potential effects of resveratrol, an anti-inflammatory phytoestrogen. Curr Med Chem 13(9):989–996

    Article  CAS  PubMed  Google Scholar 

  • Lakatta EG (1993) Cardiovascular regulatory mechanisms in advanced age. Physiol Rev 73(2):413–467

    CAS  PubMed  Google Scholar 

  • Leeuwenburgh C, Prolla TA (2006) Genetics, redox signaling, oxidative stress, and apoptosis in Mammalian aging. Antioxid Redox Signal 8(3–4):503–505

    Article  CAS  PubMed  Google Scholar 

  • Leeuwenburgh C, Wagner P, Holloszy JO, Sohal RS, Heinecke JW (1997) Caloric restriction attenuates dityrosine cross-linking of cardiac and skeletal muscle proteins in aging mice. Arch Biochem Biophys 346(1):74–80

    Article  CAS  PubMed  Google Scholar 

  • Lim JJ, Liu Y, Khin Sandar Win E, Bian JS (2008) Vasoconstrictive effect of hydrogen sulfide involves downregulation of cAMP in vascular smooth muscle cells. Am J Physiol Cell Physiol 295(5):C1261–C1270

    Article  CAS  PubMed  Google Scholar 

  • Lowicka E, Beltowski J (2007) Hydrogen sulfide (H2S)—the third gas of interest for pharmacologists. Pharmacol Rep 59(1):4–24

    CAS  PubMed  Google Scholar 

  • Marzetti E, Wohlgemuth SE, Lees HA, Chung HY, Giovannini S, Leeuwenburgh C (2008) Age-related activation of mitochondrial caspase-independent apoptotic signaling in rat gastrocnemius muscle. Mech Ageing Dev 129(9):542–549

    Article  CAS  PubMed  Google Scholar 

  • Minamiyama Y, Bito Y, Takemura S, Takahashi Y, Kodai S, Mizuguchi S, Nishikawa Y, Suehiro S, Okada S (2007) Calorie restriction improves cardiovascular risk factors via reduction of mitochondrial reactive oxygen species in type II diabetic rats. J Pharmacol Exp Ther 320(2):535–543

    Article  CAS  PubMed  Google Scholar 

  • Olson KR (2005) Vascular actions of hydrogen sulfide in nonmammalian vertebrates. Antioxid Redox Signal 7(5–6):804–812

    Article  CAS  PubMed  Google Scholar 

  • Olson KR (2009) Is hydrogen sulfide a circulating “Gasotransmitter” in vertebrate blood? Biochim Biophys Acta 1787(7):856–863

    Article  CAS  PubMed  Google Scholar 

  • Olson KR, Donald JA (2009) Nervous control of circulation—the role of gasotransmitters, NO, CO, and H(2)S. Acta Histochem 111(3):244–256

    Article  CAS  PubMed  Google Scholar 

  • Olson KR, Dombkowski RA, Russell MJ, Doellman MM, Head SK, Whitfield NL, Madden JA (2006) Hydrogen sulfide as an oxygen sensor/transducer in vertebrate hypoxic vasoconstriction and hypoxic vasodilation. J Exp Biol 209(Pt 20):4011–4023

    Article  CAS  PubMed  Google Scholar 

  • Olson KR, Forgan LG, Dombkowski RA, Forster ME (2008) Oxygen dependency of hydrogen sulfide-mediated vasoconstriction in cyclostome aortas. J Exp Biol 211(Pt 14):2205–2213

    Article  CAS  PubMed  Google Scholar 

  • Payne AM, Dodd SL, Leeuwenburgh C (2003) Life-long calorie restriction in Fischer 344 rats attenuates age-related loss in skeletal muscle-specific force and reduces extracellular space. J Appl Physiol 95(6):2554–2562

    PubMed  Google Scholar 

  • Pryor WA, Houk KN, Foote CS, Fukuto JM, Ignarro LJ, Squadrito GL, Davies KJ (2006) Free radical biology and medicine: it's a gas, man! Am J Physiol Regul Integr Comp Physiol 291(3):R491–R511

    CAS  PubMed  Google Scholar 

  • Raitakari M, Ilvonen T, Ahotupa M, Lehtimaki T, Harmoinen A, Suominen P, Elo J, Hartiala J, Raitakari OT (2004) Weight reduction with very-low-caloric diet and endothelial function in overweight adults: role of plasma glucose. Arterioscler Thromb Vasc Biol 24(1):124–128

    Article  CAS  PubMed  Google Scholar 

  • Sasaki S, Higashi Y, Nakagawa K, Kimura M, Noma K, Sasaki S, Hara K, Matsuura H, Goto C, Oshima T, Chayama K (2002) A low-calorie diet improves endothelium-dependent vasodilation in obese patients with essential hypertension. Am J Hypertens 15(4 Pt 1):302–309

    Article  CAS  PubMed  Google Scholar 

  • Schmucker DL (1998) Aging and the liver: an update. J Gerontol A Biol Sci Med Sci 53(5):B315–B320

    CAS  PubMed  Google Scholar 

  • Sharifi AM, Mohseni S, Nekoparvar S, Larijani B, Fakhrzadeh H, Oryan S (2008) Effect of caloric restriction on nitric oxide production, ACE activity, and blood pressure regulation in rats. Acta Physiol Hung 95(1):55–63

    Article  CAS  PubMed  Google Scholar 

  • Shibuya N, Tanaka M, Yoshida M, Ogasawara Y, Togawa T, Ishii K, Kimura H (2008) 3-Mercaptopyruvate sulfurtransferase produces hydrogen sulfide and bound sulfane sulfur in the brain. Antioxid Redox Signal 11(4):703–714

    Google Scholar 

  • Shibuya N, Mikami Y, Kimura Y, Nagahara N, Kimura H (2009) Vascular endothelium expresses 3-mercaptopyruvate sulfurtransferase and produces hydrogen sulfide. J Biochem 146(5):623–626

    Article  CAS  PubMed  Google Scholar 

  • Stipanuk MH, Beck PW (1982) Characterization of the enzymic capacity for cysteine desulphhydration in liver and kidney of the rat. Biochem J 206(2):267–277

    CAS  PubMed  Google Scholar 

  • Szabo C (2007) Hydrogen sulphide and its therapeutic potential. Nat Rev Drug Discov 6(11):917–935

    Article  CAS  PubMed  Google Scholar 

  • Taddei S, Virdis A, Ghiadoni L, Versari D, Salvetti A (2006) Endothelium, aging, and hypertension. Curr Hypertens Rep 8(1):84–89

    Article  CAS  PubMed  Google Scholar 

  • Tanaka Y, Funabiki M, Michikawa H, Koike K (2006) Effects of aging on alpha1-adrenoceptor mechanisms in the isolated mouse aortic preparation. J Smooth Muscle Res 42(4):131–138

    Article  PubMed  Google Scholar 

  • Ungvari Z, Parrado-Fernandez C, Csiszar A, de Cabo R (2008) Mechanisms underlying caloric restriction and lifespan regulation: implications for vascular aging. Circ Res 102(5):519–528

    Article  CAS  PubMed  Google Scholar 

  • van der Loo B, Labugger R, Skepper JN, Bachschmid M, Kilo J, Powell JM, Palacios-Callender M, Erusalimsky JD, Quaschning T, Malinski T, Gygi D, Ullrich V, Luscher TF (2000) Enhanced peroxynitrite formation is associated with vascular aging. J Exp Med 192(12):1731–1744

    Article  PubMed  Google Scholar 

  • van der Loo B, Bachschmid M, Labugger R, Schildknecht S, Kilo J, Hahn R, Palacios-Callender M, Luscher TF (2005) Expression and activity patterns of nitric oxide synthases and antioxidant enzymes reveal a substantial heterogeneity between cardiac and vascular aging in the rat. Biogerontology 6(5):325–334

    Article  CAS  PubMed  Google Scholar 

  • Wallace JL (2007) Hydrogen sulfide-releasing anti-inflammatory drugs. Trends Pharmacol Sci 28(10):501–505

    Article  CAS  PubMed  Google Scholar 

  • Wang R (2002) Two's company, three's a crowd: can H2S be the third endogenous gaseous transmitter? FASEB J 16(13):1792–1798

    Article  CAS  PubMed  Google Scholar 

  • Wang YF, Mainali P, Tang CS, Shi L, Zhang CY, Yan H, Liu XQ, Du JB (2008) Effects of nitric oxide and hydrogen sulfide on the relaxation of pulmonary arteries in rats. Chin Med J (Engl) 121(5):420–423

    CAS  Google Scholar 

  • Webb GD, Lim LH, Oh VM, Yeo SB, Cheong YP, Ali MY, El Oakley R, Lee CN, Wong PS, Caleb MG, Salto-Tellez M, Bhatia M, Chan ES, Taylor EA, Moore PK (2008) Contractile and vasorelaxant effects of hydrogen sulfide and its biosynthesis in the human internal mammary artery. J Pharmacol Exp Ther 324(2):876–882

    Article  CAS  PubMed  Google Scholar 

  • 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(3):765–768

    Article  CAS  PubMed  Google Scholar 

  • Whiteman M, Li L, Kostetski I, Chu SH, Siau JL, Bhatia M, Moore PK (2006) Evidence for the formation of a novel nitrosothiol from the gaseous mediators nitric oxide and hydrogen sulphide. Biochem Biophys Res Commun 343(1):303–310

    Article  CAS  PubMed  Google Scholar 

  • Whitfield NL, Kreimier EL, Verdial FC, Skovgaard N, Olson KR (2008) A Reappraisal of H2S/sulfide concentration in vertebrate blood and its potential significance in ischemic preconditioning and vascular signaling. Am J Physiol Regul Integr Comp Physiol 294:1930–1937

    Google Scholar 

  • Wood CE, Chen GF, Keller-Wood M (2005) Expression of nitric oxide synthase isoforms is reduced in late-gestation ovine fetal brainstem. Am J Physiol Regul Integr Comp Physiol 289(2):R613–R619

    CAS  PubMed  Google Scholar 

  • Yang H, Shi M, Story J, Richardson A, Guo Z (2004) Food restriction attenuates age-related increase in the sensitivity of endothelial cells to oxidized lipids. J Gerontol A Biol Sci Med Sci 59(4):316–323

    PubMed  Google Scholar 

  • Yang G, Wu L, Jiang B, Yang W, Qi J, Cao K, Meng Q, Mustafa AK, Mu W, Zhang S, Snyder SH, Wang R (2008) H2S as a physiologic vasorelaxant: hypertension in mice with deletion of cystathionine gamma-lyase. Science 322(5901):587–590

    Article  CAS  PubMed  Google Scholar 

  • Zanardo RC, Brancaleone V, Distrutti E, Fiorucci S, Cirino G, Wallace JL (2006) Hydrogen sulfide is an endogenous modulator of leukocyte-mediated inflammation. FASEB J 20(12):2118–2120

    Article  CAS  PubMed  Google Scholar 

  • Zeeh J, Platt D (2002) The aging liver: structural and functional changes and their consequences for drug treatment in old age. Gerontology 48(3):121–127

    Article  CAS  PubMed  Google Scholar 

  • Zhao W, Wang R (2002) H(2)S-induced vasorelaxation and underlying cellular and molecular mechanisms. Am J Physiol Heart Circ Physiol 283(2):H474–H480

    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(21):6008–6016

    Article  CAS  PubMed  Google Scholar 

  • Zhao W, Ndisang JF, Wang R (2003) Modulation of endogenous production of H2S in rat tissues. Can J Physiol Pharmacol 81(9):848–853

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We would like to thank Dr. Christy Carter for donation of rat aorta tissue used in the myography experiments. This work was supported by National Institute of Health T32 HL083810 to BP, National Institute of Health AG21042 to CL and National Science Foundation IBN-0422139 to DJ.

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Authors and Affiliations

  1. Department of Biology, University of Florida, Gainesville, FL, 32611, USA

    Benjamin L. Predmore, Maikel J. Alendy, Khadija I. Ahmed & David Julian

  2. Department of Aging and Geriatrics, University of Florida, Gainesville, FL, 32611, USA

    Christiaan Leeuwenburgh

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  1. Benjamin L. Predmore
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  2. Maikel J. Alendy
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Correspondence to David Julian.

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Predmore, B.L., Alendy, M.J., Ahmed, K.I. et al. The hydrogen sulfide signaling system: changes during aging and the benefits of caloric restriction. AGE 32, 467–481 (2010). https://doi.org/10.1007/s11357-010-9150-z

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