C. elegans aging is modulated by hydrogen sulfide and the sulfhydrylase/cysteine synthase cysl-2

PLoS ONE

Volumn 8, Issue 11, 2013, Pages

  Qabazard, Bedoor ^a   Ahmed, Samanza ^a   Li, Ng ^a,c   Arlt, Volker M ^a   Moore, Philip K ^b   Stürzenbaum, Stephen R ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^c AGENCY FOR SCIENCE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

CYSTEINE SYNTHASE; DICHLOROMETHANE; HYDROGEN PEROXIDE; HYDROGEN SULFIDE; MORPHOLIN 4 IUM 4 METHOXYPHENYL(MORPHOLINO) PHOSPHINODITHIOATE; PROTEIN CYSL 2; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG;

ADULT; AGING; ANIMAL CELL; ARTICLE; BODY SIZE; CAENORHABDITIS ELEGANS; CELL DEATH; CELL VIABILITY; CELLULAR STRESS RESPONSE; CELLULAR STRESS SIGNAL; CONTROLLED STUDY; DEVELOPMENTAL STAGE; ENDOPLASMIC RETICULUM STRESS; ENVIRONMENTAL STRESS; ENZYME SYNTHESIS; GENE; GROWTH REGULATION; HEAT TOLERANCE; K10H10 GENE; LIFESPAN; LONGEVITY; MICROBIAL GROWTH; NONHUMAN; OXIDATIVE STRESS; REPRODUCTION; SURVIVAL RATE; TEMPERATURE STRESS;

AGING; ANIMALS; AORTA; CAENORHABDITIS ELEGANS; CATTLE; CELL DEATH; CELL SURVIVAL; CELLS, CULTURED; CYSTEINE SYNTHASE; ENDOPLASMIC RETICULUM; ENDOTHELIAL CELLS; HYDROGEN PEROXIDE; HYDROGEN SULFIDE; MORPHOLINES; ORGANOTHIOPHOSPHORUS COMPOUNDS; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES;

EID: 84892537477     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0080135     Document Type: Article

References (60)

1. Whiteman M, Le Trionnaire S, Chopra M, Fox B, Whatmore J (2011) Emerging role of hydrogen sulfide in health and disease: critical appraisal of biomarkers and pharmacological tools. Clin Sci (Lond) 121(11): 459-488. doi:10.1042/CS20110267. PubMed: 21843150.
2. Petersen LC, Degn H, Nicholls P (1977) Kinetics of the cytochrome c oxidase and reductase reactions in energized and de-energized mitochondria. Can J Biochem 55(7): 706-713. doi:10.1139/o77-102. PubMed: 196723.
3. Li L, Bhatia M, Moore PK (2006) Hydrogen sulphide - a novel mediator of inflammation? Curr Opin Pharmacol 6(2): 125-129. doi:10.1016/j.coph.2005.10.007. PubMed: 16487749.
4. Beyer K, Lao JI, Carrato C, Rodriguez-Vila A, Latorre P et al. (2004) Cystathionine beta synthase as a risk factor for Alzheimer disease. Curr Alzheimer Res 1(2): 127-133. doi:10.2174/1567205043332243. PubMed: 15975077.
5. Qu K, Chen CP, Halliwell B, Moore PK, Wong PT (2006) Hydrogen sulfide is a mediator of cerebral ischemic damage. Stroke 37(3): 889-893. doi:10.1161/01.STR.0000204184.34946.41. PubMed: 16439695.
6. 2S is impaired in non-obese diabetic (NOD) mice. Br J Pharmacol 155(5): 673-680. PubMed: 18641671.
7. Baskar R, Li L, Moore PK (2007) Hydrogen sulfide-induces DNA damage and changes in apoptotic gene expression in human lung fibroblast cells. FASEB J 21(1): 247-255. PubMed: 17116745.
8. Olshansky SJ, Perry D, Miller RA, Butler RBN (2006) In pursuit of the longevity dividend. Scientist 20(3): 28-36.
9. Miller DL, Roth MB (2007) Hydrogen sulfide increases thermotolerance and lifespan in Caenorhabditis elegans. Proc Natl Acad Sci U-S-A 104(51): 20618-20622. doi:10.1073/pnas.0710191104. PubMed: 18077331.
10. Vozdek R, Hnízda A, Krijt J, Kostrouchová M, Kožich V (2012) Novel structural arrangement of nematode cystathionine beta-synthases: characterization of Caenorhabditis elegans CBS-1. Biochem J 443(2): 535-547. doi:10.1042/BJ20111478. PubMed: 22240119.
11. Budde MW, Roth MB (2011) The response of Caenorhabditis elegans to hydrogen sulfide and hydrogen cyanide. Genetics 189(2): 521-532. doi:10.1534/genetics.111.129841. PubMed: 21840852.
12. Shen C, Shao Z, Powell-Coffman JA (2006) The Caenorhabditis elegans rhy-1 gene inhibits HIF-1 hypoxia inducible factor activity in a negative feedback loop that does not include vhl-1. Genetics 174(3): 1205-1214. doi:10.1534/genetics.106.063594. PubMed: 16980385.
13. Whiteman M, Li L, Rose P, Tan CH, Parkinson DB et al. (2010) The effect of hydrogen sulfide donors on lipopolysaccharide-induced formation of inflammatory mediators in macrophages. Antioxid Redox Signal 12(10): 1147-1154. doi:10.1089/ars.2009.2899. PubMed: 19769459.
14. Li L, Whiteman M, Guan YY, Neo KL, Cheng Y et al. (2008) Characterization of a novel, water-soluble hydrogen sulfide-releasing molecule (GYY4137): new insights into the biology of hydrogen sulfide. Circulation 117(18): 2351-2360. doi:10.1161/CIRCULATIONAHA.107.753467. PubMed: 18443240.
15. Smith JV, Luo Y (2003) Elevation of oxidative free radicals in Alzheimer's disease models can be attenuated by Ginkgo biloba extract EGb 761. J Alzheimers Dis 5(4): 287-300. PubMed: 14624024.
16. Saul N, Pietsch K, Stürzenbaum SR, Menzel R, Steinberg CEW (2011) The diversity of polyphenol action in C.elegans. J Nat Prod 74(8): 1713-1720. doi:10.1021/np200011a. PubMed: 21805983.
17. Jansen WT, Bolm M, Balling R, Chhatwal GS, Schnabel R (2002) Hydrogen peroxide-mediated killing of Caenorhabditis elegans by Streptococcus pyogenes. Infect Immun 70(9): 5202-5207. doi:10.1128/IAI.70.9.5202-5207.2002. PubMed: 12183571.
18. Lithgow GJ, White TM, Melov S, Johnson TE (1995) Thermotolerance and extended life-span conferred by single-gene mutations and induced by thermal stress. Proc Natl Acad Sci U-S-A 92(16): 7540-7544. doi:10.1073/pnas.92.16.7540. PubMed: 7638227.
19. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25(4): 402-408. doi:10.1006/meth.2001.1262. PubMed: 11846609.
20. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29(9): e45. doi:10.1093/nar/29.9.e45. PubMed: 11328886.
21. 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. PubMed: 7150244.
22. Harada H, Kurauchi M, Hayashi R, Eki T (2007) Shortened lifespan of nematode Caenorhabditis elegans after prolonged exposure to heavy metals and detergents. Ecotoxicol Environ Saf 66(3): 378-383. doi: 10.1016/j.ecoenv.2006. 02.017. PubMed: 16618507.
23. Yu F, Zhao J, Tang CS, Geng B (2010) Effect of synthesized GYY4137, a slowly releasing hydrogen sulfide donor, on cell viability and distribution of hydrogen sulfide in mice. Beijing Da Xue Xue Bao 42(5): 493-497.
24. 2S a novel cytoprotective mediator in the inflamed joint? J Cell Mol Med 16(4): 896-910. doi:10.1111/j.1582-4934.2011.01357.x. PubMed: 21679296.
25. Larsen PL (1993) Aging and resistance to oxidative damage in Caenorhabditis elegans. Proc Natl Acad Sci U-S-A 90(19): 8905-8909. doi:10.1073/pnas.90.19.8905. PubMed: 8415630.
26. Murakami S, Johnson TE (1996) A genetic pathway conferring life extension and resistance to UV stress in Caenorhabditis elegans. Genetics 143(3): 1207-1218. PubMed: 8807294.
27. Gems D, Riddle DL (2000) Defining wild-type life span in Caenorhabditis elegans. J Gerontol A Biol Sci Med Sci 55(5): B215-B219. doi:10.1093/gerona/55. 5.B215. PubMed: 10819307.
28. Li L, Wang Y, Shen W (2012) Roles of hydrogen sulfide and nitric oxide in the alleviation of cadmium-induced oxidative damage in alfalfa seedling roots. Biol-Met 25(3): 617-631. PubMed: 22538639.
29. Miller DL, Budde MW, Roth MB (2011) HIF-1 and SKN-1 coordinate the transcriptional response to hydrogen sulfide in Caenorhabditis elegans. PLOS ONE 6(9): e25476. doi:10.1371/journal.pone.0025476. PubMed: 21980473.
30. Oliveira RP, Porter Abate J, Dilks K, Landis J, Ashraf J et al. (2009) Condition-adapted stress and longevity gene regulation by Caenorhabditis elegans SKN-1/Nrf. Aging Cell 8(5): 524-541. doi: 10.1111/j.1474-9726.2009.00501.x. PubMed: 19575768.
31. Arum O, Johnson TE (2007) Reduced expression of the Caenorhabditis elegans p53 ortholog cep-1 results in increased longevity. J Gerontol A Biol Sci Med Sci 62(9): 951-959. doi:10.1093/gerona/62.9.951. PubMed: 17895432.
32. Cutler RG, Mattson MP (2001) Sphingomyelin and ceramide as regulators of development and lifespan. Mech Ageing Dev 122(9): 895-908. doi:10.1016/S0047- 6374(01)00246-9. PubMed: 11348657.
33. He X, Schuchman EH (2012) Potential role of acid sphingomyelinase in environmental health. Zhong Nan Da Xue Xue Bao Yi Xue Ban 37(2): 109-125. PubMed: 22561428.
34. Chiku T, Padovani D, Zhu W, Singh S, Vitvitsky V et al. (2009) H2S biogenesis by human cystathionine gamma-lyase leads to the novel sulfur metabolites lanthionine and homolanthionine and is responsive to the grade of hyperhomocysteinemia. J Biol Chem 284(17): 11601-11612. PubMed: 19261609.
35. 2S biogenesis via alternative trans-sulfuration reactions. J Biol Chem 284(33): 22457-22466. doi:10.1074/jbc.M109.010868. PubMed: 19531479.
36. Kabil O, Banerjee R (2010) Redox Biochemistry of Hydrogen Sulfide. J Biol Chem 285(29): 21903-21907. doi:10.1074/jbc.R110.128363. PubMed: 20448039.
37. Kabil H, Kabil O, Banerjee R, Harshman LG, Pletcher SD (2011) Increased transsulfuration mediates longevity and dietary restriction in Drosophila. Proc Natl Acad Sci USA, 108(40): 16831-16836. doi: 10.1073/pnas.1102008108. PubMed: 21930912.
38. Jensen KK, Geoghagen NS, Jin L, Holt TG, Luo Q et al. (2011) Pharmacological activation and genetic manipulation of cystathionine beta-synthase alter circulating levels of homocysteine and hydrogen sulfide in mice. Eur J Pharmacol 650(1): 86-93. doi:10.1016/j.ejphar.2010.09.080. PubMed: 20955694.
39. Guzmán MA, Navarro MA, Carnicer R, Sarría AJ, Acín S et al. (2006) Cystathionine β-synthase is essential for female reproductive function. Hum Mol Genet 15(21): 3168-3176. doi:10.1093/hmg/ddl393. PubMed: 16984962.
40. Liang R, Yu WD, Du JB, Yang LJ, Yang JJ et al. (2007) Cystathionine β synthase participates in murine oocyte maturatione mediated by homocysteine. Reprod Toxicol 24(1): 89-96. doi:10.1016/j.reprotox.2007.04.002. PubMed: 17561372.
41. Srilatha B, Hu L, Adaikan GP, Moore PK (2009) Initial characterization of hydrogen sulfide effects in female sexual function. J Sex Med 6(7): 1875-1884. doi:10.1111/j.1743-6109.2009.01291.x. PubMed: 19453900.
42. Carson RJ, Konje JC (2010) Role of hydrogen sulfide in the female reproductive tract. Expet. Rev Obstet Gynecol 5(2): 203-213. doi: 10.1586/eog.10.5.
43. Nuño-Ayala M, Guillén N, Arnal C, Lou-Bonafonte JM, de Martino A et al. (2012) Cystathionine β-synthase deficiency causes infertility by impairing decidualization and gene expression networks in uterus implantation sites. Physiol Genomics 44(14): 702-716. doi:10.1152/ physiolgenomics.00189.2010. PubMed: 22617046.
44. Watanabe M, Osada J, Aratani Y, Kluckman K, Reddick R et al. (1995) Mice deficient in cystathionine beta-synthase: animal models for mild and severe homocyst(e)inemia. Proc Natl Acad Sci U-S-A 92(5): 1585-1589. doi:10.1073/pnas.92.5.1585. PubMed: 7878023.
45. Baumbach GL, Sigmund CD, Bottiglieri T, Lentz SR (2002) Structure of Cerebral Arterioles in Cystathionine β-Synthase-Deficient Mice. Circ Res 91(10): 931-937. doi:10.1161/01.RES.0000041408.64867.1D. PubMed: 12433838.
46. Wang H, Jiang X, Yang F, Gaubatz JW, Ma L et al. (2003) Hyperhomocysteinemia accelerates atherosclerosis in cystathionine β-synthase and apolipoprotein E double knock-out mice with and without dietary perturbation. Blood 101(10): 3901-3907. doi:10.1182/blood-2002-08-2606. PubMed: 12506016.
47. Distrutti E, Mencarelli A, Santucci L, Renga B, Orlandi S et al. (2008) The methionine connection: Homocysteine and hydrogen sulfide exert opposite effects on hepatic microcirculation in rats. Hepatology 47(2): 659-667. PubMed: 18098324.
48. Stocker R, Keaney JF (2004) Role of oxidative modifications in atherosclerosis. Physiol Rev 84(4): 1381-1478. doi:10.1152/physrev.00047.2003. PubMed: 15383655.
49. Lee ZW, Zhou J, Chen CS, Zhao Y, Tan CH et al. (2011) The slow-releasing hydrogen sulfide donor, GYY4137, exhibits novel anti-cancer effects in vitro and in vivo. PLOS ONE 6(6): e21077. doi:10.1371/journal.pone.0021077. PubMed: 21701688.
50. Yang G, Sun X, Wang R (2004) Hydrogen sulfide-induced apoptosis of human aorta smooth muscle cells via the activation of mitogen-activated protein kinases and caspase-3. FASEB J 18(14): 1782-1784. PubMed: 15371330.
51. 2S, endoplasmic reticulum stress, and apoptosis of insulin-secreting beta cells. J Biol Chem 282(22): 16567-16576. doi:10.1074/jbc.M700605200. PubMed: 17430888.
52. 2S-induced pancreatic acinar cell apoptosis is mediated via JNK and p38 MAP kinase. J Cell Mol Med 12(4): 1374-1383. doi:10.1111/j.1582-4934.2008.00318.x. PubMed: 18373739.
53. Zhang JH, Dong Z, Chu L (2010) Hydrogen sulfide induces apoptosis in human periodontium cells. J Periodontal Res 45(1): 71-78. PubMed: 19602114.
54. Perry MM, Hui CK, Whiteman M, Wood ME, Adcock I et al. (2011) Hydrogen sulfide inhibits proliferation and release of IL-8 from human airway smooth muscle cells. Am J Respir Cell Mol Biol 45: 746-752. doi:10.1165/rcmb.2010- 0304OC. PubMed: 21297080.
55. Kimura Y, Kimura H (2004) Hydrogen sulfide protects neurons from oxidative stress. FASEB J 18(10): 1165-1167. PubMed: 15155563.
56. Yan SK, Chang T, Wang H, Wu L, Wang R et al. (2006) Effects of hydrogen sulfide on homocysteine-induced oxidative stress in vascular smooth muscle cells. Biochem Biophys Res Commun 351(2): 485-491. doi:10.1016/j.bbrc.2006.10. 058. PubMed: 17069760.
57. Geng B, Chang L, Pan C, Qi Y, Zhao J et al. (2004) ndogenous hydrogen sulfide regulation of myocardial injury induced by isoproterenol. Biophys Res Comm 318(3), 756-763
58. Bearden SE, Beard RS, Pfau JC (2010) Extracellular transsulfuration generates hydrogen sulfide from homocysteine and protects endothelium from redox stress. Am J Physiol 299(5): H1568-H1576. PubMed: 20817827.
59. Calvert JW, Jha S, Gundewar S, Elrod JW, Ramachandran A et al. (2009) Hydrogen sulfide mediates cardioprotection through Nrf2 signaling. Circ Res 105(4): 365-374. doi:10.1161/CIRCRESAHA.109.199919. PubMed: 19608979.
60. Fisher CD, Augustine LM, Maher JM, Nelson DM, Slitt AL et al. (2007) Induction of drug-metabolizing enzymes by garlic and allyl sulfide compounds via activation of constitutive androstane receptor and nuclear factor E2-related factor 2. Drug Metab Dispos 35(6): 995-1000. doi:10.1124/dmd.106.014340. PubMed: 17353348.