Endogenous hydrogen sulfide production is essential for dietary restriction benefits

Cell

Volumn 160, Issue 1-2, 2015, Pages 132-144

  Hine, Christopher ^a   Harputlugil, Eylul ^a   Zhang, Yue ^a   Ruckenstuhl, Christoph ^c   Lee, Byung Cheon ^b   Brace, Lear ^a   Longchamp, Alban ^a   Treviño Villarreal, Jose H ^a   Mejia, Pedro ^a   Ozaki, C Keith ^a   Wang, Rui ^e   Gladyshev, Vadim N ^b   Madeo, Frank ^c,d   Mair, William B ^a   Mitchell, James R ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

^c UNIVERSITY OF GRAZ   (Austria)

^d BIOTECHMED GRAZ   (Austria)

^e LAKEHEAD UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CYSTATHIONINE GAMMA LYASE; GLUCOSE; HYDROGEN SULFIDE; LEAD SULFIDE; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; MESSENGER RNA; MITOCHONDRIAL PROTEIN; SULFUR AMINO ACID; TRANSCRIPTION FACTOR FOXO; TRANSCRIPTION FACTOR NRF2; TRIACYLGLYCEROL; CYSTEINE; METHIONINE; NFE2L2 PROTEIN, MOUSE; TRANSCRIPTOME;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY COMPOSITION; BODY MASS; BODY WEIGHT; CAENORHABDITIS ELEGANS; CALORIC RESTRICTION; CELL DAMAGE; CELL PROTECTION; CONTROLLED STUDY; DIET RESTRICTION; DROSOPHILA; ENZYME ACTIVITY; FAT MASS; FEMALE; FLUID INTAKE; FOOD INTAKE; GLUCOSE BLOOD LEVEL; HYDRATION; IN VITRO STUDY; IN VIVO STUDY; LIFE EXTENSION; LIVER INJURY; LIVER ISCHEMIA; LIVER PROTECTION; LONGEVITY; MALE; METABOLOMICS; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTAKE; PROTEIN RESTRICTION; RAT; REPERFUSION INJURY; SMOOTH MUSCLE FIBER; STRESS; TRIACYLGLYCEROL BLOOD LEVEL; WEIGHT REDUCTION; ANIMAL; DIET; DROSOPHILA MELANOGASTER; EVOLUTION; GENETICS; INJURIES; KIDNEY; KNOCKOUT MOUSE; LIFE EXPECTANCY; LIVER; METABOLISM; PHYSIOLOGICAL STRESS; PHYSIOLOGY; SIGNAL TRANSDUCTION; VASCULARIZATION; YEAST;

RODENTIA;

ANIMALS; BIOLOGICAL EVOLUTION; CAENORHABDITIS ELEGANS; CALORIC RESTRICTION; CYSTATHIONINE GAMMA-LYASE; CYSTEINE; DIET; DROSOPHILA MELANOGASTER; FEMALE; HYDROGEN SULFIDE; KIDNEY; LIFE EXPECTANCY; LIVER; MALE; METHIONINE; MICE, KNOCKOUT; NF-E2-RELATED FACTOR 2; REPERFUSION INJURY; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL; TRANSCRIPTOME; YEASTS;

EID: 84920995923     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2014.11.048     Document Type: Article

References (52)

1. N.A. Bishop, and L. Guarente Two neurons mediate diet-restriction-induced longevity in C. elegans Nature 447 2007 545 549
2. E. Blackstone, M. Morrison, and M.B. Roth H2S induces a suspended animation-like state in mice Science 308 2005 518
3. F. Cabreiro, C. Au, K.Y. Leung, N. Vergara-Irigaray, H.M. Cochemé, T. Noori, D. Weinkove, E. Schuster, N.D. Greene, and D. Gems Metformin retards aging in C. elegans by altering microbial folate and methionine metabolism Cell 153 2013 228 239
4. E.J. Calabrese, and M.P. Mattson Hormesis provides a generalized quantitative estimate of biological plasticity J. Cell Commun. Signal. 5 2011 25 38
5. J.W. Calvert, W.A. Coetzee, and D.J. Lefer Novel insights into hydrogen sulfide - mediated cytoprotection Antioxid. Redox Signal. 12 2010 1203 1217
6. E. Cuevasanta, A. Denicola, B. Alvarez, and M.N. Möller Solubility and permeation of hydrogen sulfide in lipid membranes PLoS ONE 7 2012 e34562
7. L. Fontana, L. Partridge, and V.D. Longo Extending healthy life span - from yeast to humans Science 328 2010 321 326
8. R.C. Grandison, M.D. Piper, and L. Partridge Amino-acid imbalance explains extension of lifespan by dietary restriction in Drosophila Nature 462 2009 1061 1064
9. E. Harputlugil, C. Hine, D. Vargas, L. Robertson, B.D. Manning, and J.R. Mitchell The TSC complex is required for the benefits of dietary protein restriction on stress resistance in vivo Cell Reports 8 2014 1160 1170
10. T.M. Hildebrandt, and M.K. Grieshaber Three enzymatic activities catalyze the oxidation of sulfide to thiosulfate in mammalian and invertebrate mitochondria FEBS J. 275 2008 3352 3361
11. C.M. Hine, and J.R. Mitchell NRF2 and the phase II response in acute stress resistance induced by dietary restriction J Clin Exp Pathol S4 2012
12. T. Hu, P. Foxworthy, A. Siesky, J.V. Ficorilli, H. Gao, S. Li, M. Christe, T. Ryan, G. Cao, and P. Eacho Hepatic peroxisomal fatty acid beta-oxidation is regulated by liver X receptor alpha Endocrinology 146 2005 5380 5387
13. J.E. Johnson, and F.B. Johnson Methionine restriction activates the retrograde response and confers both stress tolerance and lifespan extension to yeast, mouse and human cells PLoS ONE 9 2014 e97729
14. H. Kabil, O. Kabil, R. Banerjee, L.G. Harshman, and S.D. Pletcher Increased transsulfuration mediates longevity and dietary restriction in Drosophila Proc. Natl. Acad. Sci. USA 108 2011 16831 16836
15. O. Kabil, V. Vitvitsky, P. Xie, and R. Banerjee The quantitative significance of the transsulfuration enzymes for H2S production in murine tissues Antioxid. Redox Signal. 15 2011 363 372
16. K. Kang, M. Zhao, H. Jiang, G. Tan, S. Pan, and X. Sun Role of hydrogen sulfide in hepatic ischemia-reperfusion-induced injury in rats Liver Transpl. 15 2009 1306 1314
17. B. Lakowski, and S. Hekimi The genetics of caloric restriction in Caenorhabditis elegans Proc. Natl. Acad. Sci. USA 95 1998 13091 13096
18. P.B. Lazarow Assay of peroxisomal beta-oxidation of fatty acids Methods Enzymol. 72 1981 315 319
19. J.I. Lee, J.E. Dominy Jr., A.K. Sikalidis, L.L. Hirschberger, W. Wang, and M.H. Stipanuk HepG2/C3A cells respond to cysteine deprivation by induction of the amino acid deprivation/integrated stress response pathway Physiol. Genomics 33 2008 218 229
20. Z.W. Lee, J. Zhou, C.S. Chen, Y. Zhao, C.H. Tan, L. Li, P.K. Moore, and L.W. Deng The slow-releasing hydrogen sulfide donor, GYY4137, exhibits novel anti-cancer effects in vitro and in vivo PLoS ONE 6 2011 e21077
21. B.C. Lee, A. Kaya, S. Ma, G. Kim, M.V. Gerashchenko, S.H. Yim, Z. Hu, L.G. Harshman, and V.N. Gladyshev Methionine restriction extends lifespan of Drosophila melanogaster under conditions of low amino-acid status Nat. Commun. 5 2014 3592
22. M.E. Levine, J.A. Suarez, S. Brandhorst, P. Balasubramanian, C.W. Cheng, F. Madia, L. Fontana, M.G. Mirisola, J. Guevara-Aguirre, and J. Wan Low protein intake is associated with a major reduction in IGF-1, cancer, and overall mortality in the 65 and younger but not older population Cell Metab. 19 2014 407 417
23. M. Liu, D.N. Grigoryev, M.T. Crow, M. Haas, M. Yamamoto, S.P. Reddy, and H. Rabb Transcription factor Nrf2 is protective during ischemic and nephrotoxic acute kidney injury in mice Kidney Int. 76 2009 277 285
24. W. Mair, I. Morantte, A.P. Rodrigues, G. Manning, M. Montminy, R.J. Shaw, and A. Dillin Lifespan extension induced by AMPK and calcineurin is mediated by CRTC-1 and CREB Nature 470 2011 404 408
25. F. Martin, J.M. van Deursen, R.A. Shivdasani, C.W. Jackson, A.G. Troutman, and P.A. Ney Erythroid maturation and globin gene expression in mice with combined deficiency of NF-E2 and nrf-2 Blood 91 1998 3459 3466
26. C.R. Mauro, M. Tao, P. Yu, J.H. Treviño-Villerreal, A. Longchamp, B.S. Kristal, C.K. Ozaki, and J.R. Mitchell Preoperative dietary restriction reduces intimal hyperplasia and protects from ischemia-reperfusion injury J. Vasc. Surg. 2014
27. D.L. Miller, and M.B. Roth Hydrogen sulfide increases thermotolerance and lifespan in Caenorhabditis elegans Proc. Natl. Acad. Sci. USA 104 2007 20618 20622
28. R.A. Miller, G. Buehner, Y. Chang, J.M. Harper, R. Sigler, and M. Smith-Wheelock Methionine-deficient diet extends mouse lifespan, slows immune and lens aging, alters glucose, T4, IGF-I and insulin levels, and increases hepatocyte MIF levels and stress resistance Aging Cell 4 2005 119 125
29. J.R. Mitchell, M. Verweij, K. Brand, M. van de Ven, N. Goemaere, S. van den Engel, T. Chu, F. Forrer, C. Müller, and M. de Jong Short-term dietary restriction and fasting precondition against ischemia reperfusion injury in mice Aging Cell 9 2010 40 53
30. K. Módis, C. Coletta, K. Erdélyi, A. Papapetropoulos, and C. Szabo Intramitochondrial hydrogen sulfide production by 3-mercaptopyruvate sulfurtransferase maintains mitochondrial electron flow and supports cellular bioenergetics FASEB J. 27 2013 601 611
31. G. Muyzer, and A.J. Stams The ecology and biotechnology of sulphate-reducing bacteria Nat. Rev. Microbiol. 6 2008 441 454
32. K.R. Olson, E.R. Deleon, Y. Gao, K. Hurley, V. Sadauskas, C. Batz, and G.F. Stoy Thiosulfate: a readily accessible source of hydrogen sulfide in oxygen sensing Am. J. Physiol. Regul. Integr. Comp. Physiol. 305 2013 R592 R603
33. N. Orentreich, J.R. Matias, A. DeFelice, and J.A. Zimmerman Low methionine ingestion by rats extends life span J. Nutr. 123 1993 269 274
34. B.D. Paul, and S.H. Snyder HS signalling through protein sulfhydration and beyond Nat. Rev. Mol. Cell Biol. 13 2012 499 507
35. K.J. Pearson, K.N. Lewis, N.L. Price, J.W. Chang, E. Perez, M.V. Cascajo, K.L. Tamashiro, S. Poosala, A. Csiszar, and Z. Ungvari Nrf2 mediates cancer protection but not prolongevity induced by caloric restriction Proc. Natl. Acad. Sci. USA 105 2008 2325 2330
36. W. Peng, L. Robertson, J. Gallinetti, P. Mejia, S. Vose, A. Charlip, T. Chu, and J.R. Mitchell Surgical stress resistance induced by single amino Acid deprivation requires gcn2 in mice Sci. Transl. Med. 4 2012 118ra111
37. B.L. Predmore, M.J. Alendy, K.I. Ahmed, C. Leeuwenburgh, and D. Julian The hydrogen sulfide signaling system: changes during aging and the benefits of caloric restriction Age (Dordr.) 32 2010 467 481
38. M. Ristow, and S. Schmeisser Extending life span by increasing oxidative stress Free Radic. Biol. Med. 51 2011 327 336
39. C. Ruckenstuhl, C. Netzberger, I. Entfellner, D. Carmona-Gutierrez, T. Kickenweiz, S. Stekovic, C. Gleixner, C. Schmid, L. Klug, and A.G. Sorgo Lifespan extension by methionine restriction requires autophagy-dependent vacuolar acidification PLoS Genet. 10 2014 e1004347
40. D.A. Sinclair Toward a unified theory of caloric restriction and longevity regulation Mech. Ageing Dev. 126 2005 987 1002
41. M.H. Stipanuk, and I. Ueki Dealing with methionine/homocysteine sulfur: cysteine metabolism to taurine and inorganic sulfur J. Inherit. Metab. Dis. 34 2011 17 32
42. P.C. Tapia Sublethal mitochondrial stress with an attendant stoichiometric augmentation of reactive oxygen species may precipitate many of the beneficial alterations in cellular physiology produced by caloric restriction, intermittent fasting, exercise and dietary phytonutrients: "Mitohormesis" for health and vitality Med. Hypotheses 66 2006 832 843
43. U. Theissen, M. Hoffmeister, M. Grieshaber, and W. Martin Single eubacterial origin of eukaryotic sulfide:quinone oxidoreductase, a mitochondrial enzyme conserved from the early evolution of eukaryotes during anoxic and sulfidic times Mol. Biol. Evol. 20 2003 1564 1574
44. A.M. Troen, E.E. French, J.F. Roberts, J. Selhub, J.M. Ordovas, L.D. Parnell, and C.Q. Lai Lifespan modification by glucose and methionine in Drosophila melanogaster fed a chemically defined diet Age (Dordr.) 29 2007 29 39
45. K. Varendi, M. Airavaara, J. Anttila, S. Vose, A. Planken, M. Saarma, J.R. Mitchell, and J.O. Andressoo Short-term preoperative dietary restriction is neuroprotective in a rat focal stroke model PLoS ONE 9 2014 e93911
46. Z. Wu, S.Q. Liu, and D. Huang Dietary restriction depends on nutrient composition to extend chronological lifespan in budding yeast Saccharomyces cerevisiae PLoS ONE 8 2013 e64448
47. S.K. Yan, T. Chang, H. Wang, L. Wu, R. Wang, and Q.H. Meng Effects of hydrogen sulfide on homocysteine-induced oxidative stress in vascular smooth muscle cells Biochem. Biophys. Res. Commun. 351 2006 485 491
48. G. Yang, L. Wu, B. Jiang, W. Yang, J. Qi, K. Cao, Q. Meng, A.K. Mustafa, W. Mu, and S. Zhang H2S as a physiologic vasorelaxant: hypertension in mice with deletion of cystathionine gamma-lyase Science 322 2008 587 590
49. Y. Zhang, Z.H. Tang, Z. Ren, S.L. Qu, M.H. Liu, L.S. Liu, and Z.S. Jiang Hydrogen sulfide, the next potent preventive and therapeutic agent in aging and age-associated diseases Mol. Cell. Biol. 33 2013 1104 1113
50. K.G. Calfee-Mason, B.T. Spear, and H.P. Glauert Vitamin E inhibits hepatic NF-kappaB activation in rats administered the hepatic tumor promoter, phenobarbital J. Nutr. 132 2002 3178 3185
51. Y. Ergul, T. Erkan, H. Uzun, H. Genc, T. Altug, and E. Erginoz Effect of vitamin C on oxidative liver injury due to isoniazid in rats Pediatr. Int. 52 2010 69 74
52. S.E. Parnell, K.K. Sulik, D.B. Dehart, and S.Y. Chen Reduction of ethanol-induced ocular abnormalities in mice through dietary administration of N-acetylcysteine Alcohol 44 2010 699 705