Hydrogen sulfide restores a normal morphological phenotype in Werner syndrome fibroblasts, attenuates oxidative damage and modulates mTOR pathway

Pharmacological Research

Volumn 74, Issue , 2013, Pages 34-44

  Talaei, F ^a   Van Praag, V M ^a   Henning, R H ^a  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

Author keywords

Aging; Autophagy; mTOR; NaHS; Progeria; Proteostasis; Werner protein

Indexed keywords

BETA GALACTOSIDASE; COLLAGEN; CYSTATHIONINE BETA SYNTHASE; CYSTATHIONINE GAMMA LYASE; FIBRONECTIN; HISTONE DEACETYLASE 3; HYDROGEN SULFIDE; LAMIN A; LAMIN C; MAMMALIAN TARGET OF RAPAMYCIN; PHOSPHO S6 RIBOSOMAL PROTEIN; PROTEIN KINASE B; PROTEIN S6; RAPAMYCIN; SENESCENCE ASSOCIATED BETA GALACTOSIDASE; SERINE; SIRTUIN 1; UNCLASSIFIED DRUG;

ADULT; ANTIOXIDANT ACTIVITY; ARTICLE; AUTOPHAGY; CANCER CELL CULTURE; CELL AGGREGATION; CELL DEATH; CELL DESTRUCTION; CELL PROTECTION; CELL STRUCTURE; CHEMICAL MODIFICATION; CONTROLLED STUDY; DRUG ACTIVITY; FEMALE; HUMAN; HUMAN CELL; MALE; MICROSCOPY; OXIDATIVE STRESS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN EXPRESSION; PROTEIN HOMEOSTASIS; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; SENESCENCE; SIGNAL TRANSDUCTION; SKIN FIBROBLAST; SULFURATION; WERNER SYNDROME;

AGING; AUTOPHAGY; MTOR; NAHS; PROGERIA; PROTEOSTASIS; WERNER PROTEIN;

ADOLESCENT; ADULT; BETA-GALACTOSIDASE; CASPASE 3; CASPASE 7; CELL LINE; FEMALE; FIBROBLASTS; HUMANS; HYDROGEN SULFIDE; MALE; MIDDLE AGED; OXIDATIVE STRESS; PHENOTYPE; REACTIVE OXYGEN SPECIES; TOR SERINE-THREONINE KINASES; WERNER SYNDROME; YOUNG ADULT;

EID: 84884797294     PISSN: 10436618     EISSN: 10961186     Source Type: Journal    
DOI: 10.1016/j.phrs.2013.04.011     Document Type: Article

References (71)

1. S.J. Thannhauser Werner's syndrome (progeria of the adult) and Rothmund's syndrome: two types of closely related heredofamilial atrophic dermatoses with juvenile cataracts and endocrine features; a critical study with five new cases. S.J. Tannhauser. Reprinted from Annals of Internal Medicine, 23:559 (1945) Advances in Experimental Medicine and Biology 190 1985 15 56
2. M. Goto, R.W. Miller, Y. Ishikawa, and H. Sugano Excess of rare cancers in Werner syndrome (adult progeria) Cancer Epidemiology, Biomarkers and Prevention 5 1996 239 246
3. C.E. Yu, J. Oshima, Y.H. Fu, E.M. Wijsman, F. Hisama, and R. Alisch Positional cloning of the Werner's syndrome gene Science 272 1996 258 262 (Pubitemid 26119137)
4. R.M. Brosh Jr., J.K. Karow, E.J. White, N.D. Shaw, I.D. Hickson, and V.A. Bohr Potent inhibition of Werner and bloom helicases by DNA minor groove binding drugs Nucleic Acids Research 28 2000 2420 2430 (Pubitemid 30349049)
5. A.S. Multani, and S. Chang WRN at telomeres: implications for aging and cancer Journal of Cell Science 120 2007 713 721 (Pubitemid 46523473)
6. G.P. Dimri, X. Lee, G. Basile, M. Acosta, G. Scott, and C. Roskelley A biomarker that identifies senescent human cells in culture and in aging skin in vivo Proceedings of the National Academy of Sciences of the United States of America 92 1995 9363 9367
7. F.J. Mao, J.M. Sidorova, J.M. Lauper, M.J. Emond, and R.J. Monnat The human WRN and BLM RecQ helicases differentially regulate cell proliferation and survival after chemotherapeutic DNA damage Cancer Research 70 2010 6548 6555
8. L. Crabbe, A. Jauch, C.M. Naeger, H. Holtgreve-Grez, and J. Karlseder Telomere dysfunction as a cause of genomic instability in Werner syndrome Proceedings of the National Academy of Sciences of the United States of America 104 2007 2205 2210 (Pubitemid 46391376)
9. S. Chang, A.S. Multani, N.G. Cabrera, M.L. Naylor, P. Laud, and D. Lombard Essential role of limiting telomeres in the pathogenesis of Werner syndrome Nature Genetics 36 2004 877 882 (Pubitemid 39014107)
10. D.B. Lombard, C. Beard, B. Johnson, R.A. Marciniak, J. Dausman, and R. Bronson Mutations in the WRN gene in mice accelerate mortality in a p53-null background Molecular and Cellular Biology 20 2000 3286 3291 (Pubitemid 30215040)
11. J. Tyedmers, A. Mogk, and B. Bukau Cellular strategies for controlling protein aggregation Nature Reviews Molecular Cell Biology 11 2010 777 788
12. C. Soto Unfolding the role of protein misfolding in neurodegenerative diseases Nature Reviews Neuroscience 4 2003 49 60 (Pubitemid 37271088)
13. F. Talaei Aberrations in proteostasis orchestrate: the genotypic and phenotypic changes in aging American Journal of Molecular and Cellular Biology 1 2012 1 16
14. C.N. Oliver, B.W. Ahn, E.J. Moerman, S. Goldstein, and E.R. Stadtman Age-related changes in oxidized proteins Journal of Biological Chemistry 262 1987 5488 5491 (Pubitemid 17104155)
15. H. Mirzaei, and F. Regnier Protein: protein aggregation induced by protein oxidation Journal of Chromatography B: Analytical Technologies in the Biomedical and Life Sciences 873 2008 8 14
16. B. Friguet Oxidized protein degradation and repair in ageing and oxidative stress FEBS Letters 580 2006 2910 2916 (Pubitemid 43729157)
17. N. Ticozzi, A. Ratti, and V. Silani Protein aggregation and defective RNA metabolism as mechanisms for motor neuron damage CNS and Neurological Disorders Drug Targets 9 2010 285 296
18. A.B. Lindner, and A. Demarez Protein aggregation as a paradigm of aging Biochimica et Biophysica Acta 1790 2009 980 996
19. C. Von Kobbe, A. May, C. Grandori, and V.A. Bohr Werner syndrome cells escape hydrogen peroxide-induced cell proliferation arrest FASEB Journal 18 2004 1970 1972 (Pubitemid 39602301)
20. K. Arioshi, K. Suzuki, M. Goto, M. Watanabe, and S. Kodama Increased chromosome instability and accumulation of DNA double-strand breaks in Werner syndrome cells Journal of Radiation Research 48 2007 219 231 (Pubitemid 46884356)
21. R.G. Faragher, I.R. Kill, J.A. Hunter, F.M. Pope, C. Tannock, and S. Shall The gene responsible for Werner syndrome may be a cell division "counting" gene Proceedings of the National Academy of Sciences of the United States of America 90 1993 12030 12034 (Pubitemid 24008774)
22. K. Yang, J. Kwon, J. Rhim, J. Choi, S. Kim, and S. Lee Differential expression of extracellular matrix proteins in senescent and young human fibroblasts: a comparative proteomics and microarray study Molecules and Cells 32 2011 99 106
23. M. Goto Hierarchical deterioration of body systems in Werner's syndrome: implications for normal ageing Mechanisms of Ageing and Development 98 1997 239 254 (Pubitemid 27466061)
24. D. Yonezawa, F. Sekiguchi, M. Miyamoto, E. Taniguchi, M. Honjo, and T. Masuko A protective role of hydrogen sulfide against oxidative stress in rat gastric mucosal epithelium Toxicology 241 2007 11 18 (Pubitemid 47599777)
25. Y. Kimura, and H. Kimura Hydrogen sulfide protects neurons from oxidative stress FASEB Journal 18 2004 1165 1167 (Pubitemid 39561558)
26. H.J. Lee, M.M. Mariappan, D. Feliers, R.C. Cavaglieri, K. Sataranatarajan, and H.E. Abboud Hydrogen sulfide inhibits high glucose-induced matrix protein synthesis by activating AMP-activated protein kinase in renal epithelial cells Journal of Biological Chemistry 287 2012 4451 4461
27. K.G. Foster, and D.C. Fingar Mammalian target of rapamycin (mTOR): conducting the cellular signaling symphony Journal of Biological Chemistry 285 2010 14071 14077
28. E.A. Dunlop, and A.R. Tee Mammalian target of rapamycin complex 1: signalling inputs, substrates and feedback mechanisms Cellular Signalling 21 2009 827 835
29. D.A. Lee, E. Assoku, and V. Doyle A specific quantitative assay for collagen synthesis by cells seeded in collagen-based biomaterials using sirius red F3B precipitation Journal of Materials Science Materials in Medicine 9 1998 47 51 (Pubitemid 28031771)
30. F. Talaei, M.N. Hylkema, H.R. Bouma, A.S. Boerema, A.M. Strijkstra, and R.H. Henning Reversible remodeling of lung tissue during hibernation in the Syrian hamster Journal of Experimental Biology 214 2011 1276 1282
31. G. Marino, and C. Lopez-Otin Autophagy and aging: new lessons from progeroid mice Autophagy 4 2008 807 809
32. N. Mizushima, A. Yamamoto, M. Matsui, T. Yoshimori, and Y. Ohsumi In vivo analysis of autophagy in response to nutrient starvation using transgenic mice expressing a fluorescent autophagosome marker Molecular Biology of the Cell 15 2004 1101 1111 (Pubitemid 38316219)
33. R. Zoncu, A. Efeyan, and D.M. Sabatini mTOR: from growth signal integration to cancer, diabetes and ageing Nature Reviews Molecular Cell Biology 12 2011 21 35
34. C. Adelfalk, H. Scherthan, M. Hirsch-Kauffmann, and M. Schweiger Nuclear deformation characterizes Werner syndrome cells Cell Biology International 29 2005 1032 1037 (Pubitemid 41739828)
35. R.V. Turaga, E.R. Paquet, M. Sild, J. Vignard, C. Garand, and F.B. Johnson The Werner syndrome protein affects the expression of genes involved in adipogenesis and inflammation in addition to cell cycle and DNA damage responses Cell Cycle 8 2009 2080 2092
36. J. Huang, Q. Gan, L. Han, J. Li, H. Zhang, and Y. Sun SIRT1 overexpression antagonizes cellular senescence with activated ERK/S6k1 signaling in human diploid fibroblasts PLoS ONE 3 2008 e1710
37. X. Zeng, and T.J. Kinsella Mammalian target of rapamycin and S6 kinase 1 positively regulate 6-thioguanine-induced autophagy Cancer Research 68 2008 2384 2390 (Pubitemid 351521813)
38. M. Ogata, S. Hino, A. Saito, K. Morikawa, S. Kondo, and S. Kanemoto Autophagy is activated for cell survival after endoplasmic reticulum stress Molecular and Cellular Biology 26 2006 9220 9231 (Pubitemid 44904418)
39. R. Scherz-Shouval, and Z. Elazar Regulation of autophagy by ROS: physiology and pathology Trends in Biochemical Sciences 36 2011 30 38
40. S.V. Avery Molecular targets of oxidative stress Biochemical Journal 434 2011 201 210
41. M.A. Arslan, M. Chikina, P. Csermely, and C. Soti Misfolded proteins inhibit proliferation and promote stress-induced death in SV40-transformed mammalian cells FASEB Journal 26 2012 766 777
42. C.G. Proud mTORC1 signalling and mRNA translation Biochemical Society Transactions 37 2009 227 231
43. M.V. Blagosklonny Progeria, rapamycin and normal aging: recent breakthrough Aging (Albany NY) 3 2011 685 691
44. J.H. Reiling, and D.M. Sabatini Increased mTORC1 signaling UPRegulates stress Molecular Cell 29 2008 533 535 (Pubitemid 351374689)
45. B. Bilanges, and B. Vanhaesebroeck A new tool to dissect the function of p70 S6 kinase Biochemical Journal 431 2010 e1 e3
46. A. Hahn-Windgassen, V. Nogueira, C.C. Chen, J.E. Skeen, N. Sonenberg, and N. Hay Akt activates the mammalian target of rapamycin by regulating cellular ATP level and AMPK activity Journal of Biological Chemistry 280 2005 32081 32089 (Pubitemid 41361813)
47. K. Cao, J.J. Graziotto, C.D. Blair, J.R. Mazzulli, M.R. Erdos, and D. Krainc Rapamycin reverses cellular phenotypes and enhances mutant protein clearance in Hutchinson-Gilford progeria syndrome cells Science Translational Medicine 3 2011 89ra58
48. J.J. Graziotto, K. Cao, F.S. Collins, and D. Krainc Rapamycin activates autophagy in Hutchinson-Gilford progeria syndrome: implications for normal aging and age-dependent neurodegenerative disorders Autophagy 8 2012 147 151
49. H. Saito, and R.E. Moses Immortalization of Werner syndrome and progeria fibroblasts Experimental Cell Research 192 1991 373 379 (Pubitemid 121006952)
50. S. Kanvah, and G.B. Schuster Long-range oxidative damage to DNA: protection of guanines by a nonspecifically bound disulfide Journal of the American Chemical Society 124 2002 11286 11287
51. C. Szabo Hydrogen sulphide and its therapeutic potential Nature Reviews Drug Discovery 6 2007 917 935 (Pubitemid 350042399)
52. P. Mungli, M.S. Shetty, P. Tilak, and N. Anwar Total thiols: biomedical importance and their alteration in various disorders Online Journal of Health and Allied Sciences 8 2009 1 6
53. M. Sivonova, Z. Tatarkova, Z. Durackova, D. Dobrota, J. Lehotsky, and T. Matakova Relationship between antioxidant potential and oxidative damage to lipids, proteins and DNA in aged rats Physiological Research 56 2007 757 764
54. M. Goto, and Y. Kato Hypercoagulable state indicates an additional risk factor for atherosclerosis in Werner's syndrome Thrombosis and Haemostasis 73 1995 576 578
55. Y. Wang, X. Zhao, H. Jin, H. Wei, W. Li, and D. Bu Role of hydrogen sulfide in the development of atherosclerotic lesions in apolipoprotein E knockout mice Arteriosclerosis, Thrombosis, and Vascular Biology 29 2009 173 179
56. N. Mizushima, and T. Yoshimori How to interpret LC3 immunoblotting Autophagy 3 2007 542 545 (Pubitemid 350060049)
57. S. Ikeyama, G. Kokkonen, S. Shack, X.T. Wang, and N.J. Holbrook Loss in oxidative stress tolerance with aging linked to reduced extracellular signal-regulated kinase and Akt kinase activities FASEB Journal 16 1 2002 114 116 Epub 2001 Nov 14
58. N. Xu, N. Hegarat, E.J. Black, M.T. Scott, H. Hochegger, and D.A. Gillespie Akt/PKB suppresses DNA damage processing and checkpoint activation in late G2 Journal of Cell Biology 190 2010 297 305
59. A. Salminen, and K. Kaarniranta Regulation of the aging process by autophagy Trends in Molecular Medicine 15 2009 217 224
60. A. Salminen, and K. Kaarniranta SIRT1: regulation of longevity via autophagy Cellular Signalling 21 2009 1356 1360
61. H.S. Ghosh, M. McBurney, and P.D. Robbins SIRT1 negatively regulates the mammalian target of rapamycin PLoS ONE 5 2010 e9199
62. R.H. Wang, H.S. Kim, C. Xiao, X. Xu, O. Gavrilova, and C.X. Deng Hepatic Sirt1 deficiency in mice impairs mTorc2/Akt signaling and results in hyperglycemia, oxidative damage, and insulin resistance Journal of Clinical Investigation 121 2011 4477 4490
63. B. Geng, L. Chang, C. Pan, Y. Qi, J. Zhao, and Y. Pang Endogenous hydrogen sulfide regulation of myocardial injury induced by isoproterenol Biochemical and Biophysical Research Communications 318 2004 756 763 (Pubitemid 38624219)
64. M. Whiteman, J.S. Armstrong, S.H. Chu, S. Jia-Ling, B.S. Wong, and N.S. Cheung The novel neuromodulator hydrogen sulfide: an endogenous peroxynitrite 'scavenger'? Journal of Neurochemistry 90 2004 765 768 (Pubitemid 38989409)
65. 2S signals through protein S-sulfhydration Science Signaling 2 2009 ra72
66. G. Kashino, S. Kodama, Y. Nakayama, K. Suzuki, K. Fukase, and M. Goto Relief of oxidative stress by ascorbic acid delays cellular senescence of normal human and Werner syndrome fibroblast cells Free Radical Biology and Medicine 35 2003 438 443 (Pubitemid 37289173)
67. 2S induces a suspended animation-like state in mice Science 308 2005 518 (Pubitemid 40570576)
68. A.J. Meijer, and P. Codogno Nutrient sensing: TOR's Ragtime Nature Cell Biology 10 2008 881 883
69. C. Yang, Z. Yang, M. Zhang, Q. Dong, X. Wang, and A. Lan Hydrogen sulfide protects against chemical hypoxia-induced cytotoxicity and inflammation in HaCaT cells through inhibition of ROS/NF-kappaB/COX-2 pathway PLoS ONE 6 2011 e21971
70. R. Tamizhselvi, J. Sun, Y.H. Koh, and M. Bhatia Effect of hydrogen sulfide on the phosphatidylinositol 3-kinase-protein kinase B pathway and on caerulein-induced cytokine production in isolated mouse pancreatic acinar cells Journal of Pharmacology and Experimental Therapeutics 329 2009 1166 1177
71. 2S formation in reversible remodeling of lung tissue during hibernation in the Syrian hamster Journal of Experimental Biology 215 2012 2912 2919