Hydrogen sulfide maintains mesenchymal stem cell function and bone homeostasis via regulation of Ca2+ channel sulfhydration

Cell Stem Cell

Volumn 15, Issue 1, 2014, Pages 66-78

  Liu, Yi ^a,b   Yang, Ruili ^a   Liu, Xibao ^c   Zhou, Yu ^d   Qu, Cunye ^a   Kikuiri, Takashi ^a   Wang, Songlin ^b   Zandi, Ebrahim ^d   Du, Junbao ^e   Ambudkar, Indu S ^c   Shi, Songtao ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b CAPITAL MEDICAL UNIVERSITY   (China)

^c NATIONAL INSTITUTE OF DENTAL AND CRANIOFACIAL RESEARCH   (United States)

^d UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^e PEKING UNIVERSITY FIRST HOSPITAL   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; CALCIUM; CALCIUM CHANNEL; CYSTEINE; HYDROGEN SULFIDE; TRANSIENT RECEPTOR POTENTIAL CHANNEL; WNT PROTEIN; ALKALINE PHOSPHATASE; DITHIOTHREITOL; HYDROXYLAMINE; LIPOPROTEIN LIPASE; MITOGEN ACTIVATED PROTEIN KINASE; OSTEOCALCIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA 2; SMALL INTERFERING RNA; THIOL DERIVATIVE; TRANSCRIPTION FACTOR RUNX2; TRANSIENT RECEPTOR POTENTIAL CHANNEL M4; VANILLOID RECEPTOR 3; VANILLOID RECEPTOR 6; 3-MERCAPTOPYRUVATE SULPHURTRANSFERASE; AMINOTRANSFERASE; CALCIUM CHANNEL T TYPE; CYSTATHIONINE BETA SYNTHASE; CYSTEINE AMINOTRANSFERASE; PROTEIN KINASE C; SULFURTRANSFERASE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BONE; BONE DENSITY; BONE DEVELOPMENT; BONE MARROW; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CELL DIFFERENTIATION; CELL RENEWAL; FEMALE; HOMEOSTASIS; HUMAN; HUMAN CELL; HUMAN TISSUE; MESENCHYMAL STEM CELL; NONHUMAN; OSTEOPOROSIS; PHENOTYPE; PRIORITY JOURNAL; WNT SIGNALING PATHWAY; ANIMAL EXPERIMENT; ANIMAL MODEL; BONE MARROW DERIVED MESENCHYMAL STEM CELL; BONE MASS; BONE REGENERATION; CELL FUNCTION; CELL PROLIFERATION; CELL VIABILITY; CONTROLLED STUDY; DISULFIDE BOND; DOWN REGULATION; FLOW CYTOMETRY; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; MOUSE; OSSIFICATION; OSTEOBLAST; OSTEOPENIA; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; UPREGULATION; WESTERN BLOTTING; ANIMAL; BONE MARROW CELL; CALCIUM SIGNALING; CELL CULTURE; CHEMISTRY; GENETICS; KNOCKOUT MOUSE; MESENCHYMAL STROMA CELL; METABOLISM; PATHOLOGY; PHYSIOLOGY;

MAMMALIA; MUS;

ANIMALS; BETA CATENIN; BONE MARROW CELLS; CALCIUM CHANNELS, T-TYPE; CALCIUM SIGNALING; CELL DIFFERENTIATION; CELLS, CULTURED; CYSTATHIONINE BETA-SYNTHASE; HOMEOSTASIS; HUMANS; HYDROGEN SULFIDE; MESENCHYMAL STROMAL CELLS; MICE; MICE, KNOCKOUT; OSTEOGENESIS; OSTEOPOROSIS; PROTEIN KINASE C; RNA, SMALL INTERFERING; SULFURTRANSFERASES; TRANSAMINASES;

EID: 84904042269     PISSN: 19345909     EISSN: 18759777     Source Type: Journal    
DOI: 10.1016/j.stem.2014.03.005     Document Type: Article

References (50)

1. K. Abe, and H. Kimura The possible role of hydrogen sulfide as an endogenous neuromodulator J. Neurosci. 16 1996 1066 1071
2. L. Bao, C. Vlcek, V. Paces, and J.P. Kraus Identification and tissue distribution of human cystathionine beta-synthase mRNA isoforms Arch. Biochem. Biophys. 350 1998 95 103
3. G. Bukovska, V. Kery, and J.P. Kraus Expression of human cystathionine beta-synthase in Escherichia coli: purification and characterization Protein Expr. Purif. 5 1994 442 448
4. R. Carmel, K.H. Lau, D.J. Baylink, S. Saxena, and F.R. Singer Cobalamin and osteoblast-specific proteins N. Engl. J. Med. 319 1988 70 75
5. S. Chen, H.A. Hartmann, and G.E. Kirsch Cysteine mapping in the ion selectivity and toxin binding region of the cardiac Na+ channel pore J. Membr. Biol. 155 1997 11 25
6. W.W. Cleland Dithiothreitol, a New Protective Reagent for Sh Groups Biochemistry 3 1964 480 482
7. R.A. Dhonukshe-Rutten, S.M. Pluijm, L.C. de Groot, P. Lips, J.H. Smit, and W.A. van Staveren Homocysteine and vitamin B12 status relate to bone turnover markers, broadband ultrasound attenuation, and fractures in healthy elderly people J. Bone Miner. Res. 20 2005 921 929
8. E. Distrutti Hydrogen sulphide and pain Inflamm. Allergy Drug Targets 10 2011 123 132
9. L.M. Donovan, M.W. Moore, C.B. Gillombardo, S. Chai, and K.P. Strohl Effects of hydrogen sulfide synthesis inhibitors on posthypoxic ventilatory behavior in the C57BL/6J mouse Respiration 82 2011 522 529
10. G.L. Ellman Tissue sulfhydryl groups Arch. Biochem. Biophys. 82 1959 70 77
11. P.F. Erickson, I.H. Maxwell, L.J. Su, M. Baumann, and L.M. Glode Sequence of cDNA for rat cystathionine gamma-lyase and comparison of deduced amino acid sequence with related Escherichia coli enzymes Biochem. J. 269 1990 335 340
12. S. Fiorucci, E. Antonelli, A. Mencarelli, S. Orlandi, B. Renga, G. Rizzo, E. Distrutti, V. Shah, and A. Morelli The third gas: H2S regulates perfusion pressure in both the isolated and perfused normal rat liver and in cirrhosis Hepatology 42 2005 539 548
13. A.J. Friedenstein, R.K. Chailakhyan, N.V. Latsinik, A.F. Panasyuk, and I.V. Keiliss-Borok Stromal cells responsible for transferring the microenvironment of the hemopoietic tissues. Cloning in vitro and retransplantation in vivo Transplantation 17 1974 331 340
14. M. Gaustadnes, N. Rüdiger, K. Rasmussen, and J. Ingerslev Intermediate and severe hyperhomocysteinemia with thrombosis: a study of genetic determinants Thromb. Haemost. 83 2000 554 558
15. V. Gil, D. Gallego, and M. Jiménez Effects of inhibitors of hydrogen sulphide synthesis on rat colonic motility Br. J. Pharmacol. 164 2b 2011 485 498
16. C.G. Gjesdal, S.E. Vollset, P.M. Ueland, H. Refsum, H.E. Meyer, and G.S. Tell Plasma homocysteine, folate, and vitamin B 12 and the risk of hip fracture: the hordaland homocysteine study J. Bone Miner. Res. 22 2007 747 756
17. M. Herrmann, T. Widmann, G. Colaianni, S. Colucci, A. Zallone, and W. Herrmann Increased osteoclast activity in the presence of increased homocysteine concentrations Clin. Chem. 51 2005 2348 2353
18. M. Herrmann, N. Umanskaya, B. Wildemann, G. Colaianni, J. Schmidt, T. Widmann, A. Zallone, and W. Herrmann Accumulation of homocysteine by decreasing concentrations of folate, vitamin B12 and B6 does not influence the activity of human osteoblasts in vitro Clin. Chim. Acta 384 2007 129 134
19. M. Herrmann, N. Umanskaya, B. Wildemann, G. Colaianni, T. Widmann, A. Zallone, and W. Herrmann Stimulation of osteoblast activity by homocysteine J. Cell. Mol. Med. 12 2008 1205 1210
20. P.J. Kelly, K.L. Furie, J.P. Kistler, M. Barron, E.H. Picard, R. Mandell, and V.E. Shih Stroke in young patients with hyperhomocysteinemia due to cystathionine beta-synthase deficiency Neurology 60 2003 275 279
21. L.A. Kluijtmans, G.H. Boers, J.P. Kraus, L.P. van den Heuvel, J.R. Cruysberg, F.J. Trijbels, and H.J. Blom The molecular basis of cystathionine beta-synthase deficiency in Dutch patients with homocystinuria: effect of CBS genotype on biochemical and clinical phenotype and on response to treatment Am. J. Hum. Genet. 65 1999 59 67
22. J.M. Koh, Y.S. Lee, Y.S. Kim, D.J. Kim, H.H. Kim, J.Y. Park, K.U. Lee, and G.S. Kim Homocysteine enhances bone resorption by stimulation of osteoclast formation and activity through increased intracellular ROS generation J. Bone Miner. Res. 21 2006 1003 1011
23. N.S. Kosower, E.M. Kosower, B. Wertheim, and W.S. Correa Diamide, a new reagent for the intracellular oxidation of glutathione to the disulfide Biochem. Biophys. Res. Commun. 37 1969 593 596
24. N. Krishnan, C. Fu, D.J. Pappin, and N.K. Tonks H2S-Induced sulfhydration of the phosphatase PTP1B and its role in the endoplasmic reticulum stress response Sci. Signal. 4 2011 ra86
25. L. Li, M. Bhatia, Y.Z. Zhu, Y.C. Zhu, R.D. Ramnath, Z.J. Wang, F.B. Anuar, M. Whiteman, M. Salto-Tellez, and P.K. Moore Hydrogen sulfide is a novel mediator of lipopolysaccharide-induced inflammation in the mouse FASEB J. 19 2005 1196 1198
26. L. Li, M. Bhatia, and P.K. Moore Hydrogen sulphide - a novel mediator of inflammation? Curr. Opin. Pharmacol. 6 2006 125 129
27. L. Li, P. Rose, and P.K. Moore Hydrogen sulfide and cell signaling Annu. Rev. Pharmacol. Toxicol. 51 2011 169 187
28. C. Löf, P. Sukumaran, T. Viitanen, M. Vainio, K. Kemppainen, I. Pulli, J. Näsman, J.P. Kukkonen, and K. Törnquist Communication between the calcium and cAMP pathways regulate the expression of the TSH receptor: TRPC2 in the center of action Mol. Endocrinol. 26 2012 2046 2057
29. K.N. Maclean, M. Gaustadnes, J. Oliveriusová, M. Janosík, E. Kraus, V. Kozich, V. Kery, F. Skovby, N. Rüdiger, and J. Ingerslev et al. High homocysteine and thrombosis without connective tissue disorders are associated with a novel class of cystathionine beta-synthase (CBS) mutations Hum. Mutat. 19 2002 641 655
30. D. Mancardi, C. Penna, A. Merlino, P. Del Soldato, D.A. Wink, and P. Pagliaro Physiological and pharmacological features of the novel gasotransmitter: hydrogen sulfide Biochim. Biophys. Acta 1787 2009 864 872
31. R.R. McLean, P.F. Jacques, J. Selhub, K.L. Tucker, E.J. Samelson, K.E. Broe, M.T. Hannan, L.A. Cupples, and D.P. Kiel Homocysteine as a predictive factor for hip fracture in older persons N. Engl. J. Med. 350 2004 2042 2049
32. L.J. Melton 3rd Adverse outcomes of osteoporotic fractures in the general population J. Bone Miner. Res. 18 2003 1139 1141
33. E.W. Miles, and J.P. Kraus Cystathionine beta-synthase: structure, function, regulation, and location of homocystinuria-causing mutations J. Biol. Chem. 279 2004 29871 29874
34. H. Ogawa, K. Takahashi, S. Miura, T. Imagawa, S. Saito, M. Tominaga, and T. Ohta H(2)S functions as a nociceptive messenger through transient receptor potential ankyrin 1 (TRPA1) activation Neuroscience 218 2012 335 343
35. K.R. Olson, and J.A. Donald Nervous control of circulation - the role of gasotransmitters, NO, CO, and H2S Acta Histochem. 111 2009 244 256
36. M.F. Pittenger, A.M. Mackay, S.C. Beck, R.K. Jaiswal, R. Douglas, J.D. Mosca, M.A. Moorman, D.W. Simonetti, S. Craig, and D.R. Marshak Multilineage potential of adult human mesenchymal stem cells Science 284 1999 143 147
37. D.J. Prockop Marrow stromal cells as stem cells for nonhematopoietic tissues Science 276 1997 71 74
38. W. Sakamoto, H. Isomura, K. Fujie, Y. Deyama, A. Kato, J. Nishihira, and H. Izumi Homocysteine attenuates the expression of osteocalcin but enhances osteopontin in MC3T3-E1 preosteoblastic cells Biochim. Biophys. Acta 1740 2005 12 16
39. R.C. Simpson, and R.A. Freedland Fractors affecting the rate of gluconeogenesis from L-cysteine in the perfused rat liver J. Nutr. 106 1976 1272 1278
40. M.H. Stipanuk, and P.W. Beck Characterization of the enzymic capacity for cysteine desulphhydration in liver and kidney of the rat Biochem. J. 206 1982 267 277
41. M. Swaroop, K. Bradley, T. Ohura, T. Tahara, M.D. Roper, L.E. Rosenberg, and J.P. Kraus Rat cystathionine beta-synthase. Gene organization and alternative splicing J. Biol. Chem. 267 1992 11455 11461
42. C. Tang, X. Li, and J. Du Hydrogen sulfide as a new endogenous gaseous transmitter in the cardiovascular system Curr. Vasc. Pharmacol. 4 2006 17 22
43. R. Thaler, S. Spitzer, M. Rumpler, N. Fratzl-Zelman, K. Klaushofer, E.P. Paschalis, and F. Varga Differential effects of homocysteine and beta aminopropionitrile on preosteoblastic MC3T3-E1 cells Bone 46 2010 703 709
44. J.R. Uren, R. Ragin, and M. Chaykovsky Modulation of cysteine metabolism in mice - effects of propargylglycine and L-cyst(e)ine-degrading enzymes Biochem. Pharmacol. 27 1978 2807 2814
45. J.B. van Meurs, R.A. Dhonukshe-Rutten, S.M. Pluijm, M. van der Klift, R. de Jonge, J. Lindemans, L.C. de Groot, A. Hofman, J.C. Witteman, and J.P. van Leeuwen et al. Homocysteine levels and the risk of osteoporotic fracture N. Engl. J. Med. 350 2004 2033 2041
46. R. Wang Two's company, three's a crowd: can H2S be the third endogenous gaseous transmitter? FASEB J. 16 2002 1792 1798
47. R. Wang The gasotransmitter role of hydrogen sulfide Antioxid. Redox Signal. 5 2003 493 501
48. M. Watanabe, J. Osada, Y. Aratani, K. Kluckman, R. Reddick, M.R. Malinow, and N. Maeda Mice deficient in cystathionine beta-synthase: animal models for mild and severe homocyst(e)inemia Proc. Natl. Acad. Sci. USA 92 1995 1585 1589
49. M. Yusuf, B.T. Kwong Huat, A. Hsu, M. Whiteman, M. Bhatia, and P.K. Moore Streptozotocin-induced diabetes in the rat is associated with enhanced tissue hydrogen sulfide biosynthesis Biochem. Biophys. Res. Commun. 333 2005 1146 1152
50. G. Zhong, F. Chen, Y. Cheng, C. Tang, and J. Du The role of hydrogen sulfide generation in the pathogenesis of hypertension in rats induced by inhibition of nitric oxide synthase J. Hypertens. 21 2003 1879 1885