Sodium hydrosulfide inhibits the differentiation of osteoclast progenitor cells via NRF2-dependent mechanism

Pharmacological Research

Volumn 87, Issue , 2014, Pages 99-112

  Gambari, Laura ^a   Lisignoli, Gina ^a   Cattini, Luca ^a   Manferdini, Cristina ^a   Facchini, Andrea ^a,b   Grassi, Francesco ^a  

^a RIZZOLI ORTHOPAEDIC INSTITUTE   (Italy)

^b UNIVERSITY OF BOLOGNA   (Italy)

Author keywords

Bone; Hydrogen sulfide; Mesenchymal stem cells; NRF2; Osteoclasts; Osteoporosis; Sodium hydrosulfide

Indexed keywords

HYDROGEN SULFIDE; MESSENGER RNA; OSTEOCLAST DIFFERENTIATION FACTOR; PEROXIREDOXIN 1; REACTIVE OXYGEN METABOLITE; SODIUM HYDROSULFIDE; SULFORAPHANE; TERT BUTYLHYDROQUINONE; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG; NFE2L2 PROTEIN, HUMAN; SODIUM BISULFIDE; SULFIDE;

ANTIOXIDANT ACTIVITY; ARTICLE; CELL FUNCTION; CELL MATURATION; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DOWN REGULATION; GENE; GENE ACTIVATION; GENE SILENCING; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; IN VITRO STUDY; MESENCHYMAL STEM CELL; MONOCYTE; NQO1 GENE; NUCLEAR LOCALIZATION SIGNAL; OSTEOCLAST; OSTEOCLAST ACTIVITY; OSTEOCLASTOGENESIS; PRDX1 GENE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; UPREGULATION; CELL CULTURE; CELL DIFFERENTIATION; CELL SURVIVAL; CYTOLOGY; DRUG EFFECTS; MESENCHYMAL STROMA CELL; METABOLISM; STEM CELL;

CELL DIFFERENTIATION; CELL SURVIVAL; CELLS, CULTURED; HUMANS; MESENCHYMAL STROMAL CELLS; MONOCYTES; NF-E2-RELATED FACTOR 2; OSTEOCLASTS; RANK LIGAND; REACTIVE OXYGEN SPECIES; STEM CELLS; SULFIDES;

EID: 84904570079     PISSN: 10436618     EISSN: 10961186     Source Type: Journal    
DOI: 10.1016/j.phrs.2014.06.014     Document Type: Article

References (55)

1. 2S: a landscape view of gas biology Keio J Med 51 March (1) 2002 1 10
2. M. Vandiver, and S.H. Snyder Hydrogen sulfide: a gasotransmitter of clinical relevance J Mol Med (Berl) 90 March (3) 2012 255 263
3. C. Szabo Hydrogen sulphide and its therapeutic potential Nat Rev Drug Discov 6 November (11) 2007 917 935 (Pubitemid 350042399)
4. 2S is impaired in non-obese diabetic (NOD) mice Br J Pharmacol 155 November (5) 2008 673 680
5. S. Fiorucci, E. Antonelli, E. Distrutti, G. Rizzo, A. Mencarelli, and S. Orlandi et al. Inhibition of hydrogen sulfide generation contributes to gastric injury caused by anti-inflammatory nonsteroidal drugs Gastroenterology 129 October (4) 2005 1210 1224 (Pubitemid 41446861)
6. M. Whiteman, J.S. Armstrong, S.H. Chu, S. Jia-Ling, B.S. Wong, and N.S.B. Cheung et al. The novel neuromodulator hydrogen sulfide: an endogenous peroxynitrite 'scavenger'? J Neurochem 90 August (3) 2004 765 768 (Pubitemid 38989409)
7. R. Hattner, B.N. Epker, and H.M. Frost Suggested sequential mode of control of changes in cell behaviour in adult bone remodelling Nature 206 May (983) 1965 489 490
8. E.M. Hauge, D. Qvesel, E.F. Eriksen, L. Mosekilde, and F. Melsen Cancellous bone remodeling occurs in specialized compartments lined by cells expressing osteoblastic markers J Bone Miner Res 16 September (9) 2001 1575 1582 (Pubitemid 32786425)
9. A.M. Parfitt The bone remodeling compartment: a circulatory function for bone lining cells J Bone Miner Res 16 September (9) 2001 1583 1585 (Pubitemid 32786426)
10. K. Tanaka, M. Hashizume, M. Mihara, H. Yoshida, M. Suzuki, and Y. Matsumoto Anti-interleukin-6 receptor antibody prevents systemic bone mass loss via reducing the number of osteoclast precursors in bone marrow in a collagen-induced arthritis model Clin Exp Immunol 175 February (2) 2014 172 180
11. C.T. Ritchlin, S.A. Haas-Smith, P. Li, D.G. Hicks, and E.M. Schwarz Mechanisms of TNF-alpha- and RANKL-mediated osteoclastogenesis and bone resorption in psoriatic arthritis J Clin Invest 111 March (6) 2003 821 831 (Pubitemid 37074957)
12. M. Ishii, J. Kikuta, Y. Shimazu, M. Meier-Schellersheim, and R.N. Germain Chemorepulsion by blood S1P regulates osteoclast precursor mobilization and bone remodeling in vivo J Exp Med 207 December (13) 2010 2793 2798
13. J.R. Edwards, and G.R. Mundy Advances in osteoclast biology: old findings and new insights from mouse models Nat Rev Rheumatol 7 April (4) 2011 235 243
14. T. Wada, T. Nakashima, N. Hiroshi, and J.M. Penninger RANKL-RANK signaling in osteoclastogenesis and bone disease Trends Mol Med 12 January (1) 2006 17 25 (Pubitemid 43089652)
15. N.K. Lee, Y.G. Choi, J.Y. Baik, S.Y. Han, D.W. Jeong, and Y.S. Bae et al. A crucial role for reactive oxygen species in RANKL-induced osteoclast differentiation Blood 106 August (3) 2005 852 859 (Pubitemid 41076424)
16. F. Grassi, G. Tell, M. Robbie-Ryan, Y. Gao, M. Terauchi, and X. Yang et al. Oxidative stress causes bone loss in estrogen-deficient mice through enhanced bone marrow dendritic cell activation Proc Natl Acad Sci U S A 104 September (38) 2007 15087 15092 (Pubitemid 47619597)
17. J.M. Lean, J.T. Davies, K. Fuller, C.J. Jagger, B. Kirstein, and G.A. Partington et al. A crucial role for thiol antioxidants in estrogen-deficiency bone loss J Clin Invest 112 September (6) 2003 915 923 (Pubitemid 38063749)
18. J. Tsay, Z. Yang, F.P. Ross, S. Cunningham-Rundles, H. Lin, and R. Coleman et al. Bone loss caused by iron overload in a murine model: importance of oxidative stress Blood 116 October (14) 2010 2582 2589
19. Y. Kimura, Y. Goto, and H. Kimura Hydrogen sulfide increases glutathione production and suppresses oxidative stress in mitochondria Antioxid Redox Signal 12 January (1) 2010 1 13
20. J.M. Hourihan, J.G. Kenna, and J.D. Hayes The gasotransmitter hydrogen sulfide induces nrf2-target genes by inactivating the keap1 ubiquitin ligase substrate adaptor through formation of a disulfide bond between cys-226 and cys-613 Antioxid Redox Signal 19 August (5) 2013 465 481
21. K. Irie, D. Ekuni, T. Yamamoto, M. Morita, K. Yaegaki, and H. Ii et al. A single application of hydrogen sulphide induces a transient osteoclast differentiation with RANKL expression in the rat model Arch Oral Biol 54 August (8) 2009 723 729
22. K. Irie, D. Ekuni, T. Tomofuji, Y. Endo, K. Kasuyama, and K. Yaegaki et al. Combined effects of hydrogen sulfide and lipopolysaccharide on osteoclast differentiation in rats J Periodontol 83 April (4) 2012 522 527
23. H. Ii, T. Imai, K. Yaegaki, K. Irie, D. Ekuni, and M. Morita Oral malodorous compound induces osteoclast differentiation without receptor activator of nuclear factor kappaB ligand J Periodontol 81 November (11) 2010 1691 1697
24. S.K. Lee, J.H. Chung, S.C. Choi, Q.S. Auh, Y.M. Lee, and S.I. Lee et al. Sodium hydrogen sulfide inhibits nicotine and lipopolysaccharide-induced osteoclastic differentiation and reversed osteoblastic differentiation in human periodontal ligament cells J Cell Biochem 114 May (5) 2013 1183 1193
25. B.Y. Shin, S.H. Jin, I.J. Cho, and S.H. Ki Nrf2-ARE pathway regulates induction of Sestrin-2 expression Free Radic Biol Med 53 August (4) 2012 834 841
26. D. Vauzour, M. Buonfiglio, G. Corona, J. Chirafisi, K. Vafeiadou, and C. Angeloni et al. Sulforaphane protects cortical neurons against 5-S-cysteinyl-dopamine-induced toxicity through the activation of ERK1/2, Nrf-2 and the upregulation of detoxification enzymes Mol Nutr Food Res 54 April (4) 2010 532 542
27. F. Grassi, C. Manferdini, L. Cattini, A. Piacentini, E. Gabusi, and A. Facchini et al. T cell suppression by osteoclasts in vitro J Cell Physiol 226 April (4) 2011 982 990
28. G. Lisignoli, S. Cristino, A. Piacentini, S. Toneguzzi, F. Grassi, and C. Cavallo et al. Cellular and molecular events during chondrogenesis of human mesenchymal stromal cells grown in a three-dimensional hyaluronan based scaffold Biomaterials 26 October (28) 2005 5677 5686 (Pubitemid 40616838)
29. F. Bouillaud, and F. Blachier Mitochondria sulfide: a very old story of poisoning, feeding, and signaling? Antioxid Redox Signal 15 July (2) 2011 379 391
30. R. Venugopaland, and A.K. Jaiswal Nrf1 Nrf2 positively and c-Fos and Fra1 negatively regulate the human antioxidant response element-mediated expression of NAD(P)H:quinone oxidoreductase1 gene Proc Natl Acad Sci U S A 93 December (25) 1996 14960 14965
31. T. Nguyen, P.J. Sherratt, H.C. Huang, C.S. Yang, and C.B. Pickett Increased protein stability as a mechanism that enhances Nrf2-mediated transcriptional activation of the antioxidant response element, Degradation of Nrf2 by the 26 S proteasome J Biol Chem 278 February (7) 2003 4536 4541 (Pubitemid 36800950)
32. H. Kanzaki, F. Shinohara, M. Kajiya, and T. Kodama The Keap1/Nrf2 protein axis plays a role in osteoclast differentiation by regulating intracellular reactive oxygen species signaling J Biol Chem 288 August (32) 2013 23009 23020
33. K.W. Kang, S.J. Lee, J.W. Park, and S.G. Kim Phosphatidylinositol 3-kinase regulates nuclear translocation of NF-E2-related factor 2 through actin rearrangement in response to oxidative stress Mol Pharmacol 62 November (5) 2002 1001 1010 (Pubitemid 35222491)
34. D.C. Yang, H.J. Tsay, S.Y. Lin, S.H. Chiou, M.J. Li, and T.J. Chang et al. cAMP/PKA regulates osteogenesis, adipogenesis and ratio of RANKL/OPG mRNA expression in mesenchymal stem cells by suppressing leptin PLoS ONE 3 February (2) 2008 e1540
35. L. Dalle Carbonare, M.T. Valenti, M. Zanatta, L. Donatelli, and V. Lo Cascio Circulating mesenchymal stem cells with abnormal osteogenic differentiation in patients with osteoporosis Arthritis Rheum 60 November (11) 2009 3356 3365
36. M. Zaidi Skeletal remodeling in health and disease Nat Med 13 July (7) 2007 791 801 (Pubitemid 47038187)
37. J. Frantzias, J.G. Logan, P. Mollat, A. Sparatore, P. Del Soldato, and S.H. Ralston et al. Hydrogen sulphide-releasing diclofenac derivatives inhibit breast cancer-induced osteoclastogenesis in vitro and prevent osteolysis ex vivo Br J Pharmacol 165 March (6) 2012 1914 1925
38. E.W. Bradley, and M.J. Oursler Osteoclast culture and resorption assays Methods Mol Biol 455 2008 19 35
39. J. Furne, A. Saeed, and M.D. Levitt Whole tissue hydrogen sulfide concentrations are orders of magnitude lower than presently accepted values Am J Physiol Regul Integr Comp Physiol 295 November (5) 2008 R1479 R1485
40. S.C. Manolagas From estrogen-centric to aging and oxidative stress: a revised perspective of the pathogenesis of osteoporosis Endocr Rev 31 June (3) 2010 266 300
41. H. Ha, H.B. Kwak, S.W. Lee, H.M. Jin, H.M. Kim, and H.H. Kim et al. Reactive oxygen species mediate RANK signaling in osteoclasts Exp Cell Res 301 December (2) 2004 119 127 (Pubitemid 39504965)
42. Z.S. Xu, X.Y. Wang, D.M. Xiao, L.F. Hu, M. Lu, and Z.Y. Wu et al. Hydrogen sulfide protects MC3T3-E1 osteoblastic cells against H2O2-induced oxidative damage-implications for the treatment of osteoporosis Free Radic Biol Med 50 May (10) 2011 1314 1323
43. L.F. Hu, M. Lu, Z.Y. Wu, P.T. Wong, and J.S. Bian Hydrogen sulfide inhibits rotenone-induced apoptosis via preservation of mitochondrial function Mol Pharmacol 75 January (1) 2009 27 34
44. T.W. Kensler, N. Wakabayashi, and S. Biswal Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway Annu Rev Pharmacol Toxicol 47 2007 89 116
45. K. Itoh, N. Wakabayashi, Y. Katoh, T. Ishii, K. Igarashi, and J.D. Engel et al. Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domain Genes Dev 13 January (1) 1999 76 86 (Pubitemid 29045117)
46. H.C. Huang, T. Nguyen, and C.B. Pickett Regulation of the antioxidant response element by protein kinase C-mediated phosphorylation of NF-E2-related factor 2 Proc Natl Acad Sci U S A 97 November (23) 2000 12475 12480
47. G. Yang, K. Zhao, Y. Ju, S. Mani, Q. Cao, and S. Puukila et al. Hydrogen sulfide protects against cellular senescence via S-sulfhydration of Keap1 and activation of Nrf2 Antioxid Redox Signal 18 May (15) 2013 1906 1919
48. K. Taguchi, H. Motohashi, and M. Yamamoto Molecular mechanisms of the Keap1-Nrf2 pathway in stress response and cancer evolution Genes Cells 16 February (2) 2011 123 140
49. N. Wakabayashi, S.L. Slocum, J.J. Skoko, S. Shin, and T.W. Kensler When NRF2 talks, who's listening? Antioxid Redox Signal 13 December (11) 2010 1649 1663
50. P. Bergstrom, H.C. Andersson, Y. Gao, J.O. Karlsson, C. Nodin, and M.F.M. Anderson et al. Repeated transient sulforaphane stimulation in astrocytes leads to prolonged Nrf2-mediated gene expression and protection from superoxide-induced damage Neuropharmacology 60 February-March (2-3) 2011 343 353
51. Y. Abiko, T. Miura, B.H. Phuc, Y. Shinkai, and Y. Kumagai Participation of covalent modification of Keap1 in the activation of Nrf2 by tert-butylbenzoquinone, an electrophilic metabolite of butylated hydroxyanisole Toxicol Appl Pharmacol 255 August (1) 2011 32 39
52. T. Rana, M.A. Schultz, M.L. Freeman, and S. Biswas Loss of Nrf2 accelerates ionizing radiation-induced bone loss by upregulating RANKL Free Radic Biol Med 53 December (12) 2012 2298 2307
53. C. Liaoand, and Y. Hua Effect of hydrogen sulphide on the expression of osteoprotegerin and receptor activator of NF-kappaB ligand in human periodontal ligament cells induced by tension-force stimulation Arch Oral Biol 58 December (12) 2013 1784 1790
54. B.L. Predmore, K. Kondo, S. Bhushan, M.A. Zlatopolsky, A.L. King, and J.P.D.B. Aragon The polysulfide diallyl trisulfide protects the ischemic myocardium by preservation of endogenous hydrogen sulfide and increasing nitric oxide bioavailability Am J Physiol Heart Circ Physiol 302 June (11) 2012 H2410 H2418
55. M. Mukherjee, A.S. Das, S. Mitra, and C. Mitra Prevention of bone loss by oil extract of garlic (Allium sativum Linn.) in an ovariectomized rat model of osteoporosis Phytother Res 18 May (5) 2004 389 394 (Pubitemid 38758242)