Loss of Nrf2 accelerates ionizing radiation-induced bone loss by upregulating RANKL

Free Radical Biology and Medicine

Volumn 53, Issue 12, 2012, Pages 2298-2307

  Rana, Tapasi ^a   Schultz, Michelle A ^a   Freeman, Michael L ^a,b   Biswas, Swati ^a,b  

^a Department of Radiation Oncology ^*  (United States)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Bone loss; Free radicals; Ionizing radiation; N acetylcysteine; Nrf2; Osteoblast differentiation; Oxidative stress; RANKL; Reactive oxygen species

Indexed keywords

ACETYLCYSTEINE; ANTIOXIDANT; FREE RADICAL; OSTEOCLAST DIFFERENTIATION FACTOR; REACTIVE OXYGEN METABOLITE; TRANSCRIPTION FACTOR NRF2;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE ATROPHY; BONE MINERALIZATION; CALVARIA; CELL DIFFERENTIATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; FEMALE; FETUS; GENE EXPRESSION REGULATION; HISTOPATHOLOGY; IONIZING RADIATION; IRRADIATION; LOSS OF FUNCTION MUTATION; MALE; MORPHOMETRICS; MOUSE; NONHUMAN; OSTEOBLAST; OSTEOCLAST; OXIDATIVE STRESS; PRIORITY JOURNAL; RADIATION EXPOSURE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UPREGULATION;

MUS;

EID: 84870211726     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2012.10.536     Document Type: Article

References (67)

1. J.E. Wall, S.C. Kaste, C.A. Greenwald, J.J. Jenkins, E.C. Douglass, and C.B. Pratt Fractures in children treated with radiotherapy for soft tissue sarcoma Orthopedics 19 1996 657 664 (Pubitemid 26269423)
2. K.M. Schmeler, A. Jhingran, R.B. Iyer, C.C. Sun, P.J. Eifel, P.T. Soliman, P.T. Ramirez, M. Frumovitz, D.C. Bodurka, and A.K. Sood Pelvic fractures after radiotherapy for cervical cancer: implications for survivors Cancer 116 2010 625 630
3. J.W. Hopewell Radiation-therapy effects on bone density Med. Pediatr. Oncol. 41 2003 208 211 (Pubitemid 36910129)
4. S.A. Hamilton, M.J. Pecaut, D.S. Gridley, N.D. Travis, E.R. Bandstra, J.S. Willey, G.A. Nelson, and T.A. Bateman A murine model for bone loss from therapeutic and space-relevant sources of radiation J. Appl. Physiol. 101 2006 789 793 (Pubitemid 44352290)
5. E.R. Bandstra, M.J. Pecaut, E.R. Anderson, J.S. Willey, F. De Carlo, S.R. Stock, D.S. Gridley, G.A. Nelson, H.G. Levine, and T.A. Bateman Long-term dose response of trabecular bone in mice to proton radiation Radiat. Res. 169 2008 607 614 (Pubitemid 351793450)
6. D. Jia, D. Gaddy, L.J. Suva, and P.M. Corry Rapid loss of bone mass and strength in mice after abdominal irradiation Radiat. Res. 176 2011 624 635
7. X. Cao, X. Wu, D. Frassica, B. Yu, L. Pang, L. Xian, M. Wan, W. Lei, M. Armour, E. Tryggestad, J. Wong, C.Y. Wen, W.W. Lu, and F.J. Frassica Irradiation induces bone injury by damaging bone marrow microenvironment for stem cells Proc. Natl. Acad. Sci. USA 108 2011 1609 1614
8. J.D. Wernle, T.A. Damron, M.J. Allen, and K.A. Mann Local irradiation alters bone morphology and increases bone fragility in a mouse model J. Biomech. 43 2010 2738 2746
9. J.H. Hwang, S.H. Song, J.K. Lee, N.W. Lee, and K.W. Lee Bone mineral density after concurrent chemoradiation in patients with uterine cervical cancer Menopause 17 2010 416 420
10. H. Kondo, K. Yumoto, J.S. Alwood, R. Mojarrab, A. Wang, E.A. Almeida, N.D. Searby, C.L. Limoli, and R.K. Globus Oxidative stress and gamma radiation-induced cancellous bone loss with musculoskeletal disuse J. Appl. Physiol. 108 2010 152 161
11. X.C. Bai, D. Lu, J. Bai, H. Zheng, Z.Y. Ke, X.M. Li, and S.Q. Luo Oxidative stress inhibits osteoblastic differentiation of bone cells by ERK and NF-κB Biochem. Biophys. Res. Commun. 314 2004 197 207 (Pubitemid 38058389)
12. N. Mody, F. Parhami, T.A. Sarafian, and L.L. Demer Oxidative stress modulates osteoblastic differentiation of vascular and bone cells Free Radic. Biol. Med. 31 2001 509 519 (Pubitemid 32728438)
13. H. Isomura, K. Fujie, K. Shibata, N. Inoue, T. Iizuka, G. Takebe, K. Takahashi, J. Nishihira, H. Izumi, and W. Sakamoto Bone metabolism and oxidative stress in postmenopausal rats with iron overload Toxicology 197 2004 93 100 (Pubitemid 38293418)
14. I.R. Garrett, B.F. Boyce, R.O. Oreffo, L. Bonewald, J. Poser, and G.R. Mundy Oxygen-derived free radicals stimulate osteoclastic bone resorption in rodent bone in vitro and in vivo J. Clin. Invest. 85 1990 632 639 (Pubitemid 20087462)
15. S. Basu, K. Michaelsson, H. Olofsson, S. Johansson, and H. Melhus Association between oxidative stress and bone mineral density Biochem. Biophys. Res. Commun. 288 2001 275 279 (Pubitemid 32999758)
16. D. Maggio, M. Barabani, M. Pierandrei, M.C. Polidori, M. Catani, P. Mecocci, U. Senin, R. Pacifici, and A. Cherubini Marked decrease in plasma antioxidants in aged osteoporotic women: results of a cross-sectional study J. Clin. Endocrinol. Metab. 88 2003 1523 1527 (Pubitemid 36623364)
17. S. Yalin, S. Bagis, G. Polat, N. Dogruer, S. Cenk Aksit, R. Hatungil, and C. Erdogan Is there a role of free oxygen radicals in primary male osteoporosis? Clin. Exp. Rheumatol. 23 2005 689 692 (Pubitemid 41300714)
18. R.A. Mangiafico, G. Malaponte, P. Pennisi, G. Li Volti, G. Trovato, M. Mangiafico, Y. Bevelacqua, F. Mazza, and C.E. Fiore Increased formation of 8-iso-prostaglandin F(2alpha) is associated with altered bone metabolism and lower bone mass in hypercholesterolaemic subjects J. Intern. Med. 261 2007 587 596 (Pubitemid 46835982)
19. B. Ostman, K. Michaelsson, J. Helmersson, L. Byberg, R. Gedeborg, H. Melhus, and S. Basu Oxidative stress and bone mineral density in elderly men: antioxidant activity of α-tocopherol Free Radic. Biol. Med. 47 2009 668 673
20. M.A. Sanchez-Rodriguez, M. Ruiz-Ramos, E. Correa-Munoz, and V.M. Mendoza-Nunez Oxidative stress as a risk factor for osteoporosis in elderly Mexicans as characterized by antioxidant enzymes BMC Musculoskeletal Disord 8 2007 124
21. E. Hinoi, T. Takarada, S. Fujimori, L. Wang, M. Iemata, K. Uno, and Y. Yoneda Nuclear factor E2 p45-related factor 2 negatively regulates chondrogenesis Bone 40 2007 337 344 (Pubitemid 46054553)
22. M.K. Kwak, N. Wakabayashi, J.L. Greenlaw, M. Yamamoto, and T.W. Kensler Antioxidants enhance mammalian proteasome expression through the Keap1-Nrf2 signaling pathway Mol. Cell. Biol. 23 2003 8786 8794 (Pubitemid 37433379)
23. L. Leung, M. Kwong, S. Hou, C. Lee, and J.Y. Chan Deficiency of the Nrf1 and Nrf2 transcription factors results in early embryonic lethality and severe oxidative stress J. Biol. Chem. 278 2003 48021 48029 (Pubitemid 37523252)
24. H. Zhu, L. Zhang, K. Itoh, M. Yamamoto, D. Ross, M.A. Trush, J.L. Zweier, and Y. Li Nrf2 controls bone marrow stromal cell susceptibility to oxidative and electrophilic stress Free Radic. Biol. Med. 41 2006 132 143 (Pubitemid 43866458)
25. Y. Aoki, H. Sato, N. Nishimura, S. Takahashi, K. Itoh, and M. Yamamoto Accelerated DNA adduct formation in the lung of the Nrf2 knockout mouse exposed to diesel exhaust Toxicol. Appl. Pharmacol. 173 2001 154 160 (Pubitemid 32587648)
26. K. Chan, and Y.W. Kan Nrf2 is essential for protection against acute pulmonary injury in mice Proc. Natl. Acad. Sci. USA 96 1999 12731 12736 (Pubitemid 29513571)
27. A. Enomoto, K. Itoh, E. Nagayoshi, J. Haruta, T. Kimura, T. O'Connor, T. Harada, and M. Yamamoto High sensitivity of Nrf2 knockout mice to acetaminophen hepatotoxicity associated with decreased expression of ARE-regulated drug metabolizing enzymes and antioxidant genes Toxicol. Sci. 59 2001 169 177 (Pubitemid 32117993)
28. A. Hirayama, K. Yoh, S. Nagase, A. Ueda, K. Itoh, N. Morito, K. Hirayama, S. Takahashi, M. Yamamoto, and A. Koyama EPR imaging of reducing activity in Nrf2 transcriptional factor-deficient mice Free Radic. Biol. Med. 34 2003 1236 1242 (Pubitemid 36513966)
29. K. Chan, X.D. Han, and Y.W. Kan An important function of Nrf2 in combating oxidative stress: detoxification of acetaminophen Proc. Natl. Acad. Sci. USA 98 2001 4611 4616 (Pubitemid 32295024)
30. H.Y. Cho, A.E. Jedlicka, S.P. Reddy, T.W. Kensler, M. Yamamoto, L.Y. Zhang, and S.R. Kleeberger Role of NRF2 in protection against hyperoxic lung injury in mice Am. J. Respir. Cell Mol. Biol. 26 2002 175 182 (Pubitemid 34107870)
31. H.Y. Cho, A.E. Jedlicka, S.P. Reddy, L.Y. Zhang, T.W. Kensler, and S.R. Kleeberger Linkage analysis of susceptibility to hyperoxia: Nrf2 is a candidate gene Am. J. Respir. Cell Mol. Biol. 26 2002 42 51 (Pubitemid 34029819)
32. K. Yoh, K. Itoh, A. Enomoto, A. Hirayama, N. Yamaguchi, M. Kobayashi, N. Morito, A. Koyama, M. Yamamoto, and S. Takahashi Nrf2-deficient female mice develop lupus-like autoimmune nephritis Kidney Int. 60 2001 1343 1353 (Pubitemid 32960028)
33. S. Braun, C. Hanselmann, M.G. Gassmann, U. auf dem Keller, C. Born-Berclaz, K. Chan, Y.W. Kan, and S. Werner Nrf2 transcription factor, a novel target of keratinocyte growth factor action which regulates gene expression and inflammation in the healing skin wound Mol. Cell. Biol. 22 2002 5492 5505 (Pubitemid 34755759)
34. S. Ozgocmen, H. Kaya, E. Fadillioglu, R. Aydogan, and Z. Yilmaz Role of antioxidant systems, lipid peroxidation, and nitric oxide in postmenopausal osteoporosis Mol. Cell. Biochem. 295 2007 45 52 (Pubitemid 46157985)
35. N.K. Lee, Y.G. Choi, J.Y. Baik, S.Y. Han, D.W. Jeong, Y.S. Bae, N. Kim, and S.Y. Lee A crucial role for reactive oxygen species in RANKL-induced osteoclast differentiation Blood 106 2005 852 859 (Pubitemid 41076424)
36. E.L. Travis, G. Rachakonda, X. Zhou, K. Korhonen, K.R. Sekhar, S. Biswas, and M.L. Freeman NRF2 deficiency reduces life span of mice administered thoracic irradiation Free Radic. Biol. Med. 51 2011 1175 1183
37. S. Siva, B. Chesson, Y. Aarons, N. Clements, T. Kron, M. MacManus, and D. Ball Implementation of a lung radiosurgery program: technical considerations and quality assurance in an Australian institution J. Med. Imaging Radiat. Oncol 56 2012 354 361
38. J.W. Goldwein Effects of radiation therapy on skeletal growth in childhood Clin. Orthop. Relat. Res. 262 1991 101 107
39. L.O. Ohrnell, R. Branemark, J. Nyman, P. Nilsson, and P. Thomsen Effects of irradiation on the biomechanics of osseointegration: an experimental in vivo study in rats Scand. J. Plast. Reconstr. Surg. Hand Surg. 31 1997 281 293 (Pubitemid 27510994)
40. Biswas, S.; Nyman, J.S.; Alvarez, J.; Chakrabarti, A.; Ayres, A.; Sterling, J.; Edwards, J.; Rana, T.; Johnson, R.; Perrien, D.S.; Lonning, S.; Shyr, Y.; Matrisian, L.M.; Mundy, G.R. Anti-transforming growth factor ss antibody treatment rescues bone loss and prevents breast cancer metastasis to bone. PLoS One 6:e27090.
41. T.A. Beyer, and S. Werner The cytoprotective Nrf2 transcription factor controls insulin receptor signaling in the regenerating liver Cell Cycle 7 2008 874 878 (Pubitemid 351573780)
42. C.G. Bellows, J.N. Heersche, and J.E. Aubin Effects of dexamethasone on expression and maintenance of cartilage in serum-containing cultures of calvaria cells Cell Tissue Res 256 1989 145 151 (Pubitemid 19096371)
43. P.G. Robey, and J.D. Termine Human bone cells in vitro Calcif. Tissue Int. 37 1985 453 460 (Pubitemid 15250110)
44. X.C. Bai, D. Lu, A.L. Liu, Z.M. Zhang, X.M. Li, Z.P. Zou, W.S. Zeng, B.L. Cheng, and S.Q. Luo Reactive oxygen species stimulates receptor activator of NF-kappaB ligand expression in osteoblast J. Biol. Chem. 280 2005 17497 17506 (Pubitemid 41389222)
45. J.S. Willey, S.A. Lloyd, M.E. Robbins, J.D. Bourland, H. Smith-Sielicki, L.C. Bowman, R.W. Norrdin, and T.A. Bateman Early increase in osteoclast number in mice after whole-body irradiation with 2 Gy X rays Radiat. Res. 170 2008 388 392
46. M.L. Morse, and R.H. Dahl Cellular glutathione is a key to the oxygen effect in radiation damage Nature 271 1978 660 662 (Pubitemid 8278945)
47. L. Revesz, H. Bergstrand, and H. Modig Intrinsic nonprotein sulphydryl levels and cellular radiosensitivity Nature 198 1963 1275 1277
48. 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
49. M. McMahon, K. Itoh, M. Yamamoto, S.A. Chanas, C.J. Henderson, L.I. McLellan, C.R. Wolf, C. Cavin, and J.D. Hayes The Cap'n'Collar basic leucine zipper transcription factor Nrf2 (NF-E2 p45-related factor 2) controls both constitutive and inducible expression of intestinal detoxification and glutathione biosynthetic enzymes Cancer Res. 61 2001 3299 3307 (Pubitemid 32695017)
50. J. Alam, D. Stewart, C. Touchard, S. Boinapally, A.M. Choi, and J.L. Cook Nrf2, a Cap'n'Collar transcription factor, regulates induction of the heme oxygenase-1 gene J. Biol. Chem. 274 1999 26071 26078
51. H.R. Moinova, and R.T. Mulcahy Up-regulation of the human γ-glutamylcysteine synthetase regulatory subunit gene involves binding of Nrf-2 to an electrophile responsive element Biochem. Biophys. Res. Commun 261 1999 661 668 (Pubitemid 29408115)
52. X. Cao, X. Wu, D. Frassica, B. Yu, L. Pang, L. Xian, M. Wan, W. Lei, M. Armour, E. Tryggestad, J. Wong, C.Y. Wen, W.W. Lu, and F.J. Frassica Irradiation induces bone injury by damaging bone marrow microenvironment for stem cells Proc. Natl. Acad. Sci. USA 108 2011 1609 1614
53. E. Seeman Bone modeling and remodeling Crit. Rev. Eukaryotic Gene Expression 19 2009 219 233
54. J.M. Gimble, C.E. Robinson, X. Wu, and K.A. Kelly The function of adipocytes in the bone marrow stroma: an update Bone 19 1996 421 428
55. J.N. Beresford, J.H. Bennett, C. Devlin, P.S. Leboy, and M.E. Owen Evidence for an inverse relationship between the differentiation of adipocytic and osteogenic cells in rat marrow stromal cell cultures J. Cell Sci. 102 Pt 2 1992 341 351
56. D.V. Chartoumpekis, P.G. Ziros, G.P. Sykiotis, A. Zaravinos, A.I. Psyrogiannis, V.E. Kyriazopoulou, D.A. Spandidos, and I.G. Habeos Nrf2 activation diminishes during adipocyte differentiation of ST2 cells Int. J. Mol. Med. 28 2011 823 828
57. H. Lee, Y.J. Lee, H. Choi, E.H. Ko, and J.W. Kim Reactive oxygen species facilitate adipocyte differentiation by accelerating mitotic clonal expansion J. Biol. Chem. 284 2009 10601 10609
58. E. Hinoi, S. Fujimori, L. Wang, H. Hojo, K. Uno, and Y. Yoneda Nrf2 negatively regulates osteoblast differentiation via interfering with Runx2-dependent transcriptional activation J. Biol. Chem. 281 2006 18015 18024 (Pubitemid 44035601)
59. J. Zhang, C. Niu, L. Ye, H. Huang, X. He, W.G. Tong, J. Ross, J. Haug, T. Johnson, J.Q. Feng, S. Harris, L.M. Wiedemann, Y. Mishina, and L. Li Identification of the haematopoietic stem cell niche and control of the niche size Nature 425 2003 836 841 (Pubitemid 37351467)
60. F. Gori, L.C. Hofbauer, C.R. Dunstan, T.C. Spelsberg, S. Khosla, and B.L. Riggs The expression of osteoprotegerin and RANK ligand and the support of osteoclast formation by stromal-osteoblast lineage cells is developmentally regulated Endocrinology 141 2000 4768 4776 (Pubitemid 32055158)
61. L.M. Calvi, G.B. Adams, K.W. Weibrecht, J.M. Weber, D.P. Olson, M.C. Knight, R.P. Martin, E. Schipani, P. Divieti, F.R. Bringhurst, L.A. Milner, H.M. Kronenberg, and D.T. Scadden Osteoblastic cells regulate the haematopoietic stem cell niche Nature 425 2003 841 846 (Pubitemid 37351468)
62. D.L. Lacey, E. Timms, H.L. Tan, M.J. Kelley, C.R. Dunstan, T. Burgess, R. Elliott, A. Colombero, G. Elliott, S. Scully, H. Hsu, J. Sullivan, N. Hawkins, E. Davy, C. Capparelli, A. Eli, Y.X. Qian, S. Kaufman, I. Sarosi, V. Shalhoub, G. Senaldi, J. Guo, J. Delaney, and W.J. Boyle Osteoprotegerin ligand is a cytokine that regulates osteoclast differentiation and activation Cell 93 1998 165 176 (Pubitemid 28180851)
63. H. Yasuda, N. Shima, N. Nakagawa, K. Yamaguchi, M. Kinosaki, S. Mochizuki, A. Tomoyasu, K. Yano, M. Goto, A. Murakami, E. Tsuda, T. Morinaga, K. Higashio, N. Udagawa, N. Takahashi, and T. Suda Osteoclast differentiation factor is a ligand for osteoprotegerin/osteoclastogenesis-inhibitory factor and is identical to TRANCE/RANKL Proc. Natl. Acad. Sci. USA 95 1998 3597 3602
64. W.S. Simonet, D.L. Lacey, C.R. Dunstan, M. Kelley, M.S. Chang, R. Luthy, H.Q. Nguyen, S. Wooden, L. Bennett, T. Boone, G. Shimamoto, M. DeRose, R. Elliott, A. Colombero, H.L. Tan, G. Trail, J. Sullivan, E. Davy, N. Bucay, L. Renshaw-Gegg, T.M. Hughes, D. Hill, W. Pattison, P. Campbell, S. Sander, G. Van, J. Tarpley, P. Derby, R. Lee, and W.J. Boyle Osteoprotegerin: a novel secreted protein involved in the regulation of bone density Cell 89 1997 309 319 (Pubitemid 27199902)
65. H. Yasuda, N. Shima, N. Nakagawa, S.I. Mochizuki, K. Yano, N. Fujise, Y. Sato, M. Goto, K. Yamaguchi, M. Kuriyama, T. Kanno, A. Murakami, E. Tsuda, T. Morinaga, and K. Higashio Identity of osteoclastogenesis inhibitory factor (OCIF) and osteoprotegerin (OPG): a mechanism by which OPG/OCIF inhibits osteoclastogenesis in vitro Endocrinology 139 1998 1329 1337 (Pubitemid 28510154)
66. K.H. Baek, K.W. Oh, W.Y. Lee, S.S. Lee, M.K. Kim, H.S. Kwon, E.J. Rhee, J.H. Han, K.H. Song, B.Y. Cha, K.W. Lee, and M.I. Kang Association of oxidative stress with postmenopausal osteoporosis and the effects of hydrogen peroxide on osteoclast formation in human bone marrow cell cultures Calcif. Tissue Int. 87 2010 226 235
67. J.T. McDonald, K. Kim, A.J. Norris, E. Vlashi, T.M. Phillips, C. Lagadec, L. Della Donna, J. Ratikan, H. Szelag, L. Hlatky, and W.H. McBride Ionizing radiation activates the Nrf2 antioxidant response Cancer Res. 70 2010 8886 8895