Bach1 regulates osteoclastogenesis in a mouse model via both heme oxygenase 1-dependent and heme oxygenase 1-independent pathways

Arthritis and Rheumatism

Volumn 64, Issue 5, 2012, Pages 1518-1528

  Hama, Maasa ^a   Kirino, Yohei ^a   Takeno, Mitsuhiro ^a   Takase, Kaoru ^a   Miyazaki, Takuya ^a   Yoshimi, Ryusuke ^a   Ueda, Atsuhisa ^a   Itoh Nakadai, Ari ^b   Muto, Akihiko ^b   Igarashi, Kazuhiko ^b   Ishigatsubo, Yoshiaki ^a  

^a YOKOHAMA CITY UNIVERSITY   (Japan)

^b TOHOKU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ACID PHOSPHATASE; B LYMPHOCYTE INDUCED MATURATION PROTEIN 1; COLONY STIMULATING FACTOR 1; HEME OXYGENASE 1; MITOGEN ACTIVATED PROTEIN KINASE 14; MITOGEN ACTIVATED PROTEIN KINASE P38; OSTEOCLAST DIFFERENTIATION FACTOR; PROTEIN BACH1; PROTEIN C FOS; REPRESSOR PROTEIN; SHORT HAIRPIN RNA; STRESS ACTIVATED PROTEIN KINASE; TARTARIC ACID; TRANSCRIPTION FACTOR NFAT3; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 6; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW; CALVARIA; CELL DIFFERENTIATION; DOWN REGULATION; ENZYME PHOSPHORYLATION; IN VITRO STUDY; IN VIVO STUDY; INTRACELLULAR SIGNALING; MACROPHAGE; MOUSE; NONHUMAN; OSTEOCLAST; OSTEOCLASTOGENESIS; OSTEOLYSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ACID PHOSPHATASE; ANIMALS; BASIC-LEUCINE ZIPPER TRANSCRIPTION FACTORS; BIOLOGICAL MARKERS; BONE MARROW CELLS; BONE RESORPTION; CELLS, CULTURED; DOWN-REGULATION; GENE EXPRESSION REGULATION; GENE SILENCING; HEME OXYGENASE-1; ISOENZYMES; MACROPHAGE COLONY-STIMULATING FACTOR; MACROPHAGES; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MODELS, ANIMAL; OSTEOCLASTS; RANK LIGAND; RNA, SMALL INTERFERING; SKULL; TRANSDUCTION, GENETIC; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84860491929     PISSN: 00043591     EISSN: 15290131     Source Type: Journal    
DOI: 10.1002/art.33497     Document Type: Article

References (49)

1. Firestein GS,. Evolving concepts of rheumatoid arthritis. Nature 2003; 423: 356-61.
2. Takayanagi H,. Osteoimmunology and the effects of the immune system on bone. Nat Rev Rheumatol 2009; 5: 667-76.
3. Takayanagi H, Oda H, Yamamoto S, Kawaguchi H, Tanaka S, Nishikawa T, et al. A new mechanism of bone destruction in rheumatoid arthritis: synovial fibroblasts induce osteoclastogenesis. Biochem Biophys Res Commun 1997; 240: 279-86.
4. Boyle WJ, Simonet WS, Lacey DL,. Osteoclast differentiation and activation. Nature 2003; 423: 337-42.
5. Takayanagi H, Kim S, Koga T, Nishina H, Isshiki M, Yoshida H, et al. Induction and activation of the transcription factor NFATc1 (NFAT2) integrate RANKL signaling in terminal differentiation of osteoclasts. Dev Cell 2002; 3: 889-901.
6. Gohda J, Akiyama T, Koga T, Takayanagi H, Tanaka S, Inoue J,. RANK-mediated amplification of TRAF6 signaling leads to NFATc1 induction during osteoclastogenesis. EMBO J 2005; 24: 790-9.
7. Nishikawa K, Nakashima T, Hayashi M, Fukunaga T, Kato S, Kodama T, et al. Blimp1-mediated repression of negative regulators is required for osteoclast differentiation. Proc Natl Acad Sci U S A 2010; 107: 3117-22.
8. Dore RK, Cohen SB, Lane NE, Palmer W, Shergy W, Zhou L, et al. Effects of denosumab on bone mineral density and bone turnover in patients with rheumatoid arthritis receiving concurrent glucocorticoids or bisphosphonates. Ann Rheum Dis 2010; 69: 872-5.
9. Otterbein LE, Soares MP, Yamashita K, Bach FH,. Heme oxygenase-1: unleashing the protective properties of heme. Trends Immunol 2003; 24: 449-55.
10. Kirino M, Kirino Y, Takeno M, Nagashima Y, Takahashi K, Kobayashi M, et al. Heme oxygenase 1 attenuates the development of atopic dermatitis-like lesions in mice: implications for human disease. J Allergy Clin Immunol 2008; 122: 290-7.e8.
11. Takeda Y, Takeno M, Iwasaki M, Kobayashi H, Kirino Y, Ueda A, et al. Chemical induction of HO-1 suppresses lupus nephritis by reducing local iNOS expression and synthesis of anti-dsDNA antibody. Clin Exp Immunol 2004; 138: 237-44.
12. Kobayashi H, Takeno M, Saito T, Takeda Y, Kirino Y, Noyori K, et al. Regulatory role of heme oxygenase 1 in inflammation of rheumatoid arthritis. Arthritis Rheum 2006; 54: 1132-42.
13. Kirino Y, Takeno M, Murakami S, Kobayashi M, Kobayashi H, Miura K, et al. Tumor necrosis factor α acceleration of inflammatory responses by down-regulating heme oxygenase 1 in human peripheral monocytes. Arthritis Rheum 2007; 56: 464-75.
14. Zwerina J, Tzima S, Hayer S, Redlich K, Hoffmann O, Hanslik-Schnabel B, et al. Heme oxygenase 1 (HO-1) regulates osteoclastogenesis and bone resorption. FASEB J 2005; 19: 2011-3.
15. Park SY, Lee SW, Shin HK, Chung WT, Lee WS, Rhim BY, et al. Cilostazol enhances apoptosis of synovial cells from rheumatoid arthritis patients with inhibition of cytokine formation via Nrf2-linked heme oxygenase 1 induction. Arthritis Rheum 2010; 62: 732-41.
16. Kataoka K, Handa H, Nishizawa M,. Induction of cellular antioxidative stress genes through heterodimeric transcription factor Nrf2/small Maf by antirheumatic gold(I) compounds. J Biol Chem 2001; 276: 34074-81.
17. Rueda B, Oliver J, Robledo G, Lopez-Nevot MA, Balsa A, Pascual-Salcedo D, et al. HO-1 promoter polymorphism associated with rheumatoid arthritis. Arthritis Rheum 2007; 56: 3953-8.
18. Wagener FA, Toonen EJ, Wigman L, Fransen J, Creemers MC, Radstake TR, et al. HMOX1 promoter polymorphism modulates the relationship between disease activity and joint damage in rheumatoid arthritis. Arthritis Rheum 2008; 58: 3388-93.
19. Oyake T, Itoh K, Motohashi H, Hayashi N, Hoshino H, Nishizawa M, et al. Bach proteins belong to a novel family of BTB-basic leucine zipper transcription factors that interact with MafK and regulate transcription through the NF-E2 site. Mol Cell Biol 1996; 16: 6083-95.
20. Sun J, Hoshino H, Takaku K, Nakajima O, Muto A, Suzuki H, et al. Hemoprotein Bach1 regulates enhancer availability of heme oxygenase-1 gene. EMBO J 2002; 21: 5216-24.
21. Sun J, Brand M, Zenke Y, Tashiro S, Groudine M, Igarashi K,. Heme regulates the dynamic exchange of Bach1 and NF-E2-related factors in the Maf transcription factor network. Proc Natl Acad Sci U S A 2004; 101: 1461-6.
22. Kaspar JW, Jaiswal AK,. Antioxidant-induced phosphorylation of tyrosine 486 leads to rapid nuclear export of Bach1 that allows Nrf2 to bind to the antioxidant response element and activate defensive gene expression. J Biol Chem 2010; 285: 153-62.
23. Suzuki H, Tashiro S, Sun J, Doi H, Satomi S, Igarashi K,. Cadmium induces nuclear export of Bach1, a transcriptional repressor of heme oxygenase-1 gene. J Biol Chem 2003; 278: 49246-53.
24. Reichard JF, Motz GT, Puga A,. Heme oxygenase-1 induction by NRF2 requires inactivation of the transcriptional repressor BACH1. Nucleic Acids Res 2007; 35: 7074-86.
25. Dohi Y, Alam J, Yoshizumi M, Sun J, Igarashi K,. Heme oxygenase-1 gene enhancer manifests silencing activity in a chromatin environment prior to oxidative stress. Antioxid Redox Signal 2006; 8: 60-7.
26. Miyazaki T, Kirino Y, Takeno M, Samukawa S, Hama M, Tanaka M, et al. Expression of heme oxygenase-1 in human leukemic cells and its regulation by transcriptional repressor Bach1. Cancer Sci 2010; 101: 1409-16.
27. Wruck CJ, Fragoulis A, Gurzynski A, Brandenburg LO, Kan YW, Chan K, et al. Role of oxidative stress in rheumatoid arthritis: insights from the Nrf2-knockout mice. Ann Rheum Dis 2011; 70: 844-50.
28. Mito S, Ozono R, Oshima T, Yano Y, Watari Y, Yamamoto Y, et al. Myocardial protection against pressure overload in mice lacking Bach1, a transcriptional repressor of heme oxygenase-1. Hypertension 2008; 51: 1570-7.
29. Watari Y, Yamamoto Y, Brydun A, Ishida T, Mito S, Yoshizumi M, et al. Ablation of the Bach1 gene leads to the suppression of atherosclerosis in Bach1 and apolipoprotein E double knockout mice. Hypertens Res 2008; 31: 783-92.
30. Koga T, Inui M, Inoue K, Kim S, Suematsu A, Kobayashi E, et al. Costimulatory signals mediated by the ITAM motif cooperate with RANKL for bone homeostasis. Nature 2004; 428: 758-63.
31. Yoshimatsu M, Kitaura H, Fujimura Y, Eguchi T, Kohara H, Morita Y, et al. IL-12 inhibits TNF-α induced osteoclastogenesis via a T cell-independent mechanism in vivo. Bone 2009; 45: 1010-6.
32. Wang ZQ, Ovitt C, Grigoriadis AE, Mohle-Steinlein U, Ruther U, Wagner EF,. Bone and haematopoietic defects in mice lacking c-fos. Nature 1992; 360: 741-5.
33. Ha H, Kwak HB, Lee SW, Jin HM, Kim HM, Kim HH, et al. Reactive oxygen species mediate RANK signaling in osteoclasts. Exp Cell Res 2004; 301: 119-27.
34. Lee NK, Choi YG, Baik JY, Han SY, Jeong DW, Bae YS, et al. A crucial role for reactive oxygen species in RANKL-induced osteoclast differentiation. Blood 2005; 106: 852-9.
35. 2+ oscillations essential for osteoclastogenesis. J Biol Chem 2010; 285: 6913-21.
36. Tanimoto T, Hattori N, Senoo T, Furonaka M, Ishikawa N, Fujitaka K, et al. Genetic ablation of the Bach1 gene reduces hyperoxic lung injury in mice: role of IL-6. Free Radic Biol Med 2009; 46: 1119-26.
37. Paine A, Eiz-Vesper B, Blasczyk R, Immenschuh S,. Signaling to heme oxygenase-1 and its anti-inflammatory therapeutic potential. Biochem Pharmacol 2010; 80: 1895-903.
38. Bohm C, Hayer S, Kilian A, Zaiss MM, Finger S, Hess A, et al. The α-isoform of p38 MAPK specifically regulates arthritic bone loss. J Immunol 2009; 183: 5938-47.
39. Ochiai K, Katoh Y, Ikura T, Hoshikawa Y, Noda T, Karasuyama H, et al. Plasmacytic transcription factor Blimp-1 is repressed by Bach2 in B cells. J Biol Chem 2006; 281: 38226-34.
40. Lam J, Takeshita S, Barker JE, Kanagawa O, Ross FP, Teitelbaum SL,. TNF-α induces osteoclastogenesis by direct stimulation of macrophages exposed to permissive levels of RANK ligand. J Clin Invest 2000; 106: 1481-8.
41. Wei S, Kitaura H, Zhou P, Ross FP, Teitelbaum SL,. IL-1 mediates TNF-induced osteoclastogenesis. J Clin Invest 2005; 115: 282-90.
42. Zou W, Hakim I, Tschoep K, Endres S, Bar-Shavit Z,. Tumor necrosis factor-α mediates RANK ligand stimulation of osteoclast differentiation by an autocrine mechanism. J Cell Biochem 2001; 83: 70-83.
43. Watanabe-Matsui M, Muto A, Matsui T, Itoh-Nakadai A, Nakajima O, Murayama K, et al. Heme regulates B-cell differentiation, antibody class switch, and heme oxygenase-1 expression in B cells as a ligand of Bach2. Blood 2011; 117: 5438-48.
44. Franke A, McGovern DP, Barrett JC, Wang K, Radford-Smith GL, Ahmad T, et al. Genome-wide meta-analysis increases to 71 the number of confirmed Crohn's disease susceptibility loci. Nat Genet 2010; 42: 1118-25.
45. Oostlander AE, Bravenboer N, Sohl E, Holzmann PJ, van der Woude CJ, Dijkstra G, et al. Histomorphometric analysis reveals reduced bone mass and bone formation in patients with quiescent Crohn's disease. Gastroenterology 2011; 140: 116-23.
46. Yarilina A, Park-Min KH, Antoniv T, Hu X, Ivashkiv LB,. TNF activates an IRF1-dependent autocrine loop leading to sustained expression of chemokines and STAT1-dependent type I interferon-response genes. Nat Immunol 2008; 9: 378-87.
47. Durand M, Boire G, Komarova SV, Dixon SJ, Sims SM, Harrison RE, et al. The increased in vitro osteoclastogenesis in patients with rheumatoid arthritis is due to increased percentage of precursors and decreased apoptosisâthe In Vitro Osteoclast Differentiation in Arthritis (IODA) study. Bone 2011; 48: 588-96.
48. MacLeod AK, McMahon M, Plummer SM, Higgins LG, Penning TM, Igarashi K, et al. Characterization of the cancer chemopreventive NRF2-dependent gene battery in human keratinocytes: demonstration that the KEAP1-NRF2 pathway, and not the BACH1-NRF2 pathway, controls cytoprotection against electrophiles as well as redox-cycling compounds. Carcinogenesis 2009; 30: 1571-80.
49. Wakabayashi N, Itoh K, Wakabayashi J, Motohashi H, Noda S, Takahashi S, et al. Keap1-null mutation leads to postnatal lethality due to constitutive Nrf2 activation. Nat Genet 2003; 35: 238-45.