NF-κB RelB negatively regulates osteoblast differentiation and bone formation

Journal of Bone and Mineral Research

Volumn 29, Issue 4, 2014, Pages 866-877

  Yao, Zhenqiang ^a   Li, Yanyun ^a   Yin, Xiaoxiang ^a   Dong, Yufeng ^a   Xing, Lianping ^a   Boyce, Brendan F ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

BONE FORMATION; MESENCHYMAL PROGENITOR CELLS; NF B; OSTEOBLASTS; RELB

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; TRANSCRIPTION FACTOR RELB; TRANSCRIPTION FACTOR RUNX2; PRIMER DNA; RELB PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE DEFECT; BONE MARROW; BONE MASS; BONE REMODELING; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; FEMALE; FRACTURE HEALING; IN VITRO STUDY; MALE; MESENCHYMAL STEM CELL; MOUSE; NONHUMAN; OSSIFICATION; OSTEOBLAST; OSTEOLYSIS; PROMOTER REGION; STROMA CELL; TIBIA; TRABECULAR BONE; ANIMAL; BONE DEVELOPMENT; C57BL MOUSE; CYTOLOGY; FLOW CYTOMETRY; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; POLYMERASE CHAIN REACTION; TRANSGENIC MOUSE;

ANIMALS; BASE SEQUENCE; BONE DEVELOPMENT; CELL DIFFERENTIATION; DNA PRIMERS; FEMALE; FLOW CYTOMETRY; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; OSTEOBLASTS; POLYMERASE CHAIN REACTION; TRANSCRIPTION FACTOR RELB;

EID: 84897909064     PISSN: 08840431     EISSN: 15234681     Source Type: Journal    
DOI: 10.1002/jbmr.2108     Document Type: Article

References (48)

1. Mundy GR., Osteoporosis and inflammation. Nutr Rev. 2007; 65 (12 Pt 2): S147-51.
2. Vallabhapurapu S, Karin M., Regulation and function of NF-kappaB transcription factors in the immune system. Annu Rev Immunol. 2009; 27: 693-733.
3. Franzoso G, Carlson L, Xing L, et al. Requirement for NF-kappaB in osteoclast and B-cell development. Genes Dev. 1997; 11 (24): 3482-96.
4. Iotsova V, Caamaño J, Loy J, Yang Y, Lewin A, Bravo R., Osteopetrosis in mice lacking NF-kappaB1 and NF-kappaB2. Nat Med. 1997; 3 (11): 1285-9.
5. Yamashita T, Yao Z, Li F, et al. NF-kappaB p50 and p52 regulate receptor activator of NF-kappaB ligand (RANKL) and tumor necrosis factor-induced osteoclast precursor differentiation by activating c-Fos and NFATc1. J Biol Chem. 2007; 282 (25): 18245-53.
6. Yao Z, Xing L, Boyce BF., NF-kappaB p100 limits TNF-induced bone resorption in mice by a TRAF3-dependent mechanism. J Clin Invest. 2009; 119 (10): 3024-34.
7. Vaira S, Alhawagri M, Anwisye I, et al. RelA/p65 promotes osteoclast differentiation by blocking a RANKL-induced apoptotic JNK pathway in mice. J Clin Invest. 2008; 118 (6): 2088-97.
8. Vaira S, Johnson T, Hirbe AC, et al. RelB is the NF-kappaB subunit downstream of NIK responsible for osteoclast differentiation. Proc Natl Acad Sci U S.A. 2008; 105 (10): 3897-902.
9. Li Y, Li A, Strait K, et al. Endogenous TNF alpha lowers maximum peak bone mass and inhibits osteoblastic Smad activation through NF-kappaB. J Bone Miner Res. 2007; 22 (5): 646-55.
10. Gilbert LC, Rubin J, Nanes MS., The p55 TNF receptor mediates TNF inhibition of osteoblast differentiation independently of apoptosis. Am J Physiol Endocrinol Metab. 2005; 288 (5): E1011-8.
11. Yamazaki M, Fukushima H, Shin M, et al. Tumor necrosis factor alpha represses bone morphogenetic protein (BMP) signaling by interfering with the DNA binding of Smads through the activation of NF-kappaB. J Biol Chem. 2009; 284 (51): 35987-95.
12. Gilbert L, He X, Farmer P, et al. Expression of the osteoblast differentiation factor RUNX2 (Cbfa1/AML3/Pebp2alpha A) is inhibited by tumor necrosis factor-alpha. J Biol Chem. 2002; 277 (4): 2695-701.
13. Chang J, Wang Z, Tang E, et al. Inhibition of osteoblastic bone formation by nuclear factor-kappaB. Nat Med. 2009; 15 (6): 682-9.
14. Alles N, Soysa NS, Hayashi J, et al. Suppression of NF-κB increases bone formation and ameliorates osteopenia in ovariectomized mice. Endocrinology. 2010; 151 (10): 4626-34.
15. Cho HH, Shin KK, Kim YJ, et al. NF-kappaB activation stimulates osteogenic differentiation of mesenchymal stem cells derived from human adipose tissue by increasing TAZ expression. J Cell Physiol. 2010; 223 (1): 168-77.
16. Hess K, Ushmorov A, Fiedler J, et al. TNF alpha promotes osteogenic differentiation of human mesenchymal stem cells by triggering the NF-kappaB signaling pathway. Bone. 2009; 45 (2): 367-76.
17. Lencel P, Delplace S, Hardouin P, Magne D., TNF-α stimulates alkaline phosphatase and mineralization through PPARγ inhibition in human osteoblasts. Bone. 2011; 48 (2): 242-9.
18. Seo Y, Fukushima H, Maruyama T, et al. Accumulation of p100, a precursor of NF-κB2, enhances osteoblastic differentiation in vitro and bone formation in vivo in aly/aly mice. Mol Endocrinol. 2012; 26 (3): 414-22.
19. Soysa NS, Alles N, Weih D, et al. The pivotal role of the alternative NF-kappaB pathway in maintenance of basal bone homeostasis and osteoclastogenesis. J Bone Miner Res. 2010; 25 (4): 809-18.
20. Elewaut D, Shaikh RB, Hammond KJ, et al. NIK-dependent RelB activation defines a unique signaling pathway for the development of V alpha 14i NKT cells. J Exp Med. 2003; 197 (12): 1623-33.
21. Burkly L, Hession C, Ogata L, et al. Expression of relB is required for the development of thymic medulla and dendritic cells. Nature. 1995; 373 (6514): 531-6.
22. Zhu H, Guo ZK, Jiang XX, et al. A protocol for isolation and culture of mesenchymal stem cells from mouse compact bone. Nat Protoc. 2010; 5 (3): 550-60.
23. Kaneki H, Guo R, Chen D, et al. Tumor necrosis factor promotes Runx2 degradation through up-regulation of Smurf1 and Smurf2 in osteoblasts. J Biol Chem. 2006; 281 (7): 4326-33.
24. Yao Z, Li P, Zhang Q, et al. Tumor necrosis factor-alpha increases circulating osteoclast precursor numbers by promoting their proliferation and differentiation in the bone marrow through up-regulation of c-Fms expression. J Biol Chem. 2006; 281 (17): 11846-55.
25. Bouxsein ML, Boyd SK, Christiansen BA, et al. Guidelines for assessment of bone microstructure in rodents using micro-computed tomography. J Bone Miner Res. 2010; 25 (7): 1468-86.
26. Dougall WC, Glaccum M, Charrier K, et al. RANK is essential for osteoclast and lymph node development. Genes Dev. 1999; 13 (18): 2412-24.
27. Lowe C, Yoneda T, Boyce BF, Chen H, Mundy GR, Soriano P., Osteopetrosis in Src-deficient mice is due to an autonomous defect of osteoclasts. Proc Natl Acad Sci U S A. 1993; 90 (10): 4485-9.
28. Mukherjee S, Raje N, Schoonmaker JA, et al. Pharmacologic targeting of a stem/progenitor population in vivo is associated with enhanced bone regeneration in mice. J Clin Invest. 2008; 118 (2): 491-504.
29. Zhao L, Huang J, Zhang H, et al. Tumor necrosis factor inhibits mesenchymal stem cell differentiation into osteoblasts via the ubiquitin E3 ligase Wwp1. Stem Cells. 2011; 29 (10): 1601-10.
30. Chang MK, Raggatt LJ, Alexander KA, et al. Osteal tissue macrophages are intercalated throughout human and mouse bone lining tissues and regulate osteoblast function in vitro and in vivo. J Immunol. 2008; 181 (2): 1232-44.
31. Nishio Y, Dong Y, Paris M, et al. Runx2-mediated regulation of the zinc finger Osterix/Sp7 gene. Gene. 2006; 372: 62-70.
32. Nakashima K, Zhou X, Kunkel G, et al. The novel zinc finger-containing transcription factor osterix is required for osteoblast differentiation and bone formation. Cell. 2002; 108 (1): 17-29.
33. Komori T., Signaling networks in RUNX2-dependent bone development. J Cell Biochem. 2011; 112 (3): 750-5.
34. Zhao C, Xiu Y, Ashton J, et al. Noncanonical NF-κB signaling regulates hematopoietic stem cell self-renewal and microenvironment interactions. Stem Cells. 2012; 30 (4): 709-18.
35. Pratap J, Galindo M, Zaidi SK, et al. Cell growth regulatory role of Runx2 during proliferative expansion of preosteoblasts. Cancer Res. 2003; 63 (17): 5357-62.
36. Zaidi SK, Pande S, Pratap J, et al. Runx2 deficiency,defective subnuclear targeting bypass senescence to promote immortalization,tumorigenic potential. Proc Natl Acad Sci U S.A. 2007; 104 (50): 19861-6.
37. Kiebala M, Polesskaya O, Yao Z, et al. Nuclear factor-kappa B family member RelB inhibits human immunodeficiency virus-1 Tat-induced tumor necrosis factor-alpha production. PLoS One. 2010; 5 (7): e11875.
38. Kitaura H, Zhou P, Kim HJ, Novack DV, Ross FP, Teitelbaum SL., M-CSF mediates TNF-induced inflammatory osteolysis. J Clin Invest. 2005; 115 (12): 3418-27.
39. Clowes JA, Riggs BL, Khosla S., The role of the immune system in the pathophysiology of osteoporosis. Immunol Rev. 2005; 208: 207-27.
40. Cao JJ, Wronski TJ, Iwaniec U, et al. Aging increases stromal/osteoblastic cell-induced osteoclastogenesis and alters the osteoclast precursor pool in the mouse. J Bone Miner Res. 2005; 20 (9): 1659-68.
41. Lam J, Takeshita S, Barker JE, et al. TNF-alpha induces osteoclastogenesis by direct stimulation of macrophages exposed to permissive levels of RANK ligand. J Clin Invest. 2000; 106 (12): 1481-8.
42. Hosny M, Sharawy M., Osteoinduction in rhesus monkeys using demineralized bone powder allografts. J Oral Maxillofac Surg. 1985; 43 (11): 837-44.
43. Tuli SM, Singh AD., The osteoninductive property of decalcified bone matrix. J Bone Joint Surg Br. 1978; 60 (1): 116-23.
44. Boomsma RA, Geenen DL., Mesenchymal stem cells secrete multiple cytokines that promote angiogenesis and have contrasting effects on chemotaxis and apoptosis. PLoS One. 2012; 7 (4): e35685.
45. Schinköthe T, Bloch W, Schmidt A., In vitro secreting profile of human mesenchymal stem cells. Stem Cells Dev. 2008; 17 (1): 199-206.
46. Oh JY, Kim MK, Shin MS, Wee WR, Lee JH., Cytokine secretion by human mesenchymal stem cells cocultured with damaged corneal epithelial cells. Cytokine. 2009; 46 (1): 100-3.
47. Furuya Y, Inagaki A, Khan M, et al. Stimulation of bone formation in cortical bone of mice treated with a receptor activator of nuclear factor-κB ligand (RANKL)-binding peptide that possesses osteoclastogenesis inhibitory activity. J Biol Chem. 2013; 288 (8): 5562-71.
48. Maruyama K, Kawagoe T, Kondo T, Akira S, Takeuchi O., TRAF family member-associated NF-κB activator (TANK) is a negative regulator of osteoclastogenesis and bone formation. J Biol Chem. 2012; 287 (34): 29114-24. Diseases