Overexpression of Bcl2 in osteoblasts inhibits osteoblast differentiation and induces osteocyte apoptosis

PLoS ONE

Volumn 6, Issue 11, 2011, Pages

  Moriishi, Takeshi ^a   Maruyama, Zenjiro ^a,b   Fukuyama, Ryo ^c   Ito, Masako ^a   Miyazaki, Toshihiro ^a   Kitaura, Hideki ^a,e   Ohnishi, Hidetake ^a,d   Furuichi, Tatsuya ^a,f   Kawai, Yosuke ^a   Masuyama, Ritsuko ^a   Komori, Hisato ^a   Takada, Kenji ^d   Kawaguchi, Hiroshi ^b   Komori, Toshihisa ^a  

^a NAGASAKI UNIVERSITY   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

^c HIROSHIMA INTERNATIONAL UNIVERSITY   (Japan)

^d OSAKA UNIVERSITY   (Japan)

^e TOHOKU UNIVERSITY   (Japan)

^f JIKEI UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN BCL 2; MESSENGER RNA;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BCL2 GENE; BONE MARROW CELL; BONE STRUCTURE; CALVARIA; CELL COUNT; CELL DIFFERENTIATION; COCULTURE; COL1A1 GENE; CONTROLLED STUDY; CORTICAL BONE; GENE; GENE OVEREXPRESSION; IN VITRO STUDY; MOUSE; NEWBORN; NONHUMAN; OSSIFICATION; OSTEOBLAST; OSTEOCALCIN GENE; OSTEOCLASTOGENESIS; OSTEOCYTE; OSTEOID; THICKNESS; WILD TYPE; ANIMAL; BONE; BONE DEVELOPMENT; CELL CULTURE; CELL PROLIFERATION; CYTOLOGY; ENZYME IMMUNOASSAY; GENETICS; IN SITU HYBRIDIZATION; MALE; METABOLISM; NORTHERN BLOTTING; PATHOLOGY; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSGENIC MOUSE; WESTERN BLOTTING;

MUS; MUS MUSCULUS;

ANIMALS; APOPTOSIS; BLOTTING, NORTHERN; BLOTTING, WESTERN; BONE AND BONES; BONE DEVELOPMENT; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; IMMUNOENZYME TECHNIQUES; IN SITU HYBRIDIZATION; MALE; MICE; MICE, TRANSGENIC; OSTEOBLASTS; OSTEOCYTES; OSTEOGENESIS; PROTO-ONCOGENE PROTEINS C-BCL-2; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER;

EID: 81255143269     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0027487     Document Type: Article

References (50)

1. Marks SC, Odgren PR, (2002) Structure and development of the skeleton. In: Bilezikian JP, Raisz LG, Rodan GA, editors. Principles of Bone Biology. Second Edition. Vol. 1 London Academic Press pp. 3-15.
2. Aubin EJ, Triffitt TJ, (2002) Mesenchymal stem cells and osteoblast differentiation. In: Bilezikian JP, Raisz LG, Rodan GA, editors. Principles of Bone Biology. Second Edition. Vol. 1 London Academic Press pp. 59-81.
3. Martin RB, (2000) Does osteocyte formation cause the nonlinear refilling of osteons? Bone 26 (1): 71-78.
4. Ehrlich PJ, Lanyon LE, (2002) Mechanical strain and bone cell function: a review. Osteoporos Int 13 (9): 688-700.
5. Knothe Tate ML, (2003) "Whither flows the fluid in bone?" An osteocyte's perspective. J Biomech 36 (10): 1409-1424.
6. Burger EH, Klein-Nulend J, (1999) Mechanotransduction in bone-role of the lacuno-canalicular network. FASEB J 13 (Suppl): S101-112.
7. Bonewald L, Johnson M, (2008) Osteocytes, mechanosensing and Wnt signaling. Bone 42 (4): 606-615.
8. Noble B, (2008) The osteocyte lineage. Arch Biochem Biophys 473 (2): 106-111.
9. O'Brien CA, Jia D, Plotkin LI, Bellido T, Powers CC, et al. (2004) Glucocorticoids act directly on osteoblasts and osteocytes to induce their apoptosis and reduce bone formation and strength. Endocrinology 145 (4): 1835-1841.
10. Kousteni S, Bellido T, Plotkin LI, O'Brien CA, Bodenner DL, et al. (2001) Nongenotropic, sex-nonspecific signaling through the estrogen or androgen receptors: dissociation from transcriptional activity. Cell 104 (5): 719-730.
11. Stanislaus D, Yang X, Liang JD, Wolfe J, Cain RL, et al. (2000) In vivo regulation of apoptosis in metaphyseal trabecular bone of young rats by synthetic human parathyroid hormone (1-34) fragment. Bone 27 (2): 209-218.
12. Gohel A, McCarthy MB, Gronowicz G, (1999) Estrogen prevents glucocorticoid-induced apoptosis in osteoblasts in vivo and in vitro. Endocrinology 140 (11): 5339-5347.
13. Weinstein RS, Jilka RL, Parfitt AM, Manolagas SC, (1998) Inhibition of osteoblastogenesis and promotion of apoptosis of osteoblasts and osteocytes by glucocorticoids. Potential mechanisms of their deleterious effects on bone. J Clin Invest 102 (2): 274-282.
14. Plotkin LI, Weinstein RS, Parfitt AM, Roberson PK, Manolagas SC, et al. (1999) Prevention of osteocyte and osteoblast apoptosis by bisphosphonates and calcitonin. J Clin Invest 104 (10): 1363-1374.
15. Jilka RL, Weinstein RS, Bellido T, Roberson P, Parfitt AM, et al. (1999) Increased bone formation by prevention of osteoblast apoptosis with parathyroid hormone. J Clin Invest 104 (4): 439-446.
16. Tomkinson A, Reeve J, Shaw RW, Noble BS, (1997) The death of osteocytes via apoptosis accompanies estrogen withdrawal in human bone. J Clin Endocrinol Metab 82 (9): 3128-3135.
17. Tsujimoto Y, (2003) Cell death regulation by the Bcl-2 protein family in the mitochondria. Journal of Cellular Physiology 195 (2): 158-167.
18. Weinstein RS, Nicholas RW, Manolagas SC, (2000) Apoptosis of osteocytes in glucocorticoid-induced osteonecrosis of the hip. J Clin Endocrinol Metab 85 (8): 2907-2912.
19. Plotkin LI, Aguirre JI, Kousteni S, Manolagas SC, Bellido T, (2005) Bisphosphonates and estrogens inhibit osteocyte apoptosis via distinct molecular mechanisms downstream of extracellular signal-regulated kinase activation. J Biol Chem 280 (8): 7317-7325.
20. Rochefort GY, Pallu S, Benhamou CL, (2010) Osteocyte: the unrecognized side of bone tissue. Osteoporos Int 21 (9): 1457-1469.
21. Jilka RL, Weinstein RS, Parfitt AM, Manolagas SC, (2007) Quantifying osteoblast and osteocyte apoptosis: challenges and rewards. J Bone Miner Res 22 (10): 1492-1501.
22. Rossert J, Eberspaecher H, de Crombrugghe B, (1995) Separate cis-acting DNA elements of the mouse pro-alpha 1(I) collagen promoter direct expression of reporter genes to different type I collagen-producing cells in transgenic mice. J Cell Biol 129 (5): 1421-1432.
23. Liu W, Toyosawa S, Furuichi T, Kanatani N, Yoshida C, et al. (2001) Overexpression of Cbfa1 in osteoblasts inhibits osteoblast maturation and causes osteopenia with multiple fractures. J Cell Biol 155 (1): 157-166.
24. Gondo Y, Nakamura K, Nakao K, Sasaoka T, Ito K, et al. (1994) Gene replacement of the p53 gene with the lacZ gene in mouse embryonic stem cells and mice by using two steps of homologous recombination. Biochem Biophys Res Commun 202 (2): 830-837.
25. Kusuzaki K, Kageyama N, Shinjo H, Takeshita H, Murata H, et al. (2000) Development of bone canaliculi during bone repair. Bone 27 (5): 655-659.
26. Maruyama Z, Yoshida CA, Furuichi T, Amizuka N, Ito M, et al. (2007) Runx2 determines bone maturity and turnover rate in postnatal bone development and is involved in bone loss in estrogen deficiency. Dev Dyn 236 (7): 1876-1890.
27. Ejiri S, Ozawa H, (1982) Scanning electron microscopic observations of rat tibia using the HCl-collagenase method. Arch Histol Jpn 45 (4): 399-404.
28. Yoshida CA, Yamamoto H, Fujita T, Furuichi T, Ito K, et al. (2004) Runx2 and Runx3 are essential for chondrocyte maturation, and Runx2 regulates limb growth through induction of Indian hedgehog. Genes Dev 18 (8): 952-963.
29. Komori T, Yagi H, Nomura S, Yamaguchi A, Sasaki K, et al. (1997) Targeted disruption of Cbfa1 results in a complete lack of bone formation owing to maturational arrest of osteoblasts. Cell 89 (5): 755-764.
30. Zhang W, Pantschenko AG, McCarthy MB, Gronowicz G, (2007) Bone-Targeted Overexpression of Bcl-2 Increases Osteoblast Adhesion and Differentiation and Inhibits Mineralization In Vitro. Calcified Tissue International 80 (2): 111-122.
31. Pantschenko AG, Zhang W, Nahounou M, McCarthy MB, Stover ML, et al. (2005) Effect of Osteoblast-Targeted Expression of Bcl-2 in Bone: Differential Response in Male and Female Mice. Journal of Bone and Mineral Research 20 (8): 1414-1429.
32. Zinkel S, Gross A, Yang E, (2006) BCL2 family in DNA damage and cell cycle control. Cell Death and Differentiation 13 (8): 1351-1359.
33. Gerald P, Linette YL, Kevin R, Stanley JK, (1996) Cross talk between cell death and cell cycle progression: BCL-2 regulates NFAT-mediated activation. Proc Natl Acad Sci USA 93: 9545-9552.
34. Brady HJ, Gil-Gomez G, Kirberg J, Berns AJ, (1996) Bax alpha perturbs T cell development and affects cell cycle entry of T cells. The EMBO Journal 15: 6991-7001.
35. Evan FL, Jay W, Qi-Zhi W, Teodora S, Amy S, Petrie HT, (1999) Bcl-2-Induced Changes in E2F Regulatory Complexes Reveal the Potential for Integrated Cell Cycle and Cell Death Functions1. Journal of Immunology 162: 5374-5379.
36. Vairo G, Soos TJ, Upton TM, Zalvide J, DeCaprio JA, et al. (2000) Bcl-2 retards cell cycle entry through p27(Kip1), pRB relative p130, and altered E2F regulation. Mol Cell Biol 20 (13): 4745-4753.
37. Limana F, Urbanek K, Chimenti S, Quaini F, Leri A, et al. (2002) Bcl-2 overexpression promotes myocyte proliferation. Proc Natl Acad Sci U S A 99 (9): 6257-6262.
38. Bornstein G, (2003) Role of the SCFSkp2 Ubiquitin Ligase in the Degradation of p21Cip1 in S Phase. Journal of Biological Chemistry 278 (28): 25752-25757.
39. O'Hagan RC, (2000) Myc-enhanced expression of Cul1 promotes ubiquitin-dependent proteolysis and cell cycle progression. Genes & Development 14 (17): 2185-2191.
40. Bartek J, Lukas J, (2007) DNA damage checkpoints: from initiation to recovery or adaptation. Current Opinion in Cell Biology 19 (2): 238-245.
41. Ke H, Parron VI, Reece J, Zhang JY, Akiyama SK, et al. (2010) BCL2 inhibits cell adhesion, spreading, and motility by enhancing actin polymerization. Cell Research 20 (4): 458-469.
42. Callagy GM, Webber MJ, Pharoah PDP, Caldas C, (2008) Meta-analysis confirms BCL2 is an independent prognostic marker in breast cancer. BMC Cancer 8 (1): 153.
43. Dawson SJ, Makretsov N, Blows FM, Driver KE, Provenzano E, et al. (2010) BCL2 in breast cancer: a favourable prognostic marker across molecular subtypes and independent of adjuvant therapy received. Br J Cancer 103 (5): 668-675.
44. Fels DR, Koumenis C, (2005) HIF-1alpha and p53: the ODD couple? Trends Biochem Sci 30 (8): 426-429.
45. Hammond EM, Giaccia AJ, (2005) The role of p53 in hypoxia-induced apoptosis. Biochem Biophys Res Commun 331 (3): 718-725.
46. Levine AJ, Feng Z, Mak TW, You H, Jin S, (2006) Coordination and communication between the p53 and IGF-1-AKT-TOR signal transduction pathways. Genes Dev 20 (3): 267-275.
47. Maurer U, Charvet C, Wagman AS, Dejardin E, Green DR, (2006) Glycogen Synthase Kinase-3 Regulates Mitochondrial Outer Membrane Permeabilization and Apoptosis by Destabilization of MCL-1. Molecular Cell 21 (6): 749-760.
48. Brunelle JK, Shroff EH, Perlman H, Strasser A, Moraes CT, et al. (2007) Loss of Mcl-1 protein and inhibition of electron transport chain together induce anoxic cell death. Mol Cell Biol 27 (4): 1222-1235.
49. Gilley J, Coffer PJ, Ham J, (2003) FOXO transcription factors directly activate bim gene expression and promote apoptosis in sympathetic neurons. J Cell Biol 162 (4): 613-622.
50. Wang Y, Liu W, Masuyama R, Fukuyama R, Ito M, et al. (2011) Pyruvate dehydrogenase kinase 4 induces bone loss at unloading by promoting osteoclastogenesis. Bone In press.