Targeted Disruption of TGFBI in Mice Reveals Its Role in Regulating Bone Mass and Bone Size through Periosteal Bone Formation
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- 作者：Hongrun Yu (1) hongrun.yu@va.gov
Jon E. Wergedal (1)
Yongliang Zhao (2)
Subburaman Mohan (1) - 关键词：TGFBI – ; β ; ig ; h3 – ; Mouse – ; Bone size – ; Bone strength
- 刊名：Calcified Tissue International
- 出版年：2012
- 出版时间：July 2012
- 年：2012
- 卷：91
- 期：1
- 页码：81-87
- 全文大小：285.7 KB
- 参考文献：1. Wergedal JE, Sheng MH, Ackert-Bicknell CL, Beamer WG, Baylink DJ (2005) Genetic variation in femur extrinsic strength in 29 different inbred strains of mice is dependent on variations in femur cross-sectional geometry and bone density. Bone 36:111–122
2. Takeshita S, Kikuno R, Tezuka K, Amann E (1993) Osteoblast-specific factor 2: cloning of a putative bone adhesion protein with homology with the insect protein fasciclin I. Biochem J 294(Pt 1):271–278
3. Horiuchi K, Amizuka N, Takeshita S, Takamatsu H, Katsuura M, Ozawa H, Toyama Y, Bonewald LF, Kudo A (1999) Identification and characterization of a novel protein, periostin, with restricted expression to periosteum and periodontal ligament and increased expression by transforming growth factor beta. J Bone Miner Res 14:1239–1249
4. Kashima TG, Nishiyama T, Shimazu K, Shimazaki M, Kii I, Grigoriadis AE, Fukayama M, Kudo A (2009) Periostin, a novel marker of intramembranous ossification, is expressed in fibrous dysplasia and in c-Fos-overexpressing bone lesions. Hum Pathol 40:226–237
5. Kii I, Amizuka N, Minqi L, Kitajima S, Saga Y, Kudo A (2006) Periostin is an extracellular matrix protein required for eruption of incisors in mice. Biochem Biophys Res Commun 342:766–772
6. Ma D, Zhang R, Sun Y, Rios HF, Haruyama N, Han X, Kulkarni AB, Qin C, Feng JQ (2011) A novel role of periostin in postnatal tooth formation and mineralization. J Biol Chem 286:4302–4309
7. Rios H, Koushik SV, Wang H, Wang J, Zhou HM, Lindsley A, Rogers R, Chen Z, Maeda M, Kruzynska-Frejtag A, Feng JQ, Conway SJ (2005) Periostin null mice exhibit dwarfism, incisor enamel defects, and an early-onset periodontal disease-like phenotype. Mol Cell Biol 25:11131–11144
8. Skonier J, Neubauer M, Madisen L, Bennett K, Plowman GD, Purchio AF (1992) cDNA cloning and sequence analysis of beta ig-h3, a novel gene induced in a human adenocarcinoma cell line after treatment with transforming growth factor-beta. DNA Cell Biol 11:511–522
9. LeBaron RG, Bezverkov KI, Zimber MP, Pavelec R, Skonier J, Purchio AF (1995) Beta IG-H3, a novel secretory protein inducible by transforming growth factor-beta, is present in normal skin and promotes the adhesion and spreading of dermal fibroblasts in vitro. J Invest Dermatol 104:844–849
10. Skonier J, Bennett K, Rothwell V, Kosowski S, Plowman G, Wallace P, Edelhoff S, Disteche C, Neubauer M, Marquardt H et al (1994) beta ig-h3: a transforming growth factor-beta-responsive gene encoding a secreted protein that inhibits cell attachment in vitro and suppresses the growth of CHO cells in nude mice. DNA Cell Biol 13:571–584
11. Thapa N, Lee BH, Kim IS (2007) TGFBIp/betaig-h3 protein: a versatile matrix molecule induced by TGF-beta. Int J Biochem Cell Biol 39:2183–2194
12. Cicek M, Vrabel A, Sturchio C, Pederson L, Hawse JR, Subramaniam M, Spelsberg TC, Oursler MJ (2011) TGF-beta inducible early gene 1 regulates osteoclast differentiation and survival by mediating the NFATc1, AKT, and MEK/ERK signaling pathways. PLoS One 6:e17522
13. Runager K, Basaiawmoit RV, Deva T, Andreasen M, Valnickova Z, Sorensen CS, Karring H, Thogersen IB, Christiansen G, Underhaug J, Kristensen T, Nielsen NC, Klintworth GK, Otzen DE, Enghild JJ (2008) Human phenotypically distinct TGFBI corneal dystrophies are linked to the stability of the fourth FAS1 domain of TGFBIp. J Biol Chem 286:4951–4958
14. Ferguson JW, Thoma BS, Mikesh MF, Kramer RH, Bennett KL, Purchio A, Bellard BJ, LeBaron RG (2003) The extracellular matrix protein betaIG-H3 is expressed at myotendinous junctions and supports muscle cell adhesion. Cell Tissue Res 313:93–105
15. Jung MY, Thapa N, Kim JE, Yang JD, Cho BC, Kim IS (2007) Recombinant tetra-cell adhesion motifs supports adhesion, migration and proliferation of keratinocytes/fibroblasts, and promotes wound healing. Exp Mol Med 39:663–672
16. Kim JE, Jeong HW, Nam JO, Lee BH, Choi JY, Park RW, Park JY, Kim IS (2002) Identification of motifs in the fasciclin domains of the transforming growth factor-beta-induced matrix protein betaig-h3 that interact with the alphavbeta5 integrin. J Biol Chem 277:46159–46165
17. Kim JE, Kim EH, Han EH, Park RW, Park IH, Jun SH, Kim JC, Young MF, Kim IS (2000) A TGF-beta-inducible cell adhesion molecule, betaig-h3, is downregulated in melorheostosis and involved in osteogenesis. J Cell Biochem 77:169–178
18. Kim JE, Kim SJ, Lee BH, Park RW, Kim KS, Kim IS (2000) Identification of motifs for cell adhesion within the repeated domains of transforming growth factor-beta-induced gene, betaig-h3. J Biol Chem 275:30907–30915
19. Kim JE, Park RW, Choi JY, Bae YC, Kim KS, Joo CK, Kim IS (2002) Molecular properties of wild-type and mutant betaIG-H3 proteins. Invest Ophthalmol Vis Sci 43:656–661
20. Nam JO, Kim JE, Jeong HW, Lee SJ, Lee BH, Choi JY, Park RW, Park JY, Kim IS (2003) Identification of the alphavbeta3 integrin-interacting motif of betaig-h3 and its anti-angiogenic effect. J Biol Chem 278:25902–25909
21. Schorderet DF, Menasche M, Morand S, Bonnel S, Buchillier V, Marchant D, Auderset K, Bonny C, Abitbol M, Munier FL (2000) Genomic characterization and embryonic expression of the mouse Bigh3 (Tgfbi) gene. Biochem Biophys Res Commun 274:267–274
22. Becker J, Erdlenbruch B, Noskova I, Schramm A, Aumailley M, Schorderet DF, Schweigerer L (2006) Keratoepithelin suppresses the progression of experimental human neuroblastomas. Cancer Res 66:5314–5321
23. Calaf GM, Echiburu-Chau C, Zhao YL, Hei TK (2008) BigH3 protein expression as a marker for breast cancer. Int J Mol Med 21:561–568
24. Genini M, Schwalbe P, Scholl FA, Schafer BW (1996) Isolation of genes differentially expressed in human primary myoblasts and embryonal rhabdomyosarcoma. Int J Cancer 66:571–577
25. Guo YS, Tang J, Chen B, Huang W, Li Y, Cui HY, Zhang X, Wang SJ, Chen ZN, Jiang J (2011) betaig-h3 regulates store-operated Ca2+ entry and promotes the invasion of human hepatocellular carcinoma cells. Cell Biol Int 35:811–817
26. Yamanaka M, Kimura F, Kagata Y, Kondoh N, Asano T, Yamamoto M, Hayakawa M (2008) BIGH3 is overexpressed in clear cell renal cell carcinoma. Oncol Rep 19:865–874
27. Zamilpa R, Rupaimoole R, Phelix CF, Somaraki-Cormier M, Haskins W, Asmis R, LeBaron RG (2009) C-terminal fragment of transforming growth factor beta-induced protein (TGFBIp) is required for apoptosis in human osteosarcoma cells. Matrix Biol 28:347–353
28. Zhang Y, Wen G, Shao G, Wang C, Lin C, Fang H, Balajee AS, Bhagat G, Hei TK, Zhao Y (2009) TGFBI deficiency predisposes mice to spontaneous tumor development. Cancer Res 69:37–44
29. Zhao Y, El-Gabry M, Hei TK (2006) Loss of Betaig-h3 protein is frequent in primary lung carcinoma and related to tumorigenic phenotype in lung cancer cells. Mol Carcinog 45:84–92
30. Zhao YL, Piao CQ, Hei TK (2002) Downregulation of Betaig-h3 gene is causally linked to tumorigenic phenotype in asbestos treated immortalized human bronchial epithelial cells. Oncogene 21:7471–7477
31. Kim BY, Olzmann JA, Choi SI, Ahn SY, Kim TI, Cho HS, Suh H, Kim EK (2009) Corneal dystrophy-associated R124H mutation disrupts TGFBI interaction with periostin and causes mislocalization to the lysosome. J Biol Chem 284:19580–19591
32. Paliwal P, Sharma A, Tandon R, Sharma N, Titiyal JS, Sen S, Kaur P, Dube D, Vajpayee RB (2010) TGFBI mutation screening and genotype–phenotype correlation in north Indian patients with corneal dystrophies. Mol Vis 16:1429–1438
33. Park SJ, Park S, Ahn HC, Kim IS, Lee BJ (2004) Conformational resemblance between the structures of integrin-activating pentapeptides derived from betaig-h3 and RGD peptide analogues in a membrane environment. Peptides 25:199–205
34. Rawe IM, Zhan Q, Burrows R, Bennett K, Cintron C (1997) Beta-ig: molecular cloning and in situ hybridization in corneal tissues. Invest Ophthalmol Vis Sci 38:893–900
35. Yun SJ, Kim MO, Kim SO, Park J, Kwon YK, Kim IS, Lee EH (2002) Induction of TGF-beta-inducible gene-h3 (betaig-h3) by TGF-beta1 in astrocytes: implications for astrocyte response to brain injury. Brain Res Mol Brain Res 107:57–64
36. Ohno S, Doi T, Tsutsumi S, Okada Y, Yoneno K, Kato Y, Tanne K (2002) RGD-CAP (βig-h3) is expressed in precartilage condensation and in prehypertrophic chondrocytes during cartilage development. Biochim Biophys Acta 1572:114–122
37. Thapa N, Kang KB, Kim IS (2005) Beta ig-h3 mediates osteoblast adhesion and inhibits differentiation. Bone 36:232–242
38. Hoersch S, Andrade-Navarro MA (2010) Periostin shows increased evolutionary plasticity in its alternatively spliced region. BMC Evol Biol 10:30
39. Bao S, Ouyang G, Bai X, Huang Z, Ma C, Liu M, Shao R, Anderson RM, Rich JN, Wang XF (2004) Periostin potently promotes metastatic growth of colon cancer by augmenting cell survival via the Akt/PKB pathway. Cancer Cell 5:329–339
40. Yoshioka N, Fuji S, Shimakage M, Kodama K, Hakura A, Yutsudo M, Inoue H, Nojima H (2002) Suppression of anchorage-independent growth of human cancer cell lines by the TRIF52/periostin/OSF-2 gene. Exp Cell Res 279:91–99
41. Masinde GL, Li X, Gu W, Wergedal J, Mohan S, Baylink DJ (2002) Quantitative trait loci for bone density in mice: the genes determining total skeletal density and femur density show little overlap in F2 mice. Calcif Tissue Int 71:421–428
42. Kesavan C, Mohan S (2010) Bone mass gained in response to external loading is preserved for several weeks following cessation of loading in 10 week C57BL/6J mice. J Musculoskelet Neuronal Interact 10:274–280
43. Wergedal JE, Sheng MH, Ackert-Bicknell CL, Beamer WG, Baylink DJ (2002) Mouse genetic model for bone strength and size phenotypes: NZB/B1NJ and RF/J inbred strains. Bone 31:670–674
44. Sheng MH, Lau KH, Beamer WG, Baylink DJ, Wergedal JE (2004) In vivo and in vitro evidence that the high osteoblastic activity in C3H/HeJ mice compared to C57BL/6J mice is intrinsic to bone cells. Bone 35:711–719
45. Ohno S, Doi T, Fujimoto K, Ijuin C, Tanaka N, Tanimoto K, Honda K, Nakahara M, Kato Y, Tanne K (2002) RGD-CAP (betaig-h3) exerts a negative regulatory function on mineralization in the human periodontal ligament. J Dent Res 81:822–825
46. Ohno S, Tanaka N, Ueki M, Honda K, Tanimoto K, Yoneno K, Ohno-Nakahara M, Fujimoto K, Kato Y, Tanne K (2005) Mechanical regulation of terminal chondrocyte differentiation via RGD-CAP/beta ig-h3 induced by TGF-beta. Connect Tissue Res 46:227–234
47. Han MS, Kim JE, Shin HI, Kim IS (2008) Expression patterns of betaig-h3 in chondrocyte differentiation during endochondral ossification. Exp Mol Med 40:453–460
48. Dieudonne SC, Kerr JM, Xu T, Sommer B, DeRubeis AR, Kuznetsov SA, Kim IS, Gehron Robey P, Young MF (1999) Differential display of human marrow stromal cells reveals unique mRNA expression patterns in response to dexamethasone. J Cell Biochem 76:231–243
49. Merle B, Garnero P (2012) The multiple facets of periostin in bone metabolism. Osteoporos Int 23:1199–1212
50. Tang Y, Wu X, Lei W, Pang L, Wan C, Shi Z, Zhao L, Nagy TR, Peng X, Hu J, Feng X, Van Hul W, Wan M, Cao X (2009) TGF-beta1-induced migration of bone mesenchymal stem cells couples bone resorption with formation. Nat Med 15:757–765 - 作者单位：1. Musculoskeletal Disease Center, Jerry L. Pettis Memorial VA Medical Center, 11201 Benton Street (151), Loma Linda, CA 92357, USA2. Center for Radiological Research, Herbert Irving Comprehensive Cancer Center, Columbia University, 630 West 168th Street, VC 11-244, New York, NY 10032, USA
- ISSN：1432-0827
文摘
Transforming growth factor-beta induced (TGFBI) and periostin are two closely related proteins in structure as well as in function. A previous study found that periostin positively regulates bone size. Here, we hypothesize that TGFBI has a similar function in bone development. To test this hypothesis, we employed TGFBI-deficient mice, which were generated by targeted disruption of the TGFBI gene. We bred these mice with C57BL/6J mice to generate homozygous TGFBI-deficient (TGFBI−/−) mice and homozygous wild-type littermates. All mice were raised to 12 weeks of age. Bone mass parameters were determined by PIXImus and micro-CT, bone strength parameters by three-point bending, and bone formation and resorption parameters by histomorphometry. We found that targeted disruption of TGFBI led to reduced body size, bone mass, bone size, and bone strength. This indicates that, like periostin, TGFBI also positively regulates bone size and that changes in bone size affect bone strength. Furthermore, there was also a significant decrease in periosteal, but not endosteal, bone formation rate of cortical bone in TGFBI−/− mice, suggesting that the observed effect of TGFBI on bone mass and bone size was largely caused by the effect of TGFBI on periosteal bone formation.