βig-h3 potentiates the profibrogenic effect of TGFβ signaling on connective tissue progenitor cells through the negative regulation of master chondrogenic genes

Tissue Engineering - Part A

Volumn 19, Issue 3-4, 2013, Pages 448-457

  Lorda Diez, Carlos I ^a   Montero, Juan A ^a   Diaz Mendoza, Manuel J ^a   Garcia Porrero, Juan A ^a   Hurle, Juan M ^a  

^a UNIVERSITY OF CANTABRIA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATION ANALYSIS; AGGREGATES; CARTILAGE; CELLS; COLLAGEN; GENE EXPRESSION; TENDONS;

CELL AGGREGATES; CHONDROGENIC; CONNECTIVE TISSUE CELLS; CONNECTIVE TISSUES; DEGENERATIVE DISEASE; FIBROUS CONNECTIVE TISSUE; GENE EXPRESSION ANALYSIS; HYPOXIC CONDITION; INITIAL STAGES; MESENCHYMAL STEM CELL; MICROENVIRONMENTS; MICROMASS; MOLECULAR BASIS; MOLECULAR MARKER; PROGENITOR CELL; REGENERATIVE MEDICINE; TRANSFORMING GROWTH FACTORS; TYPE II COLLAGENS;

CELL CULTURE;

MUS;

BETAIG H3 PROTEIN; BETAIG-H3 PROTEIN; FIBRINOLYTIC AGENT; SCLEROPROTEIN; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL; ARTICLE; CARTILAGE CELL; CELL CULTURE; CELL DIFFERENTIATION; CHICK EMBRYO; CHONDROGENESIS; CONNECTIVE TISSUE; CYTOLOGY; DRUG EFFECT; GENE EXPRESSION REGULATION; GROWTH, DEVELOPMENT AND AGING; HISTOLOGY; MESENCHYMAL STROMA CELL; MOUSE; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; CELL DIFFERENTIATION; CELLS, CULTURED; CHICK EMBRYO; CHONDROCYTES; CHONDROGENESIS; CONNECTIVE TISSUE; EXTRACELLULAR MATRIX PROTEINS; FIBRINOLYTIC AGENTS; GENE EXPRESSION REGULATION; MESENCHYMAL STROMAL CELLS; MICE; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA;

MLCS; MLOWN;

EID: 84872121165     PISSN: 19373341     EISSN: 1937335X     Source Type: Journal    
DOI: 10.1089/ten.tea.2012.0188     Document Type: Article

References (49)

1. Montero, J.A., Lorda-Diez, C.I., and Hurle, J.M. Regenerative medicine and connective tissues: cartilage versus tendon. J Tissue Eng Regenerative Med 6, 337, 2012.
2. Oka, K., Oka, S., Hosokawa, R., Bringas, P.,Jr, Brockhoff, H.C.,2nd, Nonaka, K., and Chai, Y. TGF-beta mediated Dlx5 signaling plays a crucial role in osteo-chondroprogenitor cell lineage determination during mandible development. Dev Biol 321, 303, 2008.
3. Mauviel, A. Transforming growth factor-beta: a key medi-ator of fibrosis. Methods Mol Med 117, 69, 2005.
4. Pryce, B.A., Watson, S.S., Murchison, N.D., Staverosky, J.A., Dunker, N., and Schweitzer, R. Recruitment and mainte-nance of tendon progenitors by TGFbeta signaling are essential for tendon formation. Development (Cambridge, England) 136, 1351, 2009.
5. Spagnoli, A., O'Rear, L., Chandler, R.L., Granero-Molto, F., Mortlock, D.P., Gorska, A.E., Weis, J.A., Longobardi, L., Chytil, A., Shimer, K., and Moses, H.L. TGF-beta signaling is essential for joint morphogenesis. J Cell Biol 177,1105, 2007.
6. Seo, H.S., and Serra, R. Deletion of Tgfbr2 in Prx1-cre ex-pressing mesenchyme results in defects in development of the long bones and joints. Dev Biol 310, 304, 2007.
7. Baffi, M.O., Moran, M.A., and Serra, R. Tgfbr2 regulates the maintenance of boundaries in the axial skeleton. Dev Biol 296, 363, 2006.
8. Lorda-Diez, C.I., Montero, J.A., Martinez-Cue, C., Garcia-Porrero, JA., and Hurle, J.M. Transforming growth factors beta coordinate cartilage and tendon differentiation in the developing limb mesenchyme. J Biol Chem 284, 29988, 2009.
9. Ikushima, H., and Miyazono, K. Cellular context-dependent ''colors'' of transforming growth factor-beta signaling. Can-cer Sci 101, 306, 2010.
10. Ganan, Y., Macias, D., Duterque-Coquillaud, M., Ros, M.A., and Hurle, J.M. Role of TGF beta s and BMPs as signals controlling the position of the digits and the areas of inter-digital cell death in the developing chick limb autopod. Development (Cambridge, England) 122, 2349, 1996.
11. Asou, Y., Nifuji, A., Tsuji, K., Shinomiya, K., Olson, E.N., Koopman, P., and Noda, M. Coordinated expression of scleraxis and Sox9 genes during embryonic development of tendons and cartilage. J Orthop Res 20, 827, 2002.
12. Furumatsu, T., Hachioji, M., Saiga, K., Takata, N., Yokoya-ma, Y., and Ozaki, T. Anterior cruciate ligament-derived cells have high chondrogenic potential. Biochem Biophys Res Commun 391, 1142, 2010.
13. Schorderet, D.F., Menasche, M., Morand, S., Bonnel, S., Buchillier, V., Marchant, D., Auderset, K., Bonny, C., Abit-bol, M., and Munier, F.L. Genomic characterization and embryonic expression of the mouse Bigh3 (Tgfbi) gene. Biochem Biophys Res Commun 274, 267, 2000.
14. Ohno, S., Doi, T., Tsutsumi, S., Okada, Y., Yoneno, K., Kato, Y., and Tanne, K. RGD-CAP ((beta)ig-h3) is expressed in precartilage condensation and in prehypertrophic chon-drocytes during cartilage development. Biochim Biophys Acta 1572, 114, 2002.
15. Doi, T., Ohno, S., Tanimoto, K., Honda, K., Tanaka, N., Ohno-Nakahara, M., Yoneno, K., Suzuki, A., Nakatani, Y., Ueki, M., and Tanne, K. Mechanical stimuli enhances the expression of RGD-CAP/betaig-h3 in the periodontal liga-ment. Arch Oral Biol 48, 573, 2003.
16. Ferguson, J.W., Mikesh, M.F., Wheeler, E.F., and LeBaron, R.G. Developmental expression patterns of Beta-ig (betaIG-H3) and its function as a cell adhesion protein. Mech Dev 120, 851, 2003.
17. Kawamoto, T., Noshiro, M., Shen, M., Nakamasu, K., Ha-shimoto, K., Kawashima-Ohya, Y., Gotoh, O., and Kato, Y. Structural and phylogenetic analyses of RGD-CAP/beta ig-h3, a fasciclin-like adhesion protein expressed in chick chondrocytes. Biochim Biophys Acta 1395, 288, 1998.
18. Thapa, N., Lee, B.H., and Kim, I.S. TGFBIp/betaig-h3 pro-tein: a versatile matrix molecule induced by TGF-beta. Int J Biochem Cell Biol 39, 2183, 2007.
19. Kim, J.E., Kim, S.J., Lee, B.H., Park, R.W., Kim, K.S., and Kim, I.S. Identification of motifs for cell adhesion within the repeated domains of transforming growth factor-beta-induced gene, betaig-h3. J Biol Chem 275, 30907, 2000.
20. Billings, P.C., Whitbeck, J.C., Adams, C.S., Abrams, W.R., Cohen, A.J., Engelsberg, B.N., Howard, P.S., and Rosen-bloom, J. The transforming growth factor-beta-inducible matrix protein (beta)ig-h3 interacts with fibronectin. J Biol Chem 277, 28003, 2002.
21. Oh, J.E., Kook, J.K., and Min, B.M. Beta ig-h3 induces ker-atinocyte differentiation via modulation of involucrin and transglutaminase expression through the integrin alpha3-beta1 and the phosphatidylinositol 3-kinase/Akt signaling pathway. J Biol Chem 280, 21629, 2005.
22. Lee, B.H., Bae, J.S., Park, R.W., Kim, J.E., Park, J.Y., and Kim, I.S. Betaig-H3 triggers signaling pathways mediat-ing adhesion and migration of vascular smooth muscle cells through alphavbeta5 integrin. Exp Mol Med 38, 153, 2006.
23. Poulaki, V., and Colby, K. Genetics of anterior and stromal corneal dystrophies. Semin Ophthalmol 23, 9, 2008.
24. Ivanov, S.V., Ivanova, A.V., Salnikow, K., Timofeeva, O., Subramaniam, M., and Lerman, M.I. Two novel VHL targets, TGFBI (BIGH3) and its transactivator KLF10, are up-regulated in renal clear cell carcinoma and other tumors. Biochem Biophys Res Commun 370, 536, 2008.
25. Wise, T.G., Schafer, D.J., Lambeth, L.S., Tyack, S.G., Bruce, M.P., Moore, R.J., and Doran, T.J. Characterization and comparison of chicken U6 promoters for the expression of short hairpin RNAs. Anim Biotechnol 18, 153, 2007.
26. Knepper, J.L., James, A.C., and Ming, J.E. TGIF, a gene associated with human brain defects, regulates neuronal development. Dev Dyn 235, 1482, 2006.
27. Livak, K.J., and Schmittgen, T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods (San Diego, Calif.) 25, 402, 2001.
28. Lorda-Diez, C.I., Montero, J.A., Garcia-Porrero, J.A., and Hurle, J.M. Tgfbeta2 and 3 are coexpressed with their ex-tracellular regulator Ltbp1 in the early limb bud and mod-ulate mesodermal outgrowth and BMP signaling in chicken embryos. BMC Dev Biol 10, 69, 2010.
29. Daniels, K., Reiter, R., and Solursh, M. Micromass cultures of limb and other mesenchyme. Methods Cell Biol 51, 237, 1996.
30. Han, M.S., Kim, J.E., Shin, H.I., and Kim, I.S. Expression patterns of betaig-h3 in chondrocyte differentiation during endochondral ossification. Exp Mol Med 40, 453, 2008.
31. Pieramici, S.F., and Afshari, N.A. Genetics of corneal dys-trophies: the evolving landscape. Curr Opin Ophthalmol 17, 361, 2006.
32. Choi, KY., Kim, H.J., Cho, B.C., Kim, I.S., Kim, H.J., and Ryoo, H.M. A TGF-beta-induced gene, betaig-h3, is crucial for the apoptotic disappearance of the medial edge epithe-lium in palate fusion. J Cell Biochem 107, 818, 2009.
33. Kim, H.R., and Ingham, P.W. The extracellular matrix pro-tein TGFBI promotes myofibril bundling and muscle fibre growth in the zebrafish embryo. Dev Dyn 238, 56, 2009.
34. Norris, R.A., Kern, C.B., Wessels, A., Wirrig, E.E., Mark-wald, R.R., and Mjaatvedt, C.H. Detection of betaig-H3, a TGFbeta induced gene, during cardiac development and its complementary pattern with periostin. Anat Embryol 210, 13, 2005.
35. Montero, J.A., Lorda-Diez, C.I., Ganan, Y., Macias, D., and Hurle, J.M. Activin/TGFbeta and BMP crosstalk determines digit chondrogenesis. Dev Biol 321, 343, 2008.
36. Hurle, J.M., Ros, M.A., Ganan, Y., Macias, D., Critchlow, M., and Hinchliffe, J.R. Experimental analysis of the role of ECM in the patterning of the distal tendons of the developing limb bud. Cell Differ Dev 30, 97, 1990.
37. Thomopoulos, S., Genin, G.M., and Galatz, L.M. The de-velopment and morphogenesis of the tendon-to-bone inser-tion - what development can teach us about healing -. J Musculoskelet Neuronal Interact 10, 35, 2010.
38. Akiyama, H., Chaboissier, M.C., Martin, J.F., Schedl, A., and de Crombrugghe, B. The transcription factor Sox9 has es-sential roles in successive steps of the chondrocyte differ-entiation pathway and is required for expression of Sox5 and Sox6. Genes Dev 16, 2813, 2002.
39. Amarilio, R., Viukov, S.V., Sharir, A., Eshkar-Oren, I., Johnson, R.S., and Zelzer, E. HIF1alpha regulation of Sox9 is necessary to maintain differentiation of hypoxic prechon-drogenic cells during early skeletogenesis. Development (Cambridge, England) 134, 3917, 2007.
40. Provot, S., Zinyk, D., Gunes, Y., Kathri, R., Le, Q., Kronen-berg, H.M., Johnson, R.S., Longaker, M.T., Giaccia, A.J., and Schipani, E. Hif-1alpha regulates differentiation of limb bud mesenchyme and joint development. J Cell Biol 177, 451, 2007.
41. Malladi, P., Xu, Y., Chiou, M., Giaccia, A.J., and Longaker, M.T. Hypoxia inducible factor-1alpha deficiency affects chondrogenesis of adipose-derived adult stromal cells. Tis-sue Eng 13, 1159, 2007.
42. Duval, E., Leclercq, S., Elissalde, J.M., Demoor, M., Galera, P., and Boumediene, K. Hypoxia-inducible factor 1alpha inhibits the fibroblast-like markers type I and type III colla-gen during hypoxia-induced chondrocyte redifferentiation hypoxia not only induces type II collagen and aggrecan, but it also inhibits type I and type III collagen in the hypoxia-inducible factor 1alpha-dependent redifferentiation of chondrocytes. Arthritis Rheum 60, 3038, 2009.
43. Robins, J.C., Akeno, N., Mukherjee, A., Dalal, R.R., Aronow, B.J., Koopman, P., and Clemens, T.L. Hypoxia induces chondrocyte-specific gene expression in mesenchymal cells in association with transcriptional activation of Sox9. Bone 37, 313, 2005.
44. Ito, Y., Toriuchi, N., Yoshitaka, T., Ueno-Kudoh, H., Sato, T., Yokoyama, S., Nishida, K., Akimoto, T., Takahashi, M., Miyaki, S., and Asahara, H. The Mohawk homeobox gene is a critical regulator of tendon differentiation. Proc Natl Acad Sci U S A 107, 10538, 2010.
45. Liu, W., Watson, S.S., Lan, Y., Keene, D.R., Ovitt, C.E., Liu, H., Schweitzer, R., and Jiang, R The atypical homeodomain transcription factor Mohawk controls tendon morphogene-sis. Mol Cell Biol 30, 4797, 2010.
46. Merino, R., Ganan, Y., Macias, D., Economides, A.N., Sampath, K.T., and Hurle, J.M. Morphogenesis of digits in the avian limb is controlled by FGFs, TGFbetas, and noggin through BMP signaling. Dev Biol 200, 35, 1998.
47. Denker, A.E., Nicoll, S.B., and Tuan, R.S. Formation of cartilage-like spheroids by micromass cultures of murine C3H10T1/2 cells upon treatment with transforming growth factor-beta 1. Differentiation 59, 25, 1995.
48. Johnstone, B., Hering, T.M., Caplan, A.I., Goldberg, V.M., and Yoo, J.U. In vitro chondrogenesis of bone marrow-derived mesenchymal progenitor cells. Exp Cell Res 238, 265,1998.
49. Karamboulas, K., Dranse, H.J., and Underhill, T.M. Reg-ulation of BMP-dependent chondrogenesis in early limb mesenchyme by TGFbeta signals. J Cell Sci 123, 2068, 2010.