Transforming growth factor alpha controls the transition from hypertrophic cartilage to bone during endochondral bone growth

Bone

Volumn 51, Issue 1, 2012, Pages 131-141

  Usmani, Shirine E ^a   Pest, Michael A ^a   Kim, Gunwoo ^b   Ohora, Sara N ^a   Qin, Ling ^c   Beier, Frank ^a  

^a WESTERN UNIVERSITY   (Canada)

^b Rheumatology Center at Daegu Fatima Hospital   (South Korea)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Chondrocytes; Endochondral ossification; Growth plate; Osteoclasts; Transforming growth factor alpha

Indexed keywords

COLLAGENASE 3; MESSENGER RNA; OSTEOCLAST DIFFERENTIATION FACTOR; TRANSCRIPTION FACTOR RUNX2; TRANSFORMING GROWTH FACTOR ALPHA;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BONE DEVELOPMENT; BONE GROWTH; CONTROLLED STUDY; EMBRYO; ENCHONDRAL OSSIFICATION; FEMALE; GENE; GENE EXPRESSION REGULATION; GENETIC ASSOCIATION; GROWTH PLATE; GROWTH REGULATION; GROWTH RETARDATION; KNOCKOUT MOUSE; MALE; MATRIX METALLOPROTEINASE 13 GENE; MOUSE; NEWBORN; NONHUMAN; OSTEOCLAST; PHENOTYPE; PROTEIN FUNCTION; RECEPTOR ACTIVATOR OF NUCLEAR FACTOR KAPPA B LIGAND GENE; RUNT RELATED TRANSCRIPTION FACTOR 2 GENE;

ANIMALS; BONE AND BONES; BONE DEVELOPMENT; CARTILAGE; CHONDROCYTES; FEMALE; HYPERTROPHY; MALE; MICE; MICE, KNOCKOUT; ORGAN CULTURE TECHNIQUES; TIBIA; TRANSFORMING GROWTH FACTOR ALPHA;

EID: 84861121887     PISSN: 87563282     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bone.2012.04.012     Document Type: Article

References (53)

1. Appleton C.T., Usmani S.E., Bernier S.M., Aigner T., Beier F. Transforming growth factor alpha suppression of articular chondrocyte phenotype and Sox9 expression in a rat model of osteoarthritis. Arthritis Rheum 2007, 56:3693-3705.
2. Appleton C.T., Usmani S.E., Mort J.S., Beier F. Rho/ROCK and MEK/ERK activation by transforming growth factor-alpha induces articular cartilage degradation. Lab Invest 2010, 90:20-30.
3. Appleton C.T., Pitelka V., Henry J., Beier F. Global analyses of gene expression in early experimental osteoarthritis. Arthritis Rheum 2007, 56:1854-1868.
4. Kronenberg H.M. Developmental regulation of the growth plate. Nature 2003, 423:332-336.
5. Kobayashi T., Kronenberg H. Minireview: transcriptional regulation in development of bone. Endocrinology 2005, 146:1012-1017.
6. Ballock R.T., O'Keefe R.J. The biology of the growth plate. J Bone Joint Surg Am 2003, 85-A:715-726.
7. Mackie E.J., Ahmed Y.A., Tatarczuch L., Chen K.S., Mirams M. Endochondral ossification: how cartilage is converted into bone in the developing skeleton. Int J Biochem Cell Biol 2008, 40:46-62.
8. Beier F. Cell-cycle control and the cartilage growth plate. J Cell Physiol 2005, 202:1-8.
9. Kumar V., Bustin S.A., McKay I.A. Transforming growth factor alpha. Cell Biol Int 1995, 19:373-388.
10. Dealy C.N., Scranton V., Cheng H.C. Roles of transforming growth factor-alpha and epidermal growth factor in chick limb development. Dev Biol 1998, 202:43-55.
11. Yoon Y.M., Oh C.D., Kim D.Y., Lee Y.S., Park J.W., Huh T.L., et al. Epidermal growth factor negatively regulates chondrogenesis of mesenchymal cells by modulating the protein kinase C-alpha, Erk-1, and p38 MAPK signaling pathways. J Biol Chem 2000, 275:12353-12359.
12. Huang L., Solursh M., Sandra A. The role of transforming growth factor alpha in rat craniofacial development and chondrogenesis. J Anat 1996, 189(Pt 1):73-86.
13. Wang K., Yamamoto H., Chin J.R., Werb Z., Vu T.H. Epidermal growth factor receptor-deficient mice have delayed primary endochondral ossification because of defective osteoclast recruitment. J Biol Chem 2004, 279:53848-53856.
14. Sibilia M., Wagner B., Hoebertz A., Elliott C., Marino S., Jochum W., et al. Mice humanised for the EGF receptor display hypomorphic phenotypes in skin, bone and heart. Development 2003, 130:4515-4525.
15. Ibbotson K.J., Twardzik D.R., D'Souza S.M., Hargreaves W.R., Todaro G.J., Mundy G.R. Stimulation of bone resorption in vitro by synthetic transforming growth factor-alpha. Science 1985, 228:1007-1009.
16. Ibbotson K.J., Harrod J., Gowen M., D'Souza S., Smith D.D., Winkler M.E., et al. Human recombinant transforming growth factor alpha stimulates bone resorption and inhibits formation in vitro. Proc Natl Acad Sci U S A 1986, 83:2228-2232.
17. Takahashi N., MacDonald B.R., Hon J., Winkler M.E., Derynck R., Mundy G.R., et al. Recombinant human transforming growth factor-alpha stimulates the formation of osteoclast-like cells in long-term human marrow cultures. J Clin Invest 1986, 78:894-898.
18. Zhu J., Jia X., Xiao G., Kang Y., Partridge N.C., Qin L. EGF-like ligands stimulate osteoclastogenesis by regulating expression of osteoclast regulatory factors by osteoblasts: implications for osteolytic bone metastases. J Biol Chem 2007, 282:26656-26664.
19. Mann G.B., Fowler K.J., Gabriel A., Nice E.C., Williams R.L., Dunn A.R. Mice with a null mutation of the TGF alpha gene have abnormal skin architecture, wavy hair, and curly whiskers and often develop corneal inflammation. Cell 1993, 73:249-261.
20. Agoston H., Khan S., James C.G., Gillespie J.R., Serra R., Stanton L.A., et al. C-type natriuretic peptide regulates endochondral bone growth through p38 MAP kinase-dependent and -independent pathways. BMC Dev Biol 2007, 7:18.
21. Ulici V., Hoenselaar K.D., Gillespie J.R., Beier F. The PI3K pathway regulates endochondral bone growth through control of hypertrophic chondrocyte differentiation. BMC Dev Biol 2008, 8:40.
22. Wang G., Woods A., Agoston H., Ulici V., Glogauer M., Beier F. Genetic ablation of Rac1 in cartilage results in chondrodysplasia. Dev Biol 2007, 306:612-623.
23. Ulici V., Hoenselaar K.D., Agoston H., McErlain D.D., Umoh J., Chakrabarti S., et al. The role of Akt1 in terminal stages of endochondral bone formation: angiogenesis and ossification. Bone 2009, 45:1133-1145.
24. Ulici V., James C.G., Hoenselaar K.D., Beier F. Regulation of gene expression by PI3K in mouse growth plate chondrocytes. PLoS One 2010, 5:e8866.
25. Solomon L.A., Li J.R., Berube N.G., Beier F. Loss of ATRX in chondrocytes has minimal effects on skeletal development. PLoS One 2009, 4:e7106.
26. James C.G., Stanton L.A., Agoston H., Ulici V., Underhill T.M., Beier F. Genome-wide analyses of gene expression during mouse endochondral ossification. PLoS One 2010, 5:e8693.
27. James C.G., Woods A., Underhill T.M., Beier F. The transcription factor ATF3 is upregulated during chondrocyte differentiation and represses cyclin D1 and A gene transcription. BMC Mol Biol 2006, 7:30.
28. Yan Q., Feng Q., Beier F. Endothelial nitric oxide synthase deficiency in mice results in reduced chondrocyte proliferation and endochondral bone growth. Arthritis Rheum 2010, 62:2013-2022.
29. Zhang X., Siclari V.A., Lan S., Zhu J., Koyama E., Dupuis H.L., Enomoto-Iwamoto M., Beier F., Qin L. The critical role of the epidermal growth factor receptor in endochondral ossification. J Bone Miner Res 2011, 26:2622-2633.
30. Kong Y.Y., Yoshida H., Sarosi I., Tan H.L., Timms E., Capparelli C., et al. OPGL is a key regulator of osteoclastogenesis, lymphocyte development and lymph-node organogenesis. Nature 1999, 397:315-323.
31. Usui M., Xing L., Drissi H., Zuscik M., O'Keefe R., Chen D., et al. Murine and chicken chondrocytes regulate osteoclastogenesis by producing RANKL in response to BMP2. J Bone Miner Res 2008, 23:314-325.
32. Kim N., Odgren P.R., Kim D.K., Marks S.C., Choi Y. Diverse roles of the tumor necrosis factor family member TRANCE in skeletal physiology revealed by TRANCE deficiency and partial rescue by a lymphocyte-expressed TRANCE transgene. Proc Natl Acad Sci U S A 2000, 97:10905-10910.
33. Inada M., Wang Y., Byrne M.H., Rahman M.U., Miyaura C., Lopez-Otin C., et al. Critical roles for collagenase-3 (Mmp13) in development of growth plate cartilage and in endochondral ossification. Proc Natl Acad Sci U S A 2004, 101:17192-17197.
34. Stickens D., Behonick D.J., Ortega N., Heyer B., Hartenstein B., Yu Y., et al. Altered endochondral bone development in matrix metalloproteinase 13-deficient mice. Development 2004, 131:5883-5895.
35. Vu T.H., Shipley J.M., Bergers G., Berger J.E., Helms J.A., Hanahan D., et al. MMP-9/gelatinase B is a key regulator of growth plate angiogenesis and apoptosis of hypertrophic chondrocytes. Cell 1998, 93:411-422.
36. Inada M., Yasui T., Nomura S., Miyake S., Deguchi K., Himeno M., et al. Maturational disturbance of chondrocytes in Cbfa1-deficient mice. Dev Dyn 1999, 214:279-290.
37. Kim I.S., Otto F., Zabel B., Mundlos S. Regulation of chondrocyte differentiation by Cbfa1. Mech Dev 1999, 80:159-170.
38. Jimenez M.J., Balbin M., Lopez J.M., Alvarez J., Komori T., Lopez-Otin C. Collagenase 3 is a target of Cbfa1, a transcription factor of the runt gene family involved in bone formation. Mol Cell Biol 1999, 19:4431-4442.
39. Geoffroy V., Kneissel M., Fournier B., Boyde A., Matthias P. High bone resorption in adult aging transgenic mice overexpressing cbfa1/runx2 in cells of the osteoblastic lineage. Mol Cell Biol 2002, 22:6222-6233.
40. Akagi M., Kawaguchi M., Liu W., McCarty M.F., Takeda A., Fan F., et al. Induction of neuropilin-1 and vascular endothelial growth factor by epidermal growth factor in human gastric cancer cells. Br J Cancer 2003, 88:796-802.
41. Perrotte P., Matsumoto T., Inoue K., Kuniyasu H., Eve B.Y., Hicklin D.J., et al. Anti-epidermal growth factor receptor antibody C225 inhibits angiogenesis in human transitional cell carcinoma growing orthotopically in nude mice. Clin Cancer Res 1999, 5:257-265.
42. Gerber H.P., Ferrara N. Angiogenesis and bone growth. Trends Cardiovasc Med 2000, 10:223-228.
43. De Luca A., Gallo M., Aldinucci D., Ribatti D., Lamura L., D'Alessio A., De Filippi R., Pinto A., Normanno N. The role of the EGFR ligand/receptor system in the secretion of angiogenic factors in mesenchymal stem cells. J Cell Physiol. 2011, 226(8):2131-2138.
44. Gerber H.P., Vu T.H., Ryan A.M., Kowalski J., Werb Z., Ferrara N. VEGF couples hypertrophic cartilage remodeling, ossification and angiogenesis during endochondral bone formation. Nat Med 1999, 5:623-628.
45. Holmbeck K., Bianco P., Caterina J., Yamada S., Kromer M., Kuznetsov S.A., et al. MT1-MMP-deficient mice develop dwarfism, osteopenia, arthritis, and connective tissue disease due to inadequate collagen turnover. Cell 1999, 99:81-92.
46. Harris R.C., Chung E., Coffey R.J. EGF receptor ligands. Exp Cell Res 2003, 284:2-13.
47. Luetteke N.C., Qiu T.H., Fenton S.E., Troyer K.L., Riedel R.F., Chang A., et al. Targeted inactivation of the EGF and amphiregulin genes reveals distinct roles for EGF receptor ligands in mouse mammary gland development. Development 1999, 126:2739-2750.
48. Schneider M.R., Dahlhoff M., Herbach N., Renner-Mueller I., Dalke C., Puk O., et al. Betacellulin overexpression in transgenic mice causes disproportionate growth, pulmonary hemorrhage syndrome, and complex eye pathology. Endocrinology 2005, 146:5237-5246.
49. Chan S.Y., Wong R.W. Expression of epidermal growth factor in transgenic mice causes growth retardation. J Biol Chem 2000, 275:38693-38698.
50. Qin L., Tamasi J., Raggatt L., Li X., Feyen J.H., Lee D.C., et al. Amphiregulin is a novel growth factor involved in normal bone development and in the cellular response to parathyroid hormone stimulation. J Biol Chem 2005, 280:3974-3981.
51. Schneider M.R., Sibilia M., Erben R.G. The EGFR network in bone biology and pathology. Trends Endocrinol Metab 2009, 20:517-524.
52. Nilsson O., Baron J. Impact of growth plate senescence on catch-up growth and epiphyseal fusion. Pediatr Nephrol 2005, 20:319-322.
53. Nilsson O., Baron J. Fundamental limits on longitudinal bone growth: growth plate senescence and epiphyseal fusion. Trends Endocrinol Metab 2004, 15:370-374.