MT1-MMP Inactivates ADAM9 to Regulate FGFR2 Signaling and Calvarial Osteogenesis

Developmental Cell

Volumn 22, Issue 6, 2012, Pages 1176-1190

  Chan, Kui Ming ^a,b   Wong, Hoi Leong Xavier ^a,b   Jin, Guoxiang ^a,b   Liu, Baohua ^a,b   Cao, Renhai ^c   Cao, Yihai ^c   Lehti, Kaisa ^d   Tryggvason, Karl ^c   Zhou, Zhongjun ^a,b  

^a UNIVERSITY OF HONG KONG   (China)

^b UNIVERSITY OF HONG KONG   (Hong Kong)

^c KAROLINSKA INSTITUTE   (Sweden)

^d UNIVERSITY OF HELSINKI   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

FIBROBLAST GROWTH FACTOR RECEPTOR 2; MATRIX METALLOPROTEINASE; MATRIX METALLOPROTEINASE 14;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BONE DEVELOPMENT; BONE GROWTH; CALVARIA; CELL PROLIFERATION; CONTROLLED STUDY; MOUSE; NONHUMAN; OSTEOBLAST; PRIORITY JOURNAL; PROTEIN DEGRADATION; UPREGULATION;

ADAM PROTEINS; ANIMALS; CELLS, CULTURED; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MATRIX METALLOPROTEINASE 14; MEMBRANE PROTEINS; MICE; OSTEOBLASTS; OSTEOGENESIS; RECEPTOR, FIBROBLAST GROWTH FACTOR, TYPE 2; SIGNAL TRANSDUCTION; SKULL;

MUS;

EID: 84862120224     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2012.04.014     Document Type: Article

References (50)

1. Barbolina M.V., Stack M.S. Membrane type 1-matrix metalloproteinase: substrate diversity in pericellular proteolysis. Semin. Cell Dev. Biol. 2008, 19:24-33.
2. Cabrita M.A., Christofori G. Sprouty proteins: antagonists of endothelial cell signaling and more. Thromb. Haemost. 2003, 90:586-590.
3. Catela C., Bilbao-Cortes D., Slonimsky E., Kratsios P., Rosenthal N., Te Welscher P. Multiple congenital malformations of Wolf-Hirschhorn syndrome are recapitulated in Fgfrl1 null mice. Dis. Model. Mech. 2009, 2:283-294.
4. Celli G., LaRochelle W.J., Mackem S., Sharp R., Merlino G. Soluble dominant-negative receptor uncovers essential roles for fibroblast growth factors in multi-organ induction and patterning. EMBO J. 1998, 17:1642-1655.
5. Deng C.X., Wynshaw-Boris A., Shen M.M., Daugherty C., Ornitz D.M., Leder P. Murine FGFR-1 is required for early postimplantation growth and axial organization. Genes Dev. 1994, 8:3045-3057.
6. Ding B.S., Nolan D.J., Guo P., Babazadeh A.O., Cao Z., Rosenwaks Z., Crystal R.G., Simons M., Sato T.N., Worgall S., et al. Endothelial-derived angiocrine signals induce and sustain regenerative lung alveolarization. Cell 2011, 147:539-553.
7. Foster B.A., Evangelou A., Gingrich J.R., Kaplan P.J., DeMayo F., Greenberg N.M. Enforced expression of FGF-7 promotes epithelial hyperplasia whereas a dominant negative FGFR2iiib promotes the emergence of neuroendocrine phenotype in prostate glands of transgenic mice. Differentiation 2002, 70:624-632.
8. Fürthauer M., Lin W., Ang S.L., Thisse B., Thisse C. Sef is a feedback-induced antagonist of Ras/MAPK-mediated FGF signalling. Nat. Cell Biol. 2002, 4:170-174.
9. Holmbeck K., Bianco P., Caterina J., Yamada S., Kromer M., Kuznetsov S.A., Mankani M., Robey P.G., Poole A.R., Pidoux I., et al. MT1-MMP-deficient mice develop dwarfism, osteopenia, arthritis, and connective tissue disease due to inadequate collagen turnover. Cell 1999, 99:81-92.
10. Holmbeck K., Bianco P., Chrysovergis K., Yamada S., Birkedal-Hansen H. MT1-MMP-dependent, apoptotic remodeling of unmineralized cartilage: a critical process in skeletal growth. J. Cell Biol. 2003, 163:661-671.
11. Holmbeck K., Bianco P., Pidoux I., Inoue S., Billinghurst R.C., Wu W., Chrysovergis K., Yamada S., Birkedal-Hansen H., Poole A.R. The metalloproteinase MT1-MMP is required for normal development and maintenance of osteocyte processes in bone. J. Cell Sci. 2005, 118:147-156.
12. Ignelzi M.A., Wang W., Young A.T. Fibroblast growth factors lead to increased Msx2 expression and fusion in calvarial sutures. J. Bone Miner. Res. 2003, 18:751-759.
13. Inoue K., Mikuni-Takagaki Y., Oikawa K., Itoh T., Inada M., Noguchi T., Park J.S., Onodera T., Krane S.M., Noda M., Itohara S. A crucial role for matrix metalloproteinase 2 in osteocytic canalicular formation and bone metabolism. J. Biol. Chem. 2006, 281:33814-33824.
14. Kim H.J., Rice D.P., Kettunen P.J., Thesleff I. FGF-, BMP- and Shh-mediated signalling pathways in the regulation of cranial suture morphogenesis and calvarial bone development. Development 1998, 125:1241-1251.
15. Kim H.J., Lee M.H., Park H.S., Park M.H., Lee S.W., Kim S.Y., Choi J.Y., Shin H.I., Kim H.J., Ryoo H.M. Erk pathway and activator protein 1 play crucial roles in FGF2-stimulated premature cranial suture closure. Dev. Dyn. 2003, 227:335-346.
16. Levi E., Fridman R., Miao H.Q., Ma Y.S., Yayon A., Vlodavsky I. Matrix metalloproteinase 2 releases active soluble ectodomain of fibroblast growth factor receptor 1. Proc. Natl. Acad. Sci. USA 1996, 93:7069-7074.
17. Li S., Quarto N., Longaker M.T. Activation of FGF signaling mediates proliferative and osteogenic differences between neural crest derived frontal and mesoderm parietal derived bone. PLoS One 2010, 5:e14033.
18. Liu C., Xu P., Lamouille S., Xu J., Derynck R. TACE-mediated ectodomain shedding of the type I TGF-beta receptor downregulates TGF-beta signaling. Mol. Cell 2009, 35:26-36.
19. Liu Z., Xu J., Colvin J.S., Ornitz D.M. Coordination of chondrogenesis and osteogenesis by fibroblast growth factor 18. Genes Dev. 2002, 16:859-869.
20. Maas R., Chen Y.P., Bei M., Woo I., Satokata I. The role of Msx genes in mammalian development. Ann. N Y Acad. Sci. 1996, 785:171-181.
21. Maretzky T., Le Gall S.M., Worpenberg-Pietruk S., Eder J., Overall C.M., Huang X.Y., Poghosyan Z., Edwards D.R., Blobel C.P. Src stimulates fibroblast growth factor receptor-2 shedding by an ADAM15 splice variant linked to breast cancer. Cancer Res. 2009, 69:4573-4576.
22. Maretzky T., Yang G., Ouerfelli O., Overall C.M., Worpenberg S., Hassiepen U., Eder J., Blobel C.P. Characterization of the catalytic activity of the membrane-anchored metalloproteinase ADAM15 in cell-based assays. Biochem. J. 2009, 420:105-113.
23. Maretzky T., Zhou W., Huang X.Y., Blobel C.P. A transforming Src mutant increases the bioavailability of EGFR ligands via stimulation of the cell-surface metalloproteinase ADAM17. Oncogene 2011, 30:611-618.
24. Maruyama T., Mirando A.J., Deng C.X., Hsu W. The balance of WNT and FGF signaling influences mesenchymal stem cell fate during skeletal development. Sci. Signal. 2010, 3:ra40.
25. Miettinen P.J., Chin J.R., Shum L., Slavkin H.C., Shuler C.F., Derynck R., Werb Z. Epidermal growth factor receptor function is necessary for normal craniofacial development and palate closure. Nat. Genet. 1999, 22:69-73.
26. Miraoui H., Marie P.J. Fibroblast growth factor receptor signaling crosstalk in skeletogenesis. Sci. Signal. 2010, 3:re9.
27. Montero A., Okada Y., Tomita M., Ito M., Tsurukami H., Nakamura T., Doetschman T., Coffin J.D., Hurley M.M. Disruption of the fibroblast growth factor-2 gene results in decreased bone mass and bone formation. J. Clin. Invest. 2000, 105:1085-1093.
28. Mosig R.A., Dowling O., DiFeo A., Ramirez M.C., Parker I.C., Abe E., Diouri J., Aqeel A.A., Wylie J.D., Oblander S.A., et al. Loss of MMP-2 disrupts skeletal and craniofacial development and results in decreased bone mineralization, joint erosion and defects in osteoblast and osteoclast growth. Hum. Mol. Genet. 2007, 16:1113-1123.
29. Oblander S.A., Zhou Z., Gálvez B.G., Starcher B., Shannon J.M., Durbeej M., Arroyo A.G., Tryggvason K., Apte S.S. Distinctive functions of membrane type 1 matrix-metalloprotease (MT1-MMP or MMP-14) in lung and submandibular gland development are independent of its role in pro-MMP-2 activation. Dev. Biol. 2005, 277:255-269.
30. Ohbayashi N., Shibayama M., Kurotaki Y., Imanishi M., Fujimori T., Itoh N., Takada S. FGF18 is required for normal cell proliferation and differentiation during osteogenesis and chondrogenesis. Genes Dev. 2002, 16:870-879.
31. Onguchi T., Han K.Y., Chang J.H., Azar D.T. Membrane type-1 matrix metalloproteinase potentiates basic fibroblast growth factor-induced corneal neovascularization. Am. J. Pathol. 2009, 174:1564-1571.
32. Ornitz D.M., Marie P.J. FGF signaling pathways in endochondral and intramembranous bone development and human genetic disease. Genes Dev. 2002, 16:1446-1465.
33. Peduto L. ADAM9 as a potential target molecule in cancer. Curr. Pharm. Des. 2009, 15:2282-2287.
34. Peduto L., Reuter V.E., Shaffer D.R., Scher H.I., Blobel C.P. Critical function for ADAM9 in mouse prostate cancer. Cancer Res. 2005, 65:9312-9319.
35. Powers C.J., McLeskey S.W., Wellstein A. Fibroblast growth factors, their receptors and signaling. Endocr. Relat. Cancer 2000, 7:165-197.
36. Ramasamy S.K., Mailleux A.A., Gupte V.V., Mata F., Sala F.G., Veltmaat J.M., Del Moral P.M., De Langhe S., Parsa S., Kelly L.K., et al. Fgf10 dosage is critical for the amplification of epithelial cell progenitors and for the formation of multiple mesenchymal lineages during lung development. Dev. Biol. 2007, 307:237-247.
37. Rice D.P., Aberg T., Chan Y., Tang Z., Kettunen P.J., Pakarinen L., Maxson R.E., Thesleff I. Integration of FGF and TWIST in calvarial bone and suture development. Development 2000, 127:1845-1855.
38. Satokata I., Maas R. Msx1 deficient mice exhibit cleft palate and abnormalities of craniofacial and tooth development. Nat. Genet. 1994, 6:348-356.
39. Satokata I., Ma L., Ohshima H., Bei M., Woo I., Nishizawa K., Maeda T., Takano Y., Uchiyama M., Heaney S., et al. Msx2 deficiency in mice causes pleiotropic defects in bone growth and ectodermal organ formation. Nat. Genet. 2000, 24:391-395.
40. Schneider M.R., Sibilia M., Erben R.G. The EGFR network in bone biology and pathology. Trends Endocrinol. Metab. 2009, 20:517-524.
41. Sleeman M., Fraser J., McDonald M., Yuan S., White D., Grandison P., Kumble K., Watson J.D., Murison J.G. Identification of a new fibroblast growth factor receptor, FGFR5. Gene 2001, 271:171-182.
42. Smith T.G., Sweetman D., Patterson M., Keyse S.M., Münsterberg A. Feedback interactions between MKP3 and ERK MAP kinase control scleraxis expression and the specification of rib progenitors in the developing chick somite. Development 2005, 132:1305-1314.
43. Sugiyama N., Varjosalo M., Meller P., Lohi J., Chan K.M., Zhou Z., Alitalo K., Taipale J., Keski-Oja J., Lehti K. FGF receptor-4 (FGFR4) polymorphism acts as an activity switch of a membrane type 1 matrix metalloproteinase-FGFR4 complex. Proc. Natl. Acad. Sci. USA 2010, 107:15786-15791.
44. Trueb B. Biology of FGFRL1, the fifth fibroblast growth factor receptor. Cell. Mol. Life Sci. 2011, 68:951-964.
45. Werb Z. ECM and cell surface proteolysis: regulating cellular ecology. Cell 1997, 91:439-442.
46. Weskamp G., Cai H., Brodie T.A., Higashyama S., Manova K., Ludwig T., Blobel C.P. Mice lacking the metalloprotease-disintegrin MDC9 (ADAM9) have no evident major abnormalities during development or adult life. Mol. Cell. Biol. 2002, 22:1537-1544.
47. Xu X., Weinstein M., Li C., Naski M., Cohen R.I., Ornitz D.M., Leder P., Deng C. Fibroblast growth factor receptor 2 (FGFR2)-mediated reciprocal regulation loop between FGF8 and FGF10 is essential for limb induction. Development 1998, 125:753-765.
48. Yamaguchi T.P., Harpal K., Henkemeyer M., Rossant J. fgfr-1 is required for embryonic growth and mesodermal patterning during mouse gastrulation. Genes Dev. 1994, 8:3032-3044.
49. Yu K., Xu J., Liu Z., Sosic D., Shao J., Olson E.N., Towler D.A., Ornitz D.M. Conditional inactivation of FGF receptor 2 reveals an essential role for FGF signaling in the regulation of osteoblast function and bone growth. Development 2003, 130:3063-3074.
50. Zhou Z., Apte S.S., Soininen R., Cao R., Baaklini G.Y., Rauser R.W., Wang J., Cao Y., Tryggvason K. Impaired endochondral ossification and angiogenesis in mice deficient in membrane-type matrix metalloproteinase I. Proc. Natl. Acad. Sci. USA 2000, 97:4052-4057.