Divergent upstream osteogenic events contribute to the differential modulation of MG63 cell osteoblast differentiation by MMP-1 (collagenase-1) and MMP-13 (collagenase-3)

Matrix Biology

Volumn 30, Issue 4, 2011, Pages 281-289

  Hayami, Takayuki ^a   Kapila, Yvonne L ^a   Kapila, Sunil ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

Author keywords

Alkaline phosphatase; MMP 1; MMP 13; Osteoblast differentiation; Transcription factors

Indexed keywords

ALKALINE PHOSPHATASE; BONE MORPHOGENETIC PROTEIN 2; BONE SIALOPROTEIN; COLLAGENASE 3; INTERSTITIAL COLLAGENASE; OSTEOCALCIN; TRANSCRIPTION FACTOR DLX5; TRANSCRIPTION FACTOR MSX2; TRANSCRIPTION FACTOR OSTERIX; TRANSCRIPTION FACTOR RUNX2; TRANSFORMING GROWTH FACTOR BETA1;

ARTICLE; BONE DEVELOPMENT; CELL DIFFERENTIATION; CELL LINE; CELL MATURATION; CELL SPECIFICITY; CONTROLLED STUDY; ENZYME ACTIVITY; HUMAN; HUMAN CELL; MESENCHYMAL STEM CELL; OSTEOBLAST; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

ALKALINE PHOSPHATASE; ANTIGENS, DIFFERENTIATION; CELL DIFFERENTIATION; CELL LINE; ENZYME ASSAYS; GENE EXPRESSION REGULATION; HUMANS; MATRIX METALLOPROTEINASE 1; MATRIX METALLOPROTEINASE 13; OSTEOBLASTS; RECOMBINANT PROTEINS; RNA INTERFERENCE; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 79958164768     PISSN: 0945053X     EISSN: 15691802     Source Type: Journal    
DOI: 10.1016/j.matbio.2011.04.003     Document Type: Article

References (50)

1. Abraham L.A., MacKie E.J. Modulation of osteoblast-like cell behavior by activation of protease-activated receptor-1. J. Bone Miner. Res. 1999, 14:1320-1329.
2. Almazin S.M., Dziak R., Andreana S., Ciancio S.G. The effect of doxycycline hyclate, chlorhexidine gluconate, and minocycline hydrochloride on osteoblastic proliferation and differentiation in vitro. J. Periodontol. 2009, 80:999-1005.
3. Andrianarivo A.G., Robinson J.A., Mann K.G., Tracy R.P. Growth on type I collagen promotes expression of the osteoblastic phenotype in human osteosarcoma MG-63 cells. J. Cell. Physiol. 1992, 153:256-265.
4. Aronow M.A., Gerstenfeld L.C., Owen T.A., Tassinari M.S., Stein G.S., Lian J.B. Factors that promote progressive development of the osteoblast phenotype in cultured fetal rat calvaria cells. J. Cell. Physiol. 1990, 143:213-221.
5. Beck G.R., Sullivan E.C., Moran E., Zerler B. Relationship between alkaline phosphatase levels, osteopontin expression, and mineralization in differentiating MC3T3-E1 osteoblasts. J. Cell. Biochem. 1998, 68:269-280.
6. Burrage P.S., Mix K.S., Brinckerhoff C.E. Matrix metalloproteinases: role in arthritis. Front. Biosci. 2006, 11:529-543.
7. Chien H.H., Lin W.L., Cho M.I. Interleukin-1beta-induced release of matrix proteins into culture media causes inhibition of mineralization of nodules formed by periodontal ligament cells in vitro. Calcif. Tissue Int. 1999, 64:402-413.
8. D'Alonzo R.C., Kowalski A.J., Denhardt D.T., Nickols G.A., Partridge N.C. Regulation of collagenase-3 and osteocalcin gene expression by collagen and osteopontin in differentiating MC3T3-E1 cells. J. Biol. Chem. 2002, 277:24788-24798.
9. Franceschi R.T., Iyer B.S. Relationship between collagen synthesis and expression of the osteoblast phenotype in MC3T3-E1 cells. J. Bone Miner. Res. 1992, 7:235-246.
10. Franceschi R.T., Iyer B.S., Cui Y. Effects of ascorbic acid on collagen matrix formation and osteoblast differentiation in murine MC3T3-E1 cells. J. Bone Miner. Res. 1994, 9:843-854.
11. Fujimoto N., Iwata K. Use of EIA to measure MMPs and TIMPs. Martix Metalloproteinase Protocols 2001, 347-358. Humana Press Inc, Totowa. I.M. Clark (Ed.).
12. Gennari L., Bilezikian J.P. Glucocorticoid-induced osteoporosis: hope on the HORIZON. Lancet 2009, 373:1225-1226.
13. Globus R.K., Moursi A., Zimmerman D., Lull J., Damsky C. Integrin-extracellular matrix interactions in connective tissue remodeling and osteoblast differentiation. ASGSB Bull. 1995, 8:19-28.
14. Goldberg G.I., Wilhelm S.M., Kronberger A., Bauer E.A., Grant G.A., Eisen A.Z. Human fibroblast collagenase. Complete primary structure and homology to an oncogene transformation-induced rat protein. J. Biol. Chem. 1986, 261:6600-6605.
15. Gomes P.S., Fernandes M.H. Effect of therapeutic levels of doxycycline and minocycline in the proliferation and differentiation of human bone marrow osteoblastic cells. Arch. Oral Biol. 2007, 52:251-259.
16. Gomes P.S., Santos J.D., Fernandes M.H. Cell-induced response by tetracyclines on human bone marrow colonized hydroxyapatite and bonelike. Acta Biomater. 2008, 4:630-637.
17. Hayami T., Zhang Q., Kapila Y., Kapila S. Dexamethasone's enhancement of osteoblastic markers in human periodontal ligament cells is associated with inhibition of collagenase expression. Bone 2007, 40:93-104.
18. Hayami T., Kapila Y.L., Kapila S. MMP-1 (collagenase-1) and MMP-13 (collagenase-3) differentially regulate markers of osteoblastic differentiation in osteogenic cells. Matrix Biol. 2008, 27:682-692.
19. Hayami T., Kapila Y.L., Kapila S. MMP-1's regulation of osteoblastic differentiation occurs via protease-activated receptor-1. J. Dent. Res. 2010, 89:921. Spec Iss A.
20. Holliday L.S., Vakani A., Archer L., Dolce C. Effects of matrix metalloproteinase inhibitors on bone resorption and orthodontic tooth movement. J. Dent. Res. 2003, 82:687-691.
21. Huang C.Y., Pelaez D., Dominguez-Bendala J., Garcia-Godoy F., Cheung H.S. Plasticity of stem cells derived from adult periodontal ligament. Regen. Med. 2009, 4:809-821.
22. Ikeda E., Kusaka M., Hakeda Y., Yokota K., Kumegawa M., Yamamoto S. Effect of interleukin 1 beta on osteoblastic clone MC3T3-E1 cells. Calcif. Tissue Int. 1988, 43:162-166.
23. Inada M., Wang Y., Byrne M.H., Rahman M.U., Miyaura C., Lopez-Otin C., Krane S.M. 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.
24. Jikko A., Harris S.E., Chen D., Mendrick D.L., Damsky C.H. Collagen integrin receptors regulate early osteoblast differentiation induced by BMP-2. J. Bone Miner. Res. 1999, 14:1075-1083.
25. 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.
26. Johansson N., Saarialho-Kere U., Airola K., Herva R., Nissinen L., Westermarck J., Vuorio E., Heino J., Kahari V.M. Collagenase-3 (MMP-13) is expressed by hypertrophic chondrocytes, periosteal cells, and osteoblasts during human fetal bone development. Dev. Dyn. 1997, 208:387-397.
27. Knauper V., Lopez-Otin C., Smith B., Knight G., Murphy G. Biochemical characterization of human collagenase-3. J. Biol. Chem. 1996, 271:1544-1550.
28. Komori T. Regulation of osteoblast differentiation by transcription factors. J. Cell. Biochem. 2006, 99:1233-1239.
29. Lynch M.P., Stein J.L., Stein G.S., Lian J.B. The influence of type I collagen on the development and maintenance of the osteoblast phenotype in primary and passaged rat calvarial osteoblasts: modification of expression of genes supporting cell growth, adhesion, and extracellular matrix mineralization. Exp. Cell Res. 1995, 216:35-45.
30. Martel-Pelletier J., Welsch D.J., Pelletier J.P. Metalloproteases and inhibitors in arthritic diseases. Best Pract. Res. Clin. Rheumatol. 2001, 15:805-829.
31. Mizuno M., Fujisawa R., Kuboki Y. Type I collagen-induced osteoblastic differentiation of bone-marrow cells mediated by collagen-alpha2beta1 integrin interaction. J. Cell. Physiol. 2000, 184:207-213.
32. Parikka V., Vaananen A., Risteli J., Salo T., Sorsa T., Vaananen H.K., Lehenkari P. Human mesenchymal stem cell derived osteoblasts degrade organic bone matrix in vitro by matrix metalloproteinases. Matrix Biol. 2005, 24:438-447.
33. Partridge N.C., Walling H.W., Bloch S.R., Omura T.H., Chan P.T., Pearman A.T., Chou W.Y. The regulation and regulatory role of collagenase in bone. Crit. Rev. Eukaryot. Gene Expr. 1996, 6:15-27.
34. Pei Y., Harvey A., Yu X.P., Chandrasekhar S., Thirunavukkarasu K. Differential regulation of cytokine-induced MMP-1 and MMP-13 expression by p38 kinase inhibitors in human chondrosarcoma cells: potential role of Runx2 in mediating p38 effects. Osteoarthritis Cartilage 2006, 14:749-758.
35. Reyes C.D., Garcia A.J. Alpha2beta1 integrin-specific collagen-mimetic surfaces supporting osteoblastic differentiation. J. Biomed. Mater. Res. A 2004, 69:591-600.
36. Ryoo H.M., Lee M.H., Kim Y.J. Critical molecular switches involved in BMP-2-induced osteogenic differentiation of mesenchymal cells. Gene 2006, 366:51-57.
37. Sakao K., Takahashi K.A., Arai Y., Saito M., Honjo K., Hiraoka N., Asada H., Shin-Ya M., Imanishi J., Mazda O., Kubo T. Osteoblasts derived from osteophytes produce interleukin-6, interleukin-8, and matrix metalloproteinase-13 in osteoarthritis. J. Bone Miner. Metab. 2009, 27:412-423.
38. Sasaki T., Ohyori N., Debari K., Ramamurthy N.S., Golub L.M. Effects of chemically modified tetracycline, CMT-8, on bone loss and osteoclast structure and function in osteoporotic states. Ann. N.Y. Acad. Sci. 1999, 878:347-360.
39. Schneider G.B., Zaharias R., Stanford C. Osteoblast integrin adhesion and signaling regulate mineralization. J. Dent. Res. 2001, 80:1540-1544.
40. Selvamurugan N., Jefcoat S.C., Kwok S., Kowalewski R., Tamasi J.A., Partridge N.C. Overexpression of Runx2 directed by the matrix metalloproteinase-13 promoter containing the AP-1 and Runx/RD/Cbfa sites alters bone remodeling in vivo. J. Cell. Biochem. 2006, 99:545-557.
41. Shiga M., Kapila Y.L., Zhang Q., Hayami T., Kapila S. Ascorbic acid induces collagenase-1 in human periodontal ligament cells but not in MC3T3-E1 osteoblast-like cells: potential association between collagenase expression and changes in alkaline phosphatase phenotype. J. Bone Miner. Res. 2003, 18:67-77.
42. Torii Y., Hitomi K., Tsukagoshi N. L-ascorbic acid 2-phosphate promotes osteoblastic differentiation of MC3T3-E1 mediated by accumulation of type I collagen. J. Nutr. Sci. Vitaminol. Tokyo. 1994, 40:229-238.
43. Tuckermann J.P., Pittois K., Partridge N.C., Merregaert J., Angel P. Collagenase-3 (MMP-13) and integral membrane protein 2a (Itm2a) are marker genes of chondrogenic/osteoblastic cells in bone formation: sequential temporal, and spatial expression of Itm2a, alkaline phosphatase, MMP-13, and osteocalcin in the mouse. J. Bone Miner. Res. 2000, 15:1257-1265.
44. Varghese S., Canalis E. Regulation of collagenase-3 by bone morphogenetic protein-2 in bone cell cultures. Endocrinology 1997, 138:1035-1040.
45. Varghese S., Rydziel S., Canalis E. Bone morphogenetic protein-2 suppresses collagenase-3 promoter activity in osteoblasts through a runt domain factor 2 binding site. J. Cell. Physiol. 2005, 202:391-399.
46. Wenstrup R.J., Witte D.P., Florer J.B. Abnormal differentiation in MC3T3-E1 preosteoblasts expressing a dominant-negative type I collagen mutation. Connect. Tissue Res. 1996, 35:249-257.
47. Winchester S.K., Bloch S.R., Fiacco G.J., Partridge N.C. Regulation of expression of collagenase-3 in normal, differentiating rat osteoblasts. J. Cell. Physiol. 1999, 181:479-488.
48. Xiao G., Wang D., Benson M.D., Karsenty G., Franceschi R.T. Role of the alpha2-integrin in osteoblast-specific gene expression and activation of the Osf2 transcription factor. J. Biol. Chem. 1998, 273:32988-32994.
49. Xu J., Wang W., Kapila Y., Lotz J., Kapila S. Multiple differentiation capacity of STRO-1+/CD146+ PDL mesenchymal progenitor cells. Stem Cells Dev. 2009, 18:487-496.
50. Zaragoza C., Lopez-Rivera E., Garcia-Rama C., Saura M., Martinez-Ruiz A., Lizarbe T.R., Martin-de-Lara F., Lamas S. Cbfa-1 mediates nitric oxide regulation of MMP-13 in osteoblasts. J. Cell Sci. 2006, 119:1896-1902.