Mechanical forces-induced human osteoblasts differentiation involves MMP-2/MMP-13/MT1-MMP proteolytic cascade

Journal of Cellular Biochemistry

Volumn 113, Issue 3, 2012, Pages 760-772

  Barthelemi, Stéphane ^a   Robinet, Julien ^b   Garnotel, Roselyne ^b   Antonicelli, Frank ^b   Schittly, Estelle ^a   Hornebeck, William ^b   Lorimier, Sandrine ^a,b  

^a UNIVERSITÉ DE REIMS CHAMPAGNE ARDENNE   (France)

^b CNRS   (France)

Author keywords

Bone Mineralization; Collagen Lattices; Differentiation Markers; Matrix Metalloproteinases; Osteoblast

Indexed keywords

ALKALINE PHOSPHATASE; BONE SIALOPROTEIN; COLLAGEN TYPE 1; COLLAGENASE 3; GELATINASE A; MATRIX METALLOPROTEINASE 14; OSTEOCALCIN; OSTEOPROTEGERIN; SMALL INTERFERING RNA; TISSUE INHIBITOR OF METALLOPROTEINASE 1; TISSUE INHIBITOR OF METALLOPROTEINASE 2; TRANSCRIPTION FACTOR RUNX2;

ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVATION; ENZYME ACTIVITY; HUMAN; HUMAN CELL; HUMAN TISSUE; OSTEOBLAST; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION;

BIOMECHANICS; CELL DIFFERENTIATION; CELLS, CULTURED; COLLAGEN; FEMALE; HUMANS; MALE; MATRIX METALLOPROTEINASE 13; MATRIX METALLOPROTEINASE 14; MATRIX METALLOPROTEINASE 2; OSTEOBLASTS;

EID: 84857602536     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.23401     Document Type: Article

References (55)

1. Akhouayri O, Lafage-Proust MH, Rattner A, Laroche N, Caillot-Augusseau A, Alexandre C, Vico L. 1999. Effects of static or dynamic mechanical stresses on osteoblast phenotype expression in three-dimensional contractile collagen gels. J Cell Biochem 76(2):217-230. (Pubitemid 30030770)
2. Barmina OY, Walling HW, Fiacco GJ, Freije JM, Lopez-Otin C, Jeffrey JJ, Partridge NC. 1999. Collagenase-3 binds to a specific receptor and requires the low density lipoprotein receptor-related protein for internalization. J Biol Chem 274(42):30087-30093.
3. Bellon G, Randoux A, Borel JP. 1985. A study of collagen metabolism in cell cultures by fluorometric determination of proline and hydroxyproline. Coll Relat Res 5(5):423-435. (Pubitemid 16177881)
4. Berton A, Lorimier S, Emonard H, Laurent-Maquin D, Hornebeck W, Bellon G. 2000. Contribution of the plasmin/matrix metalloproteinase cascade to the retraction of human fibroblast populated collagen lattices. Mol Cell Biol Res Commun 3(3):173-180. (Pubitemid 30430018)
5. Boudreau N, Weaver V. 2006. Forcing the third dimension. Cell 125(3):429-431.
6. Bowers GN, McComb RB, Upretti A. 1981. 4-Nitrophenyl phosphate- Characterization of high-purity materials for measuring alkaline phosphatase activity in human serum. Clin Chem 27(1):135-143. (Pubitemid 11188992)
7. Boyce BF, Xing L. 2008. Functions of RANKL/RANK/OPG in bone modeling and remodeling. Arch Biochem Biophys 473(2):139-146.
8. Buttle DJ, Ehrlich HP. 1983. Comparative studies of collagen lattice contraction utilizing a normal and a transformed cell line. J Cell Physiol 116(2):159-166. (Pubitemid 13034187)
9. Buxton PG, Bitar M, Gellynck K, Parkar M, Brown RA, Young AM, Knowles JC, Nazhat SN. 2008. Dense collagen matrix accelerates osteogenic differentiation and rescues the apoptotic response to MMP inhibition. Bone 43(2): 377-385.
10. Cozlin A, Barthelemi S, Garnotel R, Antonicelli F, Kaplan H, Hornebeck W, Lorimier S. 2006. Elastolysis induces collagenolysis in a gingival lamina propria model. J Dent Res 85(8):745-750. (Pubitemid 44297331)
11. D'alonzo RC, Kowalski AJ, Denhardt DT, Nickols GA, Partridge NC. 2002. Regulation of collagenase-3 and osteocalcin gene expression by collagen and osteopontin in differentiating MC3T3-E1 cells. J Biol Chem 277(27):24788-24798. (Pubitemid 34952011)
12. Deryugina EI, Bourdon MA, Reisfeld RA, Strongin A. 1998. Remodeling of collagen matrix by human tumor cells requires activation and cell surface association of matrix metalloproteinase-2. Cancer Res 58(16):3743-3750. (Pubitemid 28376578)
13. Filanti C, Dicksin GR, Di Martino D, Ulivi V, Sanguineti C, Romano P, Palermo C, Manduca P. 2000. The expression of metalloproteinase -2, -9 and -14 and of tissue inhibitors-1 and -2 is developmentally modulated during osteogenesis in vitro, the mature osteoblastic phenotype expressing metalloproteinase-14. J Bone Miner Res 15(11):2154-2168.
14. Fujisaki H, Hattori S. 2002. Keratinocyte apoptosis on type I collagen gel caused by lack of laminin 5/10/11 deposition and Akt signaling. Exp Cell Res 280(2):255-269. (Pubitemid 35333767)
15. Gillery P, Coustry F, Pujol JP, Borel JP. 1989. Inhibition of collagen synthesis by interleukin-1 in three-dimensional collagen lattice cultures of fibroblasts. Experientia 45(1):98-101. (Pubitemid 19031092)
16. Gordon JA, Tye CE, Sampaio AV, Underhill TM, Hunter GK, Goldberg HA. 2007. Bone sialoprotein expression enhances osteoblast differentiation and matrix mineralization in vitro. Bone 41(3):462-473. (Pubitemid 47199144)
17. Grinnell F. 2003. Fibroblast biology in three-dimensional collagen matrices. Trends Cell Biol 13(5):264-269. (Pubitemid 36556011)
18. Hayami T, Kapila YL, Kapila S. 2008. MMP-1 (collagenase-1) and MMP-13 (collagenase-3) differentially regulate markers of osteoblastic differentiation in osteogenic cells. Matrix Biol 27(8):682-692.
19. Hilliou F, Pairault J, Dominice J, Redziniak G. 1988. Growth and differentiation of 3T3-F442A preadipocytes in three-dimensional gels of native collagen. Exp Cell Res 177(2):372-381.
20. Holmbeck K, Bianco P, Pidoux I, Inoue S, Billinghurst RC, Wu W, Chrysovergis K, Yamada S, Birkedal-Hansen H, Poole AR. 2005. The metalloproteinase MT1-MMP is required for normal development and maintenance of osteocyte processes in bone. J Cell Sci 118(Pt 1):147-156. (Pubitemid 40277113)
21. Inoue K, Mikuni-Takagaki Y, Oikawa K, Itoh T, Inada M, Noguchi T, Park JS, Onodera T, Krane SM, Noda M, Itohara S. 2006. A crucial role for matrix metalloproteinase 2 in osteocytic canalicular formation and bone metabolism. J Biol Chem 281(44):33814-33824. (Pubitemid 46036758)
22. Jacob SS, Sudhakaran PR. 2001. Monocyte-macrophage differentiation in three dimensional collagen lattice. Biochim Biophys Acta 1540(1): 50-58. (Pubitemid 32710048)
23. Jain A, Karadag A, Fisher LW, Fedarko NS. 2008. Structural requirements for bone sialoprotein binding and modulation of matrix metalloproteinase-2. Biochemistry 47(38):10162-10170.
24. Jimenez M, Balbin M, Lopez J, Alvarez J, Komori T, Lopez-Otin C. 1999. Collagenase 3 is a target of Cbfa1, a transcription factor of the runt gene family involved in bone formation. Mol Cell Biol 19(6):4431-4442. (Pubitemid 29242017)
25. Karadag A, Fisher LW. 2006. Bone sialoprotein enhances migration of bone marrow stromal cells through matrices by bridging MMP-2 to alpha(v)beta3- integrin. J Bone Miner Res 21(10):1627-1636. (Pubitemid 44484608)
26. Karsdal MA, Larsen L, Engsig MT, Lou H, Ferreras M, Lochter A, Delaisse JM, Foged NT. 2002. Matrix metalloproteinase-dependent activation of latent transforming growth factor-beta controls the conversion of osteoblasts into osteocytes by blocking osteoblast apoptosis. J Biol Chem 277(46):44061-44067. (Pubitemid 36157833)
27. Karsdal MA, Andersen TA, Bonewald L, Christiansen C. 2004. Matrix metalloproteinases (MMPs) safeguard osteoblasts from apoptosis during transdifferentiation into osteocytes: MT1-MMP maintains osteocyte viability. DNA Cell Biol 23(3):155-165. (Pubitemid 38373082)
28. Kinner B, Gerstenfeld LC, Einhorn TA, Spector M. 2002. Expression of smooth muscle actin in connective tissue cells participating in fracture healing in a murine model. Bone 30(5):738-745. (Pubitemid 34467996)
29. Knäuper V, Bailey L, Worley JR, Soloway P, Patterson ML, Murphy G. 2002. Cellular activation of proMMP-13 by MT1-MMP depends on the C-terminal domain of MMP-13. FEBS Lett 532(1-2):127-130. (Pubitemid 35378666)
30. Komori T. 2006. Regulation of osteoblast differentiation by transcription factors. J Cell Biochem 99(5):1233-1239.
31. Kosaki N, Takaishi H, Kamekura S, Kimura T, Okada Y, Mingi L, Amizuka N, Chung UI, Nakamura K, Kawaguchi H, Toyama Y, D'Amiento J. 2007. Impaired bone fracture healing in matrix metalloproteinase-13 deficient mice. Biochem Biophys Res Commun 354(4):846-851. (Pubitemid 46216210)
32. Lambert CA, Soudant P, Nusgens BV, Lapierre CM. 1992. Pretranslational regulation of extracellular matrix macromolecules and collagenase expression in fibroblasts by mechanical forces. Lab Invest 66(4):444-451.
33. Langholz O, Röckel D, Mauch C, Kozlowska E, Bank I, Krieg T, Eckes B. 1995. Collagen and collagenase gene expression in three-dimensional collagen lattices are differentially regulated by alpha 1 beta 1 and alpha 2 beta 1 integrins. J Cell Biol 131(6 Pt 2):1903-1915. (Pubitemid 26007985)
34. Lieu S, Hansen E, Dedini R, Behonick D, Werb Z, Miclau T, Marcucio R, Colnot C. 2011. Impaired remodeling phase of fracture repair in the absence of matrix metalloproteinase-2. Dis Model Mech 4(2):203-211.
35. Lorimier S, Gillery P, Hornebeck W, Chastang F, Laurent-Maquin D, Bouthors S, Droulle C, Potron G, Maquart FX. 1996. Tissue origin and extracellular matrix control neutral proteinase activity in human fibroblast threedimensional cultures. J Cell Physiol 168(1):188-198. (Pubitemid 26233448)
36. Lu C, Li XY, Hu Y, Rowe RG, Weiss SJ. 2010. MT1-MMP controls human mesenchymal stem cell trafficking and differentiation. Blood 115(2):221-229.
37. Manduca P, Castagnino A, Lombardini D, Marchisio S, Soldano S, Ulivi V, Zanotti S, Garbi C, Ferrari N, Palmieri D. 2009. Role of MT1-MMP in the osteogenic differentiation. Bone 44(2):251-265.
38. Marie PJ. 2008. Transcription factors controlling osteoblastogenesis. Arch Biochem Biophys 473(2):98-105.
39. Mizuno M, Fujisawa R, Kuboki Y. 2000. Carboxyl-terminal propeptide of type I collagen (c-propeptide) modulates the action of TGF-beta on MC3T3- E1 osteoblastic cells. FEBS Lett 479(3):123-126. (Pubitemid 30616418)
40. Mosig RA, Dowling O, DiFeo A, Ramirez MCM, Parker IC, Abe E, Diouri J, Al Aqeel A, Wylie JD, Oblander SA, Madri J, Bianco P, Apte SS, Zaidi M, Doty SB, Majeska RJ, Schaffer MB, Martignetti JA. 2007. 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 16(9):1113-1123. (Pubitemid 47062731)
41. Nagase H, Visse R, Murphy G. 2006. Structure and function of matrix metalloproteinases and TIMPs. Cardiovasc Res 69(3):562-573. (Pubitemid 43139720)
42. Nakano Y, Forsprecher J, Kaartinen MT. 2010. Regulation of ATPase activity of transglutaminase 2 by MT1-MMP: Implications for mineralization of MC3T3-E1 osteoblast cultures. J Cell Physiol 223(1):260-269.
43. Parreno J, Buckley-Herd G, De-Hemptinne I, Hart DA. 2008. Osteoblastic MG-63 cell differentiation, contraction, and mRNA expression in stressrelaxed 3D collagen I gels. Mol Cell Biochem 317(1-2):21-32.
44. Pei D, Weiss SJ. 1995. Furin-dependent intracellular activation of the human stromelysin-3 zymogen. Nature 375(6528):244-247.
45. Riikonen T, Westermarck J, Koivisto L, Broberg A, Kähäri VM, Heino J. 1995. Integrin alpha 2 beta 1 is a positive regulator of collagenase (MMP-1) and collagen alpha 1(I) gene expression. J Biol Chem 270(22):13548-13552.
46. Robinet A, Fahem A, Cauchard JH, Huet E, Vincent L, Lorimier S, Antonicelli F, Soria C, Crepin M, Hornebeck W, Bellon G. 2005. Elastin-derived peptides enhance angiogenesis by promoting endothelial cell migration and tubulogenesis through upregulation of MT1-MMP. J Cell Sci 118:343-356. (Pubitemid 40277347)
47. Sabeh F, Li XY, Saunders TL, Rowe RG, Weiss SJ. 2009. Secreted versus membrane-anchored collagenases: Relative roles in fibroblast-dependent collagenolysis and invasion. J Biol Chem 284(34):23001-23011.
48. Sariahmetoglu M, Crawford BD, Leon H, Sawicka J, Li L, Ballermann BJ, Holmes C, Berthiaume LG, Holt A, Sawicki G, Schulz R. 2007. Regulation of matrix metalloproteinase-2 (MMP-2) activity by phosphorylation. FASEB J 21(10):2486-2495. (Pubitemid 47230678)
49. Schiltz C, Prouillet C, Marty C, Merciris D, Collet C, De Vernejoul MC, Geoffroy V. 2010. Bone loss induced by Runx2 over-expression in mice is blunted by osteoblastic over-expression of TIMP-1. J Cell Physiol 222(1): 219-229.
50. Stickens D, Behonick DJ, Ortega N, Heyer B, Hartenstein B, Yu Y, Fosang AJ, Schorpp-Kistner M, Angel P, Werb Z. 2004. Altered endochondral bone development in matrix metalloproteinase 13-deficient mice. Development 131(23):5883-5895. (Pubitemid 40123905)
51. Teti A, Farina AR, Villanova I, Tiberio A, Tacconelli A, Sciortino G, Chambers AF, Gulino A, Mackay AR. 1998. Activation of MMP-2 by human GCT23 giant cell tumour cells induced by osteopontin, bone sialoprotein and GRGDSP peptides is RGD and cell shape change dependent. Int J Cancer 77(1):82-93. (Pubitemid 28308556)
52. Tomasek JJ, Gabbiani G, Hinz B, Chaponnier C, Brown RA. 2002. Myofibroblasts and mechano-regulation of connective tissue remodelling. Nat Rev Mol Cell Biol 3(5):349-363. (Pubitemid 34619269)
53. Tuckerman JP, Pittois K, Partridge NC, Merregaert J, Angel P. 2000. 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 15(7):1257-1265. (Pubitemid 30413858)
54. Zhao W, Byrne MH, Wang Y, Krane SM. 2000. Osteocyte and osteoblast apoptosis and excessive bone deposition accompany failure of collagenase cleavage of collagen. J Clin Invest 106(8):941-949.
55. Zhou Z, Apte SS, Soininen R, Cao R, Baaklini GY, Rauser RW, Wang J, Cao Y, Tryggvason K. 2000. Impaired endochondral ossification and angiogenesis in mice deficient in membrane-type matrix metalloproteinase I. Proc Natl Acad Sci USA 97(8):4052-4057. (Pubitemid 30226085)