Overexpression of Runx2 directed by the matrix metalloproteinase-13 promoter containing the AP-1 and Runx/RD/Cbfa sites alters bone remodeling in vivo

Journal of Cellular Biochemistry

Volumn 99, Issue 2, 2006, Pages 545-557

  Selvamurugan, Nagarajan ^a   Jefcoat, Stephen C ^a   Kwok, Sukyee ^a   Kowalewski, Rodney ^c   Tamasi, Joseph A ^b   Partridge, Nicola C ^a  

^a RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

^b BRISTOL MYERS SQUIBB   (United States)

^c SAINT LOUIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Bone formation; Bone remodeling; Bone resorption; Collagenase 3; Matrix metalloproteinase 13; Runx2

Indexed keywords

BETA GALACTOSIDASE; BINDING PROTEIN; COLLAGENASE 3; MESSENGER RNA; PARATHYROID HORMONE; PROTEIN C JUN; PROTEIN RUNX RD CBFA; REGULATOR PROTEIN; TRANSCRIPTION FACTOR AP 1; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BINDING SITE; BONE MINERALIZATION; BONE REMODELING; CELL DIFFERENTIATION; ENZYME SPECIFICITY; ESCHERICHIA COLI; GENE; GENE MUTATION; GENE OVEREXPRESSION; MORPHOMETRICS; MOUSE; NONHUMAN; ONCOGENE C FOS; ONCOGENE C JUN; OSSIFICATION; OSTEOBLAST; OSTEOLYSIS; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DOMAIN; REGULATOR GENE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RUNX2 GENE; SKIN; TISSUE DISTRIBUTION; TOOTH; TRANSCRIPTION INITIATION; TRANSGENIC MOUSE;

ANIMALS; BASE SEQUENCE; BINDING SITES; BONE REMODELING; COLLAGENASES; CORE BINDING FACTOR ALPHA 1 SUBUNIT; CORE BINDING FACTOR ALPHA SUBUNITS; DNA PRIMERS; GENE EXPRESSION; LAC OPERON; MATRIX METALLOPROTEINASE 13; MICE; MICE, TRANSGENIC; PROMOTER REGIONS (GENETICS); RATS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TRANSCRIPTION FACTOR AP-1;

ANIMALIA; BACTERIA (MICROORGANISMS); MUS MUSCULUS;

EID: 33748940904     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.20878     Document Type: Article

References (41)

1. Aubin JE. 1998. Bone stem cells. J Cell Biochem 30-31(Suppl):73-82.
2. Balbin M, Fueyo A, Lopez JM, Diez-Itza I, Velasco G, Lopez-Otin C. 1996. Expression of collagenase-3 in the rat ovary during the ovulatory process. J Endocrinol 149:405-415.
3. Banerjee C, McCabe LR, Choi JY, Hiebert SW, Stein JL, Stein GS, Lian JB. 1997. Runt homology domain proteins in osteoblast differentiation: AML3/CBFA1 is a major component of a bone-specific complex. J Cell Biochem 66:1-8.
4. Choi JY, Pratap J, Javed A, Zaidi SK, Xing L, Balint E, Dalamangas S, Boyce B, van Wijnen AJ, Lian JB, Stein JL, Jones SN, Stein GS. 2001. Subnuclear targeting of Runx/Cbfa/AML factors is essential for tissue-specific differentiation during embryonic development. Proc Natl Acad Sci USA 98:8650-8655.
5. D'Alonzo RC, Selvamurugan N, Karsenty G, Partridge NC. 2002. Physical interaction of the activator protein-1 factors c-Fos and c-Jun with Cbfa1 for collagenase-3 promoter activation. J Biol Chem 277:816-822.
6. Davis BA, Sipe B, Gershan LA, Fiacco GJ, Lorenz TC, Jeffrey JJ, Partridge NC. 1998. Collagenase and tissue plasminogen activator production in developing rat calvariae: normal progression despite fetal exposure to microgravity. Calcif Tissue Int 63:416-422.
7. Ducy P, Zhang R, Geoffroy V, Ridall AL, Karsenty G. 1997. Osf2/Cbfa1: a transcriptional activator of osteoblast differentiation. Cell 89:747-754.
8. Ducy P, Starbuck M, Priemel M, Shen J, Pinero G, Geoffroy V, Amling M, Karsenty G. 1999. A Cbfa1-dependent genetic pathway controls bone formation beyond embryonic development. Genes Dev 13:1025-1036.
9. Geoffroy V, Kneissel M, Fournier B, Boyde A, Matthias P. 2002. High bone resorption in adult aging transgenic mice overexpressing cbfa1/runx2 in cells of the osteoblastic lineage. Mol Cell Biol 22:6222-6233.
10. Harada H, Tagashira S, Fujiwara M, Ogawa S, Katsumata T, Yamaguchi A, Komori T, Nakatsuka M. 1999. Cbfa1 isoforms exert functional differences in osteoblast differentiation. J Biol Chem 274:6972-6978.
11. Inada M, Wang Y, Byrne MH, Rahman MU, Miyaura C, Lopez-Otin C, Krane SM, 2004. Critical roles for collagenase-3 (Mmp13) in development of growth plate cartilage and in endochondral ossification. Proc Natl Acad Sci USA 101:17192-17197.
12. Kalajzic Z, Liu P, Kalajzic I, Du C, Braut A, Mina M, Canalis E, Rowe DW. 2002. Directing the expression of a green fluorescent protein transgene in differentiated osteoblasts: comparison between rat type I collagen and rat osteocalcin promoters. Bone 31:654-660.
13. Karsenty G. 1999. The genetic transformation of bone biology. Genes Dev 13:3037-3051.
14. Karsenty G. 2000. Role of Cbfa1 in osteoblast differentiation and function. Semin Cell Dev Biol 11:343-346.
15. Kern B, Shen J, Starbuck M, Karsenty G. 2001. Cbfa1 contributes to the osteoblast-specific expression of type I collagen genes. J Biol Chem 276:7101-7107.
16. Komori T. 2000. A fundamental transcription factor for bone and cartilage. Biochem Biophys Res Commun 276:813-816.
17. Komori T, Kishimoto T. 1998. Cbfa1 in bone development. Curr Opin Genet Dev 8:494-499.
18. Komori T, Yagi H, Nomura S, Yamaguchi A, Sasaki K, Deguchi K, Shimizu Y, Bronson RT, Gao YH, Inada M, Sato M, Okamoto R, Kitamura Y, Yoshiki S, Kishimoto T. 1997. Targeted disruption of Cbfa1 results in a complete lack of bone formation owing to maturational arrest of osteoblasts. Cell 89:755-764.
19. Krane SM. 2002. Genetic control of bone remodeling-insights from a rare disease. New Eng J Med 347:210-212.
20. Kusano K, Miyaura C, Inada M, Tamura T, Ito A, Nagase H, Kamoi K, Suda T. 1998. Regulation of matrix metalloproteinases (MMP-2, -3, -9, and -13) by interleukin-1 and interleukin-6 in mouse calvaria: association of MMP induction with bone resorption. Endocrinology 139:1338-1345.
21. Lee KS, Kim HJ, Li QL, Chi XZ, Ueta C, Komori T, Wozney JM, Kim EG, Choi JY, Ryoo HM, Bae SC. 2000. Runx2 is a common target of transforming growth factor beta1 and bone morphogenetic protein 2, and cooperation between Runx2 and Smad5 induces osteoblast-specific gene expression in the pluripotent mesenchymal precursor cell line C2C12. Mol Cell Biol 20:8783-8792.
22. Liu W, Toyosawa S, Furuichi T, Kanatani N, Yoshida C, Liu Y, Himeno M, Narai S, Yamaguchi A, Komori T. 2001. Overexpression of Cbfa1 in osteoblasts inhibits osteoblast maturation and causes osteopenia with multiple fractures. J Cell Biol 155:157-166.
23. Mundlos S, Otto F, Mundlos C, Mulliken JB, Aylsworth AS, Albright S, Lindhout D, Cole WG, Henn W, Knoll JH, Owen MJ, Mertelsmann R, Zabel BU, Olsen BR. 1997. Mutations involving the transcription factor CBFA1 cause cleidocranial dysplasia. Cell 89:773-779.
24. Otto F, Thornell AP, Crompton T, Denzel A, Gilmour KC, Rosewell IR, Stamp GW, Beddington RS, Mundlos S, Olsen BR, Selby PB, Owen MJ. 1997. Cbfa1, a candidate gene for cleidocranial dysplasia syndrome, is essential for osteoblast differentiation and bone development. Cell 89:765-771.
25. Parfitt AM, Drezner MK, Glorieux FH, Kanis JA, Malluche H, Meunier PJ, Ott SM, Recker RR. 1987. Bone histomorphometry: standardization of nomenclature, symbols, and units. Report of the ASBMR Histomorphometry Nomenclature Committee. J Bone Miner Res 2:595-610.
26. Partridge NC, Davis BA, Sipe B, Gershan LA, Fiacco GJ, Lorenz TC, Jeffrey JJ. 1998. Calcif Tissue Int 63:416-422.
27. Prince M, Banerjee C, Javed A, Green J, Lian JB, Stein GS, Bodine PV, Komm BS. 2001. Expression and regulation of Runx2/Cbfa1 and osteoblast phenotypic markers during the growth and differentiation of human osteoblasts. J Cell Biochem 80: 424-440.
28. Roodman GD. 1999. Cell biology of the osteoclast. Exp Hematol 27:1229-1241.
29. Sato M, Morii E, Komori T, Kawahata H, Sugimoto M, Terai K, Shimizu H, Yasui T, Ogihara H, Yasui N, Ochi T, Kitamura Y, Ito Y, Nomura S. 1998. Transcriptional regulation of osteopontin gene in vivo by PEBP2alphaA/CBFA1 and ETS1 in the skeletal tissues. Oncogene 17:1517-1525.
30. Schorpp M, Mattei MG, Herr I, Gack S, Schaper J, Angel P. 1995. Structural organization and chromosomal localization of the mouse collagenase type I gene. Biochem J 308:211-217.
31. Scott DK, Brakenhoff KD, Clohisy JC, Quinn CO, Partridge NC. 1992. Parathyroid hormone induces transcription of collagenase in rat osteoblastic cells by a mechanism using cyclic adenosine 3′,5′-monophosphate and requiring protein synthesis. Mol Endocrinol 6:2153-2159.
32. Selvamurugan N, Chou WY, Pearman AT, Pulumati MR, Partridge NC. 1998. Parathyroid hormone regulates the rat collagenase-3 promoter in osteoblastic cells through the cooperative interaction of the activator protein-1 site and the runt domain binding sequence. J Biol Chem 273:10647-10657.
33. Shum JK, Melendez JA, Jeffrey JJ. 2002. Serotonin-induced MMP-13 production is mediated via phospholipase C, protein kinase C, and ERK1/2 in rat uterine smooth muscle cells. J Biol Chem 277:42830-42840.
34. Tuckermann 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 15:1257-1265.
35. Varghese S, Ramsby ML, Jeffrey JJ, Canalis E. 1995. Basic fibroblast growth factor stimulates expression of interstitial collagenase and inhibitors of metalloproteinases in rat bone cells. Endocrinology 136:2156-2162.
36. Varghese S, Delany AM, Liang L, Gabbitas B, Jeffrey JJ, Canalis E. 1996. Transcriptional and posttranscriptional regulation of interstitial collagenase by platelet-derived growth factor BB in bone cell cultures. Endocrinology 137:431-437.
37. Varghese S, Rydziel S, Canalis E. 2000. Basic fibroblast growth factor stimulates collagenase-3 promoter activity in osteoblasts through an activator protein-1-binding site. Endocrinology 141:2185-2191.
38. Winchester SK, Selvamurugan N, D'Alonzo RC, Partridge NC. 2000. Developmental regulation of collagenase-3 mRNA in normal, differentiating osteoblasts through the activator protein-1 and the runt domain binding sites. J Biol Chem 275:23310-23318.
39. Xiao ZS, Hinson TK, Quarles LD. 1999. Cbfa1 isoform overexpression upregulates osteocalcin gene expression in non-osteoblastic and pre-osteoblastic cells. J Cell Biochem 74:596-605.
40. Zhao W, Byrne MH, Boyce BF, Krane SM. 1999. Bone resorption induced by parathyroid hormone is strikingly diminished in collagenase-resistant mutant mice. J Clin Invest 103:517-524.
41. 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 106:941-949.