International Journal of Oral Biology

The Korean Academy of Oral Biology (대한구강생물학회)
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Regulation of ADAMTS-2 by 1,25-Dihydroxyvitamin D3 in Osteoblastic Cells

  • Jeon, Eun-Young (School of Dentistry and Dental Research Institute, Seoul National University) ;
  • Kim, Hyun-Man (School of Dentistry and Dental Research Institute, Seoul National University) ;
  • Lee, Seung-Bok (School of Dentistry and Dental Research Institute, Seoul National University)
  • Published : 2006.09.30
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Abstract

Biosynthetic processing of fibrillar procollagens is essential for producing mature collagen monomers that polymerize into fibrils by a self-assembly process. The metalloproteinase ADAMTS-2 is the major enzyme that processes the N-propeptide of type I procollagen in the skin and also of type II and type III procollagens. Mutations in the ADAMTS-2 gene cause dermatospraxis in animals and Ehlers-Danlos syndrome VIIC in humans, both of which are characterized by the accumulation of type I pN-collagen and the formation of abnormal collagen fibrils in the skin. Despite its importance in procollagen processing, little is known about the regulation of ADAMTS-2 expression. Here, we demonstrate that ADAMTS-2 can be regulated by 1,25-dihydroxyvitamin D3, an inducer of type I procollagen synthesis. This steroid hormone induced ADAMTS-2 mRNA ${\sim}3-fold$ in MG-63 human osteosarcoma cells and MC3T3-E1 murine osteoblastic cells. This induction was dose- and time-dependent in MG-63 cells. In contrast, secreted ADAMTS-2 protein was increased only 1.4-fold with 1,25-dihydroxyvitamin D3. Finally, 1,25-dihydroxyvitamin D3 in the presence of ascorbate increased levels of secreted ADAMTS-2 1.9-fold over ascorbate treatment alone, which did not appreciably change ADAMTS-2 expression. These data indicate that the regulation of ADAMTS-2 is coupled with the synthesis of type I procollagen through 1,25-dihydroxyvitamin D3 signaling and may involve translational or posttranslational control.

Keywords

References

  1. Beresford JN, Gallagher JA, Russell RG. 1,25-Dihydroxyvitamin D3 and human bone-derived cells in vitro: effects on alkaline phosphatase, type I collagen and proliferation. Endocrinology. 119:1776-1785, 1986 https://doi.org/10.1210/endo-119-4-1776
  2. Bonewald LF, Kester MB, Schwartz Z, Swain LD, Khare A, Johnson TL, Leach RJ, Boyan BD. Effects of combining transforming growth factor beta and 1,25-dihydroxyvitamin D3 on differentiation of a human osteosarcoma (MG-63). J Biol Chem. 267:8943-8949, 1992
  3. Chan D, Lamande SR, Cole WG, Bateman JF. Regulation of procollagen synthesis and processing during ascorbateinduced extracellular matrix accumulation in vitro. Biochem J. 269:175-181, 1990 https://doi.org/10.1042/bj2690175
  4. Colige A, Li SW, Sieron AL, Nusgens BV, Prockop DJ, Lapiere CM. cDNA cloning and expression of bovine procollagen I N-proteinase: a new member of the superfamily of zinc-metalloproteinases with binding sites for cells and other matrix components. Proc Natl Acad Sci USA. 94:2374-2379, 1997
  5. Colige A, Sieron AL, Li SW, Schwarze U, Petty E, Wertelecki W, Wilcox W, Krakow D, Cohn DH, Reardon W, Byers PH, Lapiere CM, Prockop DJ, Nusgens BV. Human Ehlers- Danlos syndrome type VII C and bovine dermatosparaxis are caused by mutations in the procollagen I N-proteinase gene. Am J Hum Genet. 65:308-317, 1999 https://doi.org/10.1086/302504
  6. Colige A, Vandenberghe I, Thiry M, Lambert CA, Van Beeumen J, Li SW, Prockop DJ, Lapiere CM, Nusgens BV. Cloning and characterization of ADAMTS-14, a novel ADAMTS displaying high homology with ADAMTS-2 and ADAMTS-3. J Biol Chem. 277:5756-5766, 2002 https://doi.org/10.1074/jbc.M105601200
  7. Fernandes RJ, Hirohata S, Engle JM, Colige A, Cohn DH, Eyre DR, Apte SS. Procollagen II amino propeptide processing by ADAMTS-3. Insights on dermatosparaxis. J Biol Chem. 276:31502-31509, 2001 https://doi.org/10.1074/jbc.M103466200
  8. Franceschi RT, James WM, Zerlauth G. 1 alpha, 25-dihydroxyvitamin D3 specific regulation of growth, morphology, and fibronectin in a human osteosarcoma cell line. J Cell Physiol. 123:401-409, 1985 https://doi.org/10.1002/jcp.1041230316
  9. Franceschi RT, Linson CJ, Peter TC, Romano PR. Regulation of cellular adhesion and fibronectin synthesis by 1 alpha,25- dihydroxyvitamin D3. J Biol Chem. 262:4165-4171, 1987
  10. Franceschi RT, Romano PR, Park KY. Regulation of type I collagen synthesis by 1,25-dihydroxyvitamin D3 in human osteosarcoma cells. J Biol Chem. 263:18938-18945, 1988
  11. Holmes DF, Watson RB, Steinmann B, Kadler KE. Ehlers- Danlos syndrome type VIIB. Morphology of type I collagen fibrils formed in vivo and in vitro is determined by the conformation of the retained N-propeptide. J Biol Chem. 268:15758-15765, 1993
  12. Hulmes DJ, Kadler KE, Mould AP, Hojima Y, Holmes DF, Cummings C, Chapman JA, Prockop DJ. Pleomorphism in type I collagen fibrils produced by persistence of the procollagen N-propeptide. J Mol Biol. 210:337-345, 1989 https://doi.org/10.1016/0022-2836(89)90335-5
  13. Ignotz RA, Endo T, Massague J. Regulation of fibronectin and type I collagen mRNA levels by transforming growth factorbeta. J Biol Chem. 262:6443-6446, 1987
  14. Kessler E, Takahara K, Biniaminov L, Brusel M, Greenspan DS. Bone morphogenetic protein-1: the type I procollagen C-proteinase. Science. 271:360-362, 1996 https://doi.org/10.1126/science.271.5247.360
  15. Kojima T, Kozaki K, Saga S, Hashizume Y, Ishiguro N, Iwata H, Miyaishi O. Alteration of the kinetics of type I procollagen synthesis in human osteosarcoma cells by 1,25- dihydroxyvitamin D3. J Cell Biochem. 65:542-549, 1997 https://doi.org/10.1002/(SICI)1097-4644(19970615)65:4<542::AID-JCB9>3.0.CO;2-O
  16. Kurihara N, Ishizuka S, Kiyoki M, Haketa Y, Ikeda K, Kumegawa M. Effects of 1,25-dihydroxyvitamin D3 on osteoblastic MC3T3-E1 cells. Endocrinology. 118:940-947, 1986 https://doi.org/10.1210/endo-118-3-940
  17. Lajeunesse D, Kiebzak GM, Frondoza C, Sacktor B. Regulation of osteocalcin secretion by human primary bone cells and by the human osteosarcoma cell line MG-63. Bone Miner. 14:237-250, 1991 https://doi.org/10.1016/0169-6009(91)90025-U
  18. Lee S, Solow-Cordero DE, Kessler E, Takahara K, Greenspan DS. Transforming growth factor-beta regulation of bone morphogenetic protein-1/procollagen C-proteinase and related proteins in fibrogenic cells and keratinocytes. J Biol Chem. 272:19059-19066, 1997 https://doi.org/10.1074/jbc.272.30.19059
  19. Li SW, Sieron AL, Fertala A, Hojima Y, Arnold WV, Prockop DJ. The C-proteinase that processes procollagens to fibrillar collagens is identical to the protein previously identified as bone morphogenic protein-1. Proc Natl Acad Sci U S A. 93:5127-5130, 1996
  20. Li SW, Arita M, Fertala A, Bao Y, Kopen GC, Langsjo TK, Hyttinen MM, Helminen HJ, Prockop DJ. Transgenic mice with inactive alleles for procollagen N-proteinase (ADAMTS- 2) develop fragile skin and male sterility. Biochem J. 355:271-278, 2001 https://doi.org/10.1042/0264-6021:3550271
  21. Massague J. The transforming growth factor-beta family. Annu Rev Cell Biol. 6:597-641, 1990 https://doi.org/10.1146/annurev.cb.06.110190.003121
  22. Nusgens BV, Verellen-Dumoulin C, Hermanns-Le T, De Paepe A, Nuytinck L, Pierard GE, Lapiere CM. Evidence for a relationship between Ehlers-Danlos type VII C in humans and bovine dermatosparaxis. Nat Genet. 1:214-217, 1992 https://doi.org/10.1038/ng0692-214
  23. Scott IC, Blitz IL, Pappano WN, Imamura Y, Clark TG, Steiglitz BM, Thomas CL, Maas SA, Takahara K, Cho KW, Greenspan DS. Mammalian BMP-1/Tolloid-related metalloproteinases, including novel family member mammalian Tolloid-like 2, have differential enzymatic activities and distributions of expression relevant to patterning and skeletogenesis. Dev Biol. 213:283-300, 1999 https://doi.org/10.1006/dbio.1999.9383
  24. Smith LT, Wertelecki W, Milstone LM, Petty EM, Seashore MR, Braverman IM, Jenkins TG, Byers PH. Human dermatosparaxis: a form of Ehlers-Danlos syndrome that results from failure to remove the amino-terminal propeptide of type I procollagen. Am J Hum Genet. 51:235-244, 1992
  25. Suzuki N, Labosky PA, Furuta Y, Hargett L, Dunn R, Fogo AB, Takahara K, Peters DM, Greenspan DS, Hogan BL. Failure of ventral body wall closure in mouse embryos lacking a procollagen C-proteinase encoded by Bmp1, a mammalian gene related to Drosophila tolloid. Development. 122:3587-3595, 1996
  26. Wang WM, Lee S, Steiglitz BM, Scott IC, Lebares CC, Allen ML, Brenner MC, Takahara K, Greenspan DS. Transforming growth factor-beta induces secretion of activated ADAMTS- 2. A procollagen III N-proteinase. J Biol Chem. 278:19549- 19557, 2003 https://doi.org/10.1074/jbc.M300767200
  27. Watson RB, Holmes DF, Graham HK, Nusgens BV, Kadler KE. Surface located procollagen N-propeptides on dermatosparactic collagen fibrils are not cleaved by procollagen N-proteinase and do not inhibit binding of decorin to the fibril surface. J Mol Biol. 278:195-204, 1998 https://doi.org/10.1006/jmbi.1998.1680
  28. Yanagisawa J, Yanagi Y, Masuhiro Y, Suzawa M, Watanabe M, Kashiwagi K, Toriyabe T, Kawabata M, Miyazono K, Kato S. Convergence of transforming growth factor-beta and vitamin D signaling pathways on SMAD transcriptional coactivators. Science. 283:1317-1321, 1999 https://doi.org/10.1126/science.283.5406.1317