ADAM Proteins; Amino Acid Sequence; Base Sequence; Blotting, Northern; Cell Line; Cloning, Molecular; DNA Primers; Ehlers-Danlos Syndrome/enzymology; Endopeptidases/chemistry/genetics/metabolism; Humans; Molecular Sequence Data; Peptide Fragments/metabolism; Procollagen/metabolism; Procollagen N-Endopeptidase/chemistry/genetics; Protein Processing, Post-Translational; Sequence Homology, Amino Acid
Abstract :
[en] The amino and carboxyl propeptides of procollagens I and II are removed by specific enzymes as a prerequisite for fibril assembly. Null mutations in procollagen I N-propeptidase (ADAMTS-2) cause dermatosparaxis in cattle and the Ehlers-Danlos syndrome (dermatosparactic type) in humans by preventing proteolytic excision of the N-propeptide of procollagen I. We have found that procollagen II is processed normally in dermatosparactic nasal cartilage, suggesting the existence of another N-propeptidase(s). We investigated such a role for ADAMTS-3 in Swarm rat chondrosarcoma RCS-LTC cells, which fail to process the procollagen II N-propeptide. Stable transfection of RCS-LTC cells with bovine ADAMTS-2 or human ADAMTS-3 partially rescued the processing defect, suggesting that ADAMTS-3 has procollagen II N-propeptidase activity. Human skin and skin fibroblasts showed 30-fold higher mRNA levels of ADAMTS-2 than ADAMTS-3, whereas ADAMTS-3 mRNA was 5-fold higher than ADAMTS-2 mRNA in human cartilage. We propose that both ADAMTS-2 and ADAMTS-3 process procollagen II, but ADAMTS-3 is physiologically more relevant, given its preferred expression in cartilage. The findings provide an explanation for the sparing of cartilage in dermatosparaxis and, perhaps, for the relative sparing of some procollagen I-containing tissues.
Disciplines :
Biochemistry, biophysics & molecular biology
Author, co-author :
Fernandes, R. J.; University of Washington, Seattle, Washington > Dpt of Biochemistry & Dpt of Orthopaedics and Sports Medicine
Hirohata, S.; Lerner Research Institute, Cleveland Clinic Foundation, Ohio - USA > Dpt of Biomedical Engineering
Engle, J. M.; Lerner Research Institute, Cleveland Clinic Foundation, Ohio - USA > Dpt of Biomedical Engineering
Colige, Alain ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Laboratoire de Biologie des tissus conjonctifs
Cohn, D. H.; University of California, Los Angeles - UCLA > Dpt of Human Genetics and Pediatrics - S.Spielberg Pediatric Res Center
Eyre, D. R.
Apte, S. S.; Lerner Research Institute, Cleveland Clinic Foundation, Ohio - USA > Dpt of Biomedical Engineering
Language :
English
Title :
Procollagen II amino propeptide processing by ADAMTS-3. Insights on dermatosparaxis.
Publication date :
2001
Journal title :
Journal of Biological Chemistry
ISSN :
0021-9258
eISSN :
1083-351X
Publisher :
American Society for Biochemistry and Molecular Biology, Baltimore, United States - Maryland
Fukai, N., Apte, S. S., and Olsen, B. R. (1994) in Extracellular Matrix Components (Erkki, R., and Engvall, E., eds) Vol. 245, pp. 3-28, Academic Press, New York
van der Rest, M., and Garrone, R. (1991) FASEB J. 5, 2814-2823
Birk, D. E., Silver, F. H., and Trelstad, R. L. (1991) in Cell Biology of Extra. cellular Matrix (Hay, E. D., ed) 2nd Ed., pp. 221-254, Plenum Publishing Corp., New York
Olsen, B. R. (1991) in Cell Biology of Extracellular Matrix (Hay, E. D., ed) 2nd Ed., pp. 177-220, Plenum Publishing Corp., New York
Li, S. W., Sieron, A. L., Fertala, A., Hojima, Y., Arnold, W. V., and Prockop, D. J. (1996) Proc. Natl. Acad. Sci. U. S. A. 93, 5127-5130
Lapiere, C. M., Lenaers, A., and Kohn, L. D. (1971) Proc. Natl. Acad. Sci. U. S. A. 68, 3054-3058
Colige, A., Li, S. W., Sieron, A. L., Nusgens, B. V., Prockop, D. J., and Lapiere, C. M. (1997) Proc. Natl. Acad. Sci. U. S. A. 94, 2374-2379
Colige, A., Sieron, A. L., Li, S. W., Schwarze, U., Petty, E., Wertelecki, W., Wilcox, W., Krakow, D., Cohn, D. H., Reardon, W., Byers, P. H., Lapiere, C. M., Prockop, D. J., and Nusgens, B. V. (1999) Am. J. Hum. Genet. 65, 308-317
Kuno, K., Kanada, N., Nakashima, E., Fujiki, F., Ichimura, F., and Matsushima, K. (1997) J. Biol. Chem. 272, 556-562
Hurskainen, T. L., Hirohata, S., Seldin, M. F., and Apte, S. S. (1999) J. Biol. Chem. 274, 25555-25563
Fujimoto, A, Wilcox, W. R., and Cohn, D. H. (1997) Am. J. Med. Genet. 68, 25-28
Hanset, R., and Lapiere, C. M. (1974) J. Hered. 65, 356-358
Lapiere, C. M., and Nusgens, B. V. (1993) Arch. Dermatol. 129, 1316-1319
O'Hara, P. J., Read, W. K., Romane, W. M., and Bridges, C. H. (1970) Lab. Invest. 23, 307-314
Petty, E. M., Seashore, M. R., Braverman, I. M., Spiesel, S. Z., Smith, L. T., and Milstone, L. M. (1993) Arch. Dermatol. 129, 1310-1315
Reardon, W., Winter, R. M., Smith, L. T., Lake, B. D., Rossiter, M., and Baraitser, M. (1995) Clin. Dysmorphol. 4, 1-11
Smith, L. T., Wertelecki, W., Milstone, L. M., Petty, E. M., Seashore, M. R., Braverman, I. M., Jenkins, T. G., and Byers, P. H. (1992) Am. J. Hum. Genet. 51, 235-244
Wertelecki, W., Smith, L. T., and Byers, P. (1992) J. Pediatr. 121, 558-564
Nusgens, B. V., Verellen-Dumoulin, C., Hermanns-Le, T., De Paepe, A., Nuytinck, L., Pierard, G. E., and Lapiere, C. M. (1992) Nat. Genet. 1, 214-217
Li, S. W., Arita, M., Fertala, A., Bao, Y., Kopen, G. C., Langsjo, T. K., Hyttinen, M. M., Helminen, H. J., and Prockop, D. J. (2001) Biochem. J. 355, 271-278
Nagase, T., Ishikawa, K., Nakajima, D., Ohira, M., Seki, N., Miyajima, N., Tanaka, A., Kotani, H., Nomura, N., and Ohara, O. (1997) DNA Res. 4, 141-150
Fernandes, R. J. (1993) An Analysis of Collagen Synthesized by a Swarm Rat Chondrosarcoma Cell Line in Monolayer Culture, Ph.D. thesis, Dept. of Biochemistry, Rush University, Chicago, IL
Fernandes, R. J., Schmid, T. M., Harkey, M. A., and Eyre, D. R. (1997) Eur. J. Biochem. 247, 620-624
Laemmli, U. K. (1970) Nature 227, 680-685
Kozak, M. (1989) J. Cell Biol. 108, 229-241
Gavel, Y., and von Heijne, G. (1990) Protein Eng. 3, 433-442
Nardi, J. B., Martos, R., Walden, K. K., Lampe, D. J., and Robertson, H. M. (1999) Insect Biochem. Mol. Biol. 29, 883-897
Lenaers, A., Ansay, M., Nusgens, B. V., and Lapiere, C. M. (1971) Eur. J. Biochem. 23, 533-543
Dombrowski, K. E., and Prockop, D. J. (1988) J. Biol. Chem. 263, 16545-16552
Fertala, A., Sieron, A. L., Hojima, Y., Ganguly, A., and Prockop, D. J. (1994) J. Biol. Chem. 269, 11584-11589
Spranger, J., Winterpacht, A., and Zabel, B. (1994) Eur. J. Pediatr. 153, 56-65
Metsaranta, M., Garofalo, S., Decker, G., Rintala, M., de Crombrugghe, B., and Vuorio, E. (1992) J. Cell Biol. 118, 203-212
Wiestner, M., Rohde, H., Helle, O., Krieg, T., Timpl, R., and Muller, P. K. (1982) EMBO J. 1, 513-516
Kuno, K., and Matsushima, K. (1998) J. Biol. Chem. 273, 13912-13917
Tortorella, M. D., Pratta, M., Liu, R. Q., Abbaszade, I., Ross, H., Burn, T., and Arner, E. (2000) J. Biol. Chem. 275, 25791-25797
Fertala, A., Holmes, D. F., Kadler, K. E., Sieron, A. L., and Prockop, D. J. (1996) J. Biol. Chem. 271, 14864-14869
Bateman, J. F., and Golub, S. B. (1990) Biochem. J. 267, 573-577
Hojima, Y., Behta, B., Romanic, A. M., and Prockop, D. J. (1994) Anal. Biochem. 223, 173-180
Baldwin, C. T., Reginato, A. M., Smith, C., Jimenez, S. A., and Prockop, D. J. (1989) Biochem. J. 262, 521-528
