Use of Bmp1/Tll1 doubly homozygous null mice and proteomics to identify and validate in vivo substrates of bone morphogenetic protein 1/Tolloid-like metalloproteinases

Molecular and Cellular Biology

Volumn 23, Issue 13, 2003, Pages 4428-4438

  Pappano, William N ^a   Steiglitz, Barry M ^a   Scott, Ian C ^b,d   Keene, Douglas R ^c   Greenspan, Daniel S ^a,b  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^c SHRINERS HOSPITAL FOR CHILDREN   (United States)

^d ASTRAZENECA   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN; CHORDIN; COLLAGEN FIBRIL; GENE PRODUCT; METALLOPROTEINASE; PROCOLLAGEN; PROCOLLAGEN C PROTEINASE; TOLLOID LIKE 1; TOLLOID LIKE 2; TOLLOID LIKE METALLOPROTEINASE; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; BMP1 GENE; COLLAGEN SYNTHESIS; CONTROLLED STUDY; EMBRYO; EMBRYO DEATH; ENZYME ACTIVITY; ENZYME SUBSTRATE; EXTRACELLULAR MATRIX; GENE; HOMOZYGOSITY; IN VIVO STUDY; MAMMAL; MOUSE; NONHUMAN; NULL ALLELE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEOMICS; SIGNAL TRANSDUCTION; TLL1 GENE;

ALLELES; ANIMALS; BLOTTING, WESTERN; BONE MORPHOGENETIC PROTEINS; CELLS, CULTURED; COLLAGEN; COLLAGEN TYPE XI; CULTURE MEDIA; DERMIS; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; EPIDERMIS; EXTRACELLULAR MATRIX; FUNGAL PROTEINS; GENOTYPE; GLYCOPROTEINS; HOMOZYGOTE; IMMUNOBLOTTING; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MASS SPECTROMETRY; METALLOENDOPEPTIDASES; METALLOPROTEASES; MICE; MICROSCOPY, ELECTRON; MICROSCOPY, IMMUNOELECTRON; MITOGEN-ACTIVATED PROTEIN KINASES; MODELS, GENETIC; PEPTIDES; PROTEIN BINDING; PROTEINS; PROTEOME; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SUBSTRATE SPECIFICITY; TIME FACTORS;

ANIMALIA; MAMMALIA;

EID: 0038044731     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.23.13.4428-4438.2003     Document Type: Article

References (41)

1. Amano, S., I. C. Scott, K. Takahara, M. Koch, M.-F. Champliaud, D. R. Gerecke, D. R. Keene, D. L. Hudson, T. Nishiyama, S. Lee, D. S. Greenspan, and R. E. Burgeson. 2000. Bone morphogenetic protein 1 is an extracellular processing enzyme of the laminin 5 γ2 chain. J. Biol. Chem. 275:22728-22735.
2. Bateman, J. F., J. J. Pillow, T. Mascara, S. Medvedec, J. A. M. Ramshaw, and W. G. Cole. 1987. Cell-layer-associated proteolytic cleavage of the telopeptides of type 1 collagen in fibroblast culture. Biochem. J. 245:677-682.
3. Blader, P., S. Rastegar, N. Fischer, and U. Strähle. 1997. Cleavage of the BMP-4 antagonist Chordin by zebrafish Tolloid. Science 278:1937-1940.
4. Bond, J. S. and R. J. Beynon. 1995. The astacin family of metalloendopeptidases. Protein Sci. 4:1247-1261.
5. Clark, T. G., S. J. Conway, I. C. Scott, P. A. Labosky, G. Winnier, J. Bundy, B. L. M. Hogan, and D. S. Greenspan. 1999. The mammalian Tolloid-like 1 gene, Tll1, is necessary for normal seplation and positioning of the heart. Development 126:2631-2642.
6. Colige, A., S.-W. Li, A. L. Sieron, B. V. Nusgens, D. J. Prockop, and C. M. Lapière. 1997. 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.
7. Colige, A., I. Vandenberghe, M. Thiry, C. A. Lambert, J. Van Beeumen, S.-W. Li, D. J. Prockop, and C. M. Lapière. 2002. Cloning and characterization of ADAMTS-14, a novel ADAMTS displaying high homology with ADAMTS-2 and ADAMTS-3. J. Biol. Chem. 277:5756-5766.
8. Connors, S. A., J. Trout, M. Ekker, and M. C. Mullins. 1999. The role of Tolloid/mini fin in dorsoventral pattern formation of the zebrafish embryo. Development 126:3119-3130.
9. Ferguson, E. L., and K. V. Anderson. 1991. Dorsal-ventral pattern formation in the Drosophila embryo: the role of zygotically active genes. Curr. Top. Dev. Biol. 25:17-43.
10. Fernandes, R. J., S. Hirohata, J. M. Engle, A. Colige, D. H. Cohn, D. R. Eyre, and S. S. Apte. 2001. Procollagen II amino propeptide processing by ADAMTS-3. J. Biol. Chem. 276:31502-31509.
11. Fisher, L. W., J. T. Stubbs III, and M. F. Young. 1995. Antisera and cDNA probes to human and certain animal model bone matrix noncollagenous proteins. Acta Orthop. Scand. Suppl. 266:61-65.
12. Hogan, B. L. M., R. Beddington, F. Constantini, and E. Lacy. 1994. Manipulating the mouse embryo: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
13. 2-terminal propeptide, and a furin-like proprotein convertase processes the COOH-terminal propeptide of pro-α1(V) collagen. J. Biol. Chem. 273:27511-27517.
14. Kessler, E., K. Takahara, L. Biniaminov, M. Brusel, and D. S. Greenspan. 1996. Bone morphogenetic protein-1: the type I procollagen C-proteinase. Science 271:360-362.
15. Lee, S., D. E. Solow-Cordero, E. Kessler, K. Takahara, and D. S. Greenspan. 1997. Transforming growth factor-β regulation of bone morphogenetic protein-1/procollagen C-proteinase and related proteins in fibrogenic cells and keratinocytes. J. Biol. Chem. 272:19059-19066.
16. Lee, S.-T., E. Kessler, and D. S. Greenspan. 1990. Analysis of site-directed mutations in human pro-α2((I) collagen which block cleavage by the C-proteinase. J. Biol. Chem. 265:21992-21996.
17. Li, S.-W., A. L. Sieron, A. Gertala, Y. Hojima, W. V. Arnold, and D. J. Prockop. 1996. The C-proteinase that processes procollagens to fibrillar collagens is identical to the protein previously identified as bone morphogenie protein-1. Proc. Natl. Acad. Sci. USA 93:5127-5130.
18. Marqués, G., M. Musacchio, M. J. Shimell, K. Wünnenberg-Stapleton, K. W. Cho, and M. B. O'Connor. 1997. Production of a DPP activity gradient in the early Drosophila embryo through the opposing actions of the SOG and TLD proteins. Cell 91:417-426.
19. Morris, N. P., J. T. Oxford, G. B. M. Davies, B. F. Smoody, and D. R. Keene. 2000. Developmentally regulated alternative splicing of the α1(XI) collagen chain: spatial and temporal segregation of isoforms in the cartilage of fetal rat long bones. J. Histochem. Cytochem. 48:725-741.
20. O'Farrell, P. 1975. High resolution two-dimensional electrophoresis of proteins. J. Biol. Chem. 250:4007-4021.
21. Oxford, J. T., K. J. Doege, and N. P. Morris. 1995. Alternative exon splicing within the amino-terminal nontriple-helical domain of the rat pro-α1(XI) collagen chain generates multiple forms of the mRNA transcript which exhibit tissue-dependent variation. J. Biol. Chem. 270:9478-9485.
22. Pappano, W. N., I. C. Scott, T. G. Clark, R. L. Eddy, T. B. Shows, and D. S. Greenspan. 1998. Coding sequence and expression patterns of mouse chordin and mapping of the cognate mouse Chrd and human CHRD genes. Genomics 52:236-239.
23. a. Perkins, D. N., D. J. Pappin, D. M. Creasy, and J. S. Cottrell. 1999. Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 20:3551-3567.
24. Piccolo, S., E. Agius, B. Lu, S. Goodman, L. Dale, and E. M. De Robertis. 1997. Cleavage of Chordin by Xolloid metalloprotease suggests a role for proteolytic processing in the regulation of Spemann organizer activity. Cell 91:407-416.
25. Prockop, D. J., and D. J. S. Hulmes. 1994. Assembly of collagen fibrils denovo from soluble precursors: polymerization and copolymerization of procollagen, pN-collagen, and mutated collagens, p. 47-90. In P. D. Yurchenco, D. E. Birk, and R. P. Mecham (ed.), Extracellular matrix assembly and structure. Academic Press, New York, N.Y.
26. Prockop, D. J. and K. I. Kivirikko. 1995. Collagens: molecular biology, diseases, and potentials for therapy. Annu. Rev. Biochem. 64:403-434.
27. Rattenholl, A., W. M. Pappano, M. Koch, D. R. Keene, K. E. Kadler, T. Sasaki, R. Timpl, R. E. Burgeon, D. S. Greenspan, and L. Bruckner-Tuderman. 2002. Proteinases of the bone morphogenetic protein-1 family convert procollagen VII to mature anchoring fibril collagen. J. Biol. Chem. 277:26372-26378.
28. Sakai, L. Y., and D. R. Keene. 1994. Fibrillin: monomers and microfibrils. Methods Enzymol. 245:29-52.
29. Schönherr, E., P. Witsch-Prehm, B. Harrach, H. Robenek, J. Rauterberg, and H. Kresse. 1995. Interaction of biglycan with type 1 collagen. J. Biol. Chem. 270:2776-2783.
30. Scott, I. C., I. L. Blitz, W. N. Pappano, Y. Imamura, T. G. Clark, B. M. Steiglitz, C. L. Thomas, S. A. Maas, K. Takahara, K. W. Y. Cho, and D. S. Greenspan. 1999. 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.
31. Scott, I. C., I. L. Blitz, W. N. Pappano, S. A. Maas, K. W. Y. Cho, and D. S. Greenspan. 2001. Homologues of twisted gastrulation are extracellular co-factors in antagonism of BMP signalling. Nature 410:475-478.
32. Scott, I. C., Y. Imamura, W. N. Pappano, J. M. Troedel, A. D. Recklies, P. J. Roughley, and D. S. Greenspan. 2000. Bone morphogenetic protein-1 processes probiglycan. J. Biol. Chem. 275:30504-30511.
33. Steiglitz, B. M., D. R. Keene, and D. S. Greenspan. 2002. PCOLCE2 encodes a functional procollagen C-proteinase enhancer (PCPE2) that is a collagen-binding protein differing in distribution of expression and post-translational modification from the peviously described PCPE1. J. Biol. Chem. 277:49820-49830.
34. Suzuki, N., P. A. Labosky, Y. Furuta, L. Hargett, R. Dunn, A. B. Fogo, K. Takahara, D. M. P. Peters, D. S. Greenspan, and B. L. M. Hogan. 1996. 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.
35. Takahara, K., R. Brevard, G. G. Hoffman, N. Suzuki, and D. S. Greenspan. 1996. Characterization of a novel gene product (mammalian Tolloid-like) with high sequence similarity to mammalian Tolloid/bone morphogenetic protein-1. Genomics 34:157-165.
36. Takahara, K., G. E. Lyons, and D. S. Greenspan. 1994. Bone morphogenetic protein-1 and a mammalian Tolloid homologue (mTld) are encoded by alternatively spliced transcripts which are differentially expressed in some tissues. J. Biol. Chem. 269:32572-32578.
37. 2pro-α2(V) collagen heterotrimer by bone morphogenetic protein-I and furin-like proprotein convertases. J. Biol. Chem. 277:5596-5602.
38. Uzel, M. I., I. C. Scott, H. Babakhanlou-Chase, A. H. Palamakumbura, W. N. Pappano, H.-H. Hong, D. S. Greenspan, and P. C. Trackman. 2001. Multiple bone morphogenetic protein 1-related mammalian metalloproteinases process pro-lysyl oxidase at the correct physiological site and control lysyl oxidase activation in mouse embryo fibroblast cultures. J. Biol. Chem. 276:22537-22543.
39. Wozney, J. M., V. Rosen, A. J. Celeste, L. M. Mitsock, M. J. Whitters, R. W. Kriz, R. M. Hewick, and E. A. Wang. 1988. Novel regulators of bone formation: molecular clones and activities. Science 242:1528-1534.
40. Xu, T., P. Bianco, L. W. Fisher, G. Longeneeker, E. Smith, S. Goldstein, J. Bonadio, A. Boskey, A.-M. Heegaard, B. Sommer, K. Satomura, P. Dominguez, Z. Chengyan, A. B. Kulkarni, P. G. Robey, and M. F. Young. 1998. Targeted disruption of the biglycan gene leads to an osteoporosis-like phenotype in mice. Nat. Genet. 20:78-82.
41. Zhidkova, N. I., S. K. Justice, and R. Mayne. 1995. Alternative mRNA processing occurs in the variable region of the pro-α1(XI) and pro-α2(XI) collagen chains. J. Biol. Chem. 270:9486-9493.