In Vitro Mutagenesis of Caenorhabditis elegans Cuticle Collagens Identifies a Potential Subtilisin-Like Protease Cleavage Site and Demonstrates that Carboxyl Domain Disulfide Bonding Is Required for Normal Function but Not Assembly

REFERENCES

• Bachinger, H. P., P. Bruckner, R. Timpl, D. J. Prockop, and J. Engel. 1980. Folding mechanism of the triple helix in type-III collagen and type-III pN-collagen. Eur. J. Biochem. 106:619–632.
   PubMedGoogle Scholar
• Bachinger, H. P., L. I. Fessler, R. Timpl, and J. H. Fessler. 1981. Chain assembly intermediate in the biosynthesis of type III procollagen in chick embryo blood vessels. J. Biol. Chem. 256:13193–13199.
   PubMedGoogle Scholar
• Barr, P. J. 1991. Mammalian subtilisins: the long-sought dibasic processing endoproteases. Cell 66:1–3.
   PubMed Web of Science ®Google Scholar
• Betschart, B., and K. Wyss. 1990. Analysis of the cuticular collagens of Ascaris suum. Acta Trop. 47:297–305.
   PubMedGoogle Scholar
• Brenner, S. 1974. The genetics of Caenorhabditis elegans. Genetics 77:71–94.
   PubMed Web of Science ®Google Scholar
• Bruckner, P., and E. F. Eikenberry. 1981. Formation of the triple helix of type I procollagen in cellulo. Eur. J. Biochem. 140:391–395.
   Google Scholar
• Byers, P. H., and R. D. Steiner. 1992. Osteogenesis imperfecta. Annu. Rev. Med. 43:269–282.
   PubMed Web of Science ®Google Scholar
• Byers, P. H., G. A. Wallis, and M. C. Willing. 1991. Osteogenesis imperfecta: translation of mutation to phenotype. J. Med. Genet. 28:433–442.
   PubMed Web of Science ®Google Scholar
• Cole, W. G., D. Chan, G. W. Chambers, I. D. Walker, and J. F. Bateman. 1986. Deletion of 24 amino acids from the pro-alphal(I) chain of type I procollagen in a patient with the Ehlers-Danlos syndrome type VII. J. Biol. Chem. 261:5496–5503.
   PubMed Web of Science ®Google Scholar
• Cox, G. N., S. Carr, J. M. Kramer, and D. Hirsh. 1985. Genetic mapping of Caenorhabditis elegans collagen genes using DNA polymorphisms as phenotypic markers. Genetics 109:513–528.
   PubMedGoogle Scholar
• Cox, G. N., C. Fields, J. M. Kramer, B. Rosenzweig, and D. Hirsh. 1989. Sequence comparisons of developmentally regulated collagen genes of Caenorhabditis elegans. Gene 76:331–344.
   PubMedGoogle Scholar
• Cox, G. N., J. M. Kramer, and D. Hirsh. 1984. Number and organization of collagen genes in Caenorhabditis elegans. Mol. Cell. Biol. 4:2389–2395.
   PubMedGoogle Scholar
• Cox, G. N., M. Kusch, and R. S. Edgar. 1981. Cuticle of Caenorhabditis elegans: its isolation and partial characterization. J. Cell Biol. 90:7–17.
   PubMed Web of Science ®Google Scholar
• Cox, G. N., J. S. Laufer, M. Kusch, and R. S. Edgar. 1980. Genetic and phenotypic characterization of roller mutants of Caenorhabditis elegans. Genetics 95:317–339.
   PubMedGoogle Scholar
• Cox, G. N., S. Staprans, and R. S. Edgar. 1981. The cuticle of Caenorhabditis elegans. II. Stage-specific changes in ultrastructure and protein composition during postembryonic development. Dev. Biol. 86:456–470.
   PubMedGoogle Scholar
• Doege, K. J., and J. H. Fessler. 1986. Folding of carboxyl domain and assembly of procollagen I. J. Biol. Chem. 261:8924–8935.
   PubMed Web of Science ®Google Scholar
• Edgar, R. S., G. N. Cox, M. Kusch, and J. C. Politz. 1982. The cuticle of Caenorhabditis elegans. J. Nematol. 14:248–258.
   PubMedGoogle Scholar
• Edwards, M. K. Personal communication.
   Google Scholar
• Engel, J., and D. J. Prockop. 1991. The zipper-like folding of collagen triple helices and the effects of mutations that disrupt the zipper. Annu. Rev. Biophys. Chem. 20:137–152.
   PubMedGoogle Scholar
• Eyre, D., and J. M. Kramer. Unpublished results.
   Google Scholar
• Fire, A., D. Albertson, S. W. Harrison, and D. G. Moerman. 1991. Production of antisense RNA leads to effective and specific inhibition of gene expression in C elegans muscle. Development 113:503–514.
   PubMed Web of Science ®Google Scholar
• Foster, D. C., C. A. Sprecher, R. D. Holly, J. E. Gambee, K. M. Walker, and A. A. Kumar. 1990. Endoproteolytic processing of the dibasic cleavage site in the human protein C precursor in trans-fected mammalian cells: effects of sequence alterations on efficiency of cleavage. Biochemistry 29:347–354.
   PubMedGoogle Scholar
• Fujimoto, D., K. Horiuchi, and M. Hirama. 1981. Isotrityrosine, a new cross-linking amino acid isolated from Ascaris cuticle collagen. Biochem. Biophys. Res. Commun. 99:637–643.
   PubMedGoogle Scholar
• Fujimoto, D., and S. Kanaya. 1973. Cuticlin: a noncollagen structural protein from Ascaris cuticle. Arch. Biochem. Biophys. 157:1–6.
   PubMedGoogle Scholar
• Geisselsoder, J., F. Witney, and P. Yuckenberg. 1987. Efficient site-directed in vitro mutagenesis. BioTechniques 5:786–791.
   Google Scholar
• Hulmes, D. J. S. 1992. The collagen superfamily—diverse structures and assemblies. Essays Biochem. 27:49–67.
   PubMed Web of Science ®Google Scholar
• Johnson, J. J., and J. M. Kramer. Unpublished results.
   Google Scholar
• Johnstone, I. L., Y. Shafi, and J. D. Barry. 1992. Molecular analysis of mutations in the Caenorhabditis elegans collagen gene dpy-7. EMBO J. 11:3857–3863.
   PubMedGoogle Scholar
• Kingston, I. B., and J. Pettitt. 1990. Structure and expression of Ascaris suum collagen genes: a comparison with Caenorhabditis elegans. Acta Trop. 47:283–287.
   PubMedGoogle Scholar
• Kingston, I. B., S. M. Wainwright, and D. Cooper. 1989. Comparison of collagen gene sequences in Ascaris suum and Caenorhabditis elegans. Mol. Biochem. Parasitol. 37:137–146.
   PubMedGoogle Scholar
• Kramer, J. M. 1994. Structures and functions of collagens in C. elegans. FASEB J. 8:329–336.
   PubMedGoogle Scholar
• Kramer, J. M., G. N. Cox, and D. Hirsh. 1982. Comparisons of the complete sequences of two collagen genes from Caenorhabditis elegans. Cell 30:599–606.
   PubMedGoogle Scholar
• Kramer, J. M., R. P. French, E.-C. Park, and J. J. Johnson. 1990. The Caenorhabditis elegans rol-6 gene, which interacts with the sqt-1 collagen gene to determine organismal morphology, encodes a collagen. Mol. Cell. Biol. 10:2081–2089.
   PubMed Web of Science ®Google Scholar
• Kramer, J. M., and J. J. Johnson. 1993. Analysis of mutations in the sqt-1 and rol-6 collagen genes of Caenorhabditis elegans. Genetics 135:1035–1045.
   PubMedGoogle Scholar
• Kramer, J. M., J. J. Johnson, R. S. Edgar, C. Basch, and S. Roberts. 1988. The sqt-1 gene of C. elegans encodes a collagen critical for organismal morphogenesis. Cell 55:555–565.
   PubMedGoogle Scholar
• Kusch, M., and R. S. Edgar. 1986. Genetic studies of unusual loci that affect body shape of the nematode Caenorhabditis elegans and may code for cuticle structural proteins. Genetics 113:621–639.
   PubMedGoogle Scholar
• Labourdette, L., and M. Vanderrest. 1993. Analysis of the role of the COL1 domain and its adjacent cysteine-containing sequence in the chain assembly of type-IX collagen. FEBS Lett. 320:211–214.
   PubMedGoogle Scholar
• Lapiere, C. M., A. Lenaers, and L. D. Kohn. 1971. Procollagen peptidase: an enzyme excising the coordination peptides of procollagen. Proc. Natl. Acad. Sci. USA 68:3054–3058.
   PubMed Web of Science ®Google Scholar
• Lenaers, A., M. Ansay, B. V. Nusgens, and C. M. Lapiere. 1971. Collagen made of extended alpha-chains, procollagen, in genetically-defective dermatosparaxic calves. Eur. J. Biochem. 23:533–543.
   PubMedGoogle Scholar
• Levy, A. D., and J. M. Kramer. 1993. Identification, sequence and expression patterns of the Caenorhabditis elegans col-36 and col-40 collagen-encoding genes. Gene 137:281–285.
   PubMedGoogle Scholar
• Levy, A. D., J. Yang, and J. M. Kramer. 1993. Molecular and genetic analyses of the Caenorhabditis elegans dpy-2 and dpy-10 collagen genes: a variety of molecular alterations affect organismal morphology. Mol. Biol. Cell 4:803–817.
   PubMedGoogle Scholar
• Mazzorana, M., H. Gruffat, A. Sergeant, and M. Vanderrest. 1993. Mechanisms of collagen trimer formation—construction and expression of a recombinant minigene in HeLa cells reveals a direct effect of prolyl hydroxylation on chain assembly of type-XII collagen. J. Biol. Chem. 268:3029–3032.
   PubMedGoogle Scholar
• McBride, D. J., K. E. Kadler, Y. Hojima, and D. J. Prockop. 1992. Self-assembly into fibrils of a homotrimer of type-I collagen. Matrix 12:256–263.
   PubMedGoogle Scholar
• McBride, O. W., and W. F. Harrington. 1967. Helix-coil transition in collagen. Evidence for a single-stranded triple helix. Biochemistry 6:1499–1514.
   PubMed Web of Science ®Google Scholar
• Mello, C. C., J. M. Kramer, D. Stinchcomb, and V. Ambros. 1991. Efficient gene transfer in C. elegans: extrachromosomal maintenance and integration of transforming sequences. EMBO J. 10:3959–3970.
   PubMed Web of Science ®Google Scholar
• Okkema, P. G., S. W. Harrison, V. Plunger, A. Aryana, and A. Fire. 1993. Sequence requirements for myosin gene expression and regulation in Caenorhabditis elegans. Genetics 135:385–404.
   PubMed Web of Science ®Google Scholar
• Park, E.-C., and H. R. Horvitz. 1986. Mutations with dominant effects on the behavior and morphology of the nematode Caenorhabditis elegans. Genetics 113:821–852.
   PubMed Web of Science ®Google Scholar
• Park, Y.-S., and J. M. Kramer. 1990. Tandemly duplicated Caenorhabditis elegans collagen genes differ in their modes of splicing. J. Mol. Biol. 211:395–406.
   PubMedGoogle Scholar
• Park, Y.-S., and J. M. Kramer. The C. elegans sqt-1 and rol-6 collagen genes are coordinately expressed during development, but not at all stages that display mutant phenotypes. Dev. Biol., in press.
   Google Scholar
• Peters, K., J. McDowall, and A. M. Rose. 1991. Mutations in the bli-4 (I) locus of Caenorhabditis elegans disrupt both adult cuticle and early larval development. Genetics 129:95–102.
   PubMedGoogle Scholar
• Peters, K., and A. M. Rose. Personal communication.
   Google Scholar
• Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
   Google Scholar
• Shaw, L. M., and B. R. Olsen. 1991. FACIT collagens: diverse molecular bridges in extracellular matrices. Trends Biochem. Sci. 16:191–194.
   PubMed Web of Science ®Google Scholar
• Smith, L. T., W. Wertelecki, L. M. Milstone, E. M. Petty, M. R. Seashore, I. M. Braverman, T. G. Jenkins, and P. H. Byers. 1992. 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.
   PubMed Web of Science ®Google Scholar
• Stinchcomb, D. T., J. Shaw, S. H. Carr, and D. Hirsh. 1985. Extrachromosomal DNA transformation of Caenorhabditis elegans. Mol. Cell. Biol. 5:3484–3496.
   PubMed Web of Science ®Google Scholar
• Sykes, B. 1989. Inherited collagen disorders. Mol. Biol. Med. 6:19–26.
   PubMedGoogle Scholar
• Van de Ven, W. J., A. J. Roebroek, and H. L. Van Duijnhoven. 1993. Structure and function of eukaryotic proprotein processing enzymes of the subtilisin family of serine proteases. Crit. Rev. Oncogenesis 4:115–136.
   PubMed Web of Science ®Google Scholar
• von Mende, N., D. Bird, P. S. Albert, and D. L. Riddle. 1988. dpy-13: a nematode collagen gene that affects body shape. Cell 55:567–576.
   PubMedGoogle Scholar
• Watanabe, T., K. Murakami, and K. Nakayama. 1993. Positional and additive effects of basic amino acids on processing or precursor proteins within the constitutive secretory pathway. FEBS Lett. 320:215–218.
   PubMedGoogle Scholar
• Weil, D., M. D'Alessio, F. Ramirez, W. de Wet, W. G. Cole, D. Chan, and J. F. Bateman. 1989. A base substitution in the exon of a collagen gene causes alternative splicing and generates a structurally abnormal polypeptide in a patient with Ehlers-Danlos syndrome type VII. EMBO J. 8:1705–1710.
   PubMed Web of Science ®Google Scholar
• Weil, D., M. D'Alessio, F. Ramirez, and D. R. Eyre. 1990. Structural and functional characterization of a splicing mutation in the pro-alpha2(I) collagen gene of an Ehlers-Danlos type VII patient. J. Biol. Chem. 265:16007–16011.
   PubMedGoogle Scholar