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. 1984 Dec 21;12(24):9383–9394. doi: 10.1093/nar/12.24.9383

Molecular cloning and carboxyl-propeptide analysis of human type III procollagen.

H R Loidl, J M Brinker, M May, T Pihlajaniemi, S Morrow, J Rosenbloom, J C Myers
PMCID: PMC320468  PMID: 6096827

Abstract

Two human cDNA libraries prepared from normal fibroblast (GM3348) and rhabdomyosarcoma (CCL136) mRNAs were screened under cross hybridization conditions with a genomic fragment coding for exons 2 and 3 of the avian type III procollagen COOH-propeptide (Yamada, Y., Mudryj, M., Sullivan, M. and deCrombrugghe, B. (1983) J. Biol. Chem. 258, 2758-2761). One cDNA clone containing a 1.12 kb insert was isolated from the CCL136 library and later used to identify a GM3348 derived clone with a 2.4 kb insert. Comparison of the human and avian type III C-terminal propeptides revealed much more divergence in the first 54 amino acids following the terminal cysteine of the triple helical region than is present in the alpha 1(I) and alpha 2(I) procollagen chains of these species. Analysis of poly (A+) RNA from normal human fibroblast and tumor cell lines showed that they differed greatly in the relative amounts of alpha 1(I), alpha 2(I), and alpha 1(III) mRNAs. Furthermore, as we previously reported for the alpha 1(I) and alpha 2(I) transcripts, multiple mRNAs also hybridize to the cloned alpha 1(III) DNA.

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Selected References

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  1. Bentz H., Morris N. P., Murray L. W., Sakai L. Y., Hollister D. W., Burgeson R. E. Isolation and partial characterization of a new human collagen with an extended triple-helical structural domain. Proc Natl Acad Sci U S A. 1983 Jun;80(11):3168–3172. doi: 10.1073/pnas.80.11.3168. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bernard M. P., Chu M. L., Myers J. C., Ramirez F., Eikenberry E. F., Prockop D. J. Nucleotide sequences of complementary deoxyribonucleic acids for the pro alpha 1 chain of human type I procollagen. Statistical evaluation of structures that are conserved during evolution. Biochemistry. 1983 Oct 25;22(22):5213–5223. doi: 10.1021/bi00291a023. [DOI] [PubMed] [Google Scholar]
  3. Bernard M. P., Myers J. C., Chu M. L., Ramirez F., Eikenberry E. F., Prockop D. J. Structure of a cDNA for the pro alpha 2 chain of human type I procollagen. Comparison with chick cDNA for pro alpha 2(I) identifies structurally conserved features of the protein and the gene. Biochemistry. 1983 Mar 1;22(5):1139–1145. doi: 10.1021/bi00274a023. [DOI] [PubMed] [Google Scholar]
  4. Bornstein P., Sage H. Structurally distinct collagen types. Annu Rev Biochem. 1980;49:957–1003. doi: 10.1146/annurev.bi.49.070180.004521. [DOI] [PubMed] [Google Scholar]
  5. Burgeson R. E., Hebda P. A., Morris N. P., Hollister D. W. Human cartilage collagens. Comparison of cartilage collagens with human type V collagen. J Biol Chem. 1982 Jul 10;257(13):7852–7856. [PubMed] [Google Scholar]
  6. Casadaban M. J., Cohen S. N. Analysis of gene control signals by DNA fusion and cloning in Escherichia coli. J Mol Biol. 1980 Apr;138(2):179–207. doi: 10.1016/0022-2836(80)90283-1. [DOI] [PubMed] [Google Scholar]
  7. Chu M. L., Myers J. C., Bernard M. P., Ding J. F., Ramirez F. Cloning and characterization of five overlapping cDNAs specific for the human pro alpha 1(I) collagen chain. Nucleic Acids Res. 1982 Oct 11;10(19):5925–5934. doi: 10.1093/nar/10.19.5925. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Chu M. L., Williams C. J., Pepe G., Hirsch J. L., Prockop D. J., Ramirez F. Internal deletion in a collagen gene in a perinatal lethal form of osteogenesis imperfecta. Nature. 1983 Jul 7;304(5921):78–80. doi: 10.1038/304078a0. [DOI] [PubMed] [Google Scholar]
  9. Chu M. L., de Wet W., Bernard M., Ding J. F., Morabito M., Myers J., Williams C., Ramirez F. Human pro alpha 1(I) collagen gene structure reveals evolutionary conservation of a pattern of introns and exons. 1984 Jul 26-Aug 1Nature. 310(5975):337–340. doi: 10.1038/310337a0. [DOI] [PubMed] [Google Scholar]
  10. Deak S. B., Nicholls A., Pope F. M., Prockop D. J. The molecular defect in a nonlethal variant of osteogenesis imperfecta. Synthesis of pro-alpha 2(I) chains which are not incorporated into trimers of type I procollagen. J Biol Chem. 1983 Dec 25;258(24):15192–15197. [PubMed] [Google Scholar]
  11. Dickson L. A., Pihlajaniemi T., Deak S., Pope F. M., Nicholls A., Prockop D. J., Myers J. C. Nuclease S1 mapping of a homozygous mutation in the carboxyl-propeptide-coding region of the pro alpha 2(I) collagen gene in a patient with osteogenesis imperfecta. Proc Natl Acad Sci U S A. 1984 Jul;81(14):4524–4528. doi: 10.1073/pnas.81.14.4524. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Fuller F., Boedtker H. Sequence determination and analysis of the 3' region of chicken pro-alpha 1(I) and pro-alpha 2(I) collagen messenger ribonucleic acids including the carboxy-terminal propeptide sequences. Biochemistry. 1981 Feb 17;20(4):996–1006. doi: 10.1021/bi00507a054. [DOI] [PubMed] [Google Scholar]
  13. Gibson G. J., Kielty C. M., Garner C., Schor S. L., Grant M. E. Identification and partial characterization of three low-molecular-weight collagenous polypeptides synthesized by chondrocytes cultured within collagen gels in the absence and in the presence of fibronectin. Biochem J. 1983 May 1;211(2):417–426. doi: 10.1042/bj2110417. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Huerre C., Junien C., Weil D., Chu M. L., Morabito M., Van Cong N., Myers J. C., Foubert C., Gross M. S., Prockop D. J. Human type I procollagen genes are located on different chromosomes. Proc Natl Acad Sci U S A. 1982 Nov;79(21):6627–6630. doi: 10.1073/pnas.79.21.6627. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Jander R., Rauterberg J., Glanville R. W. Further characterization of the three polypeptide chains of bovine and human short-chain collagen (intima collagen). Eur J Biochem. 1983 Jun 1;133(1):39–46. doi: 10.1111/j.1432-1033.1983.tb07427.x. [DOI] [PubMed] [Google Scholar]
  16. Krieg T., Timpl R., Alitalo K., Kurkinen M., Vaheri A. Type III procollagen is the major collageneous component produced by a continuous rhabdomyosarcoma cell line. FEBS Lett. 1979 Aug 15;104(2):405–409. doi: 10.1016/0014-5793(79)80863-7. [DOI] [PubMed] [Google Scholar]
  17. Kurkinen M., Barlow D. P., Helfman D. M., Williams J. G., Hogan B. L. Isolation of cDNA clones for basal lamina components: type IV procollagen. Nucleic Acids Res. 1983 Sep 24;11(18):6199–6209. doi: 10.1093/nar/11.18.6199. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Lukens L. N., Frischauf A. M., Pawlowski P. J., Brierley G. T., Lehrach H. Construction and characterization of type II collagen complementary deoxyribonucleic acid clones. Nucleic Acids Res. 1983 Sep 10;11(17):6021–6039. doi: 10.1093/nar/11.17.6021. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Mayne R., Vail M. S., Miller E. J. Characterization of the collagen chains synthesized by cultured smooth muscle cells derived from rhesus monkey thoracic aorta. Biochemistry. 1978 Feb 7;17(3):446–452. doi: 10.1021/bi00596a011. [DOI] [PubMed] [Google Scholar]
  20. Messing J. New M13 vectors for cloning. Methods Enzymol. 1983;101:20–78. doi: 10.1016/0076-6879(83)01005-8. [DOI] [PubMed] [Google Scholar]
  21. Myers J. C., Chu M. L., Faro S. H., Clark W. J., Prockop D. J., Ramirez F. Cloning a cDNA for the pro-alpha 2 chain of human type I collagen. Proc Natl Acad Sci U S A. 1981 Jun;78(6):3516–3520. doi: 10.1073/pnas.78.6.3516. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Myers J. C., Dickson L. A., de Wet W. J., Bernard M. P., Chu M. L., Di Liberto M., Pepe G., Sangiorgi F. O., Ramirez F. Analysis of the 3' end of the human pro-alpha 2(I) collagen gene. Utilization of multiple polyadenylation sites in cultured fibroblasts. J Biol Chem. 1983 Aug 25;258(16):10128–10135. [PubMed] [Google Scholar]
  23. Myers J. C., Ramirez F., Kacian D. L., Flood M., Spiegelman S. A simple purification of avian myeloblastosis virus reverse transcriptase for full-length transcription of 35 S RNA. Anal Biochem. 1980 Jan 1;101(1):88–96. doi: 10.1016/0003-2697(80)90044-5. [DOI] [PubMed] [Google Scholar]
  24. Pihlajaniemi T., Myllylä R., Alitalo K., Vaheri A., Kivirikko K. I. Posttranslational modifications in the biosynthesis of type IV collagen by a human tumor cell line. Biochemistry. 1981 Dec 22;20(26):7409–7415. doi: 10.1021/bi00529a014. [DOI] [PubMed] [Google Scholar]
  25. Prockop D. J., Kivirikko K. I. Heritable diseases of collagen. N Engl J Med. 1984 Aug 9;311(6):376–386. doi: 10.1056/NEJM198408093110606. [DOI] [PubMed] [Google Scholar]
  26. Sage H., Trüeb B., Bornstein P. Biosynthetic and structural properties of endothelial cell type VIII collagen. J Biol Chem. 1983 Nov 10;258(21):13391–13401. [PubMed] [Google Scholar]
  27. Sandell L. J., Prentice H. L., Kravis D., Upholt W. B. Structure and sequence of the chicken type II procollagen gene. Characterization of the region encoding the carboxyl-terminal telopeptide and propeptide. J Biol Chem. 1984 Jun 25;259(12):7826–7834. [PubMed] [Google Scholar]
  28. Seyer J. M., Kang A. H. Covalent structure of collagen: amino acid sequence of alpha 1(III)-CB9 from type III collagen of human liver. Biochemistry. 1981 Apr 28;20(9):2621–2627. doi: 10.1021/bi00512a040. [DOI] [PubMed] [Google Scholar]
  29. Strom C. M., Upholt W. B. Isolation and characterization of genomic clones corresponding to the human type II procollagen gene. Nucleic Acids Res. 1984 Jan 25;12(2):1025–1038. doi: 10.1093/nar/12.2.1025. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Tate V., Finer M., Boedtker H., Doty P. Procollagen genes: further sequence studies and interspecies comparisons. Cold Spring Harb Symp Quant Biol. 1983;47(Pt 2):1039–1049. doi: 10.1101/sqb.1983.047.01.117. [DOI] [PubMed] [Google Scholar]
  31. Thomas P. S. Hybridization of denatured RNA and small DNA fragments transferred to nitrocellulose. Proc Natl Acad Sci U S A. 1980 Sep;77(9):5201–5205. doi: 10.1073/pnas.77.9.5201. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Wang S. Y., Gudas L. J. Isolation of cDNA clones specific for collagen IV and laminin from mouse teratocarcinoma cells. Proc Natl Acad Sci U S A. 1983 Oct;80(19):5880–5884. doi: 10.1073/pnas.80.19.5880. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Yamada Y., Kühn K., de Crombrugghe B. A conserved nucleotide sequence, coding for a segment of the C-propeptide, is found at the same location in different collagen genes. Nucleic Acids Res. 1983 May 11;11(9):2733–2744. doi: 10.1093/nar/11.9.2733. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Yamada Y., Liau G., Mudryj M., Obici S., de Crombrugghe B. Conservation of the sizes for one but not another class of exons in two chick collagen genes. 1984 Jul 26-Aug 1Nature. 310(5975):333–337. doi: 10.1038/310333a0. [DOI] [PubMed] [Google Scholar]
  35. Yamada Y., Mudryj M., Sullivan M., de Crombrugghe B. Isolation and characterization of a genomic clone encoding chick alpha 1 type III collagen. J Biol Chem. 1983 Mar 10;258(5):2758–2761. [PubMed] [Google Scholar]
  36. de Wet W. J., Chu M. L., Prockop D. J. The mRNAs for the pro-alpha 1(I) and pro-alpha 2(I) chains of type I procollagen are translated at the same rate in normal human fibroblasts and in fibroblasts from two variants of osteogenesis imperfecta with altered steady state ratios of the two mRNAs. J Biol Chem. 1983 Dec 10;258(23):14385–14389. [PubMed] [Google Scholar]

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