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. 1987 Jan;84(2):512–516. doi: 10.1073/pnas.84.2.512

Human collagen genes encoding basement membrane alpha 1 (IV) and alpha 2 (IV) chains map to the distal long arm of chromosome 13.

C A Griffin, B S Emanuel, J R Hansen, W K Cavenee, J C Myers
PMCID: PMC304239  PMID: 3025878

Abstract

At least 20 genes encode the structurally related collagen chains that comprise greater than 10 homo- or heterotrimeric types. Six members of this multigene family have been assigned to five chromosomes in the human genome. The two type I genes, alpha 1 and alpha 2, are located on chromosomes 17 and 7, respectively, and the alpha 1 (II) gene is located on chromosome 12. Our recent mapping of the alpha 1 (III) and alpha 2 (V) genes to the q24.3----q31 region of chromosome 2 provided the only evidence that the collagen genes are not entirely dispersed. To further determine their organization, we and others localized the alpha 1 (IV) gene to chromosome 13 and in our experiments sublocalized the gene to band q34 by in situ hybridization. Here we show the presence of the alpha 2 type IV locus also on the distal long arm of chromosome 13 by hybridizing a human alpha 2 (IV) cDNA clone to rodent-human hybrids and to metaphase chromosomes. To our knowledge, these studies represent the only demonstration of linkage between genes encoding both polypeptide chains of the same collagen type.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Alitalo K., Vaheri A., Krieg T., Timpl R. Biosynthesis of two subunits of type IV procollagen and of other basement membrane proteins by a human tumor cell line. Eur J Biochem. 1980 Aug;109(1):247–255. doi: 10.1111/j.1432-1033.1980.tb04790.x. [DOI] [PubMed] [Google Scholar]
  2. Boedtker H., Fuller F., Tate V. The structure of collagen genes. Int Rev Connect Tissue Res. 1983;10:1–63. doi: 10.1016/b978-0-12-363710-9.50007-1. [DOI] [PubMed] [Google Scholar]
  3. Brinker J. M., Gudas L. J., Loidl H. R., Wang S. Y., Rosenbloom J., Kefalides N. A., Myers J. C. Restricted homology between human alpha 1 type IV and other procollagen chains. Proc Natl Acad Sci U S A. 1985 Jun;82(11):3649–3653. doi: 10.1073/pnas.82.11.3649. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Butkowski R. J., Wieslander J., Wisdom B. J., Barr J. F., Noelken M. E., Hudson B. G. Properties of the globular domain of type IV collagen and its relationship to the Goodpasture antigen. J Biol Chem. 1985 Mar 25;260(6):3739–3747. [PubMed] [Google Scholar]
  5. Cannizzaro L. A., Emanuel B. S. An improved method for G-banding chromosomes after in situ hybridization. Cytogenet Cell Genet. 1984;38(4):308–309. doi: 10.1159/000132079. [DOI] [PubMed] [Google Scholar]
  6. Cavenee W. K., Dryja T. P., Phillips R. A., Benedict W. F., Godbout R., Gallie B. L., Murphree A. L., Strong L. C., White R. L. Expression of recessive alleles by chromosomal mechanisms in retinoblastoma. 1983 Oct 27-Nov 2Nature. 305(5937):779–784. doi: 10.1038/305779a0. [DOI] [PubMed] [Google Scholar]
  7. Cavenee W., Leach R., Mohandas T., Pearson P., White R. Isolation and regional localization of DNA segments revealing polymorphic loci from human chromosome 13. Am J Hum Genet. 1984 Jan;36(1):10–24. [PMC free article] [PubMed] [Google Scholar]
  8. Cheah K. S. Collagen genes and inherited connective tissue disease. Biochem J. 1985 Jul 15;229(2):287–303. doi: 10.1042/bj2290287. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Crouch E., Sage H., Bornstein P. Structural basis for apparent heterogeneity of collagens in human basement membranes: type IV procollagen contains two distinct chains. Proc Natl Acad Sci U S A. 1980 Feb;77(2):745–749. doi: 10.1073/pnas.77.2.745. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Deisseroth A., Nienhuis A., Lawrence J., Giles R., Turner P., Ruddle F. H. Chromosomal localization of human beta globin gene on human chromosome 11 in somatic cell hybrids. Proc Natl Acad Sci U S A. 1978 Mar;75(3):1456–1460. doi: 10.1073/pnas.75.3.1456. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Deisseroth A., Nienhuis A., Turner P., Velez R., Anderson W. F., Ruddle F., Lawrence J., Creagan R., Kucherlapati R. Localization of the human alpha-globin structural gene to chromosome 16 in somatic cell hybrids by molecular hybridization assay. Cell. 1977 Sep;12(1):205–218. doi: 10.1016/0092-8674(77)90198-2. [DOI] [PubMed] [Google Scholar]
  12. Dion A. S., Myers J. C. COOH-terminal propeptides of the major human procollagens. Structural, functional and genetic comparisons. J Mol Biol. 1987 Jan 5;193(1):127–143. doi: 10.1016/0022-2836(87)90632-2. [DOI] [PubMed] [Google Scholar]
  13. Dixit S. N. Type-IV collagens. Isolation and characterization of two structurally distinct collagen chains from bovine kidney cortices. Eur J Biochem. 1980 May;106(2):563–570. doi: 10.1111/j.1432-1033.1980.tb04604.x. [DOI] [PubMed] [Google Scholar]
  14. Elliott R. W., Barlow D., Hogan B. L. Linkage of genes for laminin B1 and B2 subunits on chromosome 1 in mouse. In Vitro Cell Dev Biol. 1985 Aug;21(8):477–484. doi: 10.1007/BF02620837. [DOI] [PubMed] [Google Scholar]
  15. Emanuel B. S., Cannizzaro L. A., Seyer J. M., Myers J. C. Human alpha 1(III) and alpha 2(V) procollagen genes are located on the long arm of chromosome 2. Proc Natl Acad Sci U S A. 1985 May;82(10):3385–3389. doi: 10.1073/pnas.82.10.3385. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Emanuel B. S., Sellinger B. T., Gudas L. J., Myers J. C. Localization of the human procollagen alpha 1(IV) gene to chromosome 13q34 by in situ hybridization. Am J Hum Genet. 1986 Jan;38(1):38–44. [PMC free article] [PubMed] [Google Scholar]
  17. Glanville R. W., Qian R. Q., Siebold B., Risteli J., Kühn K. Amino acid sequence of the N-terminal aggregation and cross-linking region (7S domain) of the alpha 1 (IV) chain of human basement membrane collagen. Eur J Biochem. 1985 Oct 1;152(1):213–219. doi: 10.1111/j.1432-1033.1985.tb09186.x. [DOI] [PubMed] [Google Scholar]
  18. Hansen M. F., Koufos A., Gallie B. L., Phillips R. A., Fodstad O., Brøgger A., Gedde-Dahl T., Cavenee W. K. Osteosarcoma and retinoblastoma: a shared chromosomal mechanism revealing recessive predisposition. Proc Natl Acad Sci U S A. 1985 Sep;82(18):6216–6220. doi: 10.1073/pnas.82.18.6216. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Haralson M. A., Federspiel S. J., Martinez-Hernandez A., Rhodes R. K., Miller E. J. Synthesis of [pro alpha 1(IV)]3 collagen molecules by cultured embryo-derived parietal yolk sac cells. Biochemistry. 1985 Oct 8;24(21):5792–5797. doi: 10.1021/bi00342a016. [DOI] [PubMed] [Google Scholar]
  20. 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]
  21. Jeffreys A. J., Craig I. W., Francke U. Localisation of the G gamma-, A gamma-, delta- and beta-globin genes on the short arm of human chromosome 11. Nature. 1979 Oct 18;281(5732):606–608. doi: 10.1038/281606a0. [DOI] [PubMed] [Google Scholar]
  22. Junien C., Weil D., Myers J. C., Van Cong N., Chu M. L., Foubert C., Gross M. S., Prockop D. J., Kaplan J. C., Ramirez F. Assignment of the human pro alpha 2(I) collagen structural gene (COLIA2) to chromosome 7 by molecular hybridization. Am J Hum Genet. 1982 May;34(3):381–387. [PMC free article] [PubMed] [Google Scholar]
  23. Kefalides N. A., Alper R., Clark C. C. Biochemistry and metabolism of basement membranes. Int Rev Cytol. 1979;61:167–228. doi: 10.1016/s0074-7696(08)61998-1. [DOI] [PubMed] [Google Scholar]
  24. Kresina T. F., Miller E. J. Isolation and characterization of basement membrane collagen from human placental tissue. Evidence for the presence of two genetically distinct collagen chains. Biochemistry. 1979 Jul 10;18(14):3089–3097. doi: 10.1021/bi00581a028. [DOI] [PubMed] [Google Scholar]
  25. Kurkinen M., Bernard M. P., Barlow D. P., Chow L. T. Characterization of 64-, 123- and 182-base-pair exons in the mouse alpha 2(IV) collagen gene. Nature. 1985 Sep 12;317(6033):177–179. doi: 10.1038/317177a0. [DOI] [PubMed] [Google Scholar]
  26. Kühn K., Glanville R. W., Babel W., Qian R. Q., Dieringer H., Voss T., Siebold B., Oberbäumer I., Schwarz U., Yamada Y. The structure of type IV collagen. Ann N Y Acad Sci. 1985;460:14–24. doi: 10.1111/j.1749-6632.1985.tb51153.x. [DOI] [PubMed] [Google Scholar]
  27. Laurie G. W., Bing J. T., Kleinman H. K., Hassell J. R., Aumailley M., Martin G. R., Feldmann R. J. Localization of binding sites for laminin, heparan sulfate proteoglycan and fibronectin on basement membrane (type IV) collagen. J Mol Biol. 1986 May 5;189(1):205–216. doi: 10.1016/0022-2836(86)90391-8. [DOI] [PubMed] [Google Scholar]
  28. Loidl H. R., Brinker J. M., May M., Pihlajaniemi T., Morrow S., Rosenbloom J., Myers J. C. Molecular cloning and carboxyl-propeptide analysis of human type III procollagen. Nucleic Acids Res. 1984 Dec 21;12(24):9383–9394. doi: 10.1093/nar/12.24.9383. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Mayne R., Wiedemann H., Dessau W., Von der Mark K., Bruckner P. Structural and immunological characterization of type IV collagen isolated from chicken tissues. Eur J Biochem. 1982 Aug;126(2):417–423. doi: 10.1111/j.1432-1033.1982.tb06796.x. [DOI] [PubMed] [Google Scholar]
  30. Mayne R., Zettergren J. G. Type IV collagen from chicken muscular tissues. Isolation and characterization of the pepsin-resistant fragments. Biochemistry. 1980 Aug 19;19(17):4065–4072. doi: 10.1021/bi00558a025. [DOI] [PubMed] [Google Scholar]
  31. Oberbäumer I., Laurent M., Schwarz U., Sakurai Y., Yamada Y., Vogeli G., Voss T., Siebold B., Glanville R. W., Kühn K. Amino acid sequence of the non-collagenous globular domain (NC1) of the alpha 1(IV) chain of basement membrane collagen as derived from complementary DNA. Eur J Biochem. 1985 Mar 1;147(2):217–224. doi: 10.1111/j.1432-1033.1985.tb08739.x. [DOI] [PubMed] [Google Scholar]
  32. Pihlajaniemi T., Tryggvason K., Myers J. C., Kurkinen M., Lebo R., Cheung M. C., Prockop D. J., Boyd C. D. cDNA clones coding for the pro-alpha1(IV) chain of human type IV procollagen reveal an unusual homology of amino acid sequences in two halves of the carboxyl-terminal domain. J Biol Chem. 1985 Jun 25;260(12):7681–7687. [PubMed] [Google Scholar]
  33. Qian R. G., Glanville R. W. Separation and characterization of two polypeptide chains from the 7S cross-linking domain of basement-membrane (type IV) collagen. Biochem J. 1984 Sep 1;222(2):447–452. doi: 10.1042/bj2220447. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Ramirez F., Bernard M., Chu M. L., Dickson L., Sangiorgi F., Weil D., De Wet W., Junien C., Sobel M. Isolation and characterization of the human fibrillar collagen genes. Ann N Y Acad Sci. 1985;460:117–129. doi: 10.1111/j.1749-6632.1985.tb51160.x. [DOI] [PubMed] [Google Scholar]
  35. Sakurai Y., Sullivan M., Yamada Y. Alpha 1 type IV collagen gene evolved differently from fibrillar collagen genes. J Biol Chem. 1986 May 25;261(15):6654–6657. [PubMed] [Google Scholar]
  36. Schuppan D., Glanville R. W., Timpl R., Dixit S. N., Kang A. H. Sequence comparison of pepsin-resistant segments of basement-membrane collagen alpha 1(IV) chains from bovine lens capsule and mouse tumour. Biochem J. 1984 May 15;220(1):227–233. doi: 10.1042/bj2200227. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Soininen R., Tikka L., Chow L., Pihlajaniemi T., Kurkinen M., Prockop D. J., Boyd C. D., Tryggvason K. Large introns in the 3' end of the gene for the pro alpha 1 (IV) chain of human basement membrane collagen. Proc Natl Acad Sci U S A. 1986 Mar;83(6):1568–1572. doi: 10.1073/pnas.83.6.1568. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Solomon E., Hiorns L. R., Spurr N., Kurkinen M., Barlow D., Hogan B. L., Dalgleish R. Chromosomal assignments of the genes coding for human types II, III, and IV collagen: a dispersed gene family. Proc Natl Acad Sci U S A. 1985 May;82(10):3330–3334. doi: 10.1073/pnas.82.10.3330. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Solomon E., Hiorns L., Dalgleish R., Tolstoshev P., Crystal R., Sykes B. Regional localization of the human alpha 2(I) collagen gene on chromosome 7 by molecular hybridization. Cytogenet Cell Genet. 1983;35(1):64–66. doi: 10.1159/000131838. [DOI] [PubMed] [Google Scholar]
  40. Solomon E., Hiorns L., Sheer D., Rowe D. Confirmation that the type I collagen gene on chromosome 17 is COL1A1 (alpha 1(I), using a human genomic probe. Ann Hum Genet. 1984 Jan;48(Pt 1):39–42. doi: 10.1111/j.1469-1809.1984.tb00831.x. [DOI] [PubMed] [Google Scholar]
  41. Strom C. M., Eddy R. L., Shows T. B. Localization of human type II procollagen gene (COL2A1) to chromosome 12. Somat Cell Mol Genet. 1984 Nov;10(6):651–655. doi: 10.1007/BF01535232. [DOI] [PubMed] [Google Scholar]
  42. Timpl R., Bruckner P., Fietzek P. Characterization of pepsin fragments of basement membrane collagen obtained from a mouse tumor. Eur J Biochem. 1979 Apr 2;95(2):255–263. doi: 10.1111/j.1432-1033.1979.tb12961.x. [DOI] [PubMed] [Google Scholar]
  43. Timpl R., Wiedemann H., van Delden V., Furthmayr H., Kühn K. A network model for the organization of type IV collagen molecules in basement membranes. Eur J Biochem. 1981 Nov;120(2):203–211. doi: 10.1111/j.1432-1033.1981.tb05690.x. [DOI] [PubMed] [Google Scholar]
  44. Tripputi P., Emanuel B. S., Croce C. M., Green L. G., Stein G. S., Stein J. L. Human histone genes map to multiple chromosomes. Proc Natl Acad Sci U S A. 1986 May;83(10):3185–3188. doi: 10.1073/pnas.83.10.3185. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Tryggvason K., Robey P. G., Martin G. R. Biosynthesis of type IV procollagens. Biochemistry. 1980 Apr 1;19(7):1284–1289. doi: 10.1021/bi00548a003. [DOI] [PubMed] [Google Scholar]
  46. Trüeb B., Gröbli B., Spiess M., Odermatt B. F., Winterhalter K. H. Basement membrane (type IV) collagen is a heteropolymer. J Biol Chem. 1982 May 10;257(9):5239–5245. [PubMed] [Google Scholar]
  47. Weber S., Engel J., Wiedemann H., Glanville R. W., Timpl R. Subunit structure and assembly of the globular domain of basement-membrane collagen type IV. Eur J Biochem. 1984 Mar 1;139(2):401–410. doi: 10.1111/j.1432-1033.1984.tb08019.x. [DOI] [PubMed] [Google Scholar]
  48. Yurchenco P. D., Furthmayr H. Self-assembly of basement membrane collagen. Biochemistry. 1984 Apr 10;23(8):1839–1850. doi: 10.1021/bi00303a040. [DOI] [PubMed] [Google Scholar]

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