Human Genetics

, Volume 77, Issue 4, pp 318–324 | Cite as

Partial structure of the human α2(IV) collagen chain and chromosomal localization of the gene (COL4A2)

  • Paul D. Killen
  • Clair A. Francomano
  • Yoshihiko Yamada
  • William S. Modi
  • Stephen J. O'Brien
Original Investigations

Summary

We have isolated a 2.1-kb cDNA clone from a human placental library encoding part of the α2 chain of collagen IV, a major structural protein of basement membranes. The DNA sequence encodes 446 amino acids in the triplehelical domain plus the 227 amino acids of the carboxy-terminal globular domain. The latter structure is composed of two homologous subdomains and is highly conserved between the α1 and α2 chains. The triple-helical domain contained seven interruptions of the Gly-X-Y repeat and these interruptions were in general larger than their counterparts in the α1 chain. DNA from human rodent hybrid cell lines was analyzed under conditions in which there was no cross-hybridization of the α2(IV) cDNA probe with the gene for the α1(IV) collagen chain. An Eco RI fragment characteristic of the α2 chain had a concordance of 0.97 with chromosome 13. This result was confirmed and extended with in situ localization of the gene at 13q34. Since the α1(IV) gene has previously been localized to 13q34, the two type IV collagen genes reside in the same chromosome region (13q34), possibly in a gene cluster. The presence of the genes for type IV collagen chains on chromosome 13 excludes a primary role for these genes in adult polycystic kidney disease and X-linked forms of hereditary nephritis.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Adams SL, Sobel ME, Howard BH, Olden K, Yamada KM, de Crombrugghe B, Pastan I (1977) Levels of translatable mRNAs for cell surface protein, collagen precursors, and two membrane proteins are altered in Rous sarcoma virus-transformed chick embryo fibroblasts. Proc Natl Acad Sci USA 74:3399–3403Google Scholar
  2. Aumailley M, Timpl R (1976) Attachment of cells to basement membrane collagen type IV. J Cell Biol 103:1569–1575Google Scholar
  3. Babel W, Glanville RW (1984) Structure of human-basement membrane (type IV) collagen. Complete amino-acid sequence of a 914-residue-long pepsin fragment from the α1(IV) chain. Eur J Biochem 143:545–556Google Scholar
  4. Boedtker H, Fuller F, Tate V (1983) The structure of collagen genes. Int Rev Connect Tissue Res 10:1–63Google Scholar
  5. Boyd CD, Weliky K, Deak SB, Christiano AM, Mackenzie JW, Sandell LJ, Tryggvason K, Magenis E (1986) The single copy gene coding for human α1(IV) procollagen is located at the terminal end of the long arm of chromosome 13. Hum Genet 74:121–125Google Scholar
  6. Brinker JM, Gudas LJ, Loidl HR, Wang S, Rosenbloom J, Kefalides NA, Myers JC (1985) Restricted homology between human α1(IV) and other procollagen chains. Proc Natl Acad Sci USA 82:3649–3653Google Scholar
  7. Carone FA, Rowland RG, Perlman SG, Ganote CE (1974) The pathogenesis of drug-induced renal cystic disease. Kidney Int 5: 411–421Google Scholar
  8. Charonis AS, Tsilibary EC, Yurchenco PD, Furthmayr H (1985) Binding of laminin to type IV collagen: a morphological study. J Cell Biol 6:1848–1853Google Scholar
  9. Church GM, Gilbert W (1984) Genomic sequencing. Proc Natl Acad Sci USA 81:1991–1995Google Scholar
  10. Cohn DH, Byers PH, Steinmann B, Gelinas RE (1986) Lethal osteogenesis imperfecta resulting from a single nucleotide change in one human pro-alpha 1(I) collagen allele. Proc Natl Acad Sci USA 83:6045–6047Google Scholar
  11. Dale RMK, McClure BA, Houchins JP (1985) A rapid singlestranded cloning strategy for producing a sequential series of overlapping clones for use in DNA sequencing: application to sequencing the corn mitochondrial 18S rDNA. Plasmid 13:31–40Google Scholar
  12. Duncan KG, Fessler LI, Bächinger HP, Fessler JH (1983) Procollagen IV. Association to tetramers. J Biol Chem 258:5869–5877Google Scholar
  13. Dutrillaux B, Viegas-Péquignot E (1981) High resolution R- and G-banding on the same preparation. Hum Genet 57:93–95Google Scholar
  14. Emanuel BS, Cannizzaro LA, Seyer JM, Myers JC (1985) Human α1(III) and α2(V) procollagen genes are located on the long arm of chromosome 5. Proc Natl Acad Sci USA 82:3385–3389Google Scholar
  15. Emanuel BS, Sellinger BT, Gudas LJ, Myers JC (1986) Localization of the human procollagen α1(IV) gene to chromosome 13q34 by in situ hybridization. Am J Hum Genet 38:38–44Google Scholar
  16. Gabow PA, Ikle DW, Holmes JH (1984) Polycystic kidney disease: prospective analysis of nonazotemic patients and family members. Ann Intern Med 101:238–247Google Scholar
  17. Glanville RW, Qian RQ, Siebold B, Risteli J, Kühn K (1985) 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 152:213–219Google Scholar
  18. Griffin CA, Emanuel BS, Hansen JR, Cavenee WK, Myers JC (1987) Human collagen genes encoding basement membrane α1(IV) and α2(IV) chains map to the distal long arm of chromosome 13. Proc Natl Acad Sci USA 84:512–516Google Scholar
  19. Harper ME, Saunders GF (1981) Localization of single copy DNA sequences on G-banded human chromosomes by in situ hybridization. Chromosoma 83:431–439Google Scholar
  20. Hay ED (1984) Cell-matrix interaction in the embryo: cell shape, cell surface, cell skeletons and their role in differentiation. In: Trelstad RL (ed) The role of extracellular matrix in development. Liss, New York, pp 1–31Google Scholar
  21. Hofmann H, Fietzek PP, Kühn K (1980) Comparative analysis of sequences of the three collagen chains α1(I), α2(I) and α1(III). Functional and genetic aspects. J Mol Biol 141:293–314Google Scholar
  22. Hofmann H, Voss T, Kühn K, Engel J (1984) Localization of flexible sites in thread-like molecules from electron micrographs. Comparisom of interstitial, basement membrane and intima collagens. J Mol Biol 172:325–343Google Scholar
  23. Huerre C, Junien C, Weil D, Chu M, Morabito M, Van Cong N, Myers JC, Foubert C, Gross MS, Prockop DJ, Boué A, Kaplan JC, de la Chanelle A, Ramirez F (1982) Human type I procollagen genes are located on different chromosomes. Proc Natl Acad Sci USA 79:6627–6630Google Scholar
  24. Jeraj K, Kim Y, Vernier RL, Fish AJ, Michael AF (1983) Absence of Goodpasture's antigen in male patients with familial nephritis. Am J Kidney Dis 11:626–629Google Scholar
  25. Junien C, Weil D, Myers JC, Van Cong N, Chu M, Foubert C, Gross MS, Prockop DJ, Kaplan JC, Ramirez F (1982) Assignment of the human proα2(I) collagen structural gene (COL1A2) to chromosome 7 by molecular hybridization. Am J Hum Genet 34:381–387Google Scholar
  26. Kashtan C, Fish AJ, Kleppel M, Yoshioka K, Michael AF (1986) Nephritogenic antigen determinants in epidermal and renal basement membranes of kindreds with Alport-type familial nephritis. J Clin Invest 78:1035–1044Google Scholar
  27. Kleinman HK, Graf J, Iwamoto Y, Kitten GT, Ogle RC, Sasaki M, Yamada Y, Martin GR, Luckenbill-Edds L (1987) Role of basement membranes in cell differentiation. Ann NY Acad Sci (in press)Google Scholar
  28. Kühn K, Glanville RW, Babel W, Qian RQ, Dieringer H, Voss T (1985) The structure of type IV collagen. Ann NY Acad Sci 460:14–24Google Scholar
  29. Laurie GW, Bing JT, Kleinman HK, Hassell JR, Aumailley M, Martin GR, Feldmann RJ (1986) Localization of binding sites for laminin, heparan sulfate proteoglycan and fibronectin on basement membrane (type IV) collagen. J Mol Biol 189:205–216Google Scholar
  30. Maniatis T, Fritsch EF, Sambrook J (1982a) Nick translation of DNA. In: Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY, pp 109–112Google Scholar
  31. Maniatis T, Fritsch EF, Sambrook J (1982b) Large-scale preparation of bacteriophage λ. In: Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY, pp 76–85Google Scholar
  32. Martin GR, Timpl R, Müller PK, Kühn K (1985) The genetically distinct collagens. TIBS 10:285–287Google Scholar
  33. Oberbäumer I, Laurent M, Schwarz U, Sakurai Y, Yamada Y, Vogeli G, Voss T, Siebold B, Glanville R, Kühn K (1985) Amino acid sequence of the non-collagenous globular domain (NC1) of the α1(IV) chain of basement membrane collagen as derived from complementary DNA. Eur J Biochem 147:217–224Google Scholar
  34. O'Brien SJ, Simonson JM, Eichelberger M (1982) Genetic analysis of hybrid cells using isozyme markers as monitors of chromosome segregation. In: Shay JW (ed) Techniques in somatic cell genetics. Plenum Press, New York, pp 513–524Google Scholar
  35. O'Brien SJ, Nash WG, Goodwin JL, Lowy DR, Chang EH (1983a) Dispersion of the ras family of transforming genes to four different chromosomes in man. Nature 302:839–842Google Scholar
  36. O'Brien SJ, Bonner TI, Cohen M, O'Connell C, Nash WG (1983b) Mapping of an endogenous retroviral sequence to human chromosome 18. Nature 303:74–77Google Scholar
  37. Perry R, Wolff S (1974) New Giemsa method for the differential staining of sister chromatids. Nature 251:156–158Google Scholar
  38. Pierschbacher MD, Rouslathti E (1984) Cell attachment activity of fibronectin can be duplicated by small synthetic fragments of the molecule. Nature 309:30–33Google Scholar
  39. Pihlajaniemi T, Tryggvason K, Myers JC, Kurkinen M, Lebo R, Cheung M, Prockop DJ, Boyd CD (1985) cDNA clones coding for the pro-α1(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 260:7681–7687Google Scholar
  40. Pytella R, Pierschbacher MD, Ginsberg MH, Plow EF, Rouslahti E (1986) Platelet membrane glycoprotein IIb/IIIa: member of a family of Arg-Gly-Asp-specific adhesion receptors. Science 231:1559–1562Google Scholar
  41. Reed KC, Mann DA (1985) Rapid transfer of DNA from agarose gels to nylon membranes. Nucleic Acids Res 13:7207–7220Google Scholar
  42. Reeders ST, Breuning MH, Davies KE, Nicholls RD, Jarman AP, Higgs DR, Pearson PL, Weatherall DJ (1985) A highly polymorphic DNA marker linked to adult polycystic kidney disease on chromosome 16. Nature 317:542–544Google Scholar
  43. Sanger F, Coulson AR, Barrell BG, Smith AJ, Roe BA (1980) Cloning in single-stranded bacteriophage as an aid to rapid DNA sequencing. J Mol Biol 143:161–178Google Scholar
  44. Schwarz U, Schuppan D, Oberbäumer I, Glanville RW, Deutzmann R, Timpl R, Kühn K (1986) Structure of mouse type IV collagen. Amino-acid sequence of the C-terminal 511-residue-long triplehelical segment of the α2(IV) chain and its comparison with the α1(IV) chain. Eur J Biochem 157:49–56Google Scholar
  45. Soininen R, Chow L, Kurkinen M, Tryggvason K, Prockop DJ (1986) The gene for the α1(IV) chain of human type IV procollagen: the exon structures do not coincide with the two structural subdomains in the globular carboxy-terminus of the protein. EMBO J 5:2821–2823Google Scholar
  46. Solomon E, Hiorns LR, Spurr N, Kurkinen M, Barlow D, Hogan BLM, Dalgleish R (1985) Chromosomal assignments of the genes coding for human types II, III, and IV collagen: a dispersed gene family. Proc Natl Acad Sci USA 82:3330–3334Google Scholar
  47. Spear GS (1973) Alport's syndrome: consideration of pathogenesis. Clin Nephrol 1:336–337Google Scholar
  48. Steinmann B, Rao VH, Vogel A, Bruckner P, Gitzelmann R, Byers PH (1984) Cysteine in the triple-helical domain of one allelic product of the alpha 1(I) gene of type I collagen produces a lethal form of osteogenesis imperfecta. J Biol Chem 259:11129–11138Google Scholar
  49. Timpl R, Martin GR (1982) Components of basement membranes. In: Furthmayr H (ed) Immunochemistry of the extracellular matrix. CRC Press, Boca Raton, Fla, pp 119–150Google Scholar
  50. Timpl R, Wiedemann H, Van Delden V, Furthmayr H, Kühn K (1981) A network model for the organization of type IV collagen molecules in basement membranes. Eur J Biochem 120:203–211Google Scholar
  51. Vracko R (1974) Basal lamina scaffold: anatomy and significance for maintenance of orderly tissue structure. Am J Pathol 77:313–346Google Scholar
  52. Weber S, Engel J, Wiedemann H, Glanville RW, Timpl R (1984) Subunit structure and assembly of the globular domain of basement-membrane collagen type IV. Eur J Biochem 139:401–410Google Scholar
  53. Wieslander J, Barr JF, Butkowski RJ, Edwards SJ, Bygren P, Heinegård D, Hudson BG (1984) Goodpasture antigen of the glomerular basement membrane: localization to noncollagenous regions of type IV collagen. Proc Natl Acad Sci USA 81:3838–3842Google Scholar
  54. Wieslander J, Langevels J, Butkowski R, Jodlowski M, Noelken M, Hudson BG (1985) Physical and immunochemical studies of the globular domain of type IV collagen. Cryptic properties of the Goodpasture antigen. J Biol Chem 260:8564–8570Google Scholar
  55. Yamada Y, Kühn K, de Crombrugghe B (1983) A conserved nucleotide sequence, coding for a segment of the C-propeptide, is found at the same location in different genes. Nucleic Acids Res 11:2733–2744Google Scholar
  56. Yurchenco PD, Tsilibary EC, Charonis AS, Furthmayr H (1986) Models for the self-assembly of basement membrane. J Histochem Cytochem 34:93–102Google Scholar

Copyright information

© Springer-Verlag 1987

Authors and Affiliations

  • Paul D. Killen
    • 1
  • Clair A. Francomano
    • 2
  • Yoshihiko Yamada
    • 1
  • William S. Modi
    • 3
  • Stephen J. O'Brien
    • 3
  1. 1.Laboratory of Developmental Biology and Anomalies, National Institute of Dental ResearchNational Institutes of HealthBethesdaUSA
  2. 2.Department of Medicine and Department of PediatricsJohns Hopkins University School of MedicineBaltimoreUSA
  3. 3.Laboratory of Viral Carcinogenesis, National Cancer InstituteNational Institute of HealthFrederickUSA

Personalised recommendations