Advertisement

Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

The α2(XI) collagen gene lies within 8 kb of Pb in the proximal portion of the murine major histocompatibility complex

Abstract

A number of serious hereditary disorders are now known to be associated with defective expression of collagen genes, and these findings have underscored the important and varied roles that the collagen family of genes must play during normal mammalian development. Although the activities of genes encoding the quantitatively major types of collagen are fairly well characterized, functions of the many minor types of collagen remain a matter of speculation. As a first step toward a functional analysis of type XI collagen, a member of this class of poorly understand “minor” collagen proteins which is expressed primarily in hyaline cartilage, we have used human probes for the gene encoding the protein's α2-subunit (COL11A2) to isolate and map homologous murine DNA sequences. Our results demonstrate that Col11a-2 is embedded within the major histocompatibility complex (MHC), within 8.4 kb of the class II pseudogene locus, Pb, and confirm that human and murine α2(XI) collagen genes are located in very similar genomic environments. The conserved location of these genes raises the possibility that type XI collagen genes may contribute to one or more of the diverse hereditary disorders known to be linked to the MHC in mouse and human.

This is a preview of subscription content, log in to check access.

References

  1. Abe, K., Wei, J.-F., Wei, F.-S., Uehara, H., Artzt, K. and Bennett, D.: Searching for coding sequences in the mammalian genome: the H-2K region of the mouse MHC is replete with genes expressed in embryos. EMBO J 7: 3441–3449, 1988.

  2. Adamson, E.: The effect of collagen on cell division, cellular differentiation and embryonic development. In J.B. Weiss and M.W. Jayson (eds.); Collagen in Health & Disease, pp. 218–243, Churchill Livingstone, Edinburgh, 1982.

  3. Bernard, M., Yoshioka, H., Rodriquez, E., Van der Rest, M., Kimura, T., Ninomiya, Y., Olsen, B.R., and Ramirez, F.: Cloning and sequencing of pro-al(XI) collagen cDNA demonstrates the Type XI belongs to the fibrillar class of collagens and reveals that the expression of the gene is not restricted to cartilagenous tissue. J Biol Chem 263: 17159–17166, 1988.

  4. Birnboim, H.C. and Doly, J.: A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucleic Acids Res 7: 1513–1519, 1979.

  5. Bonadio, J., Saunders, T.L., Tsai, E., Goldstein, S.A., Morris-Wiman, J., Brinkley, L., Dolan, D.F., Altschuler, R.A., Hawkins, J.E. Jr., Bateman, J.F., Mascara, T., and Jaenisch, R.: Transgenic mouse model of the mild dominant form of osteogenesis imperfecta. Proc Natl Acad Sci USA 87: 7145–7149, 1990.

  6. Byers, P.H.: Inherited disorders of collagen gene structure and expression. Am J Med Genet 34: 72–80, 1989.

  7. Cheah, K.S.E., Stoker, N.G., Griffin, J.R., Grosveld, F.G., and Solomon, E.: Identification and characterization of the human type II collagen gene (COL2A1). Proc Natl Acad Sci USA 82: 2555–2559, 1985.

  8. Cheah, K.S.E., Lui, V.C.H., Yu, E.C.L., and Hsu, L.C.S.: A Stul RFLP in the human a2(XI) (COL11A2) gene. Nucleic Acids Res 18: 4964, 1990.

  9. Devereux, J., Haeberli, P., and Smithies, O.: A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res 12: 387–395, 1984.

  10. Dion, A.S. and Myers, J.C.: COOH-terminal propeptides of the major human procollagens. Structural functional and genetic comparisons. J Mol Biol 193: 127–143, 1987.

  11. Dublet, B. and van der Rest, M.: Type XIV collagen, a new homotrimeric molecule extracted from fetal bovine skin and tendon, with a triple helical disulphide-bonded domain homologous to type IX and Type XII collagens. J Biol Chem 266: 6853–6858, 1991.

  12. Feinberg, A.P. and Vogelstein, B.: A technique for radiolabelling DNA restriction endonuclease fragments to high specific activity. Anal Biochem 132: 6–13, 1983.

  13. Garofalo, S., Vuorio, E., Metsaranta, M., Rosati, R., Toman, D., Vaughan, J., Lozano, G., Mayne, R., Ellard, J., Horton, W., and de Crombrugghe, B.: Reduced amounts of cartilage collagen fibrils and growth plate anomalies in transgenic mice harboring a glycine-to-cysteine mutation in the mouse type II procollagen a1-chain gene. Proc Natl Acad Sci USA 88: 9648–9652, 1991.

  14. Hanson, I.M. and Trowsdale, J.: Colinearity of novel genes in the class II regions of the MHC in mouse and human. Immunogenetics 34: 5–11, 1991.

  15. Hanson, I.M., Gorman, P., Lui, V.C.H., Cheah, K.S.E., Solomon, E., and Trowsdale, J.: The human a2(XI) collagen gene (COL11A2) maps to the centromeric border of the major histocompatibility complex on chromosome 6. Genomics 5: 925–931, 1989.

  16. Herrmann, B.G. and Frischauf, A.-M.: Isolation of genomic DNA. Methods Enzymol 152: 180–183, 1987.

  17. Kimura, T., Cheah, K.S.E., Chan, S.D., Lui, V.C.H., Mattei, M.-G., Van der Rest, M., Ono, K., Solomon, E., Ninomiya, Y., and Olson, B.R.: The human a2(XI) collagen (COL11A2) chain: Molecular cloning of cDNA and genomic DNA reveal characteristics of a fibrillar collagen with differences in genomic organization. J Biol Chem 264: 13910–13916, 1989.

  18. Klein, J., Figueroa, F., and Klein, D.: H-2 haplotypes, genes and antigens: second listing, I. Non-H-2 loci on chromosome 17. Immunogenetics 16: 285–317, 1982.

  19. Kuivaniemi, H., Tromp, G., and Prockop, D.J.: Mutations in collagen genes: causes of rare and some common diseases in humans. FASEB J 5: 2052–2060, 1991.

  20. Law, M.L., Tung, L., Morse, H.G., Beger, R., Jones, C., Cheah, K.S.E., and Solomon, E.: The human type II collagen gene (COL2A1) assigned to 12q14.3. Ann Hum Genet 50: 131–137, 1986.

  21. Niyibizi, C. and Eyre, D.R.: Identification of the cartilage a1(XI) chain in type V collagen from bovine bone. FEBS Lett 242: 314–318, 1989.

  22. Ramirez, F., Bernard, M., Chu, M.-L., Dickson, L., Sangiorgi, F., Weil, D., de Wet, W., Junien, C., and Sobel, M.: Isolation and characterisation of the human fibrillar collagen genes. NY Acad Sci 460: 117–129, 1985.

  23. Rynnanen, M., Knowlton, R.G., Parente, M.G., Chung, L.C., Chu, M.-L., and Uitto, J.: Human type VII collagen: genetic linkage of the gene (COL7A1) on chromosome 3 to dominant dystrophic Epidermolysis bullosa. Am J Hum Genet 49: 797–803, 1991.

  24. Sanger, F., Nicklen, S., and Coulson, A.R.: DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74: 5463–5467, 1977.

  25. Skow, L.C. and Donner, M.A.: The lofuc encoding aA-crystallin is closely linked to H-2K on mouse chromosome 17. Genetics 110: 723–732, 1985.

  26. Stacey, A., Bateman, J., Choi, T., Mascara, T., Cole, W., and Jaenisch, R.: Perinatal lethal osteogenesis imperfecta in transgenic mice bearing an engineered mutant pro-a1(I) collagen gene. Nature 332: 131–136, 1988.

  27. Steinmetz, M., Stephan, D., and Fischer-Lindahl, K.: Gene organization and recombinational hotspots in the murine major histocompatibility complex. Cell 44: 895–904, 1986.

  28. Stubbs, L., Huxley, C., Hogan, B.L.M., Evans, T., Fried, M., Duboule, D., and Lehrach, H.: The HOX-5 and Surfeit gene clusters are linked in the proximal portion of mouse chromosome 2. Genomics 6: 645–650, 1990.

  29. Taylor, B.A.: Recombinant inbred strains. In M.F. Lyon and A.G. Searle (eds.); Genetic Variants and Strains of the Laboratory Mouse, pp. 773–796, Oxford University Press, Oxford, UK, 1989.

  30. Tiller, G.E., Rimoin, D.L., Murray, L.W., and Cohn, D.H.: Tandem duplication within a type II collagen gene (COL2A1) exon in an individual with spondyloepiphyseal dysplasia. Proc Natl Acad Sci USA 87: 3889–3893, 1990.

  31. Tiwari, J.L., and Terasaki, P.: HLA and Disease Associations, Springer-Verlag, New York, 1985.

  32. Vandenberg, P., Khillan, J.S., Prockop, D.J., Helminen, H., Kontusaari, S., and Ala-Kokko, L.: Expression of a partially deleted gene of human type II procollagen (COL2A1) in transgenic mice produces a chondrodysplasia. Proc Natl Acad Sci USA 88: 7640–7644, 1991.

  33. Vuorio, E. and deCrombrugghe, B.: The family of collagen genes. Annu Rev Biochem 59: 837–872, 1990.

  34. Widera, G. and Flavell, R.A.: The I region of the C57BL/10 mouse: characterization and physical linkage to H2-K of an SBb-like class II pseudogene. Proc Natl Acad Sci USA 82: 55000–5504, 1985.

  35. Yoshioka, H. and Ramirez, F.: Pro-α1(XI) collagen, structure of the amino-terminal propeptide and expression of the gene in tumor cell lines. J Biol Chem 265: 6423–6426, 1990.

Download references

Author information

Correspondence to Lisa Stubbs.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Stubbs, L., Lui, V.C.H., Jim Ng, L. et al. The α2(XI) collagen gene lies within 8 kb of Pb in the proximal portion of the murine major histocompatibility complex. Mammalian Genome 4, 95–103 (1993). https://doi.org/10.1007/BF00290433

Download citation

Keywords

  • Major Histocompatibility Complex
  • Major Type
  • Collagen Gene
  • Proximal Portion
  • Hyaline Cartilage