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

Genetic and tissue-specific variation in the expression of a closely linked murine multigene family on chromosome 15 that encodes salivary and lacrimal proteins

  • 20 Accesses

  • 11 Citations

Abstract

The murine submandibular gland (SMG) produces a novel class of highly acidic salivary proteins encoded by one or more highly abundant mRNA transcripts. In inbred mice, these transcripts are encoded by members of a multigene family comprising approximately 8–12 homologues. Most, and probably all, of these homologues are clustered at a new locus near belted (bt) on chromosome 15, which we designateSpt (salivary protein). Although physically closely linked,Spt genes differ in their patterns of expression both in strains of mice and in their tissues. One gene,Spt-1, is expressed at high levels in the SMG of all inbred strains examined. This gene is also expressed at significant levels in the lacrimal gland. A second gene,Spt-2, appears to be present as a single copy in some strains and as two copies in others. This gene is expressed at high levels only in the SMG of those strains carrying two copies, andSpt-2 mRNA is not detectable in the SMG of strains carrying only one copy. In contrast toSpt-1, theSpt-2 gene is not expressed at detectable levels in the lacrimal gland.

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

References

  1. Azen, E. A., Carlson, D. M., Clements, S., Lalley, P. A., and Vanin, E. (1984). Salivary proline-rich protein genes on chromosome 8 of mouse.Science 226967.

  2. Barka, T. (1980). Biologically active polypeptides in submandibular glands.J. Histochem. Cytochem. 28836.

  3. Berger, F. G., Gross, K. W., and Watson, G. (1981). Isolation and characterisation of a DNA sequence complementary to an androgen-inducible messenger RNA from mouse kidney.J. Biol. Chem. 2567006.

  4. Chretien, M. (1977). Action of testosterone on the differentiation and secretory activity of a target organ: The submaxillary gland of the mouse.Int. Rev. Cytol. 50333.

  5. Chu, G., Vollrath, D., and Davis, R. W. (1986). Separation of large DNA molecules by contour-clamped homogeneous electric fields.Science 2341582.

  6. Church, G. M., and Gilbert, W. (1984). Genomic sequencing.Proc. Natl. Acad. Sci. USA 811991.

  7. Cox, R. A. (1968). The use of guanidinium hydrochloride in the isolation of nucleic acids.Methods Enzymol. 12B120.

  8. Craig, A. G., Mullins, J. J., McTurk, P., and Brammar, W. J. (1985). A mouse gene family associated with a major submaxillary-gland glycoprotein.Biochem. J. 225657.

  9. Dickinson, D. P., Gross, K. W., Piccini, N., and Wilson, C. M. (1984). Evolution and variation of renin genes in mice.Genetics 108651.

  10. Dickinson, D. P., Ridall, A. L., and Levine, M. J. (1987). Human submandibular gland statherin and basic histidine-rich peptide are encoded by highly abundant mRNA's derived from a common ancestral sequence.Biochem. Biophys. Res. Commun. 149784.

  11. Dickinson, D. P., Mirels, L., Tabak, L. A., and Gross, K. W. (1989). Rapid evolution of variants in a rodent multigene family encoding salivary proteins.Mol. Biol. Evol. 680.

  12. Feinberg, A. P., and Vogelstein, B. (1983). A technique for radiolabelling DNA restriction endonuclease fragments to high specific activity.Anal. Biochem. 1326.

  13. Gardiner, K., Laas, W., and Patterson, D. (1986). Fractionation of large mammalian DNA restriction fragments using vertical pulsed-field gradient gel electrophoresis.Somat. Cell Mol. Genet. 12185.

  14. Gubler, U., and Hoffman, B. J. (1983). A simple and very efficient method for generating cDNA libraries.Gene 25263.

  15. Hastie, N. D., Held, W. A., and Toole, J. J. (1979). Multiple genes coding for the androgen-regulated major urinary proteins of the mouse.Cell 17449.

  16. Hay, D. I. (1984). Specific functional salivary proteins. In Guggenheim, B. (ed.),Cariology Today Karger, Basel, pp. 98–108.

  17. Held, W. A., West, K., and Gallagher, J. F. (1977). Importance of initiation factor preparation in the translation of reovirus and globin mRNAs lacking a 5′-terminal 7-methylguanosine.J. Biol. Chem. 2528489.

  18. Herrmann, B. G., Barlow, D. P., and Lehrach, H. (1987). A large inverted duplication allows homologous recombination between chromosomes heterozygous for the proximal t complex inversion.Cell 48813.

  19. Laemmli, U. K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4.Nature 277680.

  20. Lalley, P. A., Francke, U., and Minna, J. D. (1978). Homologous genes for enolase, phosphogluconate dehydrogenase, and adenylate kinase are syntenic on mouse chromosome 4 and human chromosome 1p.Proc. Natl. Acad. Sci. USA 752382.

  21. MacKay, B. J., Pollock, J. J., Iacono, V. J., and Baum, B. J. (1984). Isolation of milligram quantities of a group of histidine-rich polypeptides from human parotid saliva.Infect. Immun. 44688.

  22. Maeda, N. (1985). Inheritance of the human salivary proline-rich proteins: a reinterpretation in terms of six loci forming two subfamilies.Biochem. Genet. 23445.

  23. Maeda, N., Kim, H.-S., Azen, E. A., and Smithies, O. (1985). Differential RNA splicing and post-translational cleavages in the human salivary proline-rich protein gene system.J. Biol. Chem. 26011123.

  24. Maniatis, T., Fritsch, E. F., and Sambrook, J. (1982a). Nick translation of DNA. InMolecular Cloning: A Laboratory Manual Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y., pp. 109–112.

  25. Maniatis, T., Fritsch, E. F., and Sambrook, J. (1982b). Preparation of buffers and solutions. InMolecular Cloning: A Laboratory Manual Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y., pp. 447–448.

  26. Minaguchi, K., and Bennick, A. (1989). Genetics of human salivary proteins.J. Dent. Res. 682.

  27. Minakata, K., and Asano, M. (1984). New protein inhibitors of cysteine proteinases in human saliva and salivary glands.Hoppe-Seyler Z. Physiol. Chem. 365399.

  28. Minna, J. D., Marshall, T. H., and Shaffer-Berman, P. V. (1975). Chinese hamster X mouse hybrid cells segregating mouse chromosomes and isozymes.Somat. Cell Genet. 1355.

  29. O'Farrell, P. H. (1975). High resolution two-dimensional electrophoresis of proteins.J. Biol. Chem. 2504007.

  30. Piccini, N., Knopf, J. L., and Gross, K. W. (1982). A DNA polymorphism, consistent with gene duplication, correlates with high renin levels in the mouse submaxillary gland.Cell 30205.

  31. Pittet, A.-C., and Schibler, U. (1985). Mouse alpha-amylase loci, Amy-1a and Amy-2a, are closely linked.J. Mol. Biol. 182359.

  32. Romer, A. S. (1970). Mouth and pharynx; Teeth, respiratory organs. InThe Vertebrate Body W. B. Saunders, Philadelphia, Chap. 11.

  33. Schibler, U., Pittet, A.-C., Young, R. A., Hagenbuchle, O., Tosi, M., Gellman, S., and Wellauer, P. K. (1982). The mouse α-amylase multigene family. Sequence organisation of members expressed in the pancreas, salivary gland and liver.J. Mol. Biol. 155247.

  34. Schibler, U., Hagenbuchle, O., Wellauer, P. K., and Pittet, A. C. (1983). Two promoters of different strengths control the transcription of the mouse alpha-amylase geneAmy-1 a in the parotid gland and the liver.Cell 33501.

  35. Shomers, J. P., Tabak, L. A., Levine, M. J., Mandel, I. D., and Ellison, S. A. (1982). The isolation of a family of cysteine-containing phosphoproteins from human submandibular-sublingual saliva.J. Dent. Res. 61973.

  36. Southern, E. M. (1975). Detection of specific sequences among DNA fragments separated by gel electrophoresis.J. Mol. Biol. 98503.

  37. Thomas, P. S. (1980). Hybridisation of denatured RNA and small DNA fragments transferred to nitrocellulose.Proc. Natl. Acad. Sci. USA 775201.

  38. Windass, J. D., Mullins, J. J., Beecroft, L. J., George, H., Meacock, P. A., Williams, B. R. G., and Brammar, W. J. (1984). Molecular cloning of cDNAs from androgen-independent mRNA species of DBA/2 mouse sub-maxillary glands.Nucleic Acids Res. 121361.

  39. Wong, R. S. C., Madapallimattam, G., and Bennick, A. (1983). The role of glandular kallikrein in the formation of a salivary proline-rich protein A by cleavage of a single band in salivary protein C.Biochem. J. 21135.

Download references

Author information

Additional information

This research was supported in part by National Institutes of Health Grants GM18684, CA33093, and GM30248 and by a UTHSC Dental Branch BRSG Award to D.P.D.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Dickinson, D.P., Abel, K., Near, J. et al. Genetic and tissue-specific variation in the expression of a closely linked murine multigene family on chromosome 15 that encodes salivary and lacrimal proteins. Biochem Genet 27, 613–637 (1989). https://doi.org/10.1007/BF00553636

Download citation

Key words

  • mouse
  • salivary protein
  • lacrimal protein
  • gene expression
  • Spt locus
  • multigene family