Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Human testis-specific PGK gene lacks introns and possesses characteristics of a processed gene

Abstract

Phosphoglycerate kinase (PGK) (ATP: 3-phospho-D-glycerate 1-phosphotransferase, EC 2.7.2.3) is a metabolic enzyme functioning in the Embden–Meyerhof pathway that converts glucose (or fructose) to pyruvate. Two functional loci for the production of PGK have been identified in the mammalian genome. PGK-1 is an X-linked gene expressed constitutively in all somatic cells and premeitotic germ cells1–4.. The human PGK-1 gene consists of 11 exons and 10 introns encompassing a region 23 kilobases (kb) in length5. PGK-2 is an autosomal gene expressed in a tissue-specific manner exclusively in the late stages of spermatogenesis3,4,6–8. In the present study, a molecular analysis of a human genomic clone of PGK-2 originally isolated by Szabo et al.9 has revealed that this autosomal sequence completely lacks introns and contains characteristics of a processed gene10,11, or 'retroposon'12,13, including the remnants of a poly(A)+ tail and bounding direct repeats. Typically such processed sequences form non-functional pseudogenes that have evolved multiple genetic lesions which preclude translation of any transcript into a functional polypeptide10. For example, an X-linked processed pseudogene of PGK-1PGK-1) in humans has been identified and shown to contain premature termination codons in all reading frames14. It was therefore unexpected to find that the intronless autosomal PGK sequence reported here is not a pseudogene, but is rather a functional gene that has retained a complete open reading frame, and is actively expressed in mammalian spermatogenesis. Both the unusual conservation of function in this processed PGK-2 gene and its tissue-specific expression in spermatogenesis are best explained as a compensatory response to the inactivation of the X-linked PGK-1 gene in spermatogenic cells before meiosis.

This is a preview of subscription content, access via your institution

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Prices may be subject to local taxes which are calculated during checkout

References

  1. Chen, S.-H., Malcolm, L. A., Yoshida, A. & Gilbert, E. R. Am. J. hum. Genet. 23, 87–91 (1971).

    CAS  PubMed  PubMed Central  Google Scholar 

  2. Kozak, L. A., McLean, G. K. & Eicher, E. M. Biochem. Genet. 11, 41–47 (1973).

    Article  Google Scholar 

  3. VandeBerg, J. L., Cooper, D. W. & Close, P. J. J. exp. Zool 198, 231–240 (1977).

    Article  Google Scholar 

  4. Kramer, J. M. & Erickson, R. P. Devl Biol. 87, 37–45 (1981).

    Article  CAS  Google Scholar 

  5. Michelson, A. M., Blake, C. C. F., Evans, S. T. & Orkin, S. H. Proc. natn. Acad. Sci. U.S.A. 82, 6965–6969 (1985).

    Article  ADS  CAS  Google Scholar 

  6. Eicher, E. M., Cherry, M. & Flaherty, L. Molec. gen. Genet. 158, 225–228 (1978).

    Article  CAS  Google Scholar 

  7. VandeBerg, J. L., Cooper, D. W. & Close, P. J. Nature new Biol. 243, 48–50 (1973).

    CAS  PubMed  Google Scholar 

  8. VandeBerg, J. L., Cooper, D. W., Sharman, G. B. & Poole, W. E. Genetics 95, 413–424 (1980).

    Article  CAS  Google Scholar 

  9. Szabo, P., Greschik, K.-H. & Siniscalco, M. Proc. natn. Acad. Sci. U.S.A. 81, 3167–3169 (1984).

    Article  ADS  CAS  Google Scholar 

  10. Vanin, E. F. A. Rev. Genet. 19, 253–272 (1985).

    Article  CAS  Google Scholar 

  11. Wagner, M. Trends Genet. 2, 134–137 (1986).

    Article  Google Scholar 

  12. Rogers, J. H. Nature 301, 460 (1983).

    Article  ADS  CAS  Google Scholar 

  13. Rogers, J. H. Int. Rev. Cytol. 93, 187–279 (1985).

    Article  CAS  Google Scholar 

  14. Michelson, A. M., Brans, G. P., Morton, C.C. & Orkin, S. H. J. biol. Chem. 260, 6982–6992 (1985).

    Article  CAS  Google Scholar 

  15. Huang, I.Y., Welch, C. D. & Yoshida, A. J. biol. Chem. 255, 6412–6420 (1980).

    Article  CAS  Google Scholar 

  16. Singer-Sam, J. et al. Proc. natn. Acad. Sci. U.S.A. 80, 802–806 (1983).

    Article  ADS  CAS  Google Scholar 

  17. Watson, H. C. et al. EMBO J. 1, 1635–1640 (1982).

    Article  CAS  Google Scholar 

  18. Singer-Sam, J. et al. Gene 32, 409–417 (1984).

    Article  CAS  Google Scholar 

  19. Willard, H. F., Goss, S. J., Holmes, M. T. & Munroe, D. L. Hum. Genet. 71, 138–143 (1985).

    Article  CAS  Google Scholar 

  20. Gartler, S. M. et al. Somatic molec. Cell Genet. 12, 395–401 (1986).

    Article  CAS  Google Scholar 

  21. VandeBerg, J. L., Cooper, D. W., Sharman, G. B. & Poole, W. E. Genetics 95, 413–424 (1980).

    Article  CAS  Google Scholar 

  22. Moos, M. & Gallwitz, D. Nucleic Acids Res. 10, 7843–7849 (1982).

    Article  CAS  Google Scholar 

  23. Moos, M. & Gallwitz, D. EMBO J. 2, 757–761 (1983).

    Article  CAS  Google Scholar 

  24. Antoine, M. & Niessing, J. Nature 310, 795–798 (1984).

    Article  ADS  CAS  Google Scholar 

  25. Stein, J. P. et al. Proc. natn. Acad. Sci. U.S.A. 80, 6485–6489 (1983).

    Article  ADS  CAS  Google Scholar 

  26. Soares, M. B. et al. Molec. cell. Biol. 5, 2090–2103 (1985).

    CAS  PubMed  PubMed Central  Google Scholar 

  27. Kramer, J. M. Devl Biol. 87, 30–36 (1981).

    Article  CAS  Google Scholar 

  28. VandeBerg, J. L., Lee, C.-Y. & Goldberg, E. J. exp. Zool. 217, 435–441 (1981).

    Article  CAS  Google Scholar 

  29. Erickson, R. P., Kramer, J. M., Rittenhouse, J. & Salkeld, A. Proc. natn. Acad. Sci. U.S.A. 77, 6086–6090 (1980).

    Article  ADS  CAS  Google Scholar 

  30. Gold, B., Fujimoto, H., Kramer, J. M., Erickson, R. P. & Hecht, N. B. Devl. Biol. 98, 392–399 (1983).

    Article  CAS  Google Scholar 

  31. Lifschitz, E. & Lindsley, D. L. Proc. natn. Acad. Sci. U.S.A. 69, 182–186 (1972).

    Article  ADS  Google Scholar 

  32. Mann, T. The Biochemistry of Semen and the Male Reproductive Tract (Wiley, New York, 1964).

    Google Scholar 

  33. Yanisch-Perron, C., Vieira, J. & Messing, J. Gene 33, 103–119 (1985).

    Article  CAS  Google Scholar 

  34. Sanger, F., Nicklen, S. & Coulson, A. R. Proc. natn. Acad. Sci U.S.A. 74, 5463–5467 (1977).

    Article  ADS  CAS  Google Scholar 

  35. Hunkapiller, M. et al. Nature 310, 105–111 (1984).

    Article  ADS  CAS  Google Scholar 

  36. Drubin, D. G., Caput, D. & Kirschner, M. W. J. Cell Biol. 98, 1090–1097 (1984).

    Article  CAS  Google Scholar 

  37. Romrell, L. J., Bellvé, A. R. & Fawcett, D. W. Devl Biol. 49, 119–131 (1976).

    Article  CAS  Google Scholar 

  38. Maniatis, T., Fritsch, E. F. & Sambrook, J. Molecular Cloning, a Laboratory Manual (Cold Spring Harbor Laboratory, New York, 1982).

    Google Scholar 

  39. Thomas, P. Proc. natn. Acad. Sci. U.S.A. 77, 5201–5205 (1980).

    Article  ADS  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

McCarrey, J., Thomas, K. Human testis-specific PGK gene lacks introns and possesses characteristics of a processed gene. Nature 326, 501–505 (1987). https://doi.org/10.1038/326501a0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/326501a0

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing