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. 1990 Feb 25;18(4):949–955. doi: 10.1093/nar/18.4.949

Molecular evolution of the human Pgk-2 retroposon.

J R McCarrey 1
PMCID: PMC330349  PMID: 2156237

Abstract

The human phosphoglycerate kinase (Pgk) gene family includes the functional, intronless Pgk-2 gene and the intronless psi hPgk-1 pseudogene, both of which are retroposons of the intron-containing Pgk-1 gene. The divergence of the Pgk-2 retroposon from Pgk-1 is compared with that of the psi hPgk-1 retroposon from Pgk-1 to reveal nucleotide characteristics diagnostic of functional genes. A comparison of the human and mouse Pgk genes indicates that Pgk-2 has evolved more rapidly than Pgk-1 since the two genes diverged early in mammalian evolution, but that the lack of introns in Pgk-2 may have diminished inter-exon variation. The hypothesis that codon bias is related to expression level is shown not to hold for the Pgk genes; however, the idea that a deficiency of TA and CG dinucleotides and an excess of TG and CT dinucleotides contributes to codon bias is supported. Finally, the hypothesis that the Pgk-2 retroposon initially included a copy of the Pgk-1 'housekeeping' promoter and subsequently evolved a tissue-specific promoter is examined and supported. It is concluded that this process involved the loss of the 5' CpG island present in the Pgk-1 gene, and that selection for cell type-specific expression of Pgk-2 at high levels has driven the divergence of this retroposon from its progenitor, Pgk-1.

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Selected References

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

  1. Adra C. N., Boer P. H., McBurney M. W. Cloning and expression of the mouse pgk-1 gene and the nucleotide sequence of its promoter. Gene. 1987;60(1):65–74. doi: 10.1016/0378-1119(87)90214-9. [DOI] [PubMed] [Google Scholar]
  2. Adra C. N., Ellis N. A., McBurney M. W. The family of mouse phosphoglycerate kinase genes and pseudogenes. Somat Cell Mol Genet. 1988 Jan;14(1):69–81. doi: 10.1007/BF01535050. [DOI] [PubMed] [Google Scholar]
  3. Aota S., Ikemura T. Diversity in G + C content at the third position of codons in vertebrate genes and its cause. Nucleic Acids Res. 1986 Aug 26;14(16):6345–6355. doi: 10.1093/nar/14.16.6345. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bennetzen J. L., Hall B. D. Codon selection in yeast. J Biol Chem. 1982 Mar 25;257(6):3026–3031. [PubMed] [Google Scholar]
  5. Bird A. P. DNA methylation and the frequency of CpG in animal DNA. Nucleic Acids Res. 1980 Apr 11;8(7):1499–1504. doi: 10.1093/nar/8.7.1499. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Boer P. H., Adra C. N., Lau Y. F., McBurney M. W. The testis-specific phosphoglycerate kinase gene pgk-2 is a recruited retroposon. Mol Cell Biol. 1987 Sep;7(9):3107–3112. doi: 10.1128/mcb.7.9.3107. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Gardiner-Garden M., Frommer M. CpG islands in vertebrate genomes. J Mol Biol. 1987 Jul 20;196(2):261–282. doi: 10.1016/0022-2836(87)90689-9. [DOI] [PubMed] [Google Scholar]
  8. Gilbert W. Why genes in pieces? Nature. 1978 Feb 9;271(5645):501–501. doi: 10.1038/271501a0. [DOI] [PubMed] [Google Scholar]
  9. Grantham R., Gautier C., Gouy M., Jacobzone M., Mercier R. Codon catalog usage is a genome strategy modulated for gene expressivity. Nucleic Acids Res. 1981 Jan 10;9(1):r43–r74. doi: 10.1093/nar/9.1.213-b. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Grosjean H., Fiers W. Preferential codon usage in prokaryotic genes: the optimal codon-anticodon interaction energy and the selective codon usage in efficiently expressed genes. Gene. 1982 Jun;18(3):199–209. doi: 10.1016/0378-1119(82)90157-3. [DOI] [PubMed] [Google Scholar]
  11. Ikemura T. Codon usage and tRNA content in unicellular and multicellular organisms. Mol Biol Evol. 1985 Jan;2(1):13–34. doi: 10.1093/oxfordjournals.molbev.a040335. [DOI] [PubMed] [Google Scholar]
  12. Kozak L. P., McLean G. K., Eicher E. M. X linkage of phosphoglycerate kinase in the mouse. Biochem Genet. 1974 Jan;11(1):41–47. doi: 10.1007/BF00486618. [DOI] [PubMed] [Google Scholar]
  13. Kramer J. M., Erickson R. P. Developmental program of PGK-1 and PGK-2 isozymes in spermatogenic cells of the mouse: specific activities and rates of synthesis. Dev Biol. 1981 Oct 15;87(1):37–45. doi: 10.1016/0012-1606(81)90058-0. [DOI] [PubMed] [Google Scholar]
  14. McCarrey J. R. Nucleotide sequence of the promoter region of a tissue-specific human retroposon: comparison with its housekeeping progenitor. Gene. 1987;61(3):291–298. doi: 10.1016/0378-1119(87)90192-2. [DOI] [PubMed] [Google Scholar]
  15. McCarrey J. R., Thomas K. Human testis-specific PGK gene lacks introns and possesses characteristics of a processed gene. Nature. 1987 Apr 2;326(6112):501–505. doi: 10.1038/326501a0. [DOI] [PubMed] [Google Scholar]
  16. Michelson A. M., Blake C. C., Evans S. T., Orkin S. H. Structure of the human phosphoglycerate kinase gene and the intron-mediated evolution and dispersal of the nucleotide-binding domain. Proc Natl Acad Sci U S A. 1985 Oct;82(20):6965–6969. doi: 10.1073/pnas.82.20.6965. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Michelson A. M., Bruns G. A., Morton C. C., Orkin S. H. The human phosphoglycerate kinase multigene family. HLA-associated sequences and an X-linked locus containing a processed pseudogene and its functional counterpart. J Biol Chem. 1985 Jun 10;260(11):6982–6992. [PubMed] [Google Scholar]
  18. Michelson A. M., Markham A. F., Orkin S. H. Isolation and DNA sequence of a full-length cDNA clone for human X chromosome-encoded phosphoglycerate kinase. Proc Natl Acad Sci U S A. 1983 Jan;80(2):472–476. doi: 10.1073/pnas.80.2.472. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Mori N., Singer-Sam J., Lee C. Y., Riggs A. D. The nucleotide sequence of a cDNA clone containing the entire coding region for mouse X-chromosome-linked phosphoglycerate kinase. Gene. 1986;45(3):275–280. doi: 10.1016/0378-1119(86)90025-9. [DOI] [PubMed] [Google Scholar]
  20. Ohno S. Codon preference is but an illusion created by the construction principle of coding sequences. Proc Natl Acad Sci U S A. 1988 Jun;85(12):4378–4382. doi: 10.1073/pnas.85.12.4378. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Ohno S. Universal rule for coding sequence construction: TA/CG deficiency-TG/CT excess. Proc Natl Acad Sci U S A. 1988 Dec;85(24):9630–9634. doi: 10.1073/pnas.85.24.9630. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Pegoraro B., Lee C. Y. Purification and characterization of two isozymes of 3-phosphoglycerate kinase from the mouse. Biochim Biophys Acta. 1978 Feb 10;522(2):423–433. doi: 10.1016/0005-2744(78)90075-x. [DOI] [PubMed] [Google Scholar]
  23. Potten H., Jendraschak E., Hauck S., Amar L. C., Avner P., Müllhofer G. Molecular cloning and sequencing of a murine pgk-1 pseudogene family. Gene. 1988 Nov 30;71(2):461–471. doi: 10.1016/0378-1119(88)90063-7. [DOI] [PubMed] [Google Scholar]
  24. Sharp P. M., Li W. H. The rate of synonymous substitution in enterobacterial genes is inversely related to codon usage bias. Mol Biol Evol. 1987 May;4(3):222–230. doi: 10.1093/oxfordjournals.molbev.a040443. [DOI] [PubMed] [Google Scholar]
  25. Sharp P. M., Tuohy T. M., Mosurski K. R. Codon usage in yeast: cluster analysis clearly differentiates highly and lowly expressed genes. Nucleic Acids Res. 1986 Jul 11;14(13):5125–5143. doi: 10.1093/nar/14.13.5125. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Shields D. C., Sharp P. M., Higgins D. G., Wright F. "Silent" sites in Drosophila genes are not neutral: evidence of selection among synonymous codons. Mol Biol Evol. 1988 Nov;5(6):704–716. doi: 10.1093/oxfordjournals.molbev.a040525. [DOI] [PubMed] [Google Scholar]
  27. Singer-Sam J., Keith D. H., Tani K., Simmer R. L., Shively L., Lindsay S., Yoshida A., Riggs A. D. Sequence of the promoter region of the gene for human X-linked 3-phosphoglycerate kinase. Gene. 1984 Dec;32(3):409–417. doi: 10.1016/0378-1119(84)90016-7. [DOI] [PubMed] [Google Scholar]
  28. Singer-Sam J., Simmer R. L., Keith D. H., Shively L., Teplitz M., Itakura K., Gartler S. M., Riggs A. D. Isolation of a cDNA clone for human X-linked 3-phosphoglycerate kinase by use of a mixture of synthetic oligodeoxyribonucleotides as a detection probe. Proc Natl Acad Sci U S A. 1983 Feb;80(3):802–806. doi: 10.1073/pnas.80.3.802. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. VandeBerg J. L. The phosphoglycerate kinase isozyme system in mammals: biochemical, genetic, developmental, and evolutionary aspects. Isozymes Curr Top Biol Med Res. 1985;12:133–187. [PubMed] [Google Scholar]

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