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Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1983 Jan;80(2):472–476. doi: 10.1073/pnas.80.2.472

Isolation and DNA sequence of a full-length cDNA clone for human X chromosome-encoded phosphoglycerate kinase.

A M Michelson, A F Markham, S H Orkin
PMCID: PMC393400  PMID: 6188151

Abstract

Phosphoglycerate kinase (PGK), a major enzyme in glycolysis, is encoded by the X chromosome in mammals. We have initiated molecular analysis of the PGK structural gene by isolating a full-length cDNA clone from a human fetal liver cDNA library. Synthetic oligonucleotide mixtures encoding two different portions of PGK were used as direct in situ hybridization probes for the cDNA library. Several classes of clones were obtained based on their hybridization at different stringencies to one or both of the PGK oligonucleotide mixtures. One clone, designated pHPGK-7e, which hybridized at high stringency to each of the synthetic probes, encoded the complete PGK protein sequence as well as 82 base pairs of 5' and 437 base pairs of 3' untranslated regions. Southern blot analysis of human genomic DNAs revealed a complex pattern of hybridizing fragments, two of which were non-X in origin. These results suggest that the human genome contains a small family of dispersed PGK or PGK-like genes.

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Selected References

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  1. Banks R. D., Blake C. C., Evans P. R., Haser R., Rice D. W., Hardy G. W., Merrett M., Phillips A. W. Sequence, structure and activity of phosphoglycerate kinase: a possible hinge-bending enzyme. Nature. 1979 Jun 28;279(5716):773–777. doi: 10.1038/279773a0. [DOI] [PubMed] [Google Scholar]
  2. Birnboim H. C., Doly J. A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucleic Acids Res. 1979 Nov 24;7(6):1513–1523. doi: 10.1093/nar/7.6.1513. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Brennand J., Chinault A. C., Konecki D. S., Melton D. W., Caskey C. T. Cloned cDNA sequences of the hypoxanthine/guanine phosphoribosyltransferase gene from a mouse neuroblastoma cell line found to have amplified genomic sequences. Proc Natl Acad Sci U S A. 1982 Mar;79(6):1950–1954. doi: 10.1073/pnas.79.6.1950. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bryant T. N., Watson H. C., Wendell P. L. Structure of yeast phosphoglycerate kinase. Nature. 1974 Jan 4;247(5435):14–17. doi: 10.1038/247014a0. [DOI] [PubMed] [Google Scholar]
  5. Buehner M., Ford G. C., Moras D., Olsen K. W., Rossman M. G. D-glyceraldehyde-3-phosphate dehydrogenase: three-dimensional structure and evolutionary significance. Proc Natl Acad Sci U S A. 1973 Nov;70(11):3052–3054. doi: 10.1073/pnas.70.11.3052. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Casadaban M. J., Cohen S. N. Analysis of gene control signals by DNA fusion and cloning in Escherichia coli. J Mol Biol. 1980 Apr;138(2):179–207. doi: 10.1016/0022-2836(80)90283-1. [DOI] [PubMed] [Google Scholar]
  7. Chen S. H., Donahue R. P., Scott C. R. Characterization of phosphoglycerate kinase from human spermatozoa. Fertil Steril. 1976 Jun;27(6):699–701. [PubMed] [Google Scholar]
  8. Chen S. H., Malcolm L. A., Yoshida A., Giblett E. R. Phosphoglycerate kinase: an X-linked polymorphism in man. Am J Hum Genet. 1971 Jan;23(1):87–91. [PMC free article] [PubMed] [Google Scholar]
  9. Daiger S. P., Wildin R. S., Su T. S. Sequences on the human Y chromosome homologous to the autosomal gene for argininosuccinate synthetase. Nature. 1982 Aug 12;298(5875):682–684. doi: 10.1038/298682a0. [DOI] [PubMed] [Google Scholar]
  10. Eicher E. M., Cherry M., Flaherty L. Autosomal phosphoglycerate kinase linked to mouse major histocompatibility complex. Mol Gen Genet. 1978 Jan 17;158(3):225–228. doi: 10.1007/BF00267193. [DOI] [PubMed] [Google Scholar]
  11. Fujii H., Chen S. H., Akatsuka J., Miwa S., Yoshida A. Use of cultured lymphoblastoid cells for the study of abnormal enzymes: molecular abnormality of a phosphoglycerate kinase variant associated with hemolytic anemia. Proc Natl Acad Sci U S A. 1981 Apr;78(4):2587–2590. doi: 10.1073/pnas.78.4.2587. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Fujii H., Krietsch W. K., Yoshida A. A single amino acid substitution (Asp leads to Asn) in a phosphoglycerate kinase variant (PGK München) associated with enzyme deficiency. J Biol Chem. 1980 Jul 10;255(13):6421–6423. [PubMed] [Google Scholar]
  13. Fujii H., Yoshida A. Molecular abnormality of phosphoglycerate kinase-Uppsala associated with chronic nonspherocytic hemolytic anemia. Proc Natl Acad Sci U S A. 1980 Sep;77(9):5461–5465. doi: 10.1073/pnas.77.9.5461. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Gilbert W. Why genes in pieces? Nature. 1978 Feb 9;271(5645):501–501. doi: 10.1038/271501a0. [DOI] [PubMed] [Google Scholar]
  15. Hitzeman R. A., Clarke L., Carbon J. Isolation and characterization of the yeast 3-phosphoglycerokinase gene (PGK) by an immunological screening technique. J Biol Chem. 1980 Dec 25;255(24):12073–12080. [PubMed] [Google Scholar]
  16. Hollis G. F., Hieter P. A., McBride O. W., Swan D., Leder P. Processed genes: a dispersed human immunoglobulin gene bearing evidence of RNA-type processing. Nature. 1982 Mar 25;296(5855):321–325. doi: 10.1038/296321a0. [DOI] [PubMed] [Google Scholar]
  17. Huang I. Y., Welch C. D., Yoshida A. Complete amino acid sequence of human phosphoglycerate kinase. Cyanogen bromide peptides and complete amino acid sequence. J Biol Chem. 1980 Jul 10;255(13):6412–6420. [PubMed] [Google Scholar]
  18. Kakidani H., Furutani Y., Takahashi H., Noda M., Morimoto Y., Hirose T., Asai M., Inayama S., Nakanishi S., Numa S. Cloning and sequence analysis of cDNA for porcine beta-neo-endorphin/dynorphin precursor. Nature. 1982 Jul 15;298(5871):245–249. doi: 10.1038/298245a0. [DOI] [PubMed] [Google Scholar]
  19. Kunkel L. M., Tantravahi U., Eisenhard M., Latt S. A. Regional localization on the human X of DNA segments cloned from flow sorted chromosomes. Nucleic Acids Res. 1982 Mar 11;10(5):1557–1578. doi: 10.1093/nar/10.5.1557. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. LYON M. F. Gene action in the X-chromosome of the mouse (Mus musculus L.). Nature. 1961 Apr 22;190:372–373. doi: 10.1038/190372a0. [DOI] [PubMed] [Google Scholar]
  21. Leder A., Swan D., Ruddle F., D'Eustachio P., Leder P. Dispersion of alpha-like globin genes of the mouse to three different chromosomes. Nature. 1981 Sep 17;293(5829):196–200. doi: 10.1038/293196a0. [DOI] [PubMed] [Google Scholar]
  22. Markham A. F., Edge M. D., Atkinson T. C., Greene A. R., Heathcliffe G. R., Newton C. R., Scanlon D. Solid phase phosphotriester synthesis of large oligodeoxyribonucleotides on a polyamide support. Nucleic Acids Res. 1980 Nov 25;8(22):5193–5205. doi: 10.1093/nar/8.22.5193. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Maxam A. M., Gilbert W. Sequencing end-labeled DNA with base-specific chemical cleavages. Methods Enzymol. 1980;65(1):499–560. doi: 10.1016/s0076-6879(80)65059-9. [DOI] [PubMed] [Google Scholar]
  24. Meera Khan P., Westerveld A., Grzeschik K. H., Deys B. F., Garson O. M., Siniscalco M. X-linkage of human phosphoglycerate kinase confirmed in man-mouse and man-Chinese hamster somatic cell hybrids. Am J Hum Genet. 1971 Nov;23(6):614–623. [PMC free article] [PubMed] [Google Scholar]
  25. Mohandas T., Sparkes R. S., Shapiro L. J. Reactivation of an inactive human X chromosome: evidence for X inactivation by DNA methylation. Science. 1981 Jan 23;211(4480):393–396. doi: 10.1126/science.6164095. [DOI] [PubMed] [Google Scholar]
  26. Nielsen J. T., Chapman V. M. Electrophoretic variation for x-chromosome-linked phosphoglycerate kinase (pgk-1) in the mouse. Genetics. 1977 Oct;87(2):319–325. doi: 10.1093/genetics/87.2.319. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Ono S. Ancient linkage groups and frozen accidents. Nature. 1973 Aug 3;244(5414):259–262. doi: 10.1038/244259a0. [DOI] [PubMed] [Google Scholar]
  28. Pegoraro B., Ansari A. A., Lee C. Y., Erickson R. P. Immunological relatedness of two isozymes of 3-phosphoglycerate kinase from the mouse. FEBS Lett. 1978 Nov 15;95(2):371–374. doi: 10.1016/0014-5793(78)81032-1. [DOI] [PubMed] [Google Scholar]
  29. 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]
  30. Persico M. G., Toniolo D., Nobile C., D'Urso M., Luzzatto L. cDNA sequences of human glucose 6-phosphate dehydrogenase cloned in pBR322. Nature. 1981 Dec 24;294(5843):778–780. doi: 10.1038/294778a0. [DOI] [PubMed] [Google Scholar]
  31. Riggs A. D. X inactivation, differentiation, and DNA methylation. Cytogenet Cell Genet. 1975;14(1):9–25. doi: 10.1159/000130315. [DOI] [PubMed] [Google Scholar]
  32. Ruddle F. H. A new era in mammalian gene mapping: somatic cell genetics and recombinant DNA methodologies. Nature. 1981 Nov 12;294(5837):115–120. doi: 10.1038/294115a0. [DOI] [PubMed] [Google Scholar]
  33. Setzer D. R., McGrogan M., Nunberg J. H., Schimke R. T. Size heterogeneity in the 3' end of dihydrofolate reductase messenger RNAs in mouse cells. Cell. 1980 Nov;22(2 Pt 2):361–370. doi: 10.1016/0092-8674(80)90346-3. [DOI] [PubMed] [Google Scholar]
  34. Shows T. B., Brown J. A. Human X-Linked genes regionally mapped utilizing X-autosome translocations and somatic cell hybrids. Proc Natl Acad Sci U S A. 1975 Jun;72(6):2125–2129. doi: 10.1073/pnas.72.6.2125. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Southern E. M. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol. 1975 Nov 5;98(3):503–517. doi: 10.1016/s0022-2836(75)80083-0. [DOI] [PubMed] [Google Scholar]
  36. Su T. S., Bock H. G., O'Brien W. E., Beaudet A. L. Cloning of cDNA for argininosuccinate synthetase mRNA and study of enzyme overproduction in a human cell line. J Biol Chem. 1981 Nov 25;256(22):11826–11831. [PubMed] [Google Scholar]
  37. Talmadge K., Gilberg W. Construction of plasmid vectors with unique PstI cloning sites in a signal sequence coding region. Gene. 1980 Dec;12(3-4):235–241. doi: 10.1016/0378-1119(80)90105-5. [DOI] [PubMed] [Google Scholar]
  38. Valentine W. N., Hsieh H. S., Paglia D. E., Anderson H. M., Baughan M. A., Jaffé E. R., Garson O. M. Hereditary hemolytic anemia associated with phosphoglycerate kinase deficiency in erythrocytes and leukocytes. A probable X-chromosome-linked syndrome. N Engl J Med. 1969 Mar 6;280(10):528–534. doi: 10.1056/NEJM196903062801003. [DOI] [PubMed] [Google Scholar]
  39. VandeBerg J. L., Cooper D. W., Close P. J. Mammalian testis phosphoglycerate kinase. Nat New Biol. 1973 May 9;243(123):48–50. [PubMed] [Google Scholar]
  40. Venolia L., Gartler S. M., Wassman E. R., Yen P., Mohandas T., Shapiro L. J. Transformation with DNA from 5-azacytidine-reactivated X chromosomes. Proc Natl Acad Sci U S A. 1982 Apr;79(7):2352–2354. doi: 10.1073/pnas.79.7.2352. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Wallace R. B., Shaffer J., Murphy R. F., Bonner J., Hirose T., Itakura K. Hybridization of synthetic oligodeoxyribonucleotides to phi chi 174 DNA: the effect of single base pair mismatch. Nucleic Acids Res. 1979 Aug 10;6(11):3543–3557. doi: 10.1093/nar/6.11.3543. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Wolf S. F., Mareni C. E., Migeon B. R. Isolation and characterization of cloned DNA sequences that hybridize to the human X chromosome. Cell. 1980 Aug;21(1):95–102. doi: 10.1016/0092-8674(80)90117-8. [DOI] [PubMed] [Google Scholar]
  43. Woods D. E., Markham A. F., Ricker A. T., Goldberger G., Colten H. R. Isolation of cDNA clones for the human complement protein factor B, a class III major histocompatibility complex gene product. Proc Natl Acad Sci U S A. 1982 Sep;79(18):5661–5665. doi: 10.1073/pnas.79.18.5661. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Yoshida A., Watanabe S., Chen S. H., Giblet E. R., Malcolm L. A. Human phosphoglycerate kinase. II. Structure of a variant enzyme. J Biol Chem. 1972 Jan 25;247(2):446–449. [PubMed] [Google Scholar]

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