Advertisement

Journal of Molecular Evolution

, Volume 29, Issue 3, pp 212–222 | Cite as

The Muridae glyceraldehyde-3-phosphate dehydrogenase family

  • S. Riad-El Sabrouty
  • J-M Blanchard
  • L. Marty
  • P. Jeanteur
  • M. Piechaczyk
Article

Summary

Although only one gene is known to be functional, numerous glyceraldehyde-3-phosphate dehydrogenase (GAPDH) related sequences are scattered throughoutMus musculus andRattus rattus genomes. In this report we show that: (1) GAPDH pseudogenes are repeated to comparable extents, at least 400 copies, in 12 other Muridae species; (2) the complete, or nearly so, sequence of GAPDH messenger RNA is amplified, and a high proportion, if not all of these copies, are intronless; (3) GAPDH pseudogenes are preferentially located in heavily methylated and DNAse I-insensitive regions of chromatin; and (4) the presence of atypical GAPDH-related mRNAs in different cellular contexts raises the possibility that more than one GAPDH gene is transcribed.

Key words

Pseudogenes Amplification Retroposition Chromatin structure DNA methylation Transcription RNA 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Alevy MC, Tsai M-J, O'Malley BW (1984) DNAse I sensitive domains of the gene coding for the glycolytic enzyme glyceraldehyde-3-phosphate dehydrogenase. Biochemistry 23:2309–2314CrossRefPubMedGoogle Scholar
  2. Anderson MLM, Young BD (1985) Quantitative filter hybridization in nucleic acid hybridization: a practical approach. In: Hames BD, Higins SJ (eds) IRL Press, Oxford-Washington DC, pp 73–111Google Scholar
  3. Arcari P, Martinelli R, Salvatore F (1984) The complete sequence of a full length cDNA for human glyceraldehyde-3-phosphate dehydrogenase: evidence for multiple mRNA species. Nucleic Acids Res 12:9179–9189PubMedGoogle Scholar
  4. Arnold HH, Dombdey H, Wiebauer K, Siddiqui MAQ (1982) Cloning, partial sequencing and expression of the glyceral-dehyde-3-phosphate dehydrogenase gene in chick embryonic heart muscle. J Biol Chem 257:9872–9877PubMedGoogle Scholar
  5. Benham FJ, Hodgkinson S, Davies KE (1984) A glyceraldehyde-3-phosphate dehydrogenase pseudogene on the short arm of the X chromosome defines a multigenic family. EMBO J 3:2635–2640PubMedGoogle Scholar
  6. Bishop JM (1983) Retroviruses and cellular oncogenes. Annu Rev Biochem 52:301–354CrossRefPubMedGoogle Scholar
  7. Bolivar F, Rodriguez RL, Greene PJ, Bettach MC, Heynecker HL, Boyer HW, Crosa JH, Falkow S (1977) Construction and characterization of new cloning vehicles. Gene 2:95–113CrossRefPubMedGoogle Scholar
  8. Bonhomme F (1986) Evolutionary relationships in the genusMus. Curr Top Microbiol Immunol 127:19–24PubMedGoogle Scholar
  9. Bruns GAP, Pierce P, Regina VM, Gerald PS (1978) Expression of GAPDH and TPI in dog rodent hybrids. Cytogenet Cell Genet 22:547–551PubMedGoogle Scholar
  10. Cedar D (1988) DNA methylation and gene activity. Cell 63: 3–4CrossRefGoogle Scholar
  11. Crick F (1979) Split genes and RNA splicing. Science 204:264–271PubMedGoogle Scholar
  12. Dani C, Piechaczyk M, Audigier Y El Sabrouty S, Cathala G, Marty L, Fort P, Blanchard J-M, Jeanteur P (1984) Characterization of the transcription products of the glyceraldehyde-3-phosphate dehydrogenase gene in Hela cells. Eur J Biochem 45:299–304CrossRefGoogle Scholar
  13. Dugaiczyk A, Haron JA, Stone EM, Dennison OE, Rothblum KN, Schwartz RJ (1983) Cloning and sequencing of a cDNA copy of glyceraldehyde-3-phosphate dehydrogenase messenger ribonucleic acid isolated from chicken muscle. Biochemistry 22:1605–1613CrossRefPubMedGoogle Scholar
  14. Ericksson K, Halkka O, Likki J, Saura A (1976) Enzyme polymorphism in feral, outbred and inbred rats. Heredity 37:341–349PubMedGoogle Scholar
  15. Flanagan JC, Lefranc M-P, Rabbitts TH (1984) Mechanisms of divergence and convergence of the human immunoglobulin alpha-1 and alpha-2 constant gene sequences. Cell 36:681–688CrossRefPubMedGoogle Scholar
  16. Fort P, Marty L, Piechaczyk M, El Sabrouty S, Dani C, Jeanteur P, Blanchard J-M (1985) Various rat adult tissues express only one major mRNA species from the GAPDH multigene family. Nucleic Acids Res 13:1431–1442PubMedGoogle Scholar
  17. Geliber J, Nathanson SG (1987) Recombination and concerted evolution of the murine MHC locus. Trends Genet 3:107–111CrossRefGoogle Scholar
  18. Hanahan D, Messelson M (1980) Plasmid screening at high colony density. Gene 10:63–67CrossRefPubMedGoogle Scholar
  19. Hanauer A, Mandel J-L (1984) The glyceraldehyde-3-phosphate dehydrogenase gene family: structure of a human cDNA of an X chromosome linked pseudogene; amazing complexity of the gene family in mouse. EMBO J 3:2627–2633PubMedGoogle Scholar
  20. Hassouna N, Michot B, Bachellerie J-P (1984) Complete nucleotide sequence of mouse 28S rRNA gene. Implication for the process of size increase of the large subunit RNA in higher eucaryotes. Nucleic Acids Res 12:3563–3583PubMedGoogle Scholar
  21. Herbschelb-Voogt E, Monteba-Van Heuvel M, Winjen LMM, Westerveld, Pearson PL, Meera Khan P (1978) Chromosomal assignment and regional localization of CS, ENO2, GAPDH, LDH B, PEP B and TPI in man. Cytogenet Cell Genet 22:482–486PubMedGoogle Scholar
  22. Jubier-Maurin V, Bellis M, Dob B, Piechaczyk M, Roizes G (1985) A comparative study of the L1 family in the genusMus: possible role of retroposition and conversion events in its concerted evolution. J Mol Biol 184:547–564CrossRefPubMedGoogle Scholar
  23. Kimura M (1983) In: Nei M, Koeh R (eds) Evolution of genes and proteins. Sinauer, Boston, pp 797–822Google Scholar
  24. Lawson GM, Tsai M-J, O'Malley BW (1980) Deoxyribonuclease I sensitivity of the non-transcribed sequences flanking 5' and 3' ends of the ovomucoid gene and of the ovalbumin and its related X and Y genes in oviduct nuclei. Biochemistry 19: 4403–4411CrossRefPubMedGoogle Scholar
  25. McLeod ARM (1982) Expression of the mRNA coding for the glyceraldehyde-3-phosphate dehydrogenase. Eur J Biochem 119:353–358Google Scholar
  26. Maxam AM, Gilbert W (1980) Sequencing end-labelled DNA with specific chemical cleavages. Meth Enzymol 65:499–560PubMedGoogle Scholar
  27. Mechti N, Piechaczyk M, Blanchard J-M, Marty L, Bonnieu A, Jeanteur P, Lebleu B (1986) Transcriptional and post-transcriptional regulation of c-myc gene in differentiating Friend cells. Nucleic Acids Res 14:9653–9666PubMedGoogle Scholar
  28. Miles MF, Hung P, Jungmann RA (1981) Cyclic AMP regulation of lactate dehydrogenase A. J Biol Chem 256:12545–12552PubMedGoogle Scholar
  29. Milner RJ, Brow MAD, Cleveland DW, Shinnick TM, Sutcliffe JG (1983) Glyceraldehyde-3-phosphate dehydrogenase protein and mRNA are both differentially expressed in adult chicken but not in chicken embryos. Nucleic Acids Res 11: 3301–3315PubMedGoogle Scholar
  30. Nevo E, Piechaczyk M (1989) GAPDH multigene family of mole rats: evolutionary and phylogenetic patterns. Mammalia (in press)Google Scholar
  31. Ollo R, Rougeon F (1983) Gene conversion and polymorphism: generation of mouse immunoglobulin gamma2a-gene allele by differential gene conversion of gamma-2b chain gene. Cell 32:515–523CrossRefPubMedGoogle Scholar
  32. Panabières F, Piechaczyk M, Rainer B, Dani C, Riad S, Marty L, Imbach J-L, Jeanteur P, Blanchard J-M (1984) Complete nucleotide sequence of the mRNA coding for the chicken muscle glyceraldehyde-3-phosphate dehydrogenase. Biochem Biophys Res Commun 118:767–773CrossRefPubMedGoogle Scholar
  33. Piechaczyk M, Blanchard J-M, Marty L, Dani C, Panabières F, El Sabrouty S, Fort P, Jeanteur P (1984a) Post-transcriptional regulation of glyceraldehyde-3-phosphate dehydrogenase gene in rat tissues. Nucleic Acids Res 12:6951–6963PubMedGoogle Scholar
  34. Piechaczyk M, Blanchard J-M, Riad-El Sabrouty S, Dani C, Marty L, Jeanteur P (1984b) Unusual high number of glyceraldehyde-3-phosphate dehydrogenase-related sequences in mouse and rat genomes. Nature 312:469–471CrossRefPubMedGoogle Scholar
  35. Piechaczyk M, Yang J-Q, Blanchard J-M, Jeanteur P, Marcu KB (1985) Post-transcriptional mechanisms are responsible for accumulation of truncated c-myc RNAs in murine plasma cell tumors. Cell 42:589–597CrossRefPubMedGoogle Scholar
  36. Sargent TD, Wu J-R, Sala-Trepat JM, Wallace RB, Reyes AA, Bonner J (1979) The rat serum albumin gene: analysis of cloned sequences. Proc Natl Acad Sci USA 76:3256–3260PubMedGoogle Scholar
  37. Slightom JG, Bechl AE, Smithies O (1980) Human fetal G-gamma and A-gamma globin genes complete nucleotide sequences suggest that DNA can be exchanged between these duplicated genes. Cell 21:515–523CrossRefGoogle Scholar
  38. Stone EM, Rothblum KN, Schwartz RJ (1985a) Intron-dependent evolution of the chicken glyceraldehyde-3-phosphate dehydrogenase gene. Nature 317:498–500CrossRefGoogle Scholar
  39. Stone EM, Rothblum KN, Alevy MC, Kuo TM, Schwartz RJ (1985b) Complete sequence of the chicken glyceraldehyde-3-phosphate dehydrogenase gene. Proc Natl Acad Sci USA 82:1628–1632PubMedGoogle Scholar
  40. Thomas P (1980) Hybridization of denatured RNA and small DNA fragments transferred to nitrocellulose. Proc Natl Acad Sci USA 77:5201–5205PubMedGoogle Scholar
  41. Tso JY, Sun X-H, Kao T-H, Reece KS, Wu R (1985) Isolation and characterization of rat and human glyceraldehyde-3-phosphate dehydrogenase cDNAs. Nucleic Acids Res 13:2485–2502PubMedGoogle Scholar
  42. Van Arsdell SW, Denison RA, Bernstein LB, Weiner AM (1981) Direct repeats flank three small nuclear RNA pseudogenes in the human genome. Cell 26:11–17CrossRefPubMedGoogle Scholar
  43. Wagner M (1986) A consideration on the origin of processed pseudogenes. Trends Genet 2:134–137CrossRefGoogle Scholar
  44. Weisbrod S (1982) Active chromatin. Nature 297:289–295CrossRefPubMedGoogle Scholar
  45. Weller P, Jeffreys AJ, Wilson V, Blanchetot A (1984) Organization of the human myoglobin gene. EMBO J 3:439–446PubMedGoogle Scholar

Copyright information

© Springer-Verlag New York Inc 1989

Authors and Affiliations

  • S. Riad-El Sabrouty
    • 1
    • 2
  • J-M Blanchard
    • 1
    • 2
  • L. Marty
    • 1
    • 2
  • P. Jeanteur
    • 1
    • 2
  • M. Piechaczyk
    • 1
    • 2
  1. 1.UA CNRS 1191, Laboratoire de Biologie MoléculaireUSTLMontpellier CedexFrance
  2. 2.Laboratoire de BiochimieCentre Paul LamarqueMontpellier CedexFrance

Personalised recommendations