Journal of Molecular Evolution

, Volume 20, Issue 3–4, pp 202–214 | Cite as

Evolution of the human sarcomeric-actin genes: Evidence for units of selection within the 3′ untranslated regions of the mRNAs

  • Peter Gunning
  • Timothy Mohun
  • Sun-Yu Ng
  • Phyllis Ponte
  • Larry Kedes
Article

Summary

The complete 3′ untranslated region (3′UTR) sequence of the human skeletal-actin gene has been compared with the corresponding regions of the rat and chicken skeletal-actin genes. This comparison reveals that the skeletal-actin 3′UTR is composed of conserved and nonconserved segments. By using genomic Southern transfer blots and thermal stability (Tm) measurements, we found that the cardiac-actin gene 3′UTR also consists of conserved and nonconserved segments. Comparison of human andXenopus laevis cardiac-actin mRNA sequences confirms the presence of a region of high similarity in the 3′UTR. We conclude that subsegments of the 3′UTRs of both skeletal- and cardiac-actin genes of birds and mammals are under considerable selective pressure. This suggests that these conserved sequences may have functional roles in actin-gene expression or regulation, and that these roles might be different for each actin isoform.

Key words

3′ untranslated regions Structural protein genes Muscle genes DNA sequence evolution 

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References

  1. Alonso S (1983) The demonstration of a fetal skeletal muscle actin mRNA in the mouse and the study of the molecular evolution of actin genes. Ph.D. thesis, University of Paris, VI, ParisGoogle Scholar
  2. Beltz GA, Jacobs KA, Eickbush TH, Cherbas PT, Kafatos FC (1983) Isolation of multigene families and determination of homologies by filter hybridization methods. Methods Enzymol 100:266–285PubMedGoogle Scholar
  3. Bernard MP, Myers JC, Chu M-L, Ramirez F, Eikenberry EF, Prockop DJ (1983) Structure of a cDNA for the pro-alpha2 chain of human type 1 procollagen. Comparison with chick cDNA for the pro-alpha2(1) identifies structurally conserved features of the protein and the gene. Biochemistry 22:1139–1145CrossRefPubMedGoogle Scholar
  4. Birchmeier C, Folk W, Birnsteil ML (1983) The terminal RNA stem-loop structure and 80 pb of spacer DNA are required for the formation of 3′ termini of sea urchin H2A mRNA. Cell 35:433–440CrossRefPubMedGoogle Scholar
  5. Childs G, Maxson R, Kedes LH (1979) Histone gene expression during sea urchin embryogenesis: isolation and characterization of early and late messenger RNAs ofStrongylocentrotus purpuratus by gene specific hybridization and template activity. Dev Biol 73:153–173PubMedGoogle Scholar
  6. Cleveland DW, Lopata MA, MacDonald RJ, Cowan DJ, Rutter WJ, Kirschner MS (1980) Number and evolutionary conservation of α-and β-tubulin and cytoplasmic β- and γ-actin genes using specific cloned cDNA probes. Cell 20:95–105CrossRefPubMedGoogle Scholar
  7. Cowan NJ, Dobner PR, Fuchs EV, Cleveland DW (1983) Expression of human alpha-tubulin genes: interspecies conservation of 3′ untranslated regions. Mol Cell Biol 3:1738–1745PubMedGoogle Scholar
  8. Denhardt DT (1966) A membrane filter technique for the detection of complementary DNA. Biochem Biophys Res Commun 23:641–646CrossRefPubMedGoogle Scholar
  9. Efstratiatis A, Posakony JW, Maniatis T, Lawn RM, O'Connell C, Spritz RA, DeRiel JK, Forget BG, Weissman SM, Slightom JL, Blechl AE, Smithies O, Baralle FE, Shoulders CC, Proudfoot NJ (1980) The structure and evolution of the human beta-globin gene family. Cell 21:653–668CrossRefPubMedGoogle Scholar
  10. Engel JN, Gunning PW, Kedes LH (1981) Isolation and characterization of human actin genes. Proc Natl Acad Sci USA 78:4674–4678PubMedGoogle Scholar
  11. Fornwald JA, Kuncio G, Peng I, Ordahl CP (1982) The complete nucleotide sequence of the chick α-actin and its evolutionary relationship to the actin gene family. Nucleic Acids Res 10:3861–3876PubMedGoogle Scholar
  12. Fyrberg EA, Bond BJ, Hershey ND, Mixter KS, Davidson N (1981) The actin genes ofDrosophila: protein coding sequences are highly conserved but intron positions are not. Cell 24:107–116CrossRefPubMedGoogle Scholar
  13. Fyrberg EA, Mahaffey JW, Bond BJ, Davidson N (1983) Transcripts of the sixDrosophila actin genes accumulate in a stage- and tissue-specific manner. Cell 33:115–123CrossRefPubMedGoogle Scholar
  14. Gunning P, Ponte P, Blau H, Kedes L (1983a) α-Skeletal and α-cardiac actin genes are co-expressed in adult human skeletal muscle and heart. Mol Cell Biol 3:1783–1791PubMedGoogle Scholar
  15. Gunning P, Ponte P, Okayama H, Engel J, Blau H, Kedes L (1983b) Isolation and characterization of full-length cDNA clones for human alpha-, beta-, and gamma-actin mRNAs: skeletal but not cytoplasmic actins have an amino terminal cysteine that is subsequently removed. Mol Cell Biol 3:787–795PubMedGoogle Scholar
  16. Hamada H, Petrino MG, Kakunaga T (1982) Molecular structure and evolutionary origin of human cardiac muscle actin gene. Proc Natl Acad Sci USA 79:5901–5905PubMedGoogle Scholar
  17. Hanauer A, Levin M, Heilig R, Daegelon D, Kahn A, Mandel JL (1983) Isolation and characterization of cDNA clones for human skeletal muscle α actin. Nucleic Acids Res 11:3503–3516PubMedGoogle Scholar
  18. Kedes L, Blau H, Gunning P, Ponte P, Chiu C-P, Bains W, Engel J, Guttman S (1984) Molecular genetics of human myogenesis. Exp Biol Med 9:202–210Google Scholar
  19. Littauer UZ, Soreq H (1982) The regulatory function of poly(A) and adjancent 3′ sequences in translated RNA. Prog Nucleic Acid Res Mol Biol 27:53–83PubMedGoogle Scholar
  20. Maniatis T, Fritsch EF, Sambrook J (1983) Molecular cloning. A laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New YorkGoogle Scholar
  21. Maxam AM, Gilbert W (1980) Sequencing end-labelled DNA with base-specific cleavage reactions. Methods Enzymol 65:499–560PubMedGoogle Scholar
  22. Minty AJ, Caravatti M, Robert B, Cohen A, Daubas P, Weydert A, Gros F, Buckingham ME (1981) Mouse actin messenger RNAs. Construction and characterization of a recombinant plasmid molecule containing a complementary DNA transcript of mouse alpha-actin mRNA. J Biol Chem 256:1008–1014PubMedGoogle Scholar
  23. Minty AJ, Alonso S, Caravatti M, Buckingham ME (1982) A fetal skeletal muscle actin mRNA in the mouse and its identity with cardiac actin mRNA. Cell 30:185–192CrossRefPubMedGoogle Scholar
  24. Minty AJ, Alonso S, Guenet JL, Buckingham M (1983) Number and organization of actin-related sequences in the mouse genome. J Mol Biol 167:77–101PubMedGoogle Scholar
  25. Miyata T, Yasunaga T, Nishida T (1980) Nucleotide sequence divergence and functional constraint in mRNA evolution. Proc Natl Acad Sci USA 77:7328–7332PubMedGoogle Scholar
  26. Needleman SB, Wunsch CD (1970) A general method applicable to the search for similarities in the amino acid sequence of two proteins, J Mol Biol 48:443–453CrossRefPubMedGoogle Scholar
  27. Ordahl CP, Cooper TA (1983) Strong homology in promoter and 3′-untranslated regions of chick and rat alpha-actin genes. Nature 303:348–349CrossRefPubMedGoogle Scholar
  28. Palmiter RD (1974) Magnesium precipitation of ribonucleoprotein complexes: expedient techniques for the isolation of undegraded polysomes and messenger ribonucleic acid. Biochemistry 13:3606–3615CrossRefPubMedGoogle Scholar
  29. Ponte P, Gunning P, Blau H, Kedes L (1983) Human actin genes are single cope for alpha-skeletal and alpha-cardiac actin, but multicopy for beta- and gamma-cytoskeletal genes: 3′-untranslated regions are isotype-specific, but are conserved in evolution. Mol Cell Biol 3:1783–1791PubMedGoogle Scholar
  30. Ponte PP, Ng S-Y, Engel J, Gunning P, Kedes L (1984) Evolutionary conservation in the untranslated regions of actin mRNAs: DNA sequence of a human beta-actin cDNA. Nucleci Acids Res 12:1687–1696Google Scholar
  31. Prentki P, Krisch HM (1982) A modified pBR322 vector with improved properties for the cloning, recovery and sequencing of blunt-ended DNA fragments. Gene 17:189–196CrossRefPubMedGoogle Scholar
  32. Rigby PW, Dieckmann M, Rhodes C, Berg P (1977) Labeling DNA to high specific activityin vitro by nick-translation with DNA polymerase I. J Mol Biol 113:237–251CrossRefPubMedGoogle Scholar
  33. Shani M, Nudel U, Zevin-Sonkin D, Zakut R, Givol D, Katcoff D, Carmon Y, Reiter J, Frischauf A, Yaffe D (1981) Skeletal muscle actin mRNA. Characterization of the 3′ untranslated region. Nucleic Acids Res 9:579–589PubMedGoogle Scholar
  34. Smith TF, Waterman MS (1981) Identification of common molecular subsequences. J Mol Biol 147:195–197CrossRefPubMedGoogle Scholar
  35. Thomas P (1980) Hybridization of denatured RNA and small fragments of DNA tranferred to nitrocellulose. Proc Nat Acad Sci USA 77:5201–5205PubMedGoogle Scholar
  36. Vandekerckhove J, Weber K (1979) The complete amino acid sequence of actins from bovine aorta, bovine heart, bovine fast skeletal muscle, and rabbit slow skeletal muscle. Differentiation 14:123–133PubMedGoogle Scholar
  37. Vandekerckhove J, Franke W, Weber K (1981) Diversity of expression of non-muscle actin in amphibia. J Mol Biol 152:413–426CrossRefPubMedGoogle Scholar
  38. Vandekerckhove J, de Couet H-G, Weber K (1983) Molecular evolution of muscle-specific actins: a protein-chemical analysis. In: dos Remedios CG, Barden JA (eds) Actin: structure and function in muscle and non-muscle cells. Academic Press, Sydney, Australia, pp 241–248Google Scholar
  39. Wilson AC, Carlson SS, White TJ (1977) Biochemical evolution. Annu Rev Biochem 46:573–639CrossRefPubMedGoogle Scholar
  40. Zakut R, Shani M, Givol D, Neuman S, Yaffe D, Nudel U (1982) The nucleotide sequence of the rat skeletal muscle actin gene. Nature 298:857–859CrossRefPubMedGoogle Scholar
  41. Zuker M, Stiegler P (1981) Optimal computer folding of large RNA sequences using thermodynamic and auxiliary information. Nucleic Acids Res 9:133–148PubMedGoogle Scholar

Copyright information

© Springer-Verlag New York Inc. 1994

Authors and Affiliations

  • Peter Gunning
    • 1
    • 3
  • Timothy Mohun
    • 2
  • Sun-Yu Ng
    • 1
    • 3
  • Phyllis Ponte
    • 1
    • 3
  • Larry Kedes
    • 1
    • 3
  1. 1.The MEDIGEN Project, Department of MedicineStanford University School of MedicinePalo AltoUSA
  2. 2.MRC Laboratory of Molecular BiologyCambridgeEngland
  3. 3.Veterans Administration Medical CenterPalo AltoUSA

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