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.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
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, Paris
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 100:266–285
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 22:1139–1145
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 35:433–440
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 73:153–173
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 20:95–105
Cowan NJ, Dobner PR, Fuchs EV, Cleveland DW (1983) Expression of human alpha-tubulin genes: interspecies conservation of 3′ untranslated regions. Mol Cell Biol 3:1738–1745
Denhardt DT (1966) A membrane filter technique for the detection of complementary DNA. Biochem Biophys Res Commun 23:641–646
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 21:653–668
Engel JN, Gunning PW, Kedes LH (1981) Isolation and characterization of human actin genes. Proc Natl Acad Sci USA 78:4674–4678
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 10:3861–3876
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 24:107–116
Fyrberg EA, Mahaffey JW, Bond BJ, Davidson N (1983) Transcripts of the sixDrosophila actin genes accumulate in a stage- and tissue-specific manner. Cell 33:115–123
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 3:1783–1791
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 3:787–795
Hamada H, Petrino MG, Kakunaga T (1982) Molecular structure and evolutionary origin of human cardiac muscle actin gene. Proc Natl Acad Sci USA 79:5901–5905
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 11:3503–3516
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 9:202–210
Littauer UZ, Soreq H (1982) The regulatory function of poly(A) and adjancent 3′ sequences in translated RNA. Prog Nucleic Acid Res Mol Biol 27:53–83
Maniatis T, Fritsch EF, Sambrook J (1983) Molecular cloning. A laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York
Maxam AM, Gilbert W (1980) Sequencing end-labelled DNA with base-specific cleavage reactions. Methods Enzymol 65:499–560
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 256:1008–1014
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 30:185–192
Minty AJ, Alonso S, Guenet JL, Buckingham M (1983) Number and organization of actin-related sequences in the mouse genome. J Mol Biol 167:77–101
Miyata T, Yasunaga T, Nishida T (1980) Nucleotide sequence divergence and functional constraint in mRNA evolution. Proc Natl Acad Sci USA 77:7328–7332
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 48:443–453
Ordahl CP, Cooper TA (1983) Strong homology in promoter and 3′-untranslated regions of chick and rat alpha-actin genes. Nature 303:348–349
Palmiter RD (1974) Magnesium precipitation of ribonucleoprotein complexes: expedient techniques for the isolation of undegraded polysomes and messenger ribonucleic acid. Biochemistry 13:3606–3615
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 3:1783–1791
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 12:1687–1696
Prentki P, Krisch HM (1982) A modified pBR322 vector with improved properties for the cloning, recovery and sequencing of blunt-ended DNA fragments. Gene 17:189–196
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 113:237–251
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 9:579–589
Smith TF, Waterman MS (1981) Identification of common molecular subsequences. J Mol Biol 147:195–197
Thomas P (1980) Hybridization of denatured RNA and small fragments of DNA tranferred to nitrocellulose. Proc Nat Acad Sci USA 77:5201–5205
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 14:123–133
Vandekerckhove J, Franke W, Weber K (1981) Diversity of expression of non-muscle actin in amphibia. J Mol Biol 152:413–426
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 241–248
Wilson AC, Carlson SS, White TJ (1977) Biochemical evolution. Annu Rev Biochem 46:573–639
Zakut R, Shani M, Givol D, Neuman S, Yaffe D, Nudel U (1982) The nucleotide sequence of the rat skeletal muscle actin gene. Nature 298:857–859
Zuker M, Stiegler P (1981) Optimal computer folding of large RNA sequences using thermodynamic and auxiliary information. Nucleic Acids Res 9:133–148
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Gunning, P., Mohun, T., Ng, SY. et al. Evolution of the human sarcomeric-actin genes: Evidence for units of selection within the 3′ untranslated regions of the mRNAs. J Mol Evol 20, 202–214 (1984). https://doi.org/10.1007/BF02104727
Issue Date:
DOI: https://doi.org/10.1007/BF02104727