Skip to main content
PMC home page
Nucleic Acids Research logoLink to Nucleic Acids Research
. 1985 May 24;13(10):3723–3737. doi: 10.1093/nar/13.10.3723

Highly conserved sequences in the 3' untranslated region of mRNAs coding for homologous proteins in distantly related species.

D Yaffe, U Nudel, Y Mayer, S Neuman
PMCID: PMC341269  PMID: 4011440

Abstract

Comparison of the nucleotide sequence of mRNAs coding for several vertebrate actins revealed a high degree of sequence homology in the 3' untranslated region (3' UTR) between those mRNAs coding for homologous (isotypic) actins in different organisms but not between mRNAs coding for very similar isoforms differing in their function or tissue specificity. A similar pattern of sequence conservation in the 3' UTR is also found in several other genes. Furthermore, while there is a great variation in the size of the 3' UTR of mRNAs coding for different proteins, mRNA coding for isotypic proteins in distantly related organisms often have 3' UTR of similar size. The data suggest that the 3' UTR may play an important role in the regulation of expression of at least some genes at the transcriptional or posttranscriptional level.

Full text

PDF
3723

Selected References

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

  1. Banerji J., Olson L., Schaffner W. A lymphocyte-specific cellular enhancer is located downstream of the joining region in immunoglobulin heavy chain genes. Cell. 1983 Jul;33(3):729–740. doi: 10.1016/0092-8674(83)90015-6. [DOI] [PubMed] [Google Scholar]
  2. Baralle F. E., Shoulders C. C., Proudfoot N. J. The primary structure of the human epsilon-globin gene. Cell. 1980 Oct;21(3):621–626. doi: 10.1016/0092-8674(80)90425-0. [DOI] [PubMed] [Google Scholar]
  3. Breathnach R., Chambon P. Organization and expression of eucaryotic split genes coding for proteins. Annu Rev Biochem. 1981;50:349–383. doi: 10.1146/annurev.bi.50.070181.002025. [DOI] [PubMed] [Google Scholar]
  4. Cooke N. E., Baxter J. D. Structural analysis of the prolactin gene suggests a separate origin for its 5' end. Nature. 1982 Jun 17;297(5867):603–606. doi: 10.1038/297603a0. [DOI] [PubMed] [Google Scholar]
  5. Cooke N. E., Coit D., Shine J., Baxter J. D., Martial J. A. Human prolactin. cDNA structural analysis and evolutionary comparisons. J Biol Chem. 1981 Apr 25;256(8):4007–4016. [PubMed] [Google Scholar]
  6. Cowan N. J., Dobner P. R., Fuchs E. V., Cleveland D. W. Expression of human alpha-tubulin genes: interspecies conservation of 3' untranslated regions. Mol Cell Biol. 1983 Oct;3(10):1738–1745. doi: 10.1128/mcb.3.10.1738. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. DeNoto F. M., Moore D. D., Goodman H. M. Human growth hormone DNA sequence and mRNA structure: possible alternative splicing. Nucleic Acids Res. 1981 Aug 11;9(15):3719–3730. doi: 10.1093/nar/9.15.3719. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Dickerson R. E. The structures of cytochrome c and the rates of molecular evolution. J Mol Evol. 1971;1(1):26–45. doi: 10.1007/BF01659392. [DOI] [PubMed] [Google Scholar]
  9. Dolan M., Dodgson J. B., Engel J. D. Analysis of the adult chicken beta-globin gene. Nucleotide sequence of the locus, microheterogeneity at the 5'-end of beta-globin mRNA, and aberrant nuclear RNA species. J Biol Chem. 1983 Mar 25;258(6):3983–3990. [PubMed] [Google Scholar]
  10. Efstratiadis A., Posakony J. W., Maniatis T., Lawn R. M., O'Connell C., Spritz R. A., DeRiel J. K., Forget B. G., Weissman S. M., Slightom J. L. The structure and evolution of the human beta-globin gene family. Cell. 1980 Oct;21(3):653–668. doi: 10.1016/0092-8674(80)90429-8. [DOI] [PubMed] [Google Scholar]
  11. Emorine L., Kuehl M., Weir L., Leder P., Max E. E. A conserved sequence in the immunoglobulin J kappa-C kappa intron: possible enhancer element. Nature. 1983 Aug 4;304(5925):447–449. doi: 10.1038/304447a0. [DOI] [PubMed] [Google Scholar]
  12. Fornwald J. A., Kuncio G., Peng I., Ordahl C. P. The complete nucleotide sequence of the chick a-actin gene and its evolutionary relationship to the actin gene family. Nucleic Acids Res. 1982 Jul 10;10(13):3861–3876. doi: 10.1093/nar/10.13.3861. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Garrels J. I., Gibson W. Identification and characterization of multiple forms of actin. Cell. 1976 Dec;9(4 Pt 2):793–805. doi: 10.1016/0092-8674(76)90142-2. [DOI] [PubMed] [Google Scholar]
  14. Gillespie G., Lloyd J., Hopkinson D., Edwards Y. The 3'-untranslated sequence of human skeletal muscle alpha-actin mRNA. J Muscle Res Cell Motil. 1984 Aug;5(4):457–464. doi: 10.1007/BF00818263. [DOI] [PubMed] [Google Scholar]
  15. Ginzburg I., Behar L., Givol D., Littauer U. Z. The nucleotide sequence of rat alpha-tubulin: 3'-end characteristics, and evolutionary conservation. Nucleic Acids Res. 1981 Jun 25;9(12):2691–2697. doi: 10.1093/nar/9.12.2691. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Green M. R., Treisman R., Maniatis T. Transcriptional activation of cloned human beta-globin genes by viral immediate-early gene products. Cell. 1983 Nov;35(1):137–148. doi: 10.1016/0092-8674(83)90216-7. [DOI] [PubMed] [Google Scholar]
  17. Gunning P., Mohun T., Ng S. Y., Ponte P., Kedes L. Evolution of the human sarcomeric-actin genes: evidence for units of selection within the 3' untranslated regions of the mRNAs. J Mol Evol. 1984;20(3-4):202–214. doi: 10.1007/BF02104727. [DOI] [PubMed] [Google Scholar]
  18. Hamada H., Petrino M. G., Kakunaga T. Molecular structure and evolutionary origin of human cardiac muscle actin gene. Proc Natl Acad Sci U S A. 1982 Oct;79(19):5901–5905. doi: 10.1073/pnas.79.19.5901. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Hanukoglu I., Tanese N., Fuchs E. Complementary DNA sequence of a human cytoplasmic actin. Interspecies divergence of 3' non-coding regions. J Mol Biol. 1983 Feb 5;163(4):673–678. doi: 10.1016/0022-2836(83)90117-1. [DOI] [PubMed] [Google Scholar]
  20. Hayashida H., Miyata T. Unusual evolutionary conservation and frequent DNA segment exchange in class I genes of the major histocompatibility complex. Proc Natl Acad Sci U S A. 1983 May;80(9):2671–2675. doi: 10.1073/pnas.80.9.2671. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Heindell H. C., Liu A., Paddock G. V., Studnicka G. M., Salser W. A. The primary sequence of rabbit alpha-globin mRNA. Cell. 1978 Sep;15(1):43–54. doi: 10.1016/0092-8674(78)90081-8. [DOI] [PubMed] [Google Scholar]
  22. Hennighausen L. G., Sippel A. E., Hobbs A. A., Rosen J. M. Comparative sequence analysis of the mRNAs coding for mouse and rat whey protein. Nucleic Acids Res. 1982 Jun 25;10(12):3733–3744. doi: 10.1093/nar/10.12.3733. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Katcoff D., Nudel U., Zevin-Sonkin D., Carmon Y., Shani M., Lehrach H., Frischauf A. M., Yaffe D. Construction of recombinant plasmids containing rat muscle actin and myosin light chain DNA sequences. Proc Natl Acad Sci U S A. 1980 Feb;77(2):960–964. doi: 10.1073/pnas.77.2.960. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Kornblihtt A. R., Vibe-Pedersen K., Baralle F. E. Isolation and characterization of cDNA clones for human and bovine fibronectins. Proc Natl Acad Sci U S A. 1983 Jun;80(11):3218–3222. doi: 10.1073/pnas.80.11.3218. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Kost T. A., Theodorakis N., Hughes S. H. The nucleotide sequence of the chick cytoplasmic beta-actin gene. Nucleic Acids Res. 1983 Dec 10;11(23):8287–8301. doi: 10.1093/nar/11.23.8287. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Kronenberg M. N., Roberts B. E., Efstratiadis A. The 3' noncoding region of beta-globin mRNA is not essential for in vitro translation. Nucleic Acids Res. 1979 Jan;6(1):153–166. doi: 10.1093/nar/6.1.153. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Lawn R. M., Efstratiadis A., O'Connell C., Maniatis T. The nucleotide sequence of the human beta-globin gene. Cell. 1980 Oct;21(3):647–651. doi: 10.1016/0092-8674(80)90428-6. [DOI] [PubMed] [Google Scholar]
  28. Lemischka I. R., Farmer S., Racaniello V. R., Sharp P. A. Nucleotide sequence and evolution of a mammalian alpha-tubulin messenger RNA. J Mol Biol. 1981 Sep 5;151(1):101–120. doi: 10.1016/0022-2836(81)90223-0. [DOI] [PubMed] [Google Scholar]
  29. Li W. H., Gojobori T., Nei M. Pseudogenes as a paradigm of neutral evolution. Nature. 1981 Jul 16;292(5820):237–239. doi: 10.1038/292237a0. [DOI] [PubMed] [Google Scholar]
  30. Liebhaber S. A., Kan Y. W. Different rates of mRNA translation balance the expression of the two human alpha-globin loci. J Biol Chem. 1982 Oct 25;257(20):11852–11855. [PubMed] [Google Scholar]
  31. Maki M., Takayanagi R., Misono K. S., Pandey K. N., Tibbetts C., Inagami T. Structure of rat atrial natriuretic factor precursor deduced from cDNA sequence. Nature. 1984 Jun 21;309(5970):722–724. doi: 10.1038/309722a0. [DOI] [PubMed] [Google Scholar]
  32. Martin S. L., Zimmer E. A., Davidson W. S., Wilson A. C., Kan Y. W. The untranslated regions of beta-globin mRNA evolve at a functional rate in higher primates. Cell. 1981 Sep;25(3):737–741. doi: 10.1016/0092-8674(81)90181-1. [DOI] [PubMed] [Google Scholar]
  33. Mayer Y., Czosnek H., Zeelon P. E., Yaffe D., Nudel U. Expression of the genes coding for the skeletal muscle and cardiac actions in the heart. Nucleic Acids Res. 1984 Jan 25;12(2):1087–1100. doi: 10.1093/nar/12.2.1087. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Melloul D., Aloni B., Calvo J., Yaffe D., Nudel U. Developmentally regulated expression of chimeric genes containing muscle actin DNA sequences in transfected myogenic cells. EMBO J. 1984 May;3(5):983–990. doi: 10.1002/j.1460-2075.1984.tb01917.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Miller A. D., Curran T., Verma I. M. c-fos protein can induce cellular transformation: a novel mechanism of activation of a cellular oncogene. Cell. 1984 Jan;36(1):51–60. doi: 10.1016/0092-8674(84)90073-4. [DOI] [PubMed] [Google Scholar]
  36. Miller W. L., Martial J. A., Baxter J. D. Molecular cloning of DNA complementary to bovine growth hormone mRNA. J Biol Chem. 1980 Aug 25;255(16):7521–7524. [PubMed] [Google Scholar]
  37. Minty A. J., Alonso S., Caravatti M., Buckingham M. E. A fetal skeletal muscle actin mRNA in the mouse and its identity with cardiac actin mRNA. Cell. 1982 Aug;30(1):185–192. doi: 10.1016/0092-8674(82)90024-1. [DOI] [PubMed] [Google Scholar]
  38. Miyata T., Hayashida H., Kikuno R., Hasegawa M., Kobayashi M., Koike K. Molecular clock of silent substitution: at least six-fold preponderance of silent changes in mitochondrial genes over those in nuclear genes. J Mol Evol. 1982;19(1):28–35. doi: 10.1007/BF02100221. [DOI] [PubMed] [Google Scholar]
  39. Miyata T., Yasunaga T., Nishida T. Nucleotide sequence divergence and functional constraint in mRNA evolution. Proc Natl Acad Sci U S A. 1980 Dec;77(12):7328–7332. doi: 10.1073/pnas.77.12.7328. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Miyata T., Yasunaga T. Rapidly evolving mouse alpha-globin-related pseudo gene and its evolutionary history. Proc Natl Acad Sci U S A. 1981 Jan;78(1):450–453. doi: 10.1073/pnas.78.1.450. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Nilson J. H., Thomason A. R., Cserbak M. T., Moncman C. L., Woychik R. P. Nucleotide sequence of a cDNA for the common alpha subunit of the bovine pituitary glycoprotein hormones. Conservation of nucleotides in the 3'-untranslated region of bovine and human pre-alpha subunit mRNAs. J Biol Chem. 1983 Apr 25;258(8):4679–4682. [PubMed] [Google Scholar]
  42. Nishioka Y., Leder P. The complete sequence of a chromosomal mouse alpha--globin gene reveals elements conserved throughout vertebrate evolution. Cell. 1979 Nov;18(3):875–882. doi: 10.1016/0092-8674(79)90139-9. [DOI] [PubMed] [Google Scholar]
  43. Nudel U., Zakut R., Shani M., Neuman S., Levy Z., Yaffe D. The nucleotide sequence of the rat cytoplasmic beta-actin gene. Nucleic Acids Res. 1983 Mar 25;11(6):1759–1771. doi: 10.1093/nar/11.6.1759. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Oikawa S., Imai M., Ueno A., Tanaka S., Noguchi T., Nakazato H., Kangawa K., Fukuda A., Matsuo H. Cloning and sequence analysis of cDNA encoding a precursor for human atrial natriuretic polypeptide. Nature. 1984 Jun 21;309(5970):724–726. doi: 10.1038/309724a0. [DOI] [PubMed] [Google Scholar]
  45. Ordahl C. P., Cooper T. A. Strong homology in promoter and 3'-untranslated regions of chick and rat alpha-actin genes. Nature. 1983 May 26;303(5915):348–349. doi: 10.1038/303348a0. [DOI] [PubMed] [Google Scholar]
  46. Page G. S., Smith S., Goodman H. M. DNA sequence of the rat growth hormone gene: location of the 5' terminus of the growth hormone mRNA and identification of an internal transposon-like element. Nucleic Acids Res. 1981 May 11;9(9):2087–2104. doi: 10.1093/nar/9.9.2087. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Ponte P., Ng S. Y., Engel J., Gunning P., Kedes L. Evolutionary conservation in the untranslated regions of actin mRNAs: DNA sequence of a human beta-actin cDNA. Nucleic Acids Res. 1984 Feb 10;12(3):1687–1696. doi: 10.1093/nar/12.3.1687. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Queen C., Baltimore D. Immunoglobulin gene transcription is activated by downstream sequence elements. Cell. 1983 Jul;33(3):741–748. doi: 10.1016/0092-8674(83)90016-8. [DOI] [PubMed] [Google Scholar]
  49. Rozek C. E., Davidson N. Drosophila has one myosin heavy-chain gene with three developmentally regulated transcripts. Cell. 1983 Jan;32(1):23–34. doi: 10.1016/0092-8674(83)90493-2. [DOI] [PubMed] [Google Scholar]
  50. Schwarzbauer J. E., Tamkun J. W., Lemischka I. R., Hynes R. O. Three different fibronectin mRNAs arise by alternative splicing within the coding region. Cell. 1983 Dec;35(2 Pt 1):421–431. doi: 10.1016/0092-8674(83)90175-7. [DOI] [PubMed] [Google Scholar]
  51. Shani M., Nudel U., Zevin-Sonkin D., Zakut R., Givol D., Katcoff D., Carmon Y., Reiter J., Frischauf A. M., Yaffe D. Skeletal muscle actin mRNA. Characterization of the 3' untranslated region. Nucleic Acids Res. 1981 Feb 11;9(3):579–589. doi: 10.1093/nar/9.3.579. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Shani M., Zevin-Sonkin D., Saxel O., Carmon Y., Katcoff D., Nudel U., Yaffe D. The correlation between the synthesis of skeletal muscle actin, myosin heavy chain, and myosin light chain and the accumulation of corresponding mRNA sequences during myogenesis. Dev Biol. 1981 Sep;86(2):483–492. doi: 10.1016/0012-1606(81)90206-2. [DOI] [PubMed] [Google Scholar]
  53. Shen S. H., Slightom J. L., Smithies O. A history of the human fetal globin gene duplication. Cell. 1981 Oct;26(2 Pt 2):191–203. doi: 10.1016/0092-8674(81)90302-0. [DOI] [PubMed] [Google Scholar]
  54. Slightom J. L., Blechl A. E., Smithies O. Human fetal G gamma- and A gamma-globin genes: complete nucleotide sequences suggest that DNA can be exchanged between these duplicated genes. Cell. 1980 Oct;21(3):627–638. doi: 10.1016/0092-8674(80)90426-2. [DOI] [PubMed] [Google Scholar]
  55. Spritz R. A., DeRiel J. K., Forget B. G., Weissman S. M. Complete nucleotide sequence of the human delta-globin gene. Cell. 1980 Oct;21(3):639–646. doi: 10.1016/0092-8674(80)90427-4. [DOI] [PubMed] [Google Scholar]
  56. Ullrich A., Gray A., Berman C., Dull T. J. Human beta-nerve growth factor gene sequence highly homologous to that of mouse. Nature. 1983 Jun 30;303(5920):821–825. doi: 10.1038/303821a0. [DOI] [PubMed] [Google Scholar]
  57. Van Beveren C., van Straaten F., Curran T., Müller R., Verma I. M. Analysis of FBJ-MuSV provirus and c-fos (mouse) gene reveals that viral and cellular fos gene products have different carboxy termini. Cell. 1983 Apr;32(4):1241–1255. doi: 10.1016/0092-8674(83)90306-9. [DOI] [PubMed] [Google Scholar]
  58. Zakut R., Shani M., Givol D., Neuman S., Yaffe D., Nudel U. Nucleotide sequence of the rat skeletal muscle actin gene. Nature. 1982 Aug 26;298(5877):857–859. doi: 10.1038/298857a0. [DOI] [PubMed] [Google Scholar]
  59. van Straaten F., Müller R., Curran T., Van Beveren C., Verma I. M. Complete nucleotide sequence of a human c-onc gene: deduced amino acid sequence of the human c-fos protein. Proc Natl Acad Sci U S A. 1983 Jun;80(11):3183–3187. doi: 10.1073/pnas.80.11.3183. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Nucleic Acids Research are provided here courtesy of Oxford University Press

RESOURCES