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PMID: 3380094 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Poly(A) shortening and degradation of the 3' A+U-rich sequences of human c-myc mRNA in a cell-free system.

Molecular and cellular biology ·Vol. 8 ·No. 4 ·1988-04-00 ·Pages 1697-708

Brewer G, Ross J

Abstract

The early steps in the degradation of human c-myc mRNA were investigated, using a previously described cell-free mRNA decay system. The first detectable step was poly(A) shortening, which generated a pool of oligoadenylated mRNA molecules. In contrast, the poly(A) of a stable mRNA, gamma globin, was not excised, even after prolonged incubation. The second step, degradation of oligoadenylated c-myc mRNA, generated decay products whose 3' termini were located within the A+U-rich portion of the 3' untranslated region. These products disappeared soon after they were formed, consistent with rapid degradation of the 3' region. In contrast, the 5' region, corresponding approximately to c-myc exon 1, was stable in vitro. The data indicate a sequential degradation pathway in which 3' region cleavages occur only after most or all of the poly(A) is removed. To account for rapid deadenylation, we suggest that the c-myc poly(A)-poly(A)-binding protein complex is readily dissociated, generating a protein-depleted poly(A) tract that is no longer resistant to nucleases.

MeSH Terms
Adenine Base Sequence Cell Line Cell-Free System Humans Kinetics Nucleotide Mapping Poly A/genetics,metabolism Proto-Oncogenes RNA, Messenger/genetics,metabolism Uracil
Chemicals
RNA, Messenger Poly A Uracil Adenine
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Brewer G
McArdle Laboratory for Cancer Research, University of Wisconsin, Madison 53706.
Ross J
References (105)
105 references, click to expand
  1. G1 and S phase mammalian cells synthesize histones at equivalent rates.
    Cell. 1980 Aug;21(1):195-204 PMID: 7407911
  2. Cytoplasmic processing of myosin heavy chain messenger RNA: evidence provided by using a recombinant DNA plasmid.
    Proc Natl Acad Sci U S A. 1980 Oct;77(10):5749-53 PMID: 6934508
  3. Translational activity and functional stability of human fibroblast beta 1 and beta 2 interferon mRNAs lacking 3'-terminal RNA sequences.
    Proc Natl Acad Sci U S A. 1981 Mar;78(3):1741-5 PMID: 6165016
  4. Expression of cellular homologues of retroviral onc genes in human hematopoietic cells.
    Proc Natl Acad Sci U S A. 1982 Apr;79(8):2490-4 PMID: 6283530
  5. Herpesvirus infection alters the steady-state levels of cellular polyadenylated RNA in polyoma virus-transformed BHK cells.
    J Virol. 1982 Jun;42(3):1131-4 PMID: 6178847
  6. Control of insulin gene expression in pancreatic beta-cells and in an insulin-producing cell line, RIN-5F cells. II. Regulation of insulin mRNA stability.
    J Biol Chem. 1985 Nov 5;260(25):13590-4 PMID: 3902821
  7. Post-transcriptional control of myc and p53 expression during differentiation of the embryonal carcinoma cell line F9.
    Nature. 1985 Oct 17-23;317(6038):636-9 PMID: 2414665
  8. Molecular cloning and regulated expression of the human c-myc gene in Escherichia coli and Saccharomyces cerevisiae: comparison of the protein products.
    Proc Natl Acad Sci U S A. 1985 Nov;82(21):7232-6 PMID: 3903749
  9. Metabolism of c-myc gene products: c-myc mRNA and protein expression in the cell cycle.
    EMBO J. 1985 Aug;4(8):2009-15 PMID: 4065102
  10. Density-dependent arrest of DNA replication is accompanied by decreased levels of c-myc mRNA in myogenic but not in differentiation-defective myoblasts.
    J Cell Physiol. 1985 Dec;125(3):465-70 PMID: 4066768
  11. The c-myc oncogene driven by immunoglobulin enhancers induces lymphoid malignancy in transgenic mice.
    Nature. 1985 Dec 12-18;318(6046):533-8 PMID: 3906410
  12. An analysis of the rate of metallothionein mRNA poly(A)-shortening using RNA blot hybridization.
    Nucleic Acids Res. 1985 Nov 25;13(22):7929-43 PMID: 2866488
  13. Platelet-derived growth factor and double-stranded ribonucleic acids stimulate expression of the same genes in 3T3 cells.
    Cell. 1985 Dec;43(3 Pt 2):793-800 PMID: 3000615
  14. Cell-specific regulation of the c-myc gene by lymphocyte mitogens and platelet-derived growth factor.
    Cell. 1983 Dec;35(3 Pt 2):603-10 PMID: 6606489
  15. Cell-cycle control of c-myc but not c-ras expression is lost following chemical transformation.
    Cell. 1984 Feb;36(2):241-7 PMID: 6692471
  16. Cell cycle regulation of mouse H3 histone mRNA metabolism.
    Mol Cell Biol. 1984 Jan;4(1):123-32 PMID: 6583492
  17. Translational control during early Dictyostelium development: possible involvement of poly(A) sequences.
    Cell. 1984 Apr;36(4):1017-25 PMID: 6142768
  18. Activation of the c-myc gene by translocation: a model for translational control.
    Proc Natl Acad Sci U S A. 1983 Dec;80(24):7476-80 PMID: 6324175
  19. Nucleotide sequence of the human c-myc locus: provocative open reading frame within the first exon.
    EMBO J. 1984 Feb;3(2):383-7 PMID: 6714223
  20. Genomic sequencing.
    Proc Natl Acad Sci U S A. 1984 Apr;81(7):1991-5 PMID: 6326095
  21. Efficient in vitro synthesis of biologically active RNA and RNA hybridization probes from plasmids containing a bacteriophage SP6 promoter.
    Nucleic Acids Res. 1984 Sep 25;12(18):7035-56 PMID: 6091052
  22. Accumulation of rare and moderately abundant mRNAs in mouse L-cells is mainly post-transcriptionally regulated.
    J Mol Biol. 1984 Oct 5;178(4):869-80 PMID: 6492167
  23. Regulated transcription of c-Ki-ras and c-myc during compensatory growth of rat liver.
    Mol Cell Biol. 1984 Aug;4(8):1493-8 PMID: 6493228
  24. Extreme instability of myc mRNA in normal and transformed human cells.
    Proc Natl Acad Sci U S A. 1984 Nov;81(22):7046-50 PMID: 6594679
  25. Proteins encoded by the human c-myc oncogene: differential expression in neoplastic cells.
    Mol Cell Biol. 1984 Nov;4(11):2486-97 PMID: 6513926
  26. The protein encoded by the human proto-oncogene c-myc.
    Proc Natl Acad Sci U S A. 1984 Dec;81(24):7742-6 PMID: 6393124
  27. Interferon regulates c-myc gene expression in Daudi cells at the post-transcriptional level.
    Proc Natl Acad Sci U S A. 1985 Feb;82(4):1151-4 PMID: 3856253
  28. Regulation of messenger RNA stability in mouse erythroleukemia cells.
    J Mol Biol. 1985 Jan 20;181(2):231-9 PMID: 3856689
  29. Increased rate of degradation of c-myc mRNA in interferon-treated Daudi cells.
    Proc Natl Acad Sci U S A. 1985 Aug;82(15):4896-9 PMID: 3860831
  30. c-myc mRNA levels in the cell cycle change in mouse erythroleukemia cells following inducer treatment.
    Proc Natl Acad Sci U S A. 1985 Aug;82(16):5323-7 PMID: 3860863
  31. Posttranscriptional mechanisms are responsible for accumulation of truncated c-myc RNAs in murine plasma cell tumors.
    Cell. 1985 Sep;42(2):589-97 PMID: 2411425
  32. c-myc gene is transcribed at high rate in G0-arrested fibroblasts and is post-transcriptionally regulated in response to growth factors.
    Nature. 1985 Oct 3-9;317(6036):443-5 PMID: 3900742
  33. Transient accumulation of c-fos RNA following serum stimulation requires a conserved 5' element and c-fos 3' sequences.
    Cell. 1985 Oct;42(3):889-902 PMID: 2414012
  34. Transcriptional arrest within the first exon is a fast control mechanism in c-myc gene expression.
    Nucleic Acids Res. 1986 Nov 11;14(21):8331-46 PMID: 3537956
  35. Intragenic pausing and anti-sense transcription within the murine c-myc locus.
    EMBO J. 1986 Nov;5(11):2859-65 PMID: 3024965
  36. Novel promoter upstream of the human c-myc gene and regulation of c-myc expression in B-cell lymphomas.
    Mol Cell Biol. 1986 Oct;6(10):3481-9 PMID: 3540591
  37. Transcriptional and posttranscriptional control of c-myc gene expression in WEHI 231 cells.
    Mol Cell Biol. 1986 Nov;6(11):4112-6 PMID: 3796600
  38. Histone mRNA degradation in vivo: the first detectable step occurs at or near the 3' terminus.
    Mol Cell Biol. 1986 Dec;6(12):4362-71 PMID: 3467177
  39. c-myc mRNA is elevated as differentiating lens cells withdraw from the cell cycle.
    Exp Cell Res. 1987 Mar;169(1):215-22 PMID: 3817014
  40. Role of transcriptional and posttranscriptional regulation in expression of histone genes in Saccharomyces cerevisiae.
    Mol Cell Biol. 1987 Feb;7(2):614-21 PMID: 3547077
  41. Presence of a c-myc transcript initiated in intron 1 in Friend erythroleukemia cells and in other murine cell types with no evidence of c-myc gene rearrangement.
    Mol Cell Biol. 1987 Feb;7(2):940-5 PMID: 3547087
  42. Structural features in the 3'-terminal region of polyribosome-bound rabbit globin messenger RNAs.
    J Biol Chem. 1986 Jan 5;261(1):397-402 PMID: 3001055
  43. Rat fibroblasts expressing high levels of human c-myc transcripts are anchorage-independent and tumorigenic.
    J Cell Physiol. 1986 Jan;126(1):107-14 PMID: 3944192
  44. Truncation of exon 1 from the c-myc gene results in prolonged c-myc mRNa stability.
    EMBO J. 1985 Dec 30;4(13B):3727-33 PMID: 4092694
  45. Differential expression of myc family genes during murine development.
    Nature. 1986 Feb 27-Mar 5;319(6056):780-3 PMID: 2419762
  46. Identification of a common nucleotide sequence in the 3'-untranslated region of mRNA molecules specifying inflammatory mediators.
    Proc Natl Acad Sci U S A. 1986 Mar;83(6):1670-4 PMID: 2419912
  47. Constitutive c-myc oncogene expression blocks mouse erythroleukaemia cell differentiation but not commitment.
    Nature. 1986 Apr 24-30;320(6064):760-3 PMID: 3458027
  48. Consequences of widespread deregulation of the c-myc gene in transgenic mice: multiple neoplasms and normal development.
    Cell. 1986 May 23;45(4):485-95 PMID: 3011271
  49. A single gene from yeast for both nuclear and cytoplasmic polyadenylate-binding proteins: domain structure and expression.
    Cell. 1986 Jun 20;45(6):827-35 PMID: 3518950
  50. Poly(A) shortening of coregulated transcripts in Drosophila.
    Dev Biol. 1986 Jun;115(2):507-10 PMID: 3011568
  51. A block to elongation is largely responsible for decreased transcription of c-myc in differentiated HL60 cells.
    Nature. 1986 Jun 12-18;321(6071):702-6 PMID: 3520340
  52. The stability of E. coli gene transcripts is dependent on determinants localized to specific mRNA segments.
    Cell. 1986 Jul 18;46(2):245-51 PMID: 3521892
  53. H4 histone messenger RNA decay in cell-free extracts initiates at or near the 3' terminus and proceeds 3' to 5'.
    J Mol Biol. 1986 Apr 20;188(4):579-93 PMID: 3525849
  54. A conserved AU sequence from the 3' untranslated region of GM-CSF mRNA mediates selective mRNA degradation.
    Cell. 1986 Aug 29;46(5):659-67 PMID: 3488815
  55. Regulation of oncogene expression in cultured aortic smooth muscle cells. Post-transcriptional control of c-myc mRNA.
    J Biol Chem. 1986 Sep 25;261(27):12865-8 PMID: 3745215
  56. Augmented expression of normal c-myc is sufficient for cotransformation of rat embryo cells with a mutant ras gene.
    Mol Cell Biol. 1985 Dec;5(12):3345-56 PMID: 3837844
  57. Induction of c-fos and c-myc mRNA by epidermal growth factor or calcium ionophore is cAMP dependent.
    Proc Natl Acad Sci U S A. 1986 Nov;83(21):8216-20 PMID: 2430281
  58. Immunochemical detection of proteins related to the human c-myc exon 1.
    EMBO J. 1986 Sep;5(9):2241-50 PMID: 2430795
  59. Regulation of insulin mRNA abundance and adenylation: dependence on hormones and matrix substrata.
    Mol Cell Biol. 1986 Jan;6(1):337-41 PMID: 2878361
  60. c-myc regulation during retinoic acid-induced differentiation of F9 cells is posttranscriptional and associated with growth arrest.
    Mol Cell Biol. 1986 Feb;6(2):518-24 PMID: 3785153
  61. mRNA polyadenylate-binding protein: gene isolation and sequencing and identification of a ribonucleoprotein consensus sequence.
    Mol Cell Biol. 1986 Aug;6(8):2932-43 PMID: 3537727
  62. Newly formed mRNA lacking polyadenylic acid enters the cytoplasm and the polyribosomes but has a shorter half-life in the absence of polyadenylic acid.
    Mol Cell Biol. 1982 May;2(5):517-25 PMID: 6981059
  63. Behavior of individual maternal pA+ RNAs during embryogenesis of Xenopus laevis.
    Dev Biol. 1982 Nov;94(1):79-86 PMID: 6130013
  64. Identification and nucleotide sequence of a human locus homologous to the v-myc oncogene of avian myelocytomatosis virus MC29.
    Nature. 1983 Feb 24;301(5902):722-5 PMID: 6298632
  65. Decay of mRNA in Escherichia coli: investigation of the fate of specific segments of transcripts.
    Proc Natl Acad Sci U S A. 1983 Feb;80(3):653-7 PMID: 6187001
  66. The protein responsible for the repeating structure of cytoplasmic poly(A)-ribonucleoprotein.
    J Cell Biol. 1983 Mar;96(3):717-21 PMID: 6833379
  67. Histone mRNA concentrations are regulated at the level of transcription and mRNA degradation.
    Proc Natl Acad Sci U S A. 1983 Apr;80(7):1849-53 PMID: 6572946
  68. Regulation of human histone gene expression: kinetics of accumulation and changes in the rate of synthesis and in the half-lives of individual histone mRNAs during the HeLa cell cycle.
    Mol Cell Biol. 1983 Apr;3(4):539-50 PMID: 6406835
  69. Coordinate regulation of multiple histone mRNAs during the cell cycle in HeLa cells.
    Nucleic Acids Res. 1983 Apr 25;11(8):2391-410 PMID: 6304651
  70. Nucleotide sequence analysis of human c-myc locus, chicken homologue, and myelocytomatosis virus MC29 transforming gene reveals a highly conserved gene product.
    Proc Natl Acad Sci U S A. 1983 Jun;80(12):3642-5 PMID: 6304729
  71. Human beta and delta globin messenger RNAs turn over at different rates.
    J Mol Biol. 1983 Jul 5;167(3):607-17 PMID: 6876159
  72. Inducible transcription of five globin genes in K562 human leukemia cells.
    Proc Natl Acad Sci U S A. 1983 Sep;80(18):5515-9 PMID: 6310580
  73. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity.
    Anal Biochem. 1983 Jul 1;132(1):6-13 PMID: 6312838
  74. The human c-myc oncogene: structural consequences of translocation into the IgH locus in Burkitt lymphoma.
    Cell. 1983 Oct;34(3):779-87 PMID: 6414718
  75. Proteins encoded by v-myc and c-myc oncogenes: identification and localization in acute leukemia virus transformants and bursal lymphoma cell lines.
    Cell. 1983 Oct;34(3):789-98 PMID: 6313208
  76. Human beta-globin promoter and coding sequences transcribed by RNA polymerase III.
    Cell. 1983 Oct;34(3):857-64 PMID: 6194893
  77. Identification of nuclear proteins encoded by viral and cellular myc oncogenes.
    Nature. 1983 Nov 17-23;306(5940):274-7 PMID: 6316149
  78. Posttranscriptional regulation of c-fos mRNA expression.
    Nucleic Acids Res. 1987 Feb 25;15(4):1643-59 PMID: 3103102
  79. Xenopus myc proto-oncogene during development: expression as a stable maternal mRNA uncoupled from cell division.
    EMBO J. 1986 Dec 20;5(13):3563-70 PMID: 3549280
  80. C-myc expression is dissociated from DNA synthesis and cell division in Xenopus oocyte and early embryonic development.
    EMBO J. 1986 Dec 20;5(13):3571-7 PMID: 3549281
  81. Expression of mouse histone genes: transcription into 3' intergenic DNA and cryptic processing sites downstream from the 3' end of the H3 gene.
    Mol Cell Biol. 1987 Mar;7(3):1039-47 PMID: 2882414
  82. Increased rates of decay and reduced levels of accumulation of the major poly(A)-associated proteins of Dictyostelium during heat shock and development.
    Proc Natl Acad Sci U S A. 1987 Apr;84(7):1858-62 PMID: 3470762
  83. An in vitro system derived from Friend erythroleukemia cells to study messenger RNA stability.
    Biochem Biophys Res Commun. 1987 Apr 29;144(2):560-8 PMID: 3472522
  84. Properties of the exonuclease activity that degrades H4 histone mRNA.
    J Biol Chem. 1987 Jul 5;262(19):9374-81 PMID: 3036856
  85. Substrate specificity of the exonuclease activity that degrades H4 histone mRNA.
    J Biol Chem. 1987 Jul 5;262(19):9382-8 PMID: 3036857
  86. Glucocorticoids enhance stability of human growth hormone mRNA.
    Mol Cell Biol. 1987 Apr;7(4):1496-507 PMID: 3037323
  87. Relatively stable population of c-myc RNA that lacks long poly(A).
    Mol Cell Biol. 1987 Jun;7(6):2052-8 PMID: 3037342
  88. A single domain of yeast poly(A)-binding protein is necessary and sufficient for RNA binding and cell viability.
    Mol Cell Biol. 1987 Sep;7(9):3268-76 PMID: 3313012
  89. Nucleotide sequence of cloned cDNA of human c-myc oncogene.
    Nature. 1983 Jun 23-29;303(5919):725-8 PMID: 6304538
  90. A particle associated with the polyadenylate segment in mammalian messenger RNA.
    Proc Natl Acad Sci U S A. 1972 Nov;69(11):3247-50 PMID: 4508317
  91. Polyadenylic acid segment in mRNA becomes shorter with age.
    Nat New Biol. 1973 Feb 28;241(113):265-8 PMID: 4511912
  92. A protein of molecular weight 78,000 bound to the polyadenylate region of eukaryotic messenger RNAs.
    Proc Natl Acad Sci U S A. 1973 Mar;70(3):924-8 PMID: 4515002
  93. Characterization of the steady-state population of messenger RNA and its poly(adenylic acid) segment in mammalian cells.
    Biochemistry. 1974 Oct 22;13(22):4633-7 PMID: 4425653
  94. Size of the polyadenylic acid region of newly synthesized globin messenger ribonucleic acid.
    J Biol Chem. 1975 May 25;250(10):3725-8 PMID: 1126933
  95. Possible relationship of poly(A) shortening to mRNA turnover.
    Proc Natl Acad Sci U S A. 1975 Mar;72(3):1077-81 PMID: 1055367
  96. Metabolism of the polyadenylate sequence of nuclear RNA and messenger RNA in mammalian cells.
    Cell. 1975 Jul;5(3):271-80 PMID: 1170955
  97. Properties of sea urchin embryo messenger RNA containing and lacking poly(A).
    Cell. 1975 Oct;6(2):171-8 PMID: 1237355
  98. Readenylation of polyadenylate-free globin messenger RNA restores its stability in vivo.
    Eur J Biochem. 1975 Nov 15;59(2):589-92 PMID: 1107033
  99. Globin mRNA species containing poly(A) segments of different lengths. Their functional stability in Xenopus oocytes.
    Eur J Biochem. 1976 Apr 15;64(1):115-21 PMID: 776610
  100. Control of breakdown of the polyadenylate sequence in mammalian polyribosomes: role of poly(adenylic acid)-protein interactions.
    Biochemistry. 1977 Jan 25;16(2):259-64 PMID: 556945
  101. Functional stabilisation of HeLa cell histone messenger RNAs injected into Xenopus oocytes by 3'-OH polyadenylation.
    Nature. 1978 Feb 9;271(5645):572-3 PMID: 563987
  102. Insertion of synthetic copies of human globin genes into bacterial plasmids.
    Nucleic Acids Res. 1978 Feb;5(2):563-81 PMID: 345245
  103. A correlation between the rate of poly(A) shortening and half-life of messenger RNA in adenovirus transformed cells.
    J Mol Biol. 1978 Nov 25;126(1):23-36 PMID: 739542
  104. Translation and stability of rat liver messenger RNA for alpha 2 mu-globulin in Xenopus oocyte. The role of terminal poly(A).
    J Biol Chem. 1979 Sep 25;254(18):8937-42 PMID: 90045
  105. Repeating structure of cytoplasmic poly(A)-ribonucleoprotein.
    Proc Natl Acad Sci U S A. 1980 Apr;77(4):1890-2 PMID: 6929525
Article Info
Journal
Molecular and cellular biology
Abbr.
Mol Cell Biol
ISSN
0270-7306
DOI
10.1128/mcb.8.4.1697-1708.1988
Published
1988-04-00
Pages
1697-708
Language
English
Region
United States
NLM ID
8109087
PMCID
PMC363330
Subset
IM
Grants
NCI NIH HHS · CA07175 · United States
NCI NIH HHS · CA09230 · United States
NCI NIH HHS · CA23076 · United States
External Links
PubMed source DOI: 10.1128/mcb.8.4.1697-1708.1988 PMC Full Text View journal details
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