Home LiteratureArticle Details
PMID: 2984214 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Effect of viral infection on host protein synthesis and mRNA association with the cytoplasmic cytoskeletal structure.

The Journal of cell biology ·Vol. 100 ·No. 4 ·1985-04-00 ·Pages 1209-18

Bonneau AM, Darveau A, Sonenberg N

Abstract

We studied the association of several eucaryotic viral and cellular mRNAs with cytoskeletal fractions derived from normal and virus-infected cells. We found that all mRNAs appear to associate with the cytoskeletal structure during protein synthesis, irrespective of their 5' and 3' terminal structures: e.g., poliovirus that lacks a 5' cap structure or reovirus and histone mRNAs that lack a 3' poly A tail associated with the cytoskeletal framework to the same extent as capped, polyadenylated actin mRNA. Cellular (actin) and viral (vesicular stomatitis virus and reovirus) mRNAs were released from the cytoskeletal framework and their translation was inhibited when cells were infected with poliovirus. In contrast, actin mRNA was not released from the cytoskeleton during vesicular stomatitis virus infection although actin synthesis was inhibited. In addition, several other conditions under which protein synthesis is inhibited did not result in the release of mRNAs from the cytoskeletal framework. We conclude that the association of mRNA with the cytoskeletal framework is required but is not sufficient for protein synthesis in eucaryotes. Furthermore, the shut-off of host protein synthesis during poliovirus infection and not vesicular stomatitis virus infection occurs by a unique mechanism that leads to the release of host mRNAs from the cytoskeleton.

MeSH Terms
Actins/genetics Animals Cell Line Chlorocebus aethiops Cytoskeleton/metabolism DNA HeLa Cells/microbiology Humans Kidney Mammalian orthoreovirus 3/physiology Nucleic Acid Hybridization Poliovirus/physiology Polyribosomes/metabolism Protein Biosynthesis RNA, Messenger/metabolism RNA, Viral/metabolism Vesicular stomatitis Indiana virus/physiology
Chemicals
Actins RNA, Messenger RNA, Viral DNA
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Bonneau A M
Darveau A
Sonenberg N
References (40)
40 references, click to expand
  1. Inhibitors of protein biosynthesis. V. Effects of emetine on protein and nucleic acid biosynthesis in HeLa cells.
    J Biol Chem. 1968 Aug 10;243(15):4089-94 PMID: 4299101
  2. Translational initiation factor and ribosome association with the cytoskeletal framework fraction from HeLa cells.
    Cell. 1984 May;37(1):85-93 PMID: 6722878
  3. Virus-induced interference in heterologously infected HeLa cells.
    J Virol. 1972 Jan;9(1):22-8 PMID: 4333542
  4. Inhibition of protein synthesis in L cells infected with vesicular stomatitis virus.
    J Virol. 1972 Jan;9(1):85-9 PMID: 4333546
  5. Purification of biologically active globin messenger RNA by chromatography on oligothymidylic acid-cellulose.
    Proc Natl Acad Sci U S A. 1972 Jun;69(6):1408-12 PMID: 4504350
  6. Selective and reversible inhibition of initiation of protein synthesis in mammalian cells.
    J Mol Biol. 1974 May 15;85(2):195-211 PMID: 4365420
  7. Membrane-bound polyribosomes in HeLa cells: association of polyadenylic acid with membranes.
    J Mol Biol. 1974 Oct 25;89(2):327-38 PMID: 4216643
  8. Methylmercury as a reversible denaturing agent for agarose gel electrophoresis.
    Anal Biochem. 1976 Jan;70(1):75-85 PMID: 1259158
  9. Stereo high-voltage electron microscopy of whole cells of the human diploid line, WI-38.
    Am J Anat. 1976 Nov;147(3):303-23 PMID: 988741
  10. Nuclear matrix of HeLa S3 cells. Polypeptide composition during adenovirus infection and in phases of the cell cycle.
    J Cell Biol. 1977 Jan;72(1):194-208 PMID: 830654
  11. A cytoskeletal structure with associated polyribosomes obtained from HeLa cells.
    Cell. 1977 Jan;10(1):67-78 PMID: 837445
  12. Labeling deoxyribonucleic acid to high specific activity in vitro by nick translation with DNA polymerase I.
    J Mol Biol. 1977 Jun 15;113(1):237-51 PMID: 881736
  13. Untranslated vesicular stomatitis virus messenger RNA after poliovirus infection.
    Virology. 1977 Jul 15;80(2):297-308 PMID: 196392
  14. Analysis of VSV mutant with attenuated cytopathogenicity: mutation in viral function, P, for inhibition of protein synthesis.
    Cell. 1977 Jun;11(2):273-81 PMID: 196757
  15. Heterogeneous nuclear RNA-protein fibers in chromatin-depleted nuclei.
    J Cell Biol. 1978 Sep;78(3):663-74 PMID: 701354
  16. The cytoskeletal framework and poliovirus metabolism.
    Cell. 1979 Feb;16(2):289 301 PMID: 222454
  17. Isolation and characterization of the nuclear matrix in Friend erythroleukemia cells: chromatin and hnRNA interactions with the nuclear matrix.
    Cell. 1979 Dec;18(4):1079-90 PMID: 293220
  18. Number and evolutionary conservation of alpha- and beta-tubulin and cytoplasmic beta- and gamma-actin genes using specific cloned cDNA probes.
    Cell. 1980 May;20(1):95-105 PMID: 6893015
  19. Synchronization of HeLa cell cultures by inhibition of DNA polymerase alpha with aphidicolin.
    Nucleic Acids Res. 1980 Jan 25;8(2):377-87 PMID: 6775308
  20. Efficient and selective initiation by yeast RNA polymerase B in a dinucleotide-primed reaction.
    Nucleic Acids Res. 1981 Jan 10;9(1):31-45 PMID: 7010311
  21. Messenger RNA is translated when associated with the cytoskeletal framework in normal and VSV-infected HeLa cells.
    Cell. 1981 Jan;23(1):113-20 PMID: 6260369
  22. The regulation of initiation of mammalian protein synthesis.
    Prog Nucleic Acid Res Mol Biol. 1981;25:127-85 PMID: 6164076
  23. The metabolism of SV40 RNA is associated with the cytoskeletal framework.
    Virology. 1981 Jun;111(2):475-87 PMID: 6264669
  24. Progressive loss of shape-responsive metabolic controls in cells with increasingly transformed phenotype.
    Cell. 1981 Jun;24(3):859-66 PMID: 6166390
  25. Nucleotide sequences of the mRNA's encoding the vesicular stomatitis virus G and M proteins determined from cDNA clones containing the complete coding regions.
    J Virol. 1981 Aug;39(2):519-28 PMID: 6268840
  26. On the association of mRNA with the cytoskeleton in uninfected and adenovirus-infected human KB cells.
    Exp Cell Res. 1981 Sep;135(1):79-91 PMID: 7286081
  27. The role of mRNA competition in regulating translation. I. Demonstration of competition in vivo.
    J Biol Chem. 1981 Nov 25;256(22):11739-46 PMID: 7298628
  28. Molecular cloning of poliovirus cDNA and determination of the complete nucleotide sequence of the viral genome.
    Proc Natl Acad Sci U S A. 1981 Aug;78(8):4887-91 PMID: 6272282
  29. Regulation of translation in L-cells infected with reovirus.
    J Mol Biol. 1981 Sep 5;151(1):35-55 PMID: 7328654
  30. Analysis of histone gene expression during the cell cycle in HeLa cells by using cloned human histone genes.
    Proc Natl Acad Sci U S A. 1982 Feb;79(3):749-53 PMID: 6461006
  31. Association of a Mr 50,000 cap-binding protein with the cytoskeleton in baby hamster kidney cells.
    Proc Natl Acad Sci U S A. 1982 May;79(9):2927-31 PMID: 7045875
  32. Regulation of protein synthesis in vesicular stomatitis virus-infected mouse L-929 cells by decreased protein synthesis initiation factor 2 activity.
    J Virol. 1982 Mar;41(3):781-91 PMID: 6284970
  33. Decreases in tubulin and actin gene expression prior to morphological differentiation of 3T3 adipocytes.
    Cell. 1982 May;29(1):53-60 PMID: 7105184
  34. Organization of the cytoplasm.
    Cold Spring Harb Symp Quant Biol. 1982;46 Pt 2:1029-40 PMID: 6955095
  35. Translational specificity in reovirus-infected mouse fibroblasts.
    J Biol Chem. 1982 Aug 25;257(16):9855-60 PMID: 7107592
  36. Inhibition of HeLa cell protein synthesis following poliovirus infection correlates with the proteolysis of a 220,000-dalton polypeptide associated with eucaryotic initiation factor 3 and a cap binding protein complex.
    J Biol Chem. 1982 Dec 25;257(24):14806-10 PMID: 6294080
  37. New initiation factor activity required for globin mRNA translation.
    J Biol Chem. 1983 May 10;258(9):5804-10 PMID: 6853548
  38. Involvement of eukaryotic initiation factor 4A in the cap recognition process.
    J Biol Chem. 1983 Sep 25;258(18):11398-403 PMID: 6604056
  39. Cell cycle regulation of mouse H3 histone mRNA metabolism.
    Mol Cell Biol. 1984 Jan;4(1):123-32 PMID: 6583492
  40. Replication of vesicular stomatitis virus. I. Viral specific RNA and nucleoprotein in infected L cells.
    Virology. 1970 Nov;42(3):732-43 PMID: 4320668
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
Published
1985-04-00
Pages
1209-18
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2113755
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com