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PMID: 11463383 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Poliovirus RNA replication requires genome circularization through a protein-protein bridge.

Molecular cell ·Vol. 7 ·No. 3 ·2001-03-00 ·Pages 581-91

Herold J, Andino R

Abstract

The mechanisms and factors involved in the replication of positive stranded RNA viruses are still unclear. Using poliovirus as a model, we show that a long-range interaction between ribonucleoprotein (RNP) complexes formed at the ends of the viral genome is necessary for RNA replication. Initiation of negative strand RNA synthesis requires a 3' poly(A) tail. Strikingly, it also requires a cloverleaf-like RNA structure located at the other end of the genome. An RNP complex formed around the 5' cloverleaf RNA structure interacts with the poly(A) binding protein bound to the 3' poly(A) tail, thus linking the ends of the viral RNA and effectively circularizing it. Formation of this circular RNP complex is required for initiation of negative strand RNA synthesis. RNA circularization may be a general replication mechanism for positive stranded RNA viruses.

MeSH Terms
Base Sequence Cell Line Cross-Linking Reagents DNA, Circular/chemistry,genetics,metabolism DNA-Binding Proteins Genome, Viral Heterogeneous-Nuclear Ribonucleoproteins Humans Mutation/genetics Nucleic Acid Conformation Poliovirus/genetics Poly A/genetics,metabolism Poly(A)-Binding Proteins Protein Binding RNA, Messenger/chemistry,genetics,metabolism RNA, Viral/biosynthesis,genetics,metabolism RNA-Binding Proteins/genetics,metabolism Regulatory Sequences, Nucleic Acid/genetics Ribonucleoproteins/genetics,metabolism Virus Replication/genetics,physiology
Chemicals
Cross-Linking Reagents DNA, Circular DNA-Binding Proteins Heterogeneous-Nuclear Ribonucleoproteins PCBP1 protein, human Poly(A)-Binding Proteins RNA, Messenger RNA, Viral RNA-Binding Proteins Ribonucleoproteins Poly A
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Herold J
Department of Microbiology and Immunology, University of California, San Francisco, 94143, USA.
Andino R
References (53)
53 references, click to expand
  1. In vivo addition of poly(A) tail and AU-rich sequences to the 3' terminus of the Sindbis virus RNA genome: a novel 3'-end repair pathway.
    J Virol. 1999 Mar;73(3):2410-9 PMID: 9971825
  2. Poly(A) tail metabolism and function in eucaryotes.
    J Biol Chem. 1993 Nov 5;268(31):22955-8 PMID: 8226806
  3. Identification of two KH domain proteins in the alpha-globin mRNP stability complex.
    EMBO J. 1995 Sep 1;14(17):4357-64 PMID: 7556077
  4. Cis-element, oriR, involved in the initiation of (-) strand poliovirus RNA: a quasi-globular multi-domain RNA structure maintained by tertiary ('kissing') interactions.
    EMBO J. 1996 Oct 1;15(19):5428-36 PMID: 8895586
  5. The structure of poliovirus replicative form.
    Nucleic Acids Res. 1980 Mar 25;8(6):1217-29 PMID: 6253931
  6. A novel in vitro replication system for Dengue virus. Initiation of RNA synthesis at the 3'-end of exogenous viral RNA templates requires 5'- and 3'-terminal complementary sequence motifs of the viral RNA.
    J Biol Chem. 1999 Nov 19;274(47):33714-22 PMID: 10559263
  7. Switch from translation to RNA replication in a positive-stranded RNA virus.
    Genes Dev. 1998 Aug 1;12(15):2293-304 PMID: 9694795
  8. eIF4 initiation factors: effectors of mRNA recruitment to ribosomes and regulators of translation.
    Annu Rev Biochem. 1999;68:913-63 PMID: 10872469
  9. Translation in mammalian cells of a gene linked to the poliovirus 5' noncoding region.
    Science. 1988 Jul 22;241(4864):445-8 PMID: 2839901
  10. Polyadenylic acid at the 3'-terminus of poliovirus RNA.
    Proc Natl Acad Sci U S A. 1972 Jul;69(7):1877-82 PMID: 4340162
  11. Starting at the beginning, middle, and end: translation initiation in eukaryotes.
    Cell. 1997 Jun 13;89(6):831-8 PMID: 9200601
  12. A stem-loop motif formed by the immediate 5' terminus of the bovine viral diarrhea virus genome modulates translation as well as replication of the viral RNA.
    J Virol. 2000 Jul;74(13):5825-35 PMID: 10846062
  13. Poliovirus requires a precise 5' end for efficient positive-strand RNA synthesis.
    J Virol. 2000 Jul;74(14):6394-400 PMID: 10864650
  14. Sufficient length of a poly(A) tail for the formation of a potential pseudoknot is required for efficient replication of bamboo mosaic potexvirus RNA.
    J Virol. 1999 Apr;73(4):2703-9 PMID: 10074116
  15. Substitutions in the protease (3Cpro) gene of poliovirus can suppress a mutation in the 5' noncoding region.
    J Virol. 1990 Feb;64(2):607-12 PMID: 2153227
  16. Poliovirus RNA synthesis utilizes an RNP complex formed around the 5'-end of viral RNA.
    EMBO J. 1993 Sep;12(9):3587-98 PMID: 8253083
  17. Cleavage of poly(A)-binding protein by enterovirus proteases concurrent with inhibition of translation in vitro.
    J Virol. 1999 Jan;73(1):718-27 PMID: 9847378
  18. A long-range interaction in Qbeta RNA that bridges the thousand nucleotides between the M-site and the 3' end is required for replication.
    RNA. 1998 Aug;4(8):948-57 PMID: 9701286
  19. 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
  20. The 5'-untranslated regions of picornavirus RNAs contain independent functional domains essential for RNA replication and translation.
    J Virol. 1994 Jul;68(7):4384-91 PMID: 8207812
  21. Complete replication of poliovirus in vitro: preinitiation RNA replication complexes require soluble cellular factors for the synthesis of VPg-linked RNA.
    J Virol. 1995 Sep;69(9):5516-27 PMID: 7636997
  22. Xenopus poly(A) binding protein: functional domains in RNA binding and protein-protein interaction.
    J Mol Biol. 1996 Feb 16;256(1):20-30 PMID: 8609610
  23. A long-range pseudoknot in Qbeta RNA is essential for replication.
    J Mol Biol. 1999 Dec 10;294(4):875-84 PMID: 10588893
  24. Cap-independent translation of poliovirus mRNA is conferred by sequence elements within the 5' noncoding region.
    Mol Cell Biol. 1988 Mar;8(3):1103-12 PMID: 2835660
  25. Two functional complexes formed by KH domain containing proteins with the 5' noncoding region of poliovirus RNA.
    RNA. 1997 Aug;3(8):882-92 PMID: 9257647
  26. An mRNA stability complex functions with poly(A)-binding protein to stabilize mRNA in vitro.
    Mol Cell Biol. 1999 Jul;19(7):4552-60 PMID: 10373504
  27. Replication-competent picornaviruses with complete genomic RNA 3' noncoding region deletions.
    J Virol. 1997 Nov;71(11):8868-74 PMID: 9343250
  28. A protein covalently linked to poliovirus genome RNA.
    Proc Natl Acad Sci U S A. 1977 Jan;74(1):59-63 PMID: 189316
  29. Assays for poliovirus polymerase, 3D(Pol), and authentic RNA replication in HeLa S10 extracts.
    Methods Enzymol. 1996;275:35-57 PMID: 9026649
  30. Covalent linkage of a protein to a defined nucleotide sequence at the 5'-terminus of virion and replicative intermediate RNAs of poliovirus.
    Proc Natl Acad Sci U S A. 1977 Mar;74(3):961-5 PMID: 191841
  31. Recognition of polyadenylate RNA by the poly(A)-binding protein.
    Cell. 1999 Sep 17;98(6):835-45 PMID: 10499800
  32. Cell-free, de novo synthesis of poliovirus.
    Science. 1991 Dec 13;254(5038):1647-51 PMID: 1661029
  33. A functional ribonucleoprotein complex forms around the 5' end of poliovirus RNA.
    Cell. 1990 Oct 19;63(2):369-80 PMID: 2170027
  34. Role of 3'-end sequences in infectivity of poliovirus transcripts made in vitro.
    J Virol. 1989 Jan;63(1):467-70 PMID: 2535751
  35. Circularization of mRNA by eukaryotic translation initiation factors.
    Mol Cell. 1998 Jul;2(1):135-40 PMID: 9702200
  36. Poly (rC) binding protein 2 forms a ternary complex with the 5'-terminal sequences of poliovirus RNA and the viral 3CD proteinase.
    RNA. 1997 Oct;3(10):1124-34 PMID: 9326487
  37. Identification and characterization of a host protein required for efficient template selection in viral RNA replication.
    Proc Natl Acad Sci U S A. 2000 Apr 11;97(8):3913-8 PMID: 10759565
  38. The 3' untranslated region of picornavirus RNA: features required for efficient genome replication.
    J Virol. 1995 Dec;69(12):7835-44 PMID: 7494295
  39. The N-terminal K homology domain of the poly(rC)-binding protein is a major determinant for binding to the poliovirus 5'-untranslated region and acts as an inhibitor of viral translation.
    J Biol Chem. 1999 Dec 31;274(53):38163-70 PMID: 10608888
  40. The mRNA poly(A)-binding protein: localization, abundance, and RNA-binding specificity.
    Exp Cell Res. 1994 Apr;211(2):400-7 PMID: 7908267
  41. Studies on the function of polyadenylic acid on poliovirus RNA.
    Cell. 1975 Sep;6(1):41-4 PMID: 170001
  42. Host protein interactions with the 3' end of bovine coronavirus RNA and the requirement of the poly(A) tail for coronavirus defective genome replication.
    J Virol. 2000 Jun;74(11):5053-65 PMID: 10799579
  43. Comparison of the replication of positive-stranded RNA viruses of plants and animals.
    Adv Virus Res. 1996;47:159-251 PMID: 8895833
  44. Characterization of DP103, a novel DEAD box protein that binds to the Epstein-Barr virus nuclear proteins EBNA2 and EBNA3C.
    J Biol Chem. 1999 Jul 2;274(27):19136-44 PMID: 10383418
  45. An RNA hairpin at the extreme 5' end of the poliovirus RNA genome modulates viral translation in human cells.
    J Virol. 1991 Feb;65(2):913-21 PMID: 1846205
  46. Conserved elements in the 3' untranslated region of flavivirus RNAs and potential cyclization sequences.
    J Mol Biol. 1987 Nov 5;198(1):33-41 PMID: 2828633
  47. 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
  48. A human RNA viral cysteine proteinase that depends upon a unique Zn2+-binding finger connecting the two domains of a papain-like fold .
    J Biol Chem. 1999 May 21;274(21):14918-25 PMID: 10329692
  49. Replication of poliovirus in Xenopus oocytes requires two human factors.
    EMBO J. 1996 Nov 1;15(21):5988-98 PMID: 8918476
  50. Translating ribosomes inhibit poliovirus negative-strand RNA synthesis.
    J Virol. 1999 Dec;73(12):10104-12 PMID: 10559325
  51. Cleavage of Poly(A)-binding protein by coxsackievirus 2A protease in vitro and in vivo: another mechanism for host protein synthesis shutoff?
    J Virol. 1999 Jan;73(1):709-17 PMID: 9847377
  52. Cytoplasmic regulatory functions of the KH-domain proteins hnRNPs K and E1/E2.
    Trends Biochem Sci. 1998 Nov;23(11):409-11 PMID: 9852755
  53. Protein-primed RNA synthesis by purified poliovirus RNA polymerase.
    Nature. 1998 May 21;393(6682):280-4 PMID: 9607767
Article Info
Journal
Molecular cell
Abbr.
Mol Cell
ISSN
1097-2765
Published
2001-03-00
Pages
581-91
Language
English
Region
United States
NLM ID
9802571
PMCID
PMC7129834
Subset
IM
Grants
NIAID NIH HHS · N01AI40085 · United States
NIAID NIH HHS · AI 40085 · United States
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