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PMID: 9426448 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Identification of a specific interaction between the coronavirus mouse hepatitis virus A59 nucleocapsid protein and packaging signal.

Virology ·Vol. 239 ·No. 1 ·1997-12-08 ·Pages 78-86

Molenkamp R, Spaan WJ

Abstract

The coronavirus mouse hepatitis virus (MHV) is an enveloped positive stranded RNA virus. In infected cells MHV produces a 3' coterminal nested set of subgenomic messenger RNAs. Only the genomic RNA, however, is encapsidated by the nucleocapsid protein and incorporated in infectious MHV virions. It is believed that an RNA packaging signal (Ps), present only in the genomic RNA, is responsible for this selectivity. Earlier studies mapped this signal to a 69-nt stem-loop structure positioned in the 3' end of ORF1b. The selective encapsidation mechanism probably initiates by specific interaction of the packaging signal with the nucleocapsid protein. In this study we demonstrate the in vitro interaction of the MHV-A59 nucleocapsid protein with the packaging signal of MHV using gel retardation and UV cross-linking assays. This interaction was observed not only with the nucleocapsid protein from infected cells but also with that from purified virions and from cells expressing a recombinant nucleocapsid protein. The specificity of the interaction was demonstrated by competition experiments with nonlabeled Ps containing RNAs, tRNA, and total cytoplasmic RNA. The results indicated that no virus specific modification of the N-protein or the presence of other viral proteins are required for this in vitro intervention. The assays described in this report provide us with a powerful tool for studying encapsidation (initiation) in more detail.

MeSH Terms
Animals Capsid/physiology Cell Line Coronavirus Infections/virology Genome, Viral Mice Murine hepatitis virus/physiology RNA, Messenger/physiology RNA, Viral/physiology Virus Replication
Chemicals
RNA, Messenger RNA, Viral
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Molenkamp R
Department of Virology, Institute of Medical Microbiology, Leiden University, The Netherlands.
Spaan W J
References (48)
48 references, click to expand
  1. Coronavirus mRNA synthesis involves fusion of non-contiguous sequences.
    EMBO J. 1983;2(10):1839-44 PMID: 6196191
  2. Phosphoproteins of murine hepatitis viruses.
    J Virol. 1979 Nov;32(2):672-5 PMID: 228084
  3. The internal open reading frame within the nucleocapsid gene of mouse hepatitis virus encodes a structural protein that is not essential for viral replication.
    J Virol. 1997 Feb;71(2):996-1003 PMID: 8995618
  4. Primary structure and translation of a defective interfering RNA of murine coronavirus.
    Virology. 1988 Oct;166(2):550-60 PMID: 2845661
  5. The arterivirus nsp4 protease is the prototype of a novel group of chymotrypsin-like enzymes, the 3C-like serine proteases.
    J Biol Chem. 1996 Mar 1;271(9):4864-71 PMID: 8617757
  6. Specific interaction between RNA phage coat proteins and RNA.
    Prog Nucleic Acid Res Mol Biol. 1991;40:185-220 PMID: 2031083
  7. Protein-RNA recognition.
    Annu Rev Biochem. 1995;64:593-620 PMID: 7574494
  8. The infectious bronchitis virus nucleocapsid protein binds RNA sequences in the 3' terminus of the genome.
    Virology. 1996 Mar 1;217(1):191-9 PMID: 8599203
  9. Identification of a sequence likely to be required for avian retroviral packaging.
    Virology. 1983 Jul 30;128(2):505-11 PMID: 6310871
  10. Localization of the RNA-binding domain of mouse hepatitis virus nucleocapsid protein.
    J Gen Virol. 1993 Sep;74 ( Pt 9):1975-9 PMID: 8397288
  11. Isolation of coronavirus envelope glycoproteins and interaction with the viral nucleocapsid.
    J Virol. 1980 Jan;33(1):449-62 PMID: 6245243
  12. Ribonucleoprotein-like structures from coronavirus particles.
    J Gen Virol. 1978 Jun;39(3):545-9 PMID: 207820
  13. The production of recombinant infectious DI-particles of a murine coronavirus in the absence of helper virus.
    Virology. 1996 Apr 1;218(1):52-60 PMID: 8615041
  14. cis-acting genomic elements and trans-acting proteins involved in the assembly of RNA viruses.
    . 1994 Feb;5(1):39-49 PMID: 32288439
  15. Murine coronavirus packaging signal confers packaging to nonviral RNA.
    J Virol. 1997 Jan;71(1):824-7 PMID: 8985424
  16. The alphaviruses: gene expression, replication, and evolution.
    Microbiol Rev. 1994 Sep;58(3):491-562 PMID: 7968923
  17. cis-Acting RNA packaging locus in the 115-nucleotide direct repeat of Rous sarcoma virus.
    J Virol. 1983 Dec;48(3):667-75 PMID: 6313966
  18. The transmissible gastroenteritis coronavirus contains a spherical core shell consisting of M and N proteins.
    J Virol. 1996 Jul;70(7):4773-7 PMID: 8676505
  19. Mutations of RNA and protein sequences involved in human immunodeficiency virus type 1 packaging result in production of noninfectious virus.
    J Virol. 1990 May;64(5):1920-6 PMID: 2109098
  20. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei.
    Nucleic Acids Res. 1983 Mar 11;11(5):1475-89 PMID: 6828386
  21. Sequence of the nucleocapsid gene from murine coronavirus MHV-A59.
    Nucleic Acids Res. 1983 Feb 11;11(3):883-91 PMID: 6687635
  22. Interactions between coronavirus nucleocapsid protein and viral RNAs: implications for viral transcription.
    J Virol. 1988 Nov;62(11):4280-7 PMID: 2845140
  23. Coronaviruses: structure and genome expression.
    J Gen Virol. 1988 Dec;69 ( Pt 12):2939-52 PMID: 3058868
  24. Sequence-specific recognition of RNA hairpins by bacteriophage antiterminators requires a conserved arginine-rich motif.
    Cell. 1989 Oct 6;59(1):207-18 PMID: 2477156
  25. Identification and characterization of a coronavirus packaging signal.
    J Virol. 1992 Jun;66(6):3522-30 PMID: 1316465
  26. Specificity of Rous sarcoma virus nucleocapsid protein in genomic RNA packaging.
    J Virol. 1992 Aug;66(8):4662-70 PMID: 1378506
  27. A subgenomic mRNA transcript of the coronavirus mouse hepatitis virus strain A59 defective interfering (DI) RNA is packaged when it contains the DI packaging signal.
    J Virol. 1997 Jul;71(7):5684-7 PMID: 9188649
  28. A domain at the 3' end of the polymerase gene is essential for encapsidation of coronavirus defective interfering RNAs.
    J Virol. 1991 Jun;65(6):3219-26 PMID: 2033672
  29. Specific interaction between coronavirus leader RNA and nucleocapsid protein.
    J Virol. 1988 Nov;62(11):4288-95 PMID: 2845141
  30. Cell tropism and expression of mouse hepatitis viruses (MHV) in mouse spinal cord cultures.
    Virology. 1982 Jun;119(2):317-31 PMID: 6281976
  31. Evidence for specificity in the encapsidation of Sindbis virus RNAs.
    J Virol. 1989 Dec;63(12):5310-8 PMID: 2585607
  32. Nucleocapsid-independent assembly of coronavirus-like particles by co-expression of viral envelope protein genes.
    EMBO J. 1996 Apr 15;15(8):2020-8 PMID: 8617249
  33. Characterization of leader RNA sequences on the virion and mRNAs of mouse hepatitis virus, a cytoplasmic RNA virus.
    Proc Natl Acad Sci U S A. 1984 Jun;81(12):3626-30 PMID: 6328522
  34. Endosomal association of a protein phosphatase with high dephosphorylating activity against a coronavirus nucleocapsid protein.
    FEBS Lett. 1991 May 6;282(2):419-24 PMID: 1674698
  35. Membrane and phospholipid binding by murine coronaviral nucleocapsid N protein.
    Virology. 1993 May;194(1):224-32 PMID: 7683155
  36. Antigenic variation among murine coronaviruses: evidence for polymorphism on the peplomer glycoprotein, E2.
    Virus Res. 1985 Jun;2(4):317-28 PMID: 2412363
  37. Sequence- and structure-specific determinants in the interaction between the RNA encapsidation signal and reverse transcriptase of avian hepatitis B viruses.
    J Virol. 1997 Jul;71(7):4971-80 PMID: 9188560
  38. Isolation and identification of virus-specific mRNAs in cells infected with mouse hepatitis virus (MHV-A59).
    Virology. 1981 Jan 30;108(2):424-34 PMID: 6258295
  39. Conserved structures and diversity of functions of RNA-binding proteins.
    Science. 1994 Jul 29;265(5172):615-21 PMID: 8036511
  40. Retroviral nucleocapsid domains mediate the specific recognition of genomic viral RNAs by chimeric Gag polyproteins during RNA packaging in vivo.
    J Virol. 1995 Oct;69(10):6445-56 PMID: 7666546
  41. Localization of an RNA-binding domain in the nucleocapsid protein of the coronavirus mouse hepatitis virus.
    Arch Virol. 1992;125(1-4):141-60 PMID: 1322650
  42. Evolution of a coronavirus during persistent infection in vitro.
    Adv Exp Med Biol. 1981;142:287-99 PMID: 6278887
  43. Sequence comparison of the N genes of five strains of the coronavirus mouse hepatitis virus suggests a three domain structure for the nucleocapsid protein.
    Virology. 1990 Nov;179(1):463-8 PMID: 2171216
  44. Specificity of ribonucleoprotein interaction determined by RNA folding during complex formulation.
    Nature. 1996 Apr 18;380(6575):646-50 PMID: 8602269
  45. Nucleocapsid protein effects on the specificity of retrovirus RNA encapsidation.
    J Virol. 1995 Sep;69(9):5716-22 PMID: 7637017
  46. Synthesis and subcellular localization of the murine coronavirus nucleocapsid protein.
    Virology. 1983 Oct 30;130(2):527-32 PMID: 6196910
  47. Identification of a region in the Sindbis virus nucleocapsid protein that is involved in specificity of RNA encapsidation.
    J Virol. 1996 May;70(5):2757-63 PMID: 8627749
  48. Characterization of two temperature-sensitive mutants of coronavirus mouse hepatitis virus strain A59 with maturation defects in the spike protein.
    J Virol. 1997 Feb;71(2):949-55 PMID: 8995612
Article Info
Journal
Virology
Abbr.
Virology
ISSN
0042-6822
Published
1997-12-08
Pages
78-86
Language
English
Region
United States
NLM ID
0110674
PMCID
PMC7130520
Subset
IM
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