Home LiteratureArticle Details
PMID: 10708442 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

cis- and trans-acting elements in flavivirus RNA replication.

Journal of virology ·Vol. 74 ·No. 7 ·2000-04-00 ·Pages 3253-63

Khromykh AA, Sedlak PL, Westaway EG

Abstract

Most of the seven flavivirus nonstructural proteins (NS1 to NS5) encoded in the distal two-thirds of the RNA positive-sense genome are believed to be essential components of RNA replication complexes. To explore the functional relationships of these components in RNA replication, we used trans-complementation analysis of full-length infectious RNAs of Kunjin (KUN) virus with a range of lethal in-frame deletions in the nonstructural coding region, using as helper a repBHK cell line stably producing functional replication complexes from KUN replicon RNA. Recently we showed that replication of KUN RNAs with large carboxy-terminal deletions including the entire RNA polymerase region in the NS5 gene, representing 34 to 75% of the NS5 coding content, could be complemented after transfection into repBHK cells. In this study we have demonstrated that KUN RNAs with deletions of 84 to 97% of the NS1 gene, or of 13 to 63% of the NS3 gene including the entire helicase region, were also complemented in repBHK cells with variable efficiencies. In contrast, KUN RNAs with deletions in any of the other four nonstructural genes NS2A, NS2B, NS4A, and NS4B were not complemented. We have also demonstrated successful trans complementation of KUN RNAs containing either combined double deletions in the NS1 and NS5 genes or triple deletions in the NS1, NS3, and NS5 genes comprising as much as 38% of the entire nonstructural coding content. Based on these and our previous complementation results, we have generated a map of cis- and trans-acting elements in RNA replication for the nonstructural coding region of the flavivirus genome. These results are discussed in the context of our model on formation and composition of the flavivirus replication complex, and we suggest molecular mechanisms by which functions of some defective components of the replication complex can be complemented by their wild-type counterparts expressed from another (helper) RNA molecule.

MeSH Terms
Animals Cell Line Cricetinae Flavivirus/genetics Genetic Complementation Test RNA, Viral/biosynthesis Sequence Deletion Viral Nonstructural Proteins/genetics
Chemicals
RNA, Viral Viral Nonstructural Proteins
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Khromykh A A
Sir Albert Sakzewski Virus Research Centre, Royal Children's Hospital, Brisbane, Queensland 4029, Australia. a.khromykh@mailbox.uq.edu.au
Sedlak P L
Westaway E G
References (46)
46 references, click to expand
  1. The serine protease and RNA-stimulated nucleoside triphosphatase and RNA helicase functional domains of dengue virus type 2 NS3 converge within a region of 20 amino acids.
    J Virol. 1999 Apr;73(4):3108-16 PMID: 10074162
  2. Genetic analysis of the yellow fever virus NS1 protein: identification of a temperature-sensitive mutation which blocks RNA accumulation.
    J Virol. 1997 Jan;71(1):291-8 PMID: 8985349
  3. Nascent flavivirus RNA colocalized in situ with double-stranded RNA in stable replication complexes.
    Virology. 1999 May 25;258(1):108-17 PMID: 10329573
  4. Homology model of the dengue 2 virus NS3 protease: putative interactions with both substrate and NS2B cofactor.
    J Gen Virol. 1999 May;80 ( Pt 5):1167-77 PMID: 10355763
  5. Mutagenesis of the NS2B-NS3-mediated cleavage site in the flavivirus capsid protein demonstrates a requirement for coordinated processing.
    J Virol. 1999 Oct;73(10):8083-94 PMID: 10482557
  6. trans-Complementation analysis of the flavivirus Kunjin ns5 gene reveals an essential role for translation of its N-terminal half in RNA replication.
    J Virol. 1999 Nov;73(11):9247-55 PMID: 10516033
  7. Efficient trans-complementation of the flavivirus kunjin NS5 protein but not of the NS1 protein requires its coexpression with other components of the viral replicase.
    J Virol. 1999 Dec;73(12):10272-80 PMID: 10559344
  8. Replication strategy of Kunjin virus: evidence for recycling role of replicative form RNA as template in semiconservative and asymmetric replication.
    Virology. 1985 Jan 15;140(1):68-79 PMID: 2578239
  9. Characterization of Kunjin virus RNA-dependent RNA polymerase: reinitiation of synthesis in vitro.
    Virology. 1987 Apr;157(2):330-7 PMID: 3029975
  10. Nucleotide and complete amino acid sequences of Kunjin virus: definitive gene order and characteristics of the virus-specified proteins.
    J Gen Virol. 1988 Jan;69 ( Pt 1):1-21 PMID: 2826659
  11. Translation mapping with the flavivirus Kunjin: gene order and anomalies in translation of Ns5.
    Virus Res. 1988 Mar;9(4):323-33 PMID: 2837017
  12. N-terminal domains of putative helicases of flavi- and pestiviruses may be serine proteases.
    Nucleic Acids Res. 1989 May 25;17(10):3889-97 PMID: 2543956
  13. Two related superfamilies of putative helicases involved in replication, recombination, repair and expression of DNA and RNA genomes.
    Nucleic Acids Res. 1989 Jun 26;17(12):4713-30 PMID: 2546125
  14. Carboxy-terminal analysis of nine proteins specified by the flavivirus Kunjin: evidence that only the intracellular core protein is truncated.
    J Gen Virol. 1989 Aug;70 ( Pt 8):2209-14 PMID: 2549188
  15. Cleavage of dengue virus NS1-NS2A requires an octapeptide sequence at the C terminus of NS1.
    J Virol. 1990 Sep;64(9):4573-7 PMID: 2143546
  16. Both nonstructural proteins NS2B and NS3 are required for the proteolytic processing of dengue virus nonstructural proteins.
    J Virol. 1991 May;65(5):2467-75 PMID: 2016768
  17. The phylogeny of RNA-dependent RNA polymerases of positive-strand RNA viruses.
    J Gen Virol. 1991 Sep;72 ( Pt 9):2197-206 PMID: 1895057
  18. Processing of the yellow fever virus nonstructural polyprotein: a catalytically active NS3 proteinase domain and NS2B are required for cleavages at dibasic sites.
    J Virol. 1991 Nov;65(11):6042-50 PMID: 1833562
  19. A short form of the tick-borne encephalitis virus NS3 protein.
    FEBS Lett. 1992 Feb 3;297(1-2):67-9 PMID: 1551439
  20. Identification and characterization of a coronavirus packaging signal.
    J Virol. 1992 Jun;66(6):3522-30 PMID: 1316465
  21. Molecular and ultrastructural analysis of heavy membrane fractions associated with the replication of Kunjin virus RNA.
    Arch Virol. 1992;125(1-4):177-91 PMID: 1322651
  22. Mutational analysis of the octapeptide sequence motif at the NS1-NS2A cleavage junction of dengue type 4 virus.
    J Virol. 1992 Dec;66(12):7225-31 PMID: 1433515
  23. Dengue 2 virus NS2B and NS3 form a stable complex that can cleave NS3 within the helicase domain.
    Virology. 1993 Apr;193(2):888-99 PMID: 8460492
  24. Subgenomic replicons of the flavivirus Kunjin: construction and applications.
    J Virol. 1997 Feb;71(2):1497-505 PMID: 8995675
  25. Internal proteolysis of the NS3 protein specified by dengue virus 2.
    J Gen Virol. 1997 Feb;78 ( Pt 2):337-41 PMID: 9018055
  26. RNA-protein interactions: involvement of NS3, NS5, and 3' noncoding regions of Japanese encephalitis virus genomic RNA.
    J Virol. 1997 May;71(5):3466-73 PMID: 9094618
  27. Proteins C and NS4B of the flavivirus Kunjin translocate independently into the nucleus.
    Virology. 1997 Jul 21;234(1):31-41 PMID: 9234944
  28. Ultrastructure of Kunjin virus-infected cells: colocalization of NS1 and NS3 with double-stranded RNA, and of NS2B with NS3, in virus-induced membrane structures.
    J Virol. 1997 Sep;71(9):6650-61 PMID: 9261387
  29. trans-Complementation of yellow fever virus NS1 reveals a role in early RNA replication.
    J Virol. 1997 Dec;71(12):9608-17 PMID: 9371625
  30. Signal peptidase cleavage at the flavivirus C-prM junction: dependence on the viral NS2B-3 protease for efficient processing requires determinants in C, the signal peptide, and prM.
    J Virol. 1998 Mar;72(3):2141-9 PMID: 9499070
  31. Deletion analysis of a defective interfering Semliki Forest virus RNA genome defines a region in the nsP2 sequence that is required for efficient packaging of the genome into virus particles.
    J Virol. 1998 May;72(5):4320-6 PMID: 9557722
  32. Virus-encoded proteinases of the Flaviviridae.
    J Gen Virol. 1998 May;79 ( Pt 5):947-59 PMID: 9603310
  33. Subcellular localization and some biochemical properties of the flavivirus Kunjin nonstructural proteins NS2A and NS4A.
    Virology. 1998 Jun 5;245(2):203-15 PMID: 9636360
  34. trans-Complementation of flavivirus RNA polymerase gene NS5 by using Kunjin virus replicon-expressing BHK cells.
    J Virol. 1998 Sep;72(9):7270-9 PMID: 9696822
  35. Analysis of RNA-dependent RNA polymerase structure and function as guided by known polymerase structures and computer predictions of secondary structure.
    Virology. 1998 Dec 20;252(2):287-303 PMID: 9878607
  36. Computer-assisted identification of a putative methyltransferase domain in NS5 protein of flaviviruses and lambda 2 protein of reovirus.
    J Gen Virol. 1993 Apr;74 ( Pt 4):733-40 PMID: 8385698
  37. Mutagenesis of the yellow fever virus NS2B protein: effects on proteolytic processing, NS2B-NS3 complex formation, and viral replication.
    J Virol. 1993 Nov;67(11):6797-807 PMID: 8411382
  38. The NS 3 nonstructural protein of flaviviruses contains an RNA triphosphatase activity.
    Virology. 1993 Nov;197(1):265-73 PMID: 8212562
  39. Completion of Kunjin virus RNA sequence and recovery of an infectious RNA transcribed from stably cloned full-length cDNA.
    J Virol. 1994 Jul;68(7):4580-8 PMID: 8207832
  40. Formation of the flavivirus envelope: role of the viral NS2B-NS3 protease.
    J Virol. 1995 Apr;69(4):1995-2003 PMID: 7884844
  41. Association between NS3 and NS5 proteins of dengue virus type 2 in the putative RNA replicase is linked to differential phosphorylation of NS5.
    J Biol Chem. 1995 Aug 11;270(32):19100-6 PMID: 7642575
  42. Evidence that flavivirus NS1-NS2A cleavage is mediated by a membrane-bound host protease in the endoplasmic reticulum.
    J Virol. 1995 Nov;69(11):7232-43 PMID: 7474145
  43. Recombinant dengue type 1 virus NS5 protein expressed in Escherichia coli exhibits RNA-dependent RNA polymerase activity.
    Virology. 1996 Feb 15;216(2):317-25 PMID: 8607261
  44. Immunolocalization of the dengue virus nonstructural glycoprotein NS1 suggests a role in viral RNA replication.
    Virology. 1996 Jun 1;220(1):232-40 PMID: 8659120
  45. Packaging signals in alphaviruses.
    J Virol. 1997 Jan;71(1):248-58 PMID: 8985344
  46. Genetic interaction of flavivirus nonstructural proteins NS1 and NS4A as a determinant of replicase function.
    J Virol. 1999 Jun;73(6):4611-21 PMID: 10233920
Article Info
Journal
Journal of virology
Abbr.
J Virol
ISSN
0022-538X
Published
2000-04-00
Pages
3253-63
Language
English
Region
United States
NLM ID
0113724
PMCID
PMC111826
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