Abstract
The hepatitis C virus RNA genome encodes a long polyprotein that is proteolytically processed into at least 10 products. The order of these cleavage products in the polyprotein is NH2-C-E1-E2-p7-NS2-NS3-NS4A-NS4B-NS5A-NS5B -COOH. A serine proteinase domain located in the N-terminal one-third of nonstructural protein NS3 mediates cleavage at four downstream sites (the 3/4A, 4A/4B, 4B/5A, and 5A/5B sites). In addition to the proteinase catalytic domain, the NS4A protein is required for processing at the 4B/5A site but not at the 5A/5B site. These cleavage events are likely to be essential for virus replication, making the serine proteinase an attractive antiviral target. Here we describe an in vitro assay where the NS3-4A polyprotein, NS3, the serine proteinase domain (the N-terminal 181 residues of NS3), and the NS4A cofactor were produced by cell-free translation and tested for trans-processing of radiolabeled substrates. Polyprotein substrates, NS4A-4B or truncated NS5A-5B, were cleaved in trans by all forms of the proteinase, whereas NS4A was also required for NS4B-5A processing. Proteolysis was abolished by substitution mutations previously shown to inactivate the proteinase or block cleavage at specific sites in vivo. Furthermore, N-terminal sequence analysis established that cleavage in vitro occurred at the authentic 4A/4B site. Translation in the presence of microsomal membranes enhanced processing for some, but not all, proteinase-substrate combinations. Trans-processing was both time and temperature dependent and was eliminated by treatment with a variety of detergents above their critical micelle concentrations. Among many common proteinase inhibitors tested, only high (millimolar) concentrations of serine proteinase inhibitors tosyllysyl chloromethyl ketone and 4-(2-aminoethyl)benzenesulfonyl fluoride inactivated the NS3 proteinase. This in vitro assay should facilitate purification and further characterization of the viral serine proteinase and identification of molecules which selectively inhibit its activity.
MeSH Terms
Animals
Cell-Free System
Gene Expression
Genome, Viral
Hepacivirus/genetics,metabolism
Intracellular Membranes/metabolism
Kinetics
Microsomes/metabolism
Protease Inhibitors/pharmacology
Protein Biosynthesis
Rabbits
Reticulocytes/metabolism
Transcription, Genetic
Viral Nonstructural Proteins/biosynthesis,metabolism
Chemicals
NS3 protein, hepatitis C virus
NS4 protein, hepatitis C virus
Protease Inhibitors
Viral Nonstructural Proteins
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Lin C
Department of Molecular Microbiology, Washington University School of Medicine, St. Louis, MO 63110-1093, USA.
Rice C M
References (20)
20 references, click to expand
-
A segment of the 5' nontranslated region of encephalomyocarditis virus RNA directs internal entry of ribosomes during in vitro translation.
J Virol. 1988 Aug;62(8):2636-43
PMID: 2839690
-
A central region in the hepatitis C virus NS4A protein allows formation of an active NS3-NS4A serine proteinase complex in vivo and in vitro.
J Virol. 1995 Jul;69(7):4373-80
PMID: 7769699
-
An assay for circulating antibodies to a major etiologic virus of human non-A, non-B hepatitis.
Science. 1989 Apr 21;244(4902):362-4
PMID: 2496467
-
Risk factors for acute non-A, non-B hepatitis in the United States and association with hepatitis C virus infection.
JAMA. 1990 Nov 7;264(17):2231-5
PMID: 2170702
-
Characterization of the hepatitis C virus-encoded serine proteinase: determination of proteinase-dependent polyprotein cleavage sites.
J Virol. 1993 May;67(5):2832-43
PMID: 8386278
-
The hepatitis C virus encodes a serine protease involved in processing of the putative nonstructural proteins from the viral polyprotein precursor.
Biochem Biophys Res Commun. 1993 Apr 30;192(2):399-406
PMID: 8387277
-
Nonstructural protein 3 of the hepatitis C virus encodes a serine-type proteinase required for cleavage at the NS3/4 and NS4/5 junctions.
J Virol. 1993 Jul;67(7):3835-44
PMID: 8389908
-
NS3 is a serine protease required for processing of hepatitis C virus polyprotein.
J Virol. 1993 Jul;67(7):4017-26
PMID: 7685406
-
Two distinct proteinase activities required for the processing of a putative nonstructural precursor protein of hepatitis C virus.
J Virol. 1993 Aug;67(8):4665-75
PMID: 8392606
-
Proteolytic processing and membrane association of putative nonstructural proteins of hepatitis C virus.
Proc Natl Acad Sci U S A. 1993 Nov 15;90(22):10773-7
PMID: 7504283
-
Production of nonstructural proteins of hepatitis C virus requires a putative viral protease encoded by NS3.
Virology. 1994 Feb;198(2):636-44
PMID: 8291245
-
Molecular model of the specificity pocket of the hepatitis C virus protease: implications for substrate recognition.
Proc Natl Acad Sci U S A. 1994 Feb 1;91(3):888-92
PMID: 8302861
-
Both NS3 and NS4A are required for proteolytic processing of hepatitis C virus nonstructural proteins.
J Virol. 1994 Jun;68(6):3753-60
PMID: 8189513
-
NS2B-3 proteinase-mediated processing in the yellow fever virus structural region: in vitro and in vivo studies.
J Virol. 1994 Jun;68(6):3794-802
PMID: 8189517
-
Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
Nature. 1970 Aug 15;227(5259):680-5
PMID: 5432063
-
Production of infectious RNA transcripts from Sindbis virus cDNA clones: mapping of lethal mutations, rescue of a temperature-sensitive marker, and in vitro mutagenesis to generate defined mutants.
J Virol. 1987 Dec;61(12):3809-19
PMID: 3479621
-
Kinetic and structural analyses of hepatitis C virus polyprotein processing.
J Virol. 1994 Aug;68(8):5045-55
PMID: 8035505
-
Specificity of the hepatitis C virus NS3 serine protease: effects of substitutions at the 3/4A, 4A/4B, 4B/5A, and 5A/5B cleavage sites on polyprotein processing.
J Virol. 1994 Nov;68(11):7525-33
PMID: 7933136
-
Hepatitis C virus NS3 serine proteinase: trans-cleavage requirements and processing kinetics.
J Virol. 1994 Dec;68(12):8147-57
PMID: 7966606
-
Isolation of a cDNA clone derived from a blood-borne non-A, non-B viral hepatitis genome.
Science. 1989 Apr 21;244(4902):359-62
PMID: 2523562