Structural analysis of hepatitis C virus core-E1 signal peptide and requirements for cleavage of the genotype 3a signal sequence by signal peptide peptidase

Journal of Virology

Volumn 86, Issue 15, 2012, Pages 7818-7828

  Oehler, Verena ^a   Filipe, Ana ^a   Montserret, Roland ^b   da Costa, Daniel ^a   Brown, Gaie ^a   Penin, François ^a,b   McLauchlan, John ^a  

^a MRC UNIVERSITY OF GLASGOW CENTRE FOR VIRUS RESEARCH   (United Kingdom)

^b UNIVERSITÉ DE LYON   (France)

Author keywords

[No Author keywords available]

Indexed keywords

HISTIDINE; PEPTIDASE;

AMINO ACID ANALYSIS; ARTICLE; CIRCULAR DICHROISM; GENE MUTATION; GENE SEQUENCE; GENE SILENCING; GENOTYPE; HEPATITIS C VIRUS; MUTATIONAL ANALYSIS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN CONFORMATION; PROTEIN DEGRADATION; PROTEIN PROCESSING; SIGNAL TRANSDUCTION; STRUCTURE ANALYSIS; VIRUS MORPHOLOGY; VIRUS PARTICLE;

ASPARTIC ACID ENDOPEPTIDASES; HEK293 CELLS; HEPACIVIRUS; HEPATITIS C; HUMANS; MUTAGENESIS; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN SORTING SIGNALS; VIRAL CORE PROTEINS;

HEPATITIS C VIRUS;

EID: 84864391185     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00457-12     Document Type: Article

References (57)

1. Ait-Goughoulte M, et al. 2006. Core protein cleavage by signal peptide peptidase is required for hepatitis C virus-like particle assembly. J. Gen. Virol. 87:855-860.
2. Bland FA, Lemberg MK, McMichael AJ, Martoglio B, Braud VM. 2003. Requirement of the proteasome for the trimming of signal peptidederived epitopes presented by the nonclassical major histocompatibility complex class I molecule HLA-E. J. Biol. Chem. 278:33747-33752.
3. Boulant S, et al. 2006. Structural determinants that target the hepatitis C virus core protein to lipid droplets. J. Biol. Chem. 281:22236-22247.
4. Boulant S, Targett-Adams P, McLauchlan J. 2007. Disrupting the association of hepatitis C virus core protein with lipid droplets correlates with a loss in production of infectious virus. J. Gen. Virol. 88:2204-2213.
5. Buck M. 1998. Trifluoroethanol and colleagues: cosolvents come of age. Recent studies with peptides and proteins. Q. Rev. Biophys. 31:297-355.
6. Clayton RF, et al. 2002. Analysis of antigenicity and topology of E2 glycoprotein present on recombinant hepatitis C virus-like particles. J. Virol. 76:7672-7682.
7. Delgrange D, et al. 2007. Robust production of infectious viral particles in Huh-7 cells by introducing mutations in hepatitis C virus structural proteins. J. Gen. Virol. 88:2495-2503.
8. Di Bisceglie AM. 1997. Hepatitis C and hepatocellular carcinoma. Hepatology 26:34S-38S.
9. Everett RD, Parada C, Gripon P, Sirma H, Orr A. 2008. Replication of ICP0-null mutant herpes simplex virus type 1 is restricted by both PML and Sp100. J. Virol. 82:2661-2672.
10. Favier A, et al. 2002. Solution structure and dynamics of crh, the Bacillus subtilis catabolite repression HPr. J. Mol. Biol. 317:131-144.
11. Health Protection Agency. 2011. Hepatitis C in the UK: 2011 report. Health Protection Agency, London, United Kingdom.
12. Hofer H, et al. 2002. Hepatocellular fat accumulation and low serum cholesterol in patients infected with HCV-3a. Am. J. Gastroenterol. 97: 2880-2885.
13. Hope RG, McElwee MJ, McLauchlan J. 2006. Efficient cleavage by signal peptide peptidase requires residues within the signal peptide between the core and E1 proteins of hepatitis C virus strain J1. J. Gen. Virol. 87:623-627.
14. Hope RG, McLauchlan J. 2000. Sequence motifs required for lipid droplet association and protein stability are unique to the hepatitis C virus core protein. J. Gen. Virol. 81:1913-1925.
15. Humphrey W, Dalke A, Schulten K. 1996. VMD: visual molecular dynamics. J. Mol. Graph. 14:33-38, 27-28.
16. Hussy P, Langen H, Mous J, Jacobsen H. 1996. Hepatitis C virus core protein: carboxy-terminal boundaries of two processed species suggest cleavage by a signal peptide peptidase. Virology 224:93-104.
17. Jhaveri R, McHutchison J, Patel K, Qiang G, Diehl AM. 2008. Specific polymorphisms in hepatitis C virus genotype 3 core protein associated with intracellular lipid accumulation. J. Infect. Dis. 197:283-291.
18. Kopp M, Murray CL, Jones CT, Rice CM. 2010. Genetic analysis of the carboxy-terminal region of the hepatitis C virus core protein. J. Virol. 84:1666-1673.
19. Koradi R, Billeter M, Wuthrich K. 1996. MOLMOL: a program for display and analysis of macromolecular structures. J. Mol. Graph. 14:51-55, 29-32.
20. Kovjazin R, et al. 2011. Signal peptides and trans-membrane regions are broadly immunogenic and have high CD8+ T cell epitope densities: implications for vaccine development. Mol. Immunol. 48:1009-1018.
21. Lavanchy D. 2011. Evolving epidemiology of hepatitis C virus. Clin. Microbiol. Infect. 17:107-115.
22. Lemberg MK, Bland FA, Weihofen A, Braud VM, Martoglio B. 2001. Intramembrane proteolysis of signal peptides: an essential step in the generation of HLA-E epitopes. J. Immunol. 167:6441-6446.
23. Lemberg MK, Martoglio B. 2002. Requirements for signal peptide peptidase-catalyzed intramembrane proteolysis. Mol. Cell 10:735-744.
24. Lindenbach BD, et al. 2005. Complete replication of hepatitis C virus in cell culture. Science 309:623-626.
25. Macdonald A, et al. 2003. The hepatitis C virus non-structural NS5A protein inhibits activating protein-1 function by perturbing ras-ERK pathway signaling. J. Biol. Chem. 278:17775-17784.
26. Martoglio B. 2003. Intramembrane proteolysis and post-targeting functions of signal peptides. Biochem. Soc. Trans. 31:1243-1247.
27. McLauchlan J, Lemberg MK, Hope G, Martoglio B. 2002. Intramembrane proteolysis promotes trafficking of hepatitis C virus core protein to lipid droplets. EMBO J. 21:3980-3988.
28. Merutka G, Dyson HJ, Wright PE. 1995. 'Random coil' 1H chemical shifts obtained as a function of temperature and trifluoroethanol concentration for the peptide series GGXGG. J. Biomol. NMR 5:14-24.
29. Miyashita H, et al. 2011. Three-dimensional structure of the signal peptide peptidase. J. Biol. Chem. 286:26188-26197.
30. Montserret R, et al. 1999. Structural analysis of the heparin-binding site of the NC1 domain of collagen XIV by CD and NMR. Biochemistry 38: 6479-6488.
31. Moradpour D, Penin F, Rice CM. 2007. Replication of hepatitis C virus. Nat. Rev. Microbiol. 5:453-463.
32. Murphy D, Chamberland J, Dandavino R, Sablon E. 2007. A new genotype of hepatitis C virus originating from central Africa. Hepatology 2007:623A.
33. Murray CL, Jones CT, Tassello J, Rice CM. 2007. Alanine scanning of the hepatitis C virus core protein reveals numerous residues essential for production of infectious virus. J. Virol. 81:10220-10231.
34. Negro F, Sanyal AJ. 2009. Hepatitis C virus, steatosis and lipid abnormalities: clinical and pathogenic data. Liver Int. 29(Suppl 2):26-37.
35. Ogino T, Fukuda H, Imajoh-Ohmi S, Kohara M, Nomoto A. 2004. Membrane binding properties and terminal residues of the mature hepatitis C virus capsid protein in insect cells. J. Virol. 78:11766-11777.
36. Okamoto K, et al. 2008. Intramembrane processing by signal peptide peptidase regulates the membrane localization of hepatitis C virus core protein and viral propagation. J. Virol. 82:8349-8361.
37. Okamoto K, Moriishi K, Miyamura T, Matsuura Y. 2004. Intramembrane proteolysis and endoplasmic reticulum retention of hepatitis C virus core protein. J. Virol. 78:6370-6380.
38. Opella SJ. 1997. NMR and membrane proteins. Nat. Struct. Biol. 4(Suppl): 845-848.
39. Pene V, Hernandez C, Vauloup-Fellous C, Garaud-Aunis J, Rosenberg AR. 2009. Sequential processing of hepatitis C virus core protein by host cell signal peptidase and signal peptide peptidase: a reassessment. J. Viral Hepat. 16:705-715.
40. Penin F, et al. 1997. Three-dimensional structure of the DNA-binding domain of the fructose repressor from Escherichia coli by 1H and 15N NMR. J. Mol. Biol. 270:496-510.
41. Pietschmann T, et al. 2006. Construction and characterization of infectious intragenotypic and intergenotypic hepatitis C virus chimeras. Proc. Natl. Acad. Sci. U. S. A. 103:7408-7413.
42. Rubbia-Brandt L, et al. 2001. Liver steatosis in chronic hepatitis C: a morphological sign suggesting infection with HCV genotype 3. Histopathology 39:119-124.
43. Rubbia-Brandt L, et al. 2000. Hepatocyte steatosis is a cytopathic effect of hepatitis C virus genotype 3. J. Hepatol. 33:106-115.
44. Schwieters CD, Kuszewski JJ, Tjandra N, Clore GM. 2003. The Xplor-NIH NMR molecular structure determination package. J. Magn. Reson. 160:65-73.
45. Shavinskaya A, Boulant S, Penin F, McLauchlan J, Bartenschlager R. 2007. The lipid droplet binding domain of hepatitis C virus core protein is a major determinant for efficient virus assembly. J. Biol. Chem. 282: 37158-37169.
46. Shaw ML, McLauchlan J, Mills PR, Patel AH, McCruden EA. 2003. Characterisation of the differences between hepatitis C virus genotype 3 and 1 glycoproteins. J. Med. Virol. 70:361-372.
47. Shen Y, Delaglio F, Cornilescu G, Bax A. 2009. TALOS+: a hybrid method for predicting protein backbone torsion angles fromNMRchemical shifts. J. Biomol. NMR 44:213-223.
48. Simmonds P, et al. 2005. Consensus proposals for a unified system of nomenclature of hepatitis C virus genotypes. Hepatology 42:962-973.
49. Targett-Adams P, et al. 2003. Live cell analysis and targeting of the lipid droplet-binding adipocyte differentiation-related protein. J. Biol. Chem. 278:15998-16007.
50. Targett-Adams P, Hope G, Boulant S, McLauchlan J. 2008. Maturation of hepatitis C virus core protein by signal peptide peptidase is required for virus production. J. Biol. Chem. 283:16850-16859.
51. Thanabal V, Omecinsky DO, Reily MD, Cody WL. 1994. The 13C chemical shifts of amino acids in aqueous solution containing organic solvents: application to the secondary structure characterization of peptides in aqueous trifluoroethanol solution. J. Biomol. NMR 4:47-59.
52. von Heijne G. 1998. Protein transport: life and death of a signal peptide. Nature 396:111-113.
53. von Heijne G. 1990. The signal peptide. J. Membr. Biol. 115:195-201.
54. Weihofen A, Binns K, Lemberg MK, Ashman K, Martoglio B. 2002. Identification of signal peptide peptidase, a presenilin-type aspartic protease. Science 296:2215-2218.
55. Whitmore L, Wallace BA. 2004. DICHROWEB, an online server for protein secondary structure analyses from circular dichroism spectroscopic data. Nucleic Acids Res. 32:W668-W673. doi:10.1093/nar/gkh371.
56. Wishart DS, Sykes BD, Richards FM. 1992. The chemical shift index: a fast and simple method for the assignment of protein secondary structure through NMR spectroscopy. Biochemistry 31:1647-1651.
57. Wüthrich K. 1986. NMR of proteins and nucleic acids. John Wiley & Sons, New York, NY.