Convergent evolution of escape from hepaciviral antagonism in primates

PLoS Biology

Volumn 10, Issue 3, 2012, Pages

  Patel, Maulik R ^a   Loo, Yueh Ming ^b   Horner, Stacy M ^b   Gale, Michael ^b   Malik, Harmit S ^a,c  

^a Fred Hutchinson Cancer Research Center   (United States)

^b UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MITOCHONDRIAL ANTIVIRAL SIGNALING PROTEIN; MITOCHONDRIAL PROTEIN; NONSTRUCTURAL PROTEIN 3; NONSTRUCTURAL PROTEIN 4A; UNCLASSIFIED DRUG; NS3 PROTEIN, HEPATITIS C VIRUS; SIGNAL TRANSDUCING ADAPTOR PROTEIN; VIRUS PROTEIN;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME BINDING; HEPATITIS C VIRUS; HUMAN; HUMAN CELL; INFECTION SENSITIVITY; MICROBIAL ACTIVITY; MOLECULAR EVOLUTION; MUTATION; NONHUMAN; PHYLOGENY; PROTEIN CLEAVAGE; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SIMIAN; VIRUS CELL INTERACTION; VIRUS INHIBITION; VIRUS REPLICATION; VIRUS STRAIN; ANIMAL; CHEMICAL STRUCTURE; CLASSIFICATION; ENZYMOLOGY; GENETIC SELECTION; GENETICS; HEPATITIS C; HOST PATHOGEN INTERACTION; METABOLISM; MOLECULAR GENETICS; PATHOGENICITY; PHYSIOLOGY; PRIMATE; PROTEIN DEGRADATION; SEQUENCE ALIGNMENT; VIROLOGY; VIRUS GENE;

GB VIRUS A; GB VIRUS C; HEPATITIS C VIRUS; MAMMALIA; PRIMATES; SIMIAE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; AMINO ACID SEQUENCE; ANIMALS; EVOLUTION, MOLECULAR; GENES, VIRAL; HEPACIVIRUS; HEPATITIS C; HOST-PATHOGEN INTERACTIONS; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PHYLOGENY; PRIMATES; PROTEOLYSIS; SELECTION, GENETIC; SEQUENCE ALIGNMENT; VIRAL NONSTRUCTURAL PROTEINS; VIRUS REPLICATION;

EID: 84858960202     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1001282     Document Type: Article

References (53)

1. Yoneyama M, Kikuchi M, Natsukawa T, Shinobu N, Imaizumi T, et al. (2004) The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat Immunol 5: 730-737.
2. Kang D. C, Gopalkrishnan R. V, Wu Q, Jankowsky E, Pyle A. M, et al. (2002) mda-5: an interferon-inducible putative RNA helicase with double-stranded RNA-dependent ATPase activity and melanoma growth-suppressive properties. Proc Natl Acad Sci U S A 99: 637-642.
3. Andrejeva J, Childs K. S, Young D. F, Carlos T. S, Stock N, et al. (2004) The V proteins of paramyxoviruses bind the IFN-inducible RNA helicase, mda-5, and inhibit its activation of the IFN-beta promoter. Proc Natl Acad Sci U S A 101: 17264-17269.
4. Seth R. B, Sun L, Ea C. K, Chen Z. J, (2005) Identification and characterization of MAVS, a mitochondrial antiviral signaling protein that activates NF-kappaB and IRF 3. Cell 122: 669-682.
5. Meylan E, Curran J, Hofmann K, Moradpour D, Binder M, et al. (2005) Cardif is an adaptor protein in the RIG-I antiviral pathway and is targeted by hepatitis C virus. Nature 437: 1167-1172.
6. Kawai T, Takahashi K, Sato S, Coban C, Kumar H, et al. (2005) IPS-1, an adaptor triggering RIG-I- and Mda5-mediated type I interferon induction. Nat Immunol 6: 981-988.
7. Xu L. G, Wang Y. Y, Han K. J, Li L. Y, Zhai Z, et al. (2005) VISA is an adapter protein required for virus-triggered IFN-beta signaling. Mol Cell 19: 727-740.
8. Li X. D, Sun L, Seth R. B, Pineda G, Chen Z. J, (2005) Hepatitis C virus protease NS3/4A cleaves mitochondrial antiviral signaling protein off the mitochondria to evade innate immunity. Proc Natl Acad Sci U S A 102: 17717-17722.
9. Graef K. M, Vreede F. T, Lau Y. F, McCall A. W, Carr S. M, et al. (2010) The PB2 subunit of the influenza virus RNA polymerase affects virulence by interacting with the mitochondrial antiviral signaling protein and inhibiting expression of beta interferon. J Virol 84: 8433-8445.
10. Iwai A, Shiozaki T, Kawai T, Akira S, Kawaoka Y, et al. (2010) Influenza A virus polymerase inhibits type I interferon induction by binding to interferon beta promoter stimulator 1. J Biol Chem 285: 32064-32074.
11. Yang Y, Liang Y, Qu L, Chen Z, Yi M, et al. (2007) Disruption of innate immunity due to mitochondrial targeting of a picornaviral protease precursor. Proc Natl Acad Sci U S A 104: 7253-7258.
12. Mukherjee A, Morosky S. A, Delorme-Axford E, Dybdahl-Sissoko N, Oberste M. S, et al. (2011) The coxsackievirus B 3C protease cleaves MAVS and TRIF to attenuate host type I interferon and apoptotic signaling. PLoS Pathog 7: e1001311 doi:10.1371/journal.ppat.1001311.
13. Paulmann D, Magulski T, Schwarz R, Heitmann L, Flehmig B, et al. (2008) Hepatitis A virus protein 2B suppresses beta interferon (IFN) gene transcription by interfering with IFN regulatory factor 3 activation. J Gen Virol 89: 1593-1604.
14. Simmonds P, (2004) Genetic diversity and evolution of hepatitis C virus-15 years on. J Gen Virol 85: 3173-3188.
15. Fields B. N, Knipe D. M, Howley P. M, (2007) Fields' virology Philadelphia Wolters Kluwer Health/Lippincott Williams & Wilkins 2 v. (xix, 3091, 3086 pp.).
16. Epstein J. H, Quan P. L, Briese T, Street C, Jabado O, et al. (2010) Identification of GBV-D, a novel GB-like flavivirus from old world frugivorous bats (Pteropus giganteus) in Bangladesh. PLoS Pathog 6: e1000972 doi:10.1371/journal.ppat.1000972.
17. Kapoor A, Simmonds P, Gerold G, Qaisar N, Jain K, et al. (2011) Characterization of a canine homolog of hepatitis C virus. Proc Natl Acad Sci U S A.
18. Elde N. C, Child S. J, Geballe A. P, Malik H. S, (2009) Protein kinase R reveals an evolutionary model for defeating viral mimicry. Nature 457: 485-489.
19. Sawyer S. L, Emerman M, Malik H. S, (2004) Ancient adaptive evolution of the primate antiviral DNA-editing enzyme APOBEC3G. PLoS Biol 2: E275 doi:10.1371/journal.pbio.0020275.
20. Sawyer S. L, Wu L. I, Emerman M, Malik H. S, (2005) Positive selection of primate TRIM5alpha identifies a critical species-specific retroviral restriction domain. Proc Natl Acad Sci U S A 102: 2832-2837.
21. Ortiz M, Guex N, Patin E, Martin O, Xenarios I, et al. (2009) Evolutionary trajectories of primate genes involved in HIV pathogenesis. Mol Biol Evol 26: 2865-2875.
22. McNatt M. W, Zang T, Hatziioannou T, Bartlett M, Fofana I. B, et al. (2009) Species-specific activity of HIV-1 Vpu and positive selection of tetherin transmembrane domain variants. PLoS Pathog 5: e1000300 doi:10.1371/journal.ppat.1000300.
23. Zhang J, Webb D. M, (2004) Rapid evolution of primate antiviral enzyme APOBEC3G. Hum Mol Genet 13: 1785-1791.
24. Song B, Gold B, O'Huigin C, Javanbakht H, Li X, et al. (2005) The B30.2(SPRY) domain of the retroviral restriction factor TRIM5alpha exhibits lineage-specific length and sequence variation in primates. J Virol 79: 6111-6121.
25. Rothenburg S, Seo E. J, Gibbs J. S, Dever T. E, Dittmar K, (2009) Rapid evolution of protein kinase PKR alters sensitivity to viral inhibitors. Nat Struct Mol Biol 16: 63-70.
26. Perelman P, Johnson W. E, Roos C, Seuanez H. N, Horvath J. E, et al. (2011) A molecular phylogeny of living primates. PLoS Genet 7: e1001342 doi:10.1371/journal.pgen.1001342.
27. Yang Z, (1997) PAML: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci 13: 555-556.
28. Yang Z, (2007) PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24: 1586-1591.
29. Kosakovsky Pond S. L, Murrell B, Fourment M, Frost S. D, Delport W, et al. (2011) A random effects branch-site model for detecting episodic diversifying selection. Mol Biol Evol.
30. Pond S. K, Muse S. V, (2005) Site-to-site variation of synonymous substitution rates. Mol Biol Evol 22: 2375-2385.
31. Zhang R, Durkin J, Windsor W. T, McNemar C, Ramanathan L, et al. (1997) Probing the substrate specificity of hepatitis C virus NS3 serine protease by using synthetic peptides. J Virol 71: 6208-6213.
32. Kim S. Y, Park K. W, Lee Y. J, Back S. H, Goo J. H, et al. (2000) In vivo determination of substrate specificity of hepatitis C virus NS3 protease: genetic assay for site-specific proteolysis. Anal Biochem 284: 42-48.
33. Johnson C. L, Owen D. M, Gale M Jr, (2007) Functional and therapeutic analysis of hepatitis C virus NS3.4A protease control of antiviral immune defense. J Biol Chem 282: 10792-10803.
34. Sumpter R Jr, Wang C, Foy E, Loo Y. M, Gale M Jr, (2004) Viral evolution and interferon resistance of hepatitis C virus RNA replication in a cell culture model. J Virol 78: 11591-11604.
35. Wang C, Pflugheber J, Sumpter R Jr, Sodora D. L, Hui D, et al. (2003) Alpha interferon induces distinct translational control programs to suppress hepatitis C virus RNA replication. J Virol 77: 3898-3912.
36. Weatherford T, Chavez D, Brasky K. M, Lanford R. E, (2009) The marmoset model of GB virus B infections: adaptation to host phenotypic variation. J Virol 83: 5806-5814.
37. Leary T. P, Desai S. M, Yamaguchi J, Chalmers M. L, Schlauder G. G, et al. (1996) Species-specific variants of GB virus A in captive monkeys. J Virol 70: 9028-9030.
38. Bukh J, Apgar C. L, (1997) Five new or recently discovered (GBV-A) virus species are indigenous to New World monkeys and may constitute a separate genus of the Flaviviridae. Virology 229: 429-436.
39. Adams N. J, Prescott L. E, Jarvis L. M, Lewis J. C, McClure M. O, et al. (1998) Detection in chimpanzees of a novel flavivirus related to GB virus-C/hepatitis G virus. J Gen Virol 79 (Pt 8): 1871-1877.
40. Birkenmeyer L. G, Desai S. M, Muerhoff A. S, Leary T. P, Simons J. N, et al. (1998) Isolation of a GB virus-related genome from a chimpanzee. J Med Virol 56: 44-51.
41. Linnen J, Wages J Jr, Zhang-Keck Z. Y, Fry K. E, Krawczynski K. Z, et al. (1996) Molecular cloning and disease association of hepatitis G virus: a transfusion-transmissible agent. Science 271: 505-508.
42. Simons J. N, Leary T. P, Dawson G. J, Pilot-Matias T. J, Muerhoff A. S, et al. (1995) Isolation of novel virus-like sequences associated with human hepatitis. Nat Med 1: 564-569.
43. Chen Z, Benureau Y, Rijnbrand R, Yi J, Wang T, et al. (2007) GB virus B disrupts RIG-I signaling by NS3/4A-mediated cleavage of the adaptor protein MAVS. J Virol 81: 964-976.
44. Li J, Han K, Xing J, Kim H. S, Rogers J, et al. (2009) Phylogeny of the macaques (Cercopithecidae: Macaca) based on Alu elements. Gene 448: 242-249.
45. Thomas D. L, Thio C. L, Martin M. P, Qi Y, Ge D, et al. (2009) Genetic variation in IL28B and spontaneous clearance of hepatitis C virus. Nature 461: 798-801.
46. Ge D, Fellay J, Thompson A. J, Simon J. S, Shianna K. V, et al. (2009) Genetic variation in IL28B predicts hepatitis C treatment-induced viral clearance. Nature 461: 399-401.
47. Charrel R. N, De Micco P, de Lamballerie X, (1999) Phylogenetic analysis of GB viruses A and C: evidence for cospeciation between virus isolates and their primate hosts. J Gen Virol 80 (Pt 9): 2329-2335.
48. Sharp P. M, Simmonds P, (2011) Evaluating the evidence for virus/host co-evolution. Curr Opin Virol 1: 436-441.
49. Emerman M, Malik H. S, (2010) Paleovirology-modern consequences of ancient viruses. PLoS Biol 8: e1000301 doi:10.1371/journal.pbio.1000301.
50. Patel M. R, Emerman M, Malik H. S, (2011) Paleovirology-ghosts and gifts of viruses past. Curr Opin Virol 1: 304-309.
51. Gilbert C, Feschotte C, (2010) Genomic fossils calibrate the long-term evolution of hepadnaviruses. PLoS Biol 8 doi:10.1371/journal.pbio.1000495.
52. Loo Y. M, Owen D. M, Li K, Erickson A. K, Johnson C. L, et al. (2006) Viral and therapeutic control of IFN-beta promoter stimulator 1 during hepatitis C virus infection. Proc Natl Acad Sci U S A 103: 6001-6006.
53. Wang C, Gale M Jr, Keller B. C, Huang H, Brown M. S, et al. (2005) Identification of FBL2 as a geranylgeranylated cellular protein required for hepatitis C virus RNA replication. Mol Cell 18: 425-434.