Flavivirus infection impairs peroxisome biogenesis and early antiviral signaling

Journal of Virology

Volumn 89, Issue 24, 2015, Pages 12349-12361

  You, Jaehwan ^a   Hou, Shangmei ^a   Malik Soni, Natasha ^a   Xu, Zaikun ^a   Kumar, Anil ^a   Rachubinski, Richard A ^a   Frappier, Lori ^a   Hobman, Tom C ^a,b,c  

^a UNIVERSITY OF ALBERTA   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITY OF ALBERTA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CAPSID PROTEIN; CELL PROTEIN; INTERFERON; INTERFERON LAMBDA 3; INTERLEUKIN 28A; INTERLEUKIN 29; MESSENGER RNA; PEROXIN 19; UNCLASSIFIED DRUG; VIRUS RNA; MEMBRANE PROTEIN; PEX19 PROTEIN, HUMAN;

ARTICLE; BIOGENESIS; COMPLEX FORMATION; CONTROLLED STUDY; DENGUE VIRUS; FLAVIVIRUS; FLAVIVIRUS INFECTION; HOST CELL; HUMAN; HUMAN CELL; IMMUNE EVASION; NONHUMAN; PEROXISOME; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN INDUCTION; PROTEIN INTERACTION; PROTEIN PURIFICATION; SIGNAL TRANSDUCTION; WEST NILE VIRUS; DENGUE; GENETICS; HEK293 CELL LINE; METABOLISM; WEST NILE FEVER;

DENGUE; DENGUE VIRUS; HEK293 CELLS; HUMANS; MEMBRANE PROTEINS; PEROXISOMES; SIGNAL TRANSDUCTION; WEST NILE FEVER; WEST NILE VIRUS;

EID: 84949844295     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01365-15     Document Type: Article

References (43)

1. Pierson TC, Diamond MS. 2013. Flaviviruses, p 747-794. In Knipe DM, Howley PM (ed), Fields virology, 6th ed, vol 1. Lippincott Williams & Wilkins, Philadelphia, PA.
2. Urbanowski MD, Hobman TC. 2013. The West Nile virus capsid protein blocks apoptosis through a phosphatidylinositol 3-kinase-dependent mechanism. J Virol 87:872-881. http://dx.doi.org/10.1128/JVI.02030-12.
3. Urbanowski MD, Ilkow CS, Hobman TC. 2008. Modulation of signaling pathways by RNA virus capsid proteins. Cell Signal 20:1227-1236. http://dx.doi.org/10.1016/j.cellsig.2007.12.018.
4. Moriya K, Fujie H, Shintani Y, Yotsuyanagi H, Tsutsumi T, Ishibashi K, Matsuura Y, Kimura S, Miyamura T, Koike K. 1998. The core protein of hepatitis C virus induces hepatocellular carcinoma in transgenic mice. Nat Med 4:1065-1067. http://dx.doi.org/10.1038/2053.
5. Xu Z, Hobman TC. 2012. The helicase activity of DDX56 is required for its role in assembly of infectious West Nile virus particles. Virology 433: 226-235. http://dx.doi.org/10.1016/j.virol.2012.08.011.
6. Xu Z, Anderson R, Hobman TC. 2011. The capsid-binding nucleolar helicase DDX56 is important for infectivity of West Nile virus. J Virol 85:5571-5580. http://dx.doi.org/10.1128/JVI.01933-10.
7. Gotte K, Girzalsky W, Linkert M, Baumgart E, Kammerer S, Kunau WH, Erdmann R. 1998. Pex19p, a farnesylated protein essential for peroxisome biogenesis. Mol Cell Biol 18:616-628.
8. Dixit E, Boulant S, Zhang Y, Lee AS, Odendall C, Shum B, Hacohen N, Chen ZJ, Whelan SP, Fransen M, Nibert ML, Superti-Furga G, Kagan JC. 2010. Peroxisomes are signaling platforms for antiviral innate immunity. Cell 141:668-681. http://dx.doi.org/10.1016/j.cell.2010.04.018.
9. Odendall C, Dixit E, Stavru F, Bierne H, Franz KM, Durbin AF, Boulant S, Gehrke L, Cossart P, Kagan JC. 2014. Diverse intracellular pathogens activate type III interferon expression from peroxisomes. Nat Immunol 15:717-726. http://dx.doi.org/10.1038/ni.2915.
10. Skolnik PR, Rabbi MF, Mathys JM, Greenberg AS. 2002. Stimulation of peroxisome proliferator-activated receptors alpha and gamma blocks HIV-1 replication and TNFalpha production in acutely infected primary blood cells, chronically infected U1 cells, and alveolar macrophages from HIV-infected subjects. J Acquir Immune Defic Syndr 31:1-10. http://dx.doi.org/10.1097/00126334-200209010-00001.
11. Sehgal N, Kumawat KL, Basu A, Ravindranath V. 2012. Fenofibrate reduces mortality and precludes neurological deficits in survivors in murine model of Japanese encephalitis viral infection. PLoS One 7:e35427. http://dx.doi.org/10.1371/journal.pone.0035427.
12. Hunt TA, Urbanowski MD, Kakani K, Law LM, Brinton MA, Hobman TC. 2007. Interactions between the West Nile virus capsid protein and the host cell-encoded phosphatase inhibitor, I2PP2A. Cell Microbiol 9:2756-2766.http://dx.doi.org/10.1111/j.1462-5822.2007.01046.x.
13. Beatch MD, Hobman TC. 2000. Rubella virus capsid associates with host cell protein p32 and localizes to mitochondria. J Virol 74:5569-5576. http://dx.doi.org/10.1128/JVI.74.12.5569-5576.2000.
14. Aitchison JD, Szilard RK, Nuttley WM, Rachubinski RA. 1992. Antibodies directed against a yeast carboxyl-terminal peroxisomal targeting signal specifically recognize peroxisomal proteins from various yeasts. Yeast 8:721-734. http://dx.doi.org/10.1002/yea.320080905.
15. Salsman J, Wang X, Frappier L. 2011. Nuclear body formation and PML body remodeling by the human cytomegalovirus protein UL35. Virology 414:119-129. http://dx.doi.org/10.1016/j.virol.2011.03.013.
16. Holowaty MN, Sheng Y, Nguyen T, Arrowsmith C, Frappier L. 2003. Protein interaction domains of the ubiquitin-specific protease, USP7/HAUSP. J Biol Chem 278:47753-47761. http://dx.doi.org/10.1074/jbc.M307200200.
17. Malik-Soni N, Frappier L. 2012. Proteomic profiling of EBNA1-host protein interactions in latent and lytic Epstein-Barr virus infections. J Virol 86:6999-7002. http://dx.doi.org/10.1128/JVI.00194-12.
18. Chen GI, Gingras AC. 2007. Affinity-purification mass spectrometry (AP-MS) of serine/threonine phosphatases. Methods 42:298-305. http://dx.doi.org/10.1016/j.ymeth.2007.02.018.
19. Salsman J, Zimmerman N, Chen T, Domagala M, Frappier L. 2008. Genome-wide screen of three herpesviruses for protein subcellular localization and alteration of PML nuclear bodies. PLoS Pathog 4:e1000100. http://dx.doi.org/10.1371/journal.ppat.1000100.
20. Matsuzono Y, Kinoshita N, Tamura S, Shimozawa N, Hamasaki M, Ghaedi K, Wanders RJ, Suzuki Y, Kondo N, Fujiki Y. 1999. Human PEX19: cDNA cloning by functional complementation, mutation analysis in a patient with Zellweger syndrome, and potential role in peroxisomal membrane assembly. Proc Natl Acad Sci U S A 96:2116-2121. http://dx.doi.org/10.1073/pnas.96.5.2116.
21. Gould SJ, Keller GA, Hosken N, Wilkinson J, Subramani S. 1989. A conserved tripeptide sorts proteins to peroxisomes. J Cell Biol 108:1657-1664.http://dx.doi.org/10.1083/jcb.108.5.1657.
22. Novoa RR, Calderita G, Arranz R, Fontana J, Granzow H, Risco C. 2005. Virus factories: associations of cell organelles for viral replication and morphogenesis. Biol Cell 97:147-172. http://dx.doi.org/10.1042/BC20040058.
23. Ilkow CS, Weckbecker D, Cho WJ, Meier S, Beatch MD, Goping IS, Herrmann JM, Hobman TC. 2010. The rubella virus capsid protein inhibits mitochondrial import. J Virol 84:119-130. http://dx.doi.org/10.1128/JVI.01348-09.
24. Claus C, Chey S, Heinrich S, Reins M, Richardt B, Pinkert S, Fechner H, Gaunitz F, Schafer I, Seibel P, Liebert UG. 2011. Involvement of p32 and microtubules in alteration of mitochondrial functions by rubella virus. J Virol 85:3881-3892. http://dx.doi.org/10.1128/JVI.02492-10.
25. Belgnaoui SM, Paz S, Hiscott J. 2011. Orchestrating the interferon antiviral response through the mitochondrial antiviral signaling (MAVS) adapter. Curr Opin Immunol 23:564-572. http://dx.doi.org/10.1016/j.coi.2011.08.001.
26. Hoivik DJ, Qualls CW, Jr, Mirabile RC, Cariello NF, Kimbrough CL, Colton HM, Anderson SP, Santostefano MJ, Morgan RJ, Dahl RR, Brown AR, Zhao Z, Mudd PN, Jr, Oliver WB, Jr, Brown HR, Miller RT. 2004. Fibrates induce hepatic peroxisome and mitochondrial proliferation without overt evidence of cellular proliferation and oxidative stress in cynomolgus monkeys. Carcinogenesis 25:1757-1769. http://dx.doi.org/10.1093/carcin/bgh182.
27. Mukhopadhyay S, Kuhn RJ, Rossmann MG. 2005. A structural perspective of the flavivirus life cycle. Nat Rev Microbiol 3:13-22. http://dx.doi.org/10.1038/nrmicro1067.
28. Smith JJ, Aitchison JD. 2013. Peroxisomes take shape. Nat Rev Mol Cell Biol 14:803-817. http://dx.doi.org/10.1038/nrm3700.
29. van der Zand A, Braakman I, Tabak HF. 2010. Peroxisomal membrane proteins insert into the endoplasmic reticulum. Mol Biol Cell 21:2057-2065.http://dx.doi.org/10.1091/mbc.E10-02-0082.
30. Jones JM, Morrell JC, Gould SJ. 2004. PEX19 is a predominantly cytosolic chaperone and import receptor for class 1 peroxisomal membrane proteins. J Cell Biol 164:57-67. http://dx.doi.org/10.1083/jcb.200304111.
31. Fang Y, Morrell JC, Jones JM, Gould SJ. 2004. PEX3 functions as a PEX19 docking factor in the import of class I peroxisomal membrane proteins. J Cell Biol 164:863-875. http://dx.doi.org/10.1083/jcb.200311131.
32. McCartney AW, Greenwood JS, Fabian MR, White KA, Mullen RT. 2005. Localization of the tomato bushy stunt virus replication protein p33 reveals a peroxisome-to-endoplasmic reticulum sorting pathway. Plant Cell 17:3513-3531. http://dx.doi.org/10.1105/tpc.105.036350.
33. Pathak KB, Sasvari Z, Nagy PD. 2008. The host Pex19p plays a role in peroxisomal localization of tombusvirus replication proteins. Virology 379:294-305. http://dx.doi.org/10.1016/j.virol.2008.06.044.
34. Mohan KV, Som I, Atreya CD. 2002. Identification of a type 1 peroxisomal targeting signal in a viral protein and demonstration of its targeting to the organelle. J Virol 76:2543-2547. http://dx.doi.org/10.1128/jvi.76.5.2543-2547.2002.
35. Watanabe H, Shiratori T, Shoji H, Miyatake S, Okazaki Y, Ikuta K, Sato T, Saito T. 1997. A novel acyl-CoA thioesterase enhances its enzymatic activity by direct binding with HIV Nef. Biochem Biophys Res Commun 238:234-239. http://dx.doi.org/10.1006/bbrc.1997.7217.
36. Liu LX, Margottin F, Le Gall S, Schwartz O, Selig L, Benarous R, Benichou S. 1997. Binding of HIV-1 Nef to a novel thioesterase enzyme correlates with Nef-mediated CD4 down-regulation. J Biol Chem 272: 13779-13785. http://dx.doi.org/10.1074/jbc.272.21.13779.
37. Cohen GB, Rangan VS, Chen BK, Smith S, Baltimore D. 2000. The human thioesterase II protein binds to a site on HIV-1 Nef critical for CD4 down-regulation. J Biol Chem 275:23097-23105. http://dx.doi.org/10.1074/jbc.M000536200.
38. Liu LX, Heveker N, Fackler OT, Arold S, Le Gall S, Janvier K, Peterlin BM, Dumas C, Schwartz O, Benichou S, Benarous R. 2000. Mutation of a conserved residue (D123) required for oligomerization of human immunodeficiency virus type 1 Nef protein abolishes interaction with human thioesterase and results in impairment of Nef biological functions. J Virol 74:5310-5319. http://dx.doi.org/10.1128/JVI.74.11.5310-5319.2000.
39. Wolff T, O'Neill RE, Palese P. 1996. Interaction cloning of NS1-I, a human protein that binds to the nonstructural NS1 proteins of influenzaA and B viruses. J Virol 70:5363-5372.
40. Tanner LB, Chng C, Guan XL, Lei Z, Rozen SG, Wenk MR. 2014. Lipidomics identifies a requirement for peroxisomal function during influenza virus replication. J Lipid Res 55:1357-1365. http://dx.doi.org/10.1194/jlr.M049148.
41. Kim SJ, Syed GH, Khan M, Chiu WW, Sohail MA, Gish RG, Siddiqui A. 2014. Hepatitis C virus triggers mitochondrial fission and attenuates apoptosis to promote viral persistence. Proc Natl Acad Sci U S A 111: 6413-6418. http://dx.doi.org/10.1073/pnas.1321114111.
42. Richards AL, Jackson WT. 2013. How positive-strand RNA viruses benefit from autophagosome maturation. J Virol 87:9966-9972. http://dx.doi.org/10.1128/JVI.00460-13.
43. Lazear HM, Daniels BP, Pinto AK, Huang AC, Vick SC, Doyle SE, Gale M, Jr, Klein RS, Diamond MS. 2015. Interferon-lambda restricts West Nile virus neuroinvasion by tightening the blood-brain barrier. Sci Transl Med 7:284ra59. http://dx.doi.org/10.1126/scitranslmed.aaa4304.