Vaccinia virus uses retromerindependent cellular retrograde transport pathways to facilitate the wrapping of intracellular mature virions during virus morphogenesis

Journal of Virology

Volumn 90, Issue 22, 2016, Pages 10120-10132

  Harrison, Kate ^a   Haga, Ismar R ^a,b   Jowers, Tali Pechenick ^a   Jasim, Seema ^a   Cintrat, Jean Christophe ^c   Gillet, Daniel ^c   Schmitt John, Thomas ^d   Digard, Paul ^a   Beard, Philippa M ^a,b  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b INSTITUTE FOR ANIMAL HEALTH   (United Kingdom)

^c DIF   (France)

^d AARHUS UNIVERSITY   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

CARRIER PROTEIN; GARP PROTEIN; MEMBRANE PROTEIN; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL TRANSPORT; CELLULAR RETROGRADE TRANSPORT; CONTROLLED STUDY; EMBRYO; FEMALE; GENE DELETION; GENE MUTATION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MOUSE; MURINE; NONHUMAN; POXVIRUS INFECTION; PRIORITY JOURNAL; VACCINIA VIRUS; VIRION; VIRUS ENVELOPE; VIRUS MORPHOGENESIS; VIRUS REPLICATION; WEIGHT REDUCTION;

EID: 84995481234     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01464-16     Document Type: Article

References (49)

1. Smith GL, Vanderplasschen A, Law M. 2002. The formation and function of extracellular enveloped vaccinia virus. J Gen Virol 83:2915-2931. http://dx.doi.org/10.1099/0022-1317-83-12-2915.
2. Moss B. 2015. Poxvirus membrane biogenesis. Virology 479-480:619-626. http://dx.doi.org/10.1016/j.virol.2015.02.003.
3. Cudmore S, Cossart P, Griffiths G, Way M. 1995. Actin-based motility of vaccinia virus. Nature 378:636-638. http://dx.doi.org/10.1038/378636a0.
4. Frischknecht F, Moreau V, Rottger S, Gonfloni S, Reckmann I, Superti-Furga G, Way M. 1999. Actin-based motility of vaccinia virus mimics receptor tyrosine kinase signalling. Nature 401:926-929. http://dx.doi.org/10.1038/44860.
5. Boulter EA, Appleyard G. 1973. Differences between extracellular and intracellular forms of poxvirus and their implications. Prog Med Virol 16:86-108.
6. Law M, Hollinshead R, Smith GL. 2002. Antibody-sensitive and antibody-resistant cell-to-cell spread by vaccinia virus: role of the A33R protein in antibody-resistant spread. J Gen Virol 83:209-222. http://dx.doi.org/10.1099/0022-1317-83-1-209.
7. Payne LG. 1980. Significance of extracellular enveloped virus in the in vitro and in vivo dissemination of vaccinia. J Gen Virol 50:89-100. http://dx.doi.org/10.1099/0022-1317-50-1-89.
8. Ward BM, Moss B. 2000. Golgi network targeting and plasma membrane internalization signals in vaccinia virus B5R envelope protein. J Virol 74: 3771-3780. http://dx.doi.org/10.1128/JVI.74.8.3771-3780.2000.
9. Husain M, Moss B. 2005. Role of receptor-mediated endocytosis in the formation of vaccinia virus extracellular enveloped particles. J Virol 79: 4080-4089. http://dx.doi.org/10.1128/JVI.79.7.4080-4089.2005.
10. Husain M, Moss B. 2003. Evidence against an essential role of COPIImediated cargo transport to the endoplasmic reticulum-Golgi intermediate compartment in the formation of the primary membrane of vaccinia virus. J Virol 77:11754-11766. http://dx.doi.org/10.1128/JVI.77.21.11754-11766.2003.
11. Tooze J, Hollinshead M, Reis B, Radsak K, Kern H. 1993. Progeny vaccinia and human cytomegalovirus particles utilize early endosomal cisternae for their envelopes. Eur J Cell Biol 60:163-178.
12. Schmelz M, Sodeik B, Ericsson M, Wolffe EJ, Shida H, Hiller G, Griffiths G. 1994. Assembly of vaccinia virus: the second wrapping cisterna is derived from the trans Golgi network. J Virol 68:130-147.
13. Sivan G, Martin SE, Myers TG, Buehler E, Szymczyk KH, Ormanoglu P, Moss B. 2013. Human genome-wide RNAi screen reveals a role for nuclear pore proteins in poxvirus morphogenesis. Proc Natl Acad Sci U S A 110:3519-3524. http://dx.doi.org/10.1073/pnas.1300708110.
14. Beard PM, Griffiths SJ, Gonzalez O, Haga IR, Pechenick Jowers T, Reynolds DK, Wildenhain J, Tekotte H, Auer M, Tyers M, Ghazal P, Zimmer R, Haas J. 2014. A loss of function analysis of host factors influencing vaccinia virus replication by RNA interference. PLoS One 9:e98431. http://dx.doi.org/10.1371/journal.pone.0098431.
15. Trousdale C, Kim K. 2015. Retromer: structure, function, and roles in mammalian disease. Eur J Cell Biol 94:513-521. http://dx.doi.org/10.1016/j.ejcb.2015.07.002.
16. Johannes L, Popoff V. 2008. Tracing the retrograde route in protein trafficking. Cell 135:1175-1187. http://dx.doi.org/10.1016/j.cell.2008.12.009.
17. Perez-Victoria FJ, Mardones GA, Bonifacino JS. 2008. Requirement of the human GARP complex for mannose 6-phosphate-receptordependent sorting of cathepsin D to lysosomes. Mol Biol Cell 19:2350-2362. http://dx.doi.org/10.1091/mbc.E07-11-1189.
18. Frohlich F, Petit C, Kory N, Christiano R, Hannibal-Bach HK, Graham M, Liu X, Ejsing CS, Farese RV, Walther TC. 2015. The GARP complex is required for cellular sphingolipid homeostasis. eLife 2015:4. http://dx.doi.org/10.7554/eLife.08712.
19. Shafaq-Zadah M, Gomes-Santos CS, Bardin S, Maiuri P, Maurin M, Iranzo J, Gautreau A, Lamaze C, Caswell P, Goud B, Johannes L. 2016. Persistent cell migration and adhesion rely on retrograde transport of beta(1) integrin. Nat Cell Biol 18:54-64. http://dx.doi.org/10.1038/ncb3287.
20. Groppelli E, Len AC, Granger LA, Jolly C. 2014. Retromer regulates HIV-1 envelope glycoprotein trafficking and incorporation into virions. PLoS Pathog 10:e1004518. http://dx.doi.org/10.1371/journal.ppat.1004518.
21. Lipovsky A, Popa A, Pimienta G, Wyler M, Bhan A, Kuruvilla L, Guie MA, Poffenberger AC, Nelson CD, Atwood WJ, DiMaio D. 2013. Genome-wide siRNA screen identifies the retromer as a cellular entry factor for human papillomavirus. Proc Natl Acad Sci U S A 110:7452-7457. http://dx.doi.org/10.1073/pnas.1302164110.
22. Nonnenmacher ME, Cintrat JC, Gillet D, Weber T. 2015. Syntaxin 5-dependent retrograde transport to the trans-Golgi network is required for adeno-associated virus transduction. J Virol 89:1673-1687. http://dx.doi.org/10.1128/JVI.02520-14.
23. Carter GC, Rodger G, Murphy BJ, Law M, Krauss O, Hollinshead M, Smith GL. 2003. Vaccinia virus cores are transported on microtubules. J Gen Virol 84:2443-2458. http://dx.doi.org/10.1099/vir.0.19271-0.
24. Haga IR, Pechenick Jowers T, Griffiths SJ, Haas J, Beard PM. 2014. TRAF2 facilitates vaccinia virus replication by promoting rapid virus entry. J Virol 88:3664-3677. http://dx.doi.org/10.1128/JVI.03013-13.
25. Pechenick Jowers T, Featherstone RJ, Reynolds DK, Brown HK, James J, Prescott A, Haga IR, Beard PM. 2015. RAB1A promotes vaccinia virus replication by facilitating the production of intracellular enveloped virions. Virology 475:66-73. http://dx.doi.org/10.1016/j.virol.2014.11.007.
26. Noel R, Gupta N, Pons V, Goudet A, Garcia-Castillo MD, Michau A, Martinez J, Buisson DA, Johannes L, Gillet D, Barbier J, Cintrat JC. 2013. N-Methyldihydroquinazolinone derivatives of Retro-2 with enhanced efficacy against Shiga toxin. J Med Chem 56:3404-3413. http://dx.doi.org/10.1021/jm4002346.
27. Gupta N, Pons V, Noel R, Buisson DA, Michau A, Johannes L, Gillet D, Barbier J, Cintrat JC. 2014. (S)-N-Methyldihydroquinazolinones are the active enantiomers of Retro-2 derived compounds against toxins. ACS Med Chem Lett 5:94-97. http://dx.doi.org/10.1021/ml400457j.
28. Herweg JA, Pons V, Becher D, Hecker M, Krohne G, Barbier J, Berger H, Rudel T, Mehlitz A. 2016. Proteomic analysis of the Simkaniacontaining vacuole: the central role of retrograde transport. Mol Microbiol 99:151-171. http://dx.doi.org/10.1111/mmi.13222.
29. Perez-Victoria FJ, Abascal-Palacios G, Tascon I, Kajava A, Magadan JG, Pioro EP, Bonifacino JS, Hierro A. 2010. Structural basis for the wobbler mouse neurodegenerative disorder caused by mutation in the Vps54 subunit of the GARP complex. Proc Natl Acad Sci U S A 107:12860-12865. http://dx.doi.org/10.1073/pnas.1004756107.
30. Schmitt-John T, Drepper C, Mussmann A, Hahn P, Kuhlmann M, Thiel C, Hafner M, Lengeling A, Heimann P, Jones JM, Meisler MH, Jockusch H. 2005. Mutation of Vps54 causes motor neuron disease and defective spermiogenesis in the wobbler mouse. Nat Genet 37:1213-1215. http://dx.doi.org/10.1038/ng1661.
31. Karlsson P, Droce A, Moser JM, Cuhlmann S, Padilla CO, Heimann P, Bartsch JW, Fuchtbauer A, Fuchtbauer EM, Schmitt-John T. 2013. Loss of vps54 function leads to vesicle traffic impairment, protein mis-sorting and embryonic lethality. Int J Mol Sci 14:10908-10925. http://dx.doi.org/10.3390/ijms140610908.
32. Engelstad M, Howard ST, Smith GL. 1992. A constitutively expressed vaccinia gene encodes a 42-kDa glycoprotein related to complement control factors that forms part of the extracellular virus envelope. Virology 188:801-810. http://dx.doi.org/10.1016/0042-6822(92)90535-W.
33. Seaman MN. 2012. The retromer complex-endosomal protein recycling and beyond. J Cell Sci 125:4693-4702. http://dx.doi.org/10.1242/jcs.103440.
34. Stechmann B, Bai SK, Gobbo E, Lopez R, Merer G, Pinchard S, Panigai L, Tenza D, Raposo G, Beaumelle B, Sauvaire D, Gillet D, Johannes L, Barbier J. 2010. Inhibition of retrograde transport protects mice from lethal ricin challenge. Cell 141:231-242. http://dx.doi.org/10.1016/j.cell.2010.01.043.
35. Canton J, Kima PE. 2012. Targeting host syntaxin-5 preferentially blocks Leishmania parasitophorous vacuole development in infected cells and limits experimental Leishmania infections. Am J Pathol 181:1348-1355. http://dx.doi.org/10.1016/j.ajpath.2012.06.041.
36. Secher T, Shima A, Hinsinger K, Cintrat JC, Johannes L, Barbier J, Gillet D, Oswald E. 2015. Retrograde trafficking inhibitor of Shiga toxins reduces morbidity and mortality of mice infected with enterohemorrhagic Escherichia coli. Antimicrob Agents Chemother 59:5010-5013. http://dx.doi.org/10.1128/AAC.00455-15.
37. Rodriguez JF, Smith GL. 1990. IPTG-dependent vaccinia virus: identification of a virus protein enabling virion envelopment by Golgi membrane and egress. Nucleic Acids Res 18:5347-5351. http://dx.doi.org/10.1093/nar/18.18.5347.
38. Blasco R, Moss B. 1991. Extracellular vaccinia virus formation and cellto-cell virus transmission are prevented by deletion of the gene encoding the 37, 000-dalton outer envelope protein. J Virol 65:5910-5920.
39. Engelstad M, Smith GL. 1993. The vaccinia virus 42-kDa envelope protein is required for the envelopment and egress of extracellular virus and for virus virulence. Virology 194:627-637. http://dx.doi.org/10.1006/viro.1993.1302.
40. Bonifacino JS, Hierro A. 2011. Transport according to GARP: receiving retrograde cargo at the trans-Golgi network. Trends Cell Biol 21:159-167. http://dx.doi.org/10.1016/j.tcb.2010.11.003.
41. Szilagyi JF, Cunningham C. 1991. Identification and characterization of a novel non-infectious herpes simplex virus-related particle. J Gen Virol 72(Pt 3):661-668. http://dx.doi.org/10.1099/0022-1317-72-3-661.
42. Ganley IG, Espinosa E, Pfeffer SR. 2008. A syntaxin 10-SNARE complex distinguishes two distinct transport routes from endosomes to the trans-Golgi in human cells. J Cell Biol 180:159-172. http://dx.doi.org/10.1083/jcb.200707136.
43. Lieu ZZ, Gleeson PA. 2010. Identification of different itineraries and retromer components for endosome-to-Golgi transport of TGN38 and Shiga toxin. Eur J Cell Biol 89:379-393. http://dx.doi.org/10.1016/j.ejcb.2009.10.021.
44. Selyunin AS, Mukhopadhyay S. 2015. A conserved structural motif mediates retrograde trafficking of Shiga toxin types 1 and 2. Traffic 16:1270-1287. http://dx.doi.org/10.1111/tra.12338.
45. Kato N, Eggers HJ, Rolly H. 1969. Inhibition of release of vaccinia virus by N1-isonicotinoly-N2-3-methyl-4-chlorobenzoylhydrazine. J Exp Med 129:795-808. http://dx.doi.org/10.1084/jem.129.4.795.
46. Schmutz C, Payne LG, Gubser J, Wittek R. 1991. A mutation in the gene encoding the vaccinia virus 37, 000-M(r) protein confers resistance to an inhibitor of virus envelopment and release. J Virol 65:3435-3442.
47. Yang G, Pevear DC, Davies MH, Collett MS, Bailey T, Rippen S, Barone L, Burns C, Rhodes G, Tohan S, Huggins JW, Baker RO, Buller RL, Touchette E, Waller K, Schriewer J, Neyts J, DeClercq E, Jones K, Hruby D, Jordan R. 2005. An orally bioavailable antipoxvirus compound (ST-246) inhibits extracellular virus formation and protects mice from lethal orthopoxvirus challenge. J Virol 79:13139-13149. http://dx.doi.org/10.1128/JVI.79.20.13139-13149.2005.
48. Duraffour S, Lorenzo MM, Zoller G, Topalis D, Grosenbach D, Hruby DE, Andrei G, Blasco R, Meyer H, Snoeck R. 2015. ST-246 is a key antiviral to inhibit the viral F13L phospholipase, one of the essential proteins for orthopoxvirus wrapping. J Antimicrob Chemother 70:1367-1380. http://dx.doi.org/10.1093/jac/dku545.
49. Sivan G, Weisberg AS, Americo JL, Moss B. 27 July 2016. Retrograde transport from early endosomes to the trans-Golgi network enables membrane wrapping and egress of vaccinia virions. J Virol. http://dx.doi.org/10.1128/JVI.01114-16.