Retrograde transport from early endosomes to the trans-Golgi network enables membrane wrapping and egress of vaccinia virus virions

Journal of Virology

Volumn 90, Issue 19, 2016, Pages 8891-8905

  Sivan, Gilad ^a   Weisberg, Andrea S ^a   Americo, Jeffrey L ^a   Moss, Bernard ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR 5; ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR 5A; CARRIER PROTEIN; F13 PROTEIN; MEMBRANE PROTEIN; RETROGRADE TRANSPORT PROTEIN; SYNAPTOBREVIN; SYNAPTOBREVIN 4; SYNTAXIN 6; UNCLASSIFIED DRUG; VACUOLAR SORTING PROTEIN 52; VACUOLAR SORTING PROTEIN 53; VACUOLAR SORTING PROTEIN 54; VIRAL PROTEIN;

ACTIN POLYMERIZATION; ARTICLE; CELL SPREADING; CELLULAR DISTRIBUTION; CONTROLLED STUDY; HUMAN; NONHUMAN; PALMITOYLATION; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN STABILITY; RNA INTERFERENCE; TRANS GOLGI NETWORK; VACCINIA VIRUS; VIRUS ASSEMBLY; VIRUS ENTRY; VIRUS RELEASE; VIRUS TRANSMISSION; CELL MEMBRANE; CONFOCAL MICROSCOPY; ELECTRON MICROSCOPY; ENDOSOME; EXOCYTOSIS; HELA CELL LINE; METABOLISM; MONKEYPOX VIRUS; PHYSIOLOGY; TRANSPORT AT THE CELLULAR LEVEL; VIRION;

BIOLOGICAL TRANSPORT; CELL MEMBRANE; ENDOSOMES; EXOCYTOSIS; HELA CELLS; HUMANS; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON; MONKEYPOX VIRUS; TRANS-GOLGI NETWORK; VACCINIA VIRUS; VIRION; VIRUS RELEASE;

EID: 84990242542     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01114-16     Document Type: Article

References (80)

1. Moss B. 2013. Poxviridae, p 2129-2159. In Knipe DM, Howley PM (ed), Fields virology, 6th ed, vol 2. Lippincott Williams & Wilkins, Hagerstown, MD
2. Condit RC, Moussatche N, Traktman P. 2006. In a nutshell: structure and assembly of the vaccinia virion. Adv Virus Res 66:31-124. http://dx.doi.org/10.1016/S0065-3527(06)66002-8
3. Smith GL, Law M. 2004. The exit of vaccinia virus from infected cells. Virus Res 106:189-197. http://dx.doi.org/10.1016/j.virusres.2004.08.015
4. Blasco R, Moss B. 1992. Role of cell-associated enveloped vaccinia virus in cell-to-cell spread. J Virol 66:4170-4179
5. Vliegen I, Yang G, Hruby D, Jordan R, Neyts J. 2012. Deletion of the vaccinia virus F13L gene results in a highly attenuated virus that mounts a protective immune response against subsequent vaccinia virus challenge. Antiviral Res 93:160-166. http://dx.doi.org/10.1016/j.antiviral.2011.11.010
6. Moss B. 2015. Poxvirus membrane biogenesis. Virology 479-480:619-626
7. Hiller G, Weber K. 1985. Golgi-derived membranes that contain an acylated viral polypeptide are used for vaccinia virus envelopment. J Virol 55:651-659
8. 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
9. 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
10. Payne L. 1978. Polypeptide composition of extracellular enveloped vaccinia virus. J Virol 27:28-37
11. 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
12. 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
13. 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
14. Wolffe EJ, Isaacs SN, Moss B. 1993. Deletion of the vaccinia virus B5R gene encoding a 42-kilodalton membrane glycoprotein inhibits extracellular virus envelope formation and dissemination. J Virol 67:4732-4741
15. Isaacs SN, Wolffe EJ, Payne LG, Moss B. 1992. Characterization of a vaccinia virus-encoded 42-kilodalton class I membrane glycoprotein component of the extracellular virus envelope. J Virol 66:7217-7224
16. Schmutz C, Rindisbacher L, Galmiche MC, Wittek R. 1995. Biochemical analysis of the major vaccinia virus envelope antigen. Virology 213:19-27. http://dx.doi.org/10.1006/viro.1995.1542
17. Grosenbach DW, Ulaeto DO, Hruby DE. 1997. Palmitylation of the vaccinia virus 37-kDa major envelope antigen. Identification of a conserved acceptor motif and biological relevance. J Biol Chem 272:1956-1964
18. Lorenzo MM, Galindo I, Griffiths G, Blasco R. 2000. Intracellular localization of vaccinia virus extracellular enveloped virus envelope proteins individually expressed using a Semliki Forest virus replicon. J Virol 74:10535-10550. http://dx.doi.org/10.1128/JVI.74.22.10535-10550.2000
19. 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
20. Sandvig K, van Deurs B. 2005. Delivery into cells: lessons learned from plant and bacterial toxins. Gene Ther 12:865-872. http://dx.doi.org/10.1038/sj.gt.3302525
21. Bantel-Schaal U, Hub B, Kartenbeck J. 2002. Endocytosis of adenoassociated virus type 5 leads to accumulation of virus particles in the Golgi compartment. J Virol 76:2340-2349. http://dx.doi.org/10.1128/jvi.76.5.2340-2349.2002
22. 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
23. Nelson CD, Carney DW, Derdowski A, Lipovsky A, Gee GV, O'Hara B, Williard P, DiMaio D, Sello JK, Atwood WJ. 2013. A retrograde trafficking inhibitor of ricin and Shiga-like toxins inhibits infection of cells by human and monkey polyomaviruses. mBio 4:e00729-13. http://dx.doi.org/10.1128/mBio.00729-13
24. 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
25. Bonifacino JS, Rojas R. 2006. Retrograde transport from endosomes to the trans-Golgi network. Nat Rev Mol Cell Biol 7:568-579. http://dx.doi.org/10.1038/nrm1985
26. Schindler C, Chen Y, Pu J, Guo X, Bonifacino JS. 2015. EARP is a multisubunit tethering complex involved in endocytic recycling. Nat Cell Biol 17:639-650. http://dx.doi.org/10.1038/ncb3129
27. 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
28. 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
29. Bengali Z, Townsley AC, Moss B. 2009. Vaccinia virus strain differences in cell attachment and entry. Virology 389:132-140. http://dx.doi.org/10.1016/j.virol.2009.04.012
30. Husain M, Moss B. 2001. Vaccinia virus F13L protein with a conserved phospholipase catalytic motif induces colocalization of the B5R envelope glycoprotein in post-Golgi vesicles. J Virol 75:7528-7542. http://dx.doi.org/10.1128/JVI.75.16.7528-7542.2001
31. Laliberte JP, Weisberg AS, Moss B. 2011. The membrane fusion step of vaccinia virus entry is cooperatively mediated by multiple viral proteins and host cell components. PLoS Pathog 7:e1002446. http://dx.doi.org/10.1371/journal.ppat.1002446
32. Davies DH, Wyatt LS, Newman FK, Earl PL, Chun S, Hernandez JE, Molina DM, Hirst S, Moss B, Frey SE, Felgner PL. 2008. Antibody profiling by proteome microarray reveals the immunogenicity of the attenuated smallpox vaccine modified vaccinia virus ankara is comparable to that of Dryvax. J Virol 82:652-663. http://dx.doi.org/10.1128/JVI.01706-07
33. Maruri-Avidal L, Domi A, Weisberg AS, Moss B. 2011. Participation of vaccinia virus L2 protein in the formation of crescent membranes and immature virions. J Virol 85:2504-2511. http://dx.doi.org/10.1128/JVI.02505-10
34. Senkevich TG, Wyatt LS, Weisberg AS, Koonin EV, Moss B. 2008. A conserved poxvirus NlpC/P60 superfamily protein contributes to vaccinia virus virulence in mice but not to replication in cell culture. Virology 374:506-514. http://dx.doi.org/10.1016/j.virol.2008.01.009
35. Bisht H, Weisberg AS, Szajner P, Moss B. 2009. Assembly and disassembly of the capsid-like external scaffold of immature virions during vaccinia virus morphogenesis. J Virol 83:9140-9150. http://dx.doi.org/10.1128/JVI.00875-09
36. Satheshkumar PS, Anton LC, Sanz P, Moss B. 2009. Inhibition of the ubiquitin-proteasome system prevents vaccinia virus DNA replication and expression of intermediate and late genes. J Virol 83:2469-2479. http://dx.doi.org/10.1128/JVI.01986-08
37. Teale A, Campbell S, Van Buuren N, Magee WC, Watmough K, Couturier B, Shipclark R, Barry M. 2009. Orthopoxviruses require a functional ubiquitin-proteasome system for productive replication. J Virol 83:2099-2108. http://dx.doi.org/10.1128/JVI.01753-08
38. Mercer J, Snijder B, Sacher R, Burkard C, Bleck CK, Stahlberg H, Pelkmans L, Helenius A. 2012. RNAi screening reveals proteasome-and cullin3-dependent stages in vaccinia virus infection. Cell Rep 2:1036-1047. http://dx.doi.org/10.1016/j.celrep.2012.09.003
39. 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
40. Perez-Victoria FJ, Bonifacino JS. 2009. Dual roles of the mammalian GARP complex in tethering and SNARE complex assembly at the trans-Golgi network. Mol Cell Biol 29:5251-5563. http://dx.doi.org/10.1128/MCB.00495-09
41. Rosa-Ferreira C, Christis C, Torres IL, Munro S. 2015. The small G protein Arl5 contributes to endosome-to-Golgi traffic by aiding the recruitment of the GARP complex to the Golgi. Biol Open 4:474-481. http://dx.doi.org/10.1242/bio.201410975
42. Laufman O, Hong W, Lev S. 2013. The COG complex interacts with multiple Golgi SNAREs and enhances fusogenic assembly of SNARE complexes. J Cell Sci 126:1506-1516. http://dx.doi.org/10.1242/jcs.122101
43. Laufman O, Hong W, Lev S. 2011. The COG complex interacts directly with Syntaxin 6 and positively regulates endosome-to-TGN retrograde transport. J Cell Biol 194:459-472. http://dx.doi.org/10.1083/jcb.201102045
44. Sacher M, Kim YG, Lavie A, Oh BH, Segev N. 2008. The TRAPP complex: insights into its architecture and function. Traffic 9:2032-2042. http://dx.doi.org/10.1111/j.1600-0854.2008.00833.x
45. McGough IJ, Cullen PJ. 2011. Recent advances in retromer biology. Traffic 12:963-971. http://dx.doi.org/10.1111/j.1600-0854.2011.01201.x
46. Townsley AC, Weisberg AS, Wagenaar TR, Moss B. 2006. Vaccinia virus entry into cells via a low pH-dependent-endosomal pathway. J Virol 80: 8899-8908. http://dx.doi.org/10.1128/JVI.01053-06
47. Gordon DE, Bond LM, Sahlender DA, Peden AA. 2010. A Targeted siRNA screen to identify SNAREs required for constitutive secretion in mammalian cells. Traffic 11:1191-1204. http://dx.doi.org/10.1111/j.1600-0854.2010.01087.x
48. Geada MM, Galindo I, Lorenzo MM, Perdiguero B, Blasco R. 2001. Movements of vaccinia virus intracellular enveloped virions with GFP tagged to the F13L envelope protein. J Gen Virol 82:2747-2760. http://dx.doi.org/10.1099/0022-1317-82-11-2747
49. Hollinshead M, Rodger G, Van Eijl H, Law M, Hollinshead R, Vaux DJ, Smith GL. 2001. Vaccinia virus utilizes microtubules for movement to the cell surface. J Cell Biol 154:389-402. http://dx.doi.org/10.1083/jcb.200104124
50. Rietdorf J, Ploubidou A, Reckmann I, Holmström A, Frischknecht F, Zettl M, Zimmerman T, Way M. 2001. Kinesin dependent movement on microtubules precedes actin based motility of vaccinia virus. Nat Cell Biol 3:992-1000. http://dx.doi.org/10.1038/ncb1101-992
51. Ward BM, Moss B. 2001. Vaccinia virus intracellular movement is associated with microtubules and independent of actin tails. J Virol 75:11651-11663 http://dx.doi.org/10.1128/JVI.75.23.11651-11663.2001
52. Ward BM, Moss B. 2001. Visualization of intracellular movement of vaccinia virus virions containing a green fluorescent protein-B5R membrane protein chimera. J Virol 75:4802-4813. http://dx.doi.org/10.1128/JVI.75.10.4802-4813.2001
53. Boulter EA, Appleyard G. 1973. Differences between extracellular and intracellular forms of poxvirus and their implications. Prog Med Virol 16:86-108
54. Payne LG. 1980. Significance of extracellular virus in the in vitro and in vivo dissemination of vaccinia virus. J Gen Virol 50:89-100. http://dx.doi.org/10.1099/0022-1317-50-1-89
55. 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
56. Stokes GV. 1976. High-voltage electron microscope study of the release of vaccinia virus from whole cells. J Virol 18:636-643
57. Herrero-Martinez E, Roberts KL, Hollinshead M, Smith GL. 2005. Vaccinia virus intracellular enveloped virions move to the cell periphery on microtubules in the absence of the A36R protein. J Gen Virol 86:2961-2968. http://dx.doi.org/10.1099/vir.0.81260-0
58. 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 RLM, 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
59. Husain M, Moss B. 2003. Intracellular trafficking of a palmitoylated membrane-associated protein component of enveloped vaccinia virus. J Virol 77:9008-9019. http://dx.doi.org/10.1128/JVI.77.16.9008-9019.2003
60. Chen YL, Honeychurch KM, Yang G, Byrd CM, Harver C, Hruby DE, Jordan R. 2009. Vaccinia virus p37 interacts with host proteins associated with LE-derived transport vesicle biogenesis. Virology J 6:44. http://dx.doi.org/10.1186/1743-422X-6-44
61. Tooze J, Hollinshead M. 1991. Tubular early endosomal networks in AtT20 and other cells. J Cell Biol 115:635-653. http://dx.doi.org/10.1083/jcb.115.3.635
62. 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
63. Lorenzo MM, Sanchez-Puig JM, Blasco R. 2012. Mutagenesis of the palmitoylation site in vaccinia virus envelope glycoprotein B5. J Gen Virol 93:733-743. http://dx.doi.org/10.1099/vir.0.039016-0
64. Ponting CP, Kerr ID. 1996. A novel family of phospholipase D homologues that includes phospholipid synthases and putative endonucleases: identification of duplicated repeats and potential active site residues. Protein Sci 5:914-922
65. Koonin EV. 1997. Evidence for a family of archaeal ATPases. Science 275:1489-1490. http://dx.doi.org/10.1126/science.275.5305.1489
66. Sung T-C, Roper RL, Zhang Y, Rudge SA, Temel R, Hammond SM, Morris AJ, Moss B, Engebrecht J, Frohman MA. 1997. Mutagenesis of phospholipase D defines a superfamily including a trans-Golgi viral protein required for poxvirus pathogenicity. EMBO J 16:4519-4530. http://dx.doi.org/10.1093/emboj/16.15.4519
67. Roper RL, Moss B. 1999. Envelope formation is blocked by mutation of a sequence related to the HKD phospholipid metabolism motif in the vaccinia virus F13L protein. J Virol 73:1108-1117
68. Husain M, Moss B. 2002. Similarities in the induction of post-Golgi vesicles by vaccinia virus F13L protein and phospholipase D. J Virol 76: 7777-7789. http://dx.doi.org/10.1128/JVI.76.15.7777-7789.2002
69. Baek S-H, Kwak J-Y, Lee SH, Lee T, Ryu SH, Uhlinger DJ, Lambeth JD. 1997. Lipase activities of p37, the major envelope protein of vaccinia virus. J Biol Chem 272:32042-32049. http://dx.doi.org/10.1074/jbc.272.51.32042
70. Kato N, Eggers HJ, Rolly H. 1969. Inhibition of release of vaccinia virus by N1-isonicotinoyl-N2-3-methyl-4-chlorobenzoylhydrazine. J Exp Med 129:795-808
71. Payne LG, Kristenson K. 1979. Mechanism of vaccinia virus release and its specific inhibition by N1-isonicatinoyl-N2-3-methyl-4-chlorobenzoylhydrazine. J Virol 32:614-622
72. Hiller G, Eibl H, Weber K. 1981. Characterization of intracellular and extracellular vaccinia virus variants: N1-isonicotinoyl-N2-3-methyl-4-chlorobenzoylhydrazine interferes with cytoplasmic virus dissemination and release. J Virol 39:903-913
73. Schmutz C, Payne LG, Gubser J, Wittek R. 1991. A mutation in the gene encoding the vaccinia virus 37,000-Mr protein confers resistance to an inhibitor of virus envelopment and release. J Virol 65:3435-3442
74. 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
75. Huggins J, GoffA, Hensley L, Mucker E, Shamblin J, Wlazlowski C, Johnson W, Chapman J, Larsen T, Twenhafel N, Karem K, Damon IK, Byrd CM, Bolken TC, Jordan R, Hruby D. 2009. Nonhuman primates are protected from smallpox virus or monkeypox virus challenges by the antiviral drug ST-246. Antimicrob Agents Chemother 53:2620-2625. http://dx.doi.org/10.1128/AAC.00021-09
76. Chinsangaram J, Honeychurch KM, Tyavanagimatt SR, Leeds JM, Bolken TC, Jones KF, Jordan R, Marbury T, Ruckle J, Mee-Lee D, Ross E, Lichtenstein I, Pickens M, Corrado M, Clarke JM, Frimm AM, Hruby DE. 2012. Safety and pharmacokinetics of the anti-orthopoxvirus compound ST-246 following a single daily oral dose for 14 days in human volunteers. Antimicrob Agents Chemother 56:4900-4905. http://dx.doi.org/10.1128/AAC.00904-12
77. 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
78. 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
79. Carney DW, Nelson CD, Ferris BD, Stevens JP, Lipovsky A, Kazakov T, DiMaio D, Atwood WJ, Sello JK. 2014. Structural optimization of a retrograde trafficking inhibitor that protects cells from infections by human polyoma-and papillomaviruses. Bioorg Med Chem 22:4836-4847. http://dx.doi.org/10.1016/j.bmc.2014.06.053
80. 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