Exocytosis of alphaherpesvirus virions, light particles, and glycoproteins uses constitutive secretory mechanisms

mBio

Volumn 7, Issue 3, 2016, Pages

  Hogue, Ian B ^a   Scherer, Julian ^a   Enquist, Lynn W ^a  

^a PRINCETON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPROTEIN; FLUORESCENT DYE; RAB PROTEIN; VIRUS ENVELOPE PROTEIN;

ARTICLE; CAUSAL ATTRIBUTION; CELL MEMBRANE; CELL SURFACE; CONTROLLED STUDY; EXOCYTOSIS; EXOSOME; HERPES SIMPLEX ENCEPHALITIS; HERPES SIMPLEX VIRUS 1; HERPES SIMPLEX VIRUS 2; NONHUMAN; PRIORITY JOURNAL; RECURRENT INFECTION; SECRETION (PROCESS); VARICELLA ZOSTER VIRUS; VIRION; VIRUS ASSEMBLY; VIRUS PARTICLE; ANIMAL; CELL LINE; CHEMISTRY; FLUORESCENCE MICROSCOPY; HUMAN; IMMUNE EVASION; METABOLISM; PATHOGENICITY; PH; PHYSIOLOGY; PIG; PROCEDURES; PROTEIN TRANSPORT; PSEUDORABIES VIRUS; TRANSPORT AT THE CELLULAR LEVEL; ULTRASTRUCTURE;

ANIMALS; BIOLOGICAL TRANSPORT; CELL LINE; CELL MEMBRANE; EXOCYTOSIS; FLUORESCENT DYES; GLYCOPROTEINS; HERPESVIRUS 1, HUMAN; HERPESVIRUS 1, SUID; HERPESVIRUS 2, HUMAN; HUMANS; HYDROGEN-ION CONCENTRATION; IMMUNE EVASION; MICROSCOPY, FLUORESCENCE; PROTEIN TRANSPORT; RAB GTP-BINDING PROTEINS; SUS SCROFA; VIRAL ENVELOPE PROTEINS; VIRION; VIRUS ASSEMBLY;

EID: 84979021947     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.00820-16     Document Type: Article

References (41)

1. Sodeik B. 2000. Mechanisms of viral transport in the cytoplasm. Trends Microbiol 8:465-472. http://dx.doi.org/10.1016/S0966-842X(00)01824-2.
2. Henaff D, Radtke K, Lippé R. 2012. Herpesviruses exploit several host compartments for envelopment. Traffic 13:1443-1449. http://dx.doi.org/10.1111/j.1600-0854.2012.01399.x.
3. Favoreel HW. 2006. The why’s of Y-based motifs in alphaherpesvirus envelope proteins. Virus Res 117:202-208. http://dx.doi.org/10.1016/j.virusres.2005.11.007.
4. Brideau AD, Enquist LW, Tirabassi RS. 2000. The role of virion membrane protein endocytosis in the herpesvirus life cycle. J Clin Virol 17: 69-82. http://dx.doi.org/10.1016/S1386-6532(00)00084-6.
5. Ndjamen B, Farley AH, Lee T, Fraser SE, Bjorkman PJ. 2014. The herpes virus Fc receptor gE-gI mediates antibody bipolar bridging to clear viral antigens from the cell surface. PLoS Pathog 10:e1003961. http://dx.doi.org/10.1371/journal.ppat.1003961.
6. Crump CM, Bruun B, Bell S, Pomeranz LE, Minson T, Browne HM. 2004. Alphaherpesvirus glycoprotein M causes the relocalization of plasma membrane proteins. J Gen Virol 85:3517-3527. http://dx.doi.org/10.1099/vir.0.80361-0.
7. Hollinshead M, Johns HL, Sayers CL, Gonzalez-Lopez C, Smith GL, Elliott G. 2012. Endocytic tubules regulated by Rab GTPases 5 and 11 are used for envelopment of herpes simplex virus. EMBO J 31:4204-4220. http://dx.doi.org/10.1038/emboj.2012.262.
8. Szilágyi JF, Cunningham C. 1991. Identification and characterization of a novel non-infectious herpes simplex virus-related particle. J Gen Virol 72:661-668. http://dx.doi.org/10.1099/0022-1317-72-3-661.
9. Meckes DG, Raab-Traub N. 2011. Microvesicles and viral infection. J Virol 85:12844-12854. http://dx.doi.org/10.1128/JVI.05853-11.
10. Kalamvoki M, Deschamps T. 2016. Extracellular vesicles during herpes simplex virus type 1 infection: an inquire. Virol J 13:63. http://dx.doi.org/10.1186/s12985-016-0518-2.
11. Johns HL, Gonzalez-Lopez C, Sayers CL, Hollinshead M, Elliott G. 2014. Rab6 dependent post-Golgi trafficking of HSV1 envelope proteins to sites of virus envelopment. Traffic 15:157-178. http://dx.doi.org/10.1111/tra.12134.
12. Zenner HL, Yoshimura S, Barr FA, Crump CM. 2011. Analysis of Rab GTPase-activating proteins indicates that Rab1a/b and Rab43 are important for herpes simplex virus 1 secondary envelopment. J Virol 85: 8012-8021. http://dx.doi.org/10.1128/JVI.00500-11.
13. Stegen C, Yakova Y, Henaff D, Nadjar J, Duron J, Lippé R. 2013. Analysis of virion-incorporated host proteins required for herpes simplex virus type 1 infection through a RNA interference screen. PLoS One 8:e53276. http://dx.doi.org/10.1371/journal.pone.0053276.
14. Grigoriev I, Splinter D, Keijzer N, Wulf PS, Demmers J, Ohtsuka T, Modesti M, Maly IV, Grosveld F, Hoogenraad CC, Akhmanova A. 2007. Rab6 regulates transport and targeting of exocytotic carriers. Dev Cell 13:305-314. http://dx.doi.org/10.1016/j.devcel.2007.06.010.
15. Hogue IB, Bosse JB, Hu J-R, Thiberge SY, Enquist LW. 2014. Cellular mechanisms of alpha herpesvirus egress: live cell fluorescence microscopy of pseudorabies virus exocytosis. PLoS Pathog 10:e1004535. http://dx.doi.org/10.1371/journal.ppat.1004535.
16. Sankaranarayanan S, De Angelis D, Rothman JE, Ryan TA. 2000. The use of pHluorins for optical measurements of presynaptic activity. Biophys J 79:2199-2208. http://dx.doi.org/10.1016/S0006-3495(00)76468-X.
17. Schmoranzer J, Goulian M, Axelrod D, Simon SM. 2000. Imaging constitutive exocytosis with total internal reflection fluorescence microscopy. J Cell Biol 149:23-32. http://dx.doi.org/10.1083/jcb.149.1.23.
18. Kenworthy AK, Nichols BJ, Remmert CL, Hendrix GM, Kumar M, Zimmerberg J, Lippincott-Schwartz J. 2004. Dynamics of putative raftassociated proteins at the cell surface. J Cell Biol 165:735-746. http://dx.doi.org/10.1083/jcb.200312170.
19. Allersma MW, Wang L, Axelrod D, Holz RW. 2004. Visualization of regulated exocytosis with a granule-membrane probe using total internal reflection microscopy. Mol Biol Cell 15:4658-4668. http://dx.doi.org/10.1091/mbc.E04-02-0149.
20. McNab AR, Desai P, Person S, Roof LL, Thomsen DR, Newcomb WW, Brown JC, Homa FL. 1998. The product of the herpes simplex virus type 1 UL25 gene is required for encapsidation but not for cleavage of replicated viral DNA. J Virol 72:1060-1070.
21. Klupp BG, Granzow H, Keil GM, Mettenleiter TC. 2006. The capsidassociated UL25 protein of the alphaherpesvirus pseudorabies virus is nonessential for cleavage and encapsidation of genomic DNA but is required for nuclear egress of capsids. J Virol 80:6235-6246. http://dx.doi.org/10.1128/JVI.02662-05.
22. Alwine JC. 2012. The human cytomegalovirus assembly compartment: a masterpiece of viral manipulation of cellular processes that facilitates assembly and egress. PLoS Pathog 8:e1002878. http://dx.doi.org/10.1371/journal.ppat.1002878.
23. Johnson DC, Baines JD. 2011. Herpesviruses remodel host membranes for virus egress. Nat Rev Microbiol 9:382-394. http://dx.doi.org/10.1038/nrmicro2559.
24. Tandon R, Mocarski ES. 2012. Viral and host control of cytomegalovirus maturation. Trends Microbiol 20:392-401. http://dx.doi.org/10.1016/j.tim.2012.04.008.
25. Das S, Vasanji A, Pellett PE. 2007. Three-dimensional structure of the human cytomegalovirus cytoplasmic virion assembly complex includes a reoriented secretory apparatus. J Virol 81:11861-11869. http://dx.doi.org/10.1128/JVI.01077-07.
26. Cepeda V, Esteban M, Fraile-Ramos A. 2010. Human cytomegalovirus final envelopment on membranes containing both trans-Golgi network and endosomal markers. Cell Microbiol 12:386-404. http://dx.doi.org/10.1111/j.1462-5822.2009.01405.x.
27. Indran SV, Britt WJ. 2011. A role for the small GTPase Rab6 in assembly of human cytomegalovirus. J Virol 85:5213-5219. http://dx.doi.org/10.1128/JVI.02605-10.
28. Das S, Pellett PE. 2011. Spatial relationships between markers for secretory and endosomal machinery in human cytomegalovirus-infected cells versus those in uninfected cells. J Virol 85:5864-5879. http://dx.doi.org/10.1128/JVI.00155-11.
29. Krzyzaniak MA, Mach M, Britt WJ. 2009. HCMV-encoded glycoprotein M (UL100) interacts with Rab11 effector protein FIP4. Traffic 10: 1439-1457. http://dx.doi.org/10.1111/j.1600-0854.2009.00967.x.
30. Mori Y, Koike M, Moriishi E, Kawabata A, Tang H, Oyaizu H, Uchiyama Y, Yamanishi K. 2008. Human herpesvirus-6 induces MVB formation, and virus egress occurs by an exosomal release pathway. Traffic 9:1728-1742. http://dx.doi.org/10.1111/j.1600-0854.2008.00796.x.
31. Grigoriev I, Yu KL, Martinez-Sanchez E, Serra-Marques A, Smal I, Meijering E, Demmers J, Peränen J, Pasterkamp RJ, van der Sluijs P, Hoogenraad CC, Akhmanova A. 2011. Rab6, Rab8, and MICAL3 cooperate in controlling docking and fusion of exocytotic carriers. Curr Biol 21:967-974. http://dx.doi.org/10.1016/j.cub.2011.04.030.
32. Hsu VW, Prekeris R. 2010. Transport at the recycling endosome. Curr Opin Cell Biol 22:528-534. http://dx.doi.org/10.1016/j.ceb.2010.05.008.
33. Fraile-Ramos A, Cepeda V, Elstak E, van der Sluijs P. 2010. Rab27a is required for human cytomegalovirus assembly. PLoS One 5:e15318. http://dx.doi.org/10.1371/journal.pone.0015318.
34. Homman-Loudiyi M, Hultenby K, Britt W, Söderberg-Nauclér C. 2003. Envelopment of human cytomegalovirus occurs by budding into Golgiderived vacuole compartments positive for gB, Rab 3, trans-Golgi network 46, and mannosidase II. J Virol 77:3191-3203. http://dx.doi.org/10.1128/JVI.77.5.3191-3203.2003.
35. Hogue IB, Bosse JB, Engel EA, Scherer J, Hu J-R, Del Rio T, Enquist LW. 2015. Fluorescent protein approaches in alpha herpesvirus research. Viruses 7:5933-5961. http://dx.doi.org/10.3390/v7112915.
36. Antinone SE, Smith GA. 2006. Two modes of herpesvirus trafficking in neurons: membrane acquisition directs motion. J Virol 80:11235-11240. http://dx.doi.org/10.1128/JVI.01441-06.
37. Taylor MP, Kratchmarov R, Enquist LW. 2013. Live cell imaging of alphaherpes virus anterograde transport and spread. J Vis Exp 2013: e50723. http://dx.doi.org/10.3791/50723.
38. Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, Preibisch S, Rueden C, Saalfeld S, Schmid B, Tinevez J-Y, White DJ, Hartenstein V, Eliceiri K, Tomancak P, Cardona A. 2012. Fiji: an open-source platform for biological-image analysis. Nat Methods 9:676-682. http://dx.doi.org/10.1038/nmeth.2019.
39. Bosse JB, Hogue IB, Feric M, Thiberge SY, Sodeik B, Brangwynne CP, EnquistLW. 2015. Remodeling nuclear architecture allows efficient transport of herpesvirus capsids by diffusion. Proc Natl Acad Sci U S A 112: E5725-E5733. http://dx.doi.org/10.1073/pnas.1513876112.
40. Soumpasis DM. 1983. Theoretical analysis of fluorescence photobleaching recovery experiments. Biophys J 41:95-97. http://dx.doi.org/10.1016/S0006-3495(83)84410-5.
41. Kang M, Day CA, Kenworthy AK, DiBenedetto E. 2012. Simplified equation to extract diffusion coefficients from confocal FRAP data. Traffic 13:1589-1600. http://dx.doi.org/10.1111/tra.12008.