Us9-independent axonal sorting and transport of the pseudorabies virus glycoprotein gM

Journal of Virology

Volumn 89, Issue 12, 2015, Pages 6511-6514

  Kratchmarov, R ^a,c   Enquist, L W ^a   Taylor, M P ^a,b  

^a PRINCETON UNIVERSITY   (United States)

^b MONTANA STATE UNIVERSITY   (United States)

^c New York Presbyterian Columbia University Medical Center   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPROTEIN M; UNCLASSIFIED DRUG; VIRUS GLYCOPROTEIN; LIPOPROTEIN; PHOSPHOPROTEIN; PSEUDORABIES VIRUS GLYCOPROTEINS; US9 PROTEIN, SUID HERPESVIRUS 1; VIRUS ENVELOPE PROTEIN; VIRUS PROTEIN;

ARTICLE; CONTROLLED STUDY; MOLECULAR DYNAMICS; NERVE FIBER; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN TARGETING; PROTEIN TRANSPORT; PSEUDORABIES VIRUS; VIRUS IDENTIFICATION; VIRUS STRAIN; METABOLISM; PHYSIOLOGY; VIROLOGY;

SUID HERPESVIRUS 1;

AXONS; HERPESVIRUS 1, SUID; LIPOPROTEINS; PHOSPHOPROTEINS; PROTEIN TRANSPORT; VIRAL ENVELOPE PROTEINS; VIRAL PROTEINS;

EID: 84929600859     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00625-15     Document Type: Article

References (31)

1. Pomeranz LE, Reynolds AE, Hengartner CJ. 2005. Molecular biology of pseudorabies virus: impact on neurovirology and veterinary medicine. Microbiol Mol Biol Rev 69:462-500. http://dx.doi.org/10.1128/MMBR.69.3.462-500.2005.
2. Granstedt AE, Bosse JB, Thiberge SY, Enquist LW. 2013. In vivo imaging of alphaherpesvirus infection reveals synchronized activity dependent on axonal sorting of viral proteins. Proc Natl Acad Sci USA 110:E3516-E3525. http://dx.doi.org/10.1073/pnas.1311062110.
3. Smith G. 2012. Herpesvirus transport to the nervous system and back again. Annu Rev Microbiol 66:153-176. http://dx.doi.org/10.1146/annurev-micro-092611-150051.
4. Tomishima MJ, Enquist LW. 2001. A conserved alpha-herpesvirus protein necessary for axonal localization of viral membrane proteins. J Cell Biol 154:741-752. http://dx.doi.org/10.1083/jcb.200011146.
5. Brideau AD, Banfield BW, Enquist LW. 1998. The Us9 gene product of pseudorabies virus, an alphaherpesvirus, is a phosphorylated, tailanchored type II membrane protein. J Virol 72:4560-4570.
6. Kramer T, Greco TM, Taylor MP, Ambrosini AE, Cristea IM, Enquist LW. 2012. Kinesin-3 mediates axonal sorting and directional transport of alphaherpesvirus particles in neurons. Cell Host Microbe 12:806-814. http://dx.doi.org/10.1016/j.chom.2012.10.013.
7. 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.
8. Mettenleiter TC, Klupp BG, Granzow H. 2009. Herpesvirus assembly: an update. Virus Research 143:222-234. http://dx.doi.org/10.1016/j.virusres.2009.03.018.
9. 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.
10. McLauchlan J, Rixon FJ. 1992. Characterization of enveloped tegument structures (L particles) produced by alphaherpesviruses: integrity of the tegument does not depend on the presence of capsid or envelope. J Gen Virol 73:269-276. http://dx.doi.org/10.1099/0022-1317-73-2-269.
11. Taylor MP, Kramer T, Lyman MG, Kratchmarov R, Enquist LW. 2012. Visualization of an alphaherpesvirus membrane protein that is essential for anterograde axonal spread of infection in neurons. mBio 3:e00063-12. http://dx.doi.org/10.1128/mBio.00063-12.
12. Liu WW, Goodhouse J, Jeon NL, Enquist LW. 2008. A microfluidic chamber for analysis of neuron-to-cell spread and axonal transport of an alpha-herpesvirus. PLoS One 3:e2382. http://dx.doi.org/10.1371/journal.pone.0002382.
13. Alemañ N, Quiroga MI, López-Peña M, Vázquez S, Guerrero FH, Nieto JM. 2003. L-particle production during primary replication of pseudorabies virus in the nasal mucosa of swine. J Virol 77:5657-5667. http://dx.doi.org/10.1128/JVI.77.10.5657-5667.2003.
14. Antinone SE, Zaichick SV, Smith GA. 2010. Resolving the assembly state of herpes simplex virus during axon transport by live-cell imaging. J Virol 84:13019-13030. http://dx.doi.org/10.1128/JVI.01296-10.
15. LaVail JH, Tauscher AN, Sucher A, Harrabi O, Brandimarti R. 2007. Viral regulation of the long distance axonal transport of herpes simplex virus nucleocapsid. Neuroscience 146:974-985. http://dx.doi.org/10.1016/j.neuroscience.2007.02.010.
16. Brideau AD, Card JP, Enquist LW. 2000. Role of pseudorabies virus Us9, a type II membrane protein, in infection of tissue culture cells and the rat nervous system. J Virol 74:834-845. http://dx.doi.org/10.1128/JVI.74.2.834-845.2000.
17. Kratchmarov R, Kramer T, Greco TM, Taylor MP, Ch'ng TH, Cristea IM, Enquist LW. 2013. Glycoproteins gE and gI are required for efficient KIF1A-dependent anterograde axonal transport of alphaherpesvirus particles in neurons. J Virol 87:9431-9440. http://dx.doi.org/10.1128/JVI.01317-13.
18. Lyman MG, Feierbach B, Curanovic D, Bisher M, Enquist LW. 2007. Pseudorabies virus Us9 directs axonal sorting of viral capsids. J Virol 81: 11363-11371. http://dx.doi.org/10.1128/JVI.01281-07.
19. Lyman MG, Curanovic D, Enquist LW. 2008. Targeting of pseudorabies virus structural proteins to axons requires association of the viral Us9 protein with lipid rafts. PLoS Pathog 4:e1000065. http://dx.doi.org/10.1371/journal.ppat.1000065.
20. 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.
21. Curanovic D, Ch'ng TH, Szpara M, Enquist L. 2009. Compartmented neuron cultures for directional infection by alpha herpesviruses. Curr Protoc Cell Biol Chapter 26:Unit 26.4. http://dx.doi.org/10.1002/0471143030.cb2604s43.
22. Jöns A, Dijkstra JM, Mettenleiter TC. 1998. Glycoproteins M and N of pseudorabies virus form a disulfide-linked complex. J Virol 72:550-557.
23. Leege T, Fuchs W, Granzow H, Kopp M, Klupp BG, Mettenleiter TC. 2009. Effects of simultaneous deletion of pUL11 and glycoprotein M on virion maturation of herpes simplex virus type 1. J Virol 83:896-907. http://dx.doi.org/10.1128/JVI.01842-08.
24. Nixdorf R, Klupp BG, Mettenleiter TC. 2001. Role of the cytoplasmic tails of pseudorabies virus glycoproteins B, E andMin intracellular localization and virion incorporation. J Gen Virol 82:215-226.
25. Brack AR, Klupp BG, Granzow H, Tirabassi R, Enquist LW, Mettenleiter TC. 2000. Role of the cytoplasmic tail of pseudorabies virus glycoprotein E in virion formation. J Virol 74:4004-4016. http://dx.doi.org/10.1128/JVI.74.9.4004-4016.2000.
26. Ren Y, Bell S, Zenner HL, Lau S.-YK, Crump CM. 2012. Glycoprotein M is important for the efficient incorporation of glycoprotein H-L into herpes simplex virus type 1 particles. J Gen Virol 93:319-329. http://dx.doi.org/10.1099/vir.0.035444-0.
27. Robinson MS. 2004. Adaptable adaptors for coated vesicles. Trends Cell Biol 14:167-174. http://dx.doi.org/10.1016/j.tcb.2004.02.002.
28. Newell-Litwa K, Seong E, Burmeister M, Faundez V. 2007. Neuronal and non-neuronal functions of the AP-3 sorting machinery. J Cell Sci 120:531-541. http://dx.doi.org/10.1242/jcs.03365.
29. 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.
30. Miranda-Saksena M, Boadle RA, Aggarwal A, Tijono B, Rixon FJ, Diefenbach RJ, Cunningham AL. 2009. Herpes simplex virus utilizes the large secretory vesicle pathway for anterograde transport of tegument and envelope proteins and for viral exocytosis from growth cones of human fetal axons. J Virol 83:3187-3199. http://dx.doi.org/10.1128/JVI.01579-08.
31. Dijkstra JM, Visser N, Mettenleiter TC, Klupp BG. 1996. Identification and characterization of pseudorabies virus glycoprotein gM as a nonessential virion component. J Virol 70:5684-5688.