Imaging the alphavirus exit pathway

Journal of Virology

Volumn 88, Issue 12, 2014, Pages 6922-6933

  Martinez, Maria Guadalupe ^a   Snapp, Erik Lee ^a   Perumal, Geoffrey S ^a   Macaluso, Frank P ^a   Kielian, Margaret ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAPSID PROTEIN; GLYCOPROTEIN E2; TUBULIN;

ALPHA VIRUS; ARTICLE; CELL MEMBRANE; CELL SURFACE; CONTROLLED STUDY; FILOPODIUM; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; SINDBIS VIRUS; VIRUS ASSEMBLY; VIRUS MUTANT; VIRUS RELEASE;

ALPHAVIRUS INFECTIONS; ANIMALS; CELL LINE; CELL MEMBRANE; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; HUMANS; SINDBIS VIRUS; VIRUS ASSEMBLY; VIRUS RELEASE;

EID: 84901369454     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00592-14     Document Type: Article

References (56)

1. GaroffH, Hewson R, Opstelten D-JE. 1998. Virus maturation by budding. Microbiol. Mol. Biol. Rev. 62:1171-1190.
2. Hunter E. 2007. Virus assembly, p 141-168. In Knipe DM, Howley PM, Griffin DE, Lamb RA, Martin MA, Roizman B, Straus SE (ed), Fields virology, 5th ed, vol 1. Lippincott Williams & Wilkins, Philadelphia, PA.
3. Weissenhorn W, Poudevigne E, Effantin G, Bassereau P. 2013. How to get out: ssRNA enveloped viruses and membrane fission. Curr. Opin. Virol. 3:159-167. http://dx.doi.org/10.1016/j.coviro.2013.03.011.
4. Weiss ER, Gottlinger H. 2011. The role of cellular factors in promoting HIV budding. J. Mol. Biol. 410:525-533. http://dx.doi.org/10.1016/j.jmb.2011.04.055.
5. Rossman JS, Jing X, Leser GP, Lamb RA. 2010. Influenza virus M2 protein mediates ESCRT-independent membrane scission. Cell 142:902-913. http://dx.doi.org/10.1016/j.cell.2010.08.029.
6. Kuhn RJ. 2007. Togaviridae: the viruses and their replication, p 1001-1022. In Knipe DM, Howley PM, Griffin DE, Lamb RA, Martin MA, Roizman B, Straus SE (ed), Fields virology, 5th ed, vol 1. Lippincott Williams& Wilkins, Philadelphia, PA.
7. Enserink M. 2007. Infectious diseases. Chikungunya: no longer a Third World disease. Science 318:1860-1861. http://dx.doi.org/10.1126/science.318.5858.1860.
8. Kuhn RJ, Rossmann MG. 2005. Structure and assembly of icosahedral enveloped RNA viruses. Adv. Virus Res. 64:263-284. http://dx.doi.org/10.1016/S0065-3527(05)64008-0.
9. Paredes AM, Brown DT, Rothnagel R, Chiu W, Schoepp RJ, Johnston RE, Prasad BVV. 1993. Three-dimensional structure of a membranecontaining virus. Proc. Natl. Acad. Sci. U. S. A. 90:9095-9099. http://dx.doi.org/10.1073/pnas.90.19.9095.
10. Li L, Jose J, Xiang Y, Kuhn RJ, Rossmann MG. 2010. Structural changes of envelope proteins during alphavirus fusion. Nature 468:705-708. http://dx.doi.org/10.1038/nature09546.
11. Voss JE, Vaney MC, Duquerroy S, Vonrhein C, Girard-Blanc C, Crublet E, Thompson A, Bricogne G, Rey FA. 2010. Glycoprotein organization of Chikungunya virus particles revealed by X-ray crystallography. Nature 468:709-712. http://dx.doi.org/10.1038/nature09555.
12. deCurtis I, Simons K. 1988. Dissection of Semliki Forest virus glycoprotein delivery from the trans-Golgi network to the cell surface in permeabilized BHK cells. Proc. Natl. Acad. Sci. U. S. A. 85:8052-8056. http://dx.doi.org/10.1073/pnas.85.21.8052.
13. Zhang X, Fugere M, Day R, Kielian M. 2003. Furin processing and proteolytic activation of Semliki Forest virus. J. Virol. 77:2981-2989. http://dx.doi.org/10.1128/JVI.77.5.2981-2989.2003.
14. GaroffH, Sjoberg M, Cheng RH. 2004. Budding of alphaviruses. Virus Res. 106:103-116. http://dx.doi.org/10.1016/j.virusres.2004.08.008.
15. Suomalainen M, Liljeström P, GaroffH. 1992. Spike proteinnucleocapsid interactions drive the budding of alphaviruses. J. Virol. 66: 4737-4747.
16. Taylor GM, Hanson PI, Kielian M. 2007. Ubiquitin depletion and dominant-negative VPS4 inhibit rhabdovirus budding without affecting alphavirus budding. J. Virol. 81:13631-13639. http://dx.doi.org/10.1128/JVI.01688-07.
17. Zhao H, Lindqvist B, GaroffH, von BonsdorffC-H, Liljeström P. 1994. A tyrosine-based motif in the cytoplasmic domain of the alphavirus envelope protein is essential for budding. EMBO J. 13:4204-4211.
18. Lee S, Owen KE, Choi H-K, Lee H, Lu G, Wengler G, Brown DT, Rossmann MG, Kuhn RJ. 1996. Identification of a protein binding site on the surface of the alphavirus nucleocapsid and its implication in virus assembly. Structure 4:531-541. http://dx.doi.org/10.1016/S0969-2126 (96)00059-7.
19. Skoging U, Vihinen M, Nilsson L, Liljeström P. 1996. Aromatic interactions define the binding of the alphavirus spike to its nucleocapsid. Structure 4:519-529. http://dx.doi.org/10.1016/S0969-2126(96)00058-5.
20. Jose J, Przybyla L, Edwards TJ, Perera R, Burgner JW, II, Kuhn RJ. 2012. Interactions of the cytoplasmic domain of Sindbis virus E2 with nucleocapsid cores promote alphavirus budding. J. Virol. 86:2585-2599. http://dx.doi.org/10.1128/JVI.05860-11.
21. Barth BU, GaroffH. 1997. The nucleocapsid-binding spike subunit E2 of Semliki Forest virus requires complex formation with the E1 subunit for activity. J. Virol. 71:7857-7865.
22. Duffus WA, Levy-Mintz P, Klimjack MR, Kielian M. 1995. Mutations in the putative fusion peptide of Semliki Forest virus affect spike protein oligomerization and virus assembly. J. Virol. 69:2471-2479.
23. Ekstrom M, Liljeström P, GaroffH. 1994. Membrane protein lateral interactions control Semliki Forest virus budding. EMBO J. 13:1058-1064.
24. von BonsdorffC-H, Harrison SC. 1978. Hexagonal glycoprotein arrays from Sindbis virus membranes. J. Virol. 28:578-583.
25. Mukhopadhyay S, Zhang W, Gabler S, Chipman PR, Strauss EG, Strauss JH, Baker TS, Kuhn RJ, Rossmann MG. 2006. Mapping the structure and function of the E1 and E2 glycoproteins in alphaviruses. Structure 14:63-73. http://dx.doi.org/10.1016/j.str.2005.07.025.
26. Brown DT, Waite MR, Pfefferkorn ER. 1972. Morphology and morphogenesis of Sindbis virus as seen with freeze-etching techniques. J. Virol. 10:524-536.
27. Birdwell CR, Strauss EG, Strauss JH. 1973. Replication of Sindbis virus. III. An electron microscopic study of virus maturation using the surface replica technique. Virology 56:429-438.
28. Pavan A, Lotti LV, Torrisi MR, Migliaccio G, Bonatti S. 1987. Regional distribution of Sindbis virus glycoproteins on the plasma membrane of infected baby hamster kidney cells. Exp. Cell Res. 168:53-62. http://dx.doi.org/10.1016/0014-4827(87)90415-0.
29. Jouvenet N, Bieniasz PD, Simon SM. 2008. Imaging the biogenesis of individual HIV-1 virions in live cells. Nature 454:236-240. http://dx.doi.org/10.1038/nature06998.
30. Gousset K, Ablan SD, Coren LV, Ono A, Soheilian F, Nagashima K, Ott DE, Freed EO. 2008. Real-time visualization of HIV-1 GAG trafficking in infected macrophages. PLoS Pathog. 4:e1000015. http://dx.doi.org/10.1371/journal.ppat.1000015.
31. Ivanchenko S, Godinez WJ, Lampe M, Krausslich HG, Eils R, Rohr K, Brauchle C, Muller B, Lamb DC. 2009. Dynamics of HIV-1 assembly and release. PLoS Pathog. 5:e1000652. http://dx.doi.org/10.1371/journal.ppat.1000652.
32. Snyder JE, Azizgolshani O, Wu B, He Y, Lee AC, Jose J, Suter DM, Knobler CM, Gelbart WM, Kuhn RJ. 2011. Rescue of infectious particles from preassembled alphavirus nucleocapsid cores. J. Virol. 85:5773-5781. http://dx.doi.org/10.1128/JVI.00039-11.
33. Dai HS, Liu Z, Jiang W, Kuhn RJ. 2013. Directed evolution of a virus exclusively utilizing human epidermal growth factor receptor as the entry receptor. J. Virol. 87:11231-11243. http://dx.doi.org/10.1128/JVI.01054-13.
34. Tsvetkova IB, Cheng F, Ma X, Moore AW, Howard B, Mukhopadhyay S, Dragnea B. 2013. Fusion of mApple and Venus fluorescent proteins to the Sindbis virus E2 protein leads to different cell-binding properties. Virus Res. 177:138-146. http://dx.doi.org/10.1016/j.virusres.2013.07.014.
35. Zheng Y, Kielian M. 2013. Imaging of the alphavirus capsid protein during virus replication. J. Virol. 87:9579-9589. http://dx.doi.org/10.1128/JVI.01299-13.
36. Bulbarelli A, Sprocati T, Barberi M, Pedrazzini E, Borgese N. 2002. Trafficking of tail-anchored proteins: transport from the endoplasmic reticulum to the plasma membrane and sorting between surface domains in polarised epithelial cells. J. Cell Sci. 115:1689-1702.
37. Meyer WJ, Johnston RE. 1993. Structural rearrangement of infecting Sindbis virions at the cell surface: mapping of newly accessible epitopes. J. Virol. 67:5117-5125.
38. Greiser-Wilke I, Moennig V, Kaaden O-R, Figueiredo LTM. 1989. Most alphaviruses share a conserved epitopic region on their nucleocapsid protein. J. Gen. Virol. 70:743-748. http://dx.doi.org/10.1099/0022-1317-70-3-743.
39. Hardwick JM, Levine B. 2000. Sindbis virus vector system for functional analysis of apoptosis regulators. Methods Enzymol. 322:492-508. http://dx.doi.org/10.1016/S0076-6879(00)22045-4.
40. Heidner HW, Johnston RE. 1994. The amino-terminal residue of Sindbis virus glycoprotein E2 influences virus maturation, specific infectivity for BHK cells, and virulence in mice. J. Virol. 68:8064-8070.
41. Giordano F, Saheki Y, Idevall-Hagren O, Colombo SF, Pirruccello M, Milosevic I, Gracheva EO, Bagriantsev SN, Borgese N, De Camilli P. 2013. PI(4,5)P(2)-dependent and Ca(2)-regulated ER-PM interactions mediated by the extended synaptotagmins. Cell 153:1494-1509. http://dx.doi.org/10.1016/j.cell.2013.05.026.
42. Shaner NC, Steinbach PA, Tsien RY. 2005. A guide to choosing fluorescent proteins. Nat. Methods 2:905-909. http://dx.doi.org/10.1038/nmeth819.
43. Liljeström P, Lusa S, Huylebroeck D, GaroffH. 1991. In vitro mutagenesis of a full-length cDNA clone of Semliki Forest virus: the small 6,000-molecular-weight membrane protein modulates virus release. J. Virol. 65: 4107-4113.
44. Chanel-Vos C, Kielian M. 2004. A conserved histidine in the ij loop of the Semliki Forest virus E1 protein plays an important role in membrane fusion. J. Virol. 78:13543-13552. http://dx.doi.org/10.1128/JVI.78.24.13543-13552.2004.
45. Dovas A, Gligorijevic B, Chen X, Entenberg D, Condeelis J, Cox D. 2011. Visualization of actin polymerization in invasive structures of macrophages and carcinoma cells using photoconvertible beta-actin-Dendra2 fusion proteins. PLoS One 6:e16485. http://dx.doi.org/10.1371/journal.pone.0016485.
46. Aronson DE, Costantini LM, Snapp EL. 2011. Superfolder GFP is fluorescent in oxidizing environments when targeted via the Sec translocon. Traffic 12:543-548. http://dx.doi.org/10.1111/j.1600-0854.2011.01168.x.
47. Larson DR, Johnson MC, Webb WW, Vogt VM. 2005. Visualization of retrovirus budding with correlated light and electron microscopy. Proc. Natl. Acad. Sci. U. S. A. 102:15453-15458. http://dx.doi.org/10.1073/pnas.0504812102.
48. Skoging-Nyberg U, Liljestrom P. 2001. M-X-I motif of Semliki Forest virus capsid protein affects nucleocapsid assembly. J. Virol. 75:4625-4632. http://dx.doi.org/10.1128/JVI.75.10.4625-4632.2001.
49. Chardin P, McCormick F. 1999. Brefeldin A: the advantage of being uncompetitive. Cell 97:153-155. http://dx.doi.org/10.1016/S0092-8674 (00)80724-2.
50. Griffiths G, Quinn P, Warren G. 1983. Dissection of the Golgi complex. I. Monensin inhibits the transport of viral membrane proteins from medial to trans Golgi cisternae in baby hamster kidney cells infected with Semliki forest virus. J. Cell Biol. 96:835-850.
51. Laakkonen P, Auvinen P, Kujala P, Kääriäinen L. 1998. Alphavirus replicase protein NSP1 induces filopodia and rearrangement of actin filaments. J. Virol. 72:10265-10269.
52. Mattila PK, Lappalainen P. 2008. Filopodia: molecular architecture and cellular functions. Nat. Rev. Mol. Cell Biol. 9:446-454. http://dx.doi.org/10.1038/nrm2406.
53. Kim S, Dynlacht BD. 2013. Assembling a primary cilium. Curr. Opin. Cell Biol. 25:506-511. http://dx.doi.org/10.1016/j.ceb.2013.04.011.
54. Johnson DC, Schlesinger MJ, Elson EL. 1981. Fluorescence photobleaching recovery measurements reveal differences in envelopment of Sindbis and vesicular stomatitis viruses. Cell 23:423-431. http://dx.doi.org/10.1016/0092-8674(81)90137-9.
55. Pavan A, Covelli E, Pascale MC, Lucania G, Bonatti S, Pinto Da Silva P, Torrisi MR. 1992. Dynamics of transmembrane proteins during Sindbis virus budding. J. Cell Sci. 102:149-155.
56. Lulla V, Kim DY, Frolova EI, Frolov I. 2013. The amino-terminal domain of alphavirus capsid protein is dispensable for viral particle assembly but regulates RNA encapsidation through cooperative functions of its subdomains. J. Virol. 87:12003-12019. http://dx.doi.org/10.1128/JVI.01960-13.