Imaging of the alphavirus capsid protein during virus replication

Journal of Virology

Volumn 87, Issue 17, 2013, Pages 9579-9589

  Zheng, Yan ^a   Kielian, Margaret ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAPSID PROTEIN; DYE;

ALPHA VIRUS; ARTICLE; CELL GRANULE; CLONE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; IMAGING; IMMUNOFLUORESCENCE; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN MOTIF; SINDBIS VIRUS; VIROGENESIS; VIRUS ASSEMBLY; VIRUS MORPHOLOGY; VIRUS NUCLEOCAPSID; VIRUS REPLICATION;

ALPHAVIRUS INFECTIONS; ANIMALS; BIOLOGICAL TRANSPORT, ACTIVE; CAPSID PROTEINS; CELL LINE; CELL MEMBRANE; CERCOPITHECUS AETHIOPS; CRICETINAE; GREEN FLUORESCENT PROTEINS; HOST-PATHOGEN INTERACTIONS; LUMINESCENT PROTEINS; SINDBIS VIRUS; VERO CELLS; VIRAL ENVELOPE PROTEINS; VIRAL NONSTRUCTURAL PROTEINS; VIRUS ASSEMBLY; VIRUS RELEASE; VIRUS REPLICATION;

EID: 84883285628     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01299-13     Document Type: Article

References (69)

1. Garoff H, Hewson R, Opstelten D-JE. 1998. Virus maturation by budding. Microbiol. Mol. Biol. Rev. 62:1171-1190.
2. 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.
3. Kuhn RJ. 2007. Togaviridae: the viruses and their replication, p 1001- 1022. In Knipe DM, Howley PM (ed), Fields virology, Fifth ed, vol 1. Lippincott, Williams and Wilkins, Philadelphia, PA.
4. Jose J, Snyder JE, Kuhn RJ. 2009. A structural and functional perspective of alphavirus replication and assembly. Future Microbiol. 4:837-856.
5. Vaney MC, Duquerroy S, Rey FA. 2013. Alphavirus structure: activation for entry at the target cell surface. Curr. Opin. Virol. 3:151-158.
6. Suomalainen M, Liljeström P, Garoff H. 1992. Spike proteinnucleocapsid interactions drive the budding of alphaviruses. J. Virol. 66: 4737-4747.
7. Zhao H, Lindqvist B, Garoff H, von Bonsdorff C-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.
8. 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.
9. 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.
10. Strauss JH, Strauss EG. 1994. The alphaviruses: gene expression, replication, and evolution. Microbiol. Rev. 58:491-562.
11. Garoff H, Sjoberg M, Cheng RH. 2004. Budding of alphaviruses. Virus Res. 106:103-116.
12. Acheson NH, Tamm I. 1967. Replication of Semliki Forest virus: an electron microscopic study. Virology 32:128-143.
13. Tellinghuisen TL, Hamburger AE, Fisher BR, Ostendorp R, Kuhn RJ. 1999. In vitro assembly of alphavirus cores by using nucleocapsid protein expressed in Escherichia coli. J. Virol. 73:5309-5319.
14. 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.
15. Cheng F, Mukhopadhyay S. 2011. Generating enveloped virus-like particles with in vitro assembled cores. Virology 413:153-160.
16. Skoging-Nyberg U, Liljestrom P. 2001. M-X-I motif of semliki forest virus capsid protein affects nucleocapsid assembly. J. Virol. 75:4625-4632.
17. Forsell K, Griffiths G, Garoff H. 1996. Preformed cytoplasmic nucleocapsids are not necessary for alphavirus budding. EMBO J. 15:6495-6505.
18. Forsell K, Xing L, Kozlovska T, Cheng RH, Garoff H. 2000. Membrane proteins organize a symmetrical virus. EMBO J. 19:5081-5091.
19. Sodeik B. 2000. Mechanisms of viral transport in the cytoplasm. Trends Microbiol. 8:465-472.
20. Scheele CM, Pfefferkorn ER. 1969. Kinetics of incorporation of structural proteins into Sindbis virions. J. Virol. 3:369-375.
21. Soderlund H, Ulmanen I. 1977. Transient association of Semliki Forest virus capsid protein with ribosomes. J. Virol. 24:907-909.
22. Ulmanen I, Soderlund H, Kaariainen L. 1976. Semliki Forest virus capsid protein associates with the 60S ribosomal subunit in infected cells. J. Virol. 20:203-210.
23. Ulmanen I, Soderlund H, Kaariainen L. 1979. Role of protein synthesis in the assembly of Semliki forest virus nucleocapsid. Virology 99:265-276.
24. Wengler G, Gros C. 1996. Analyses of the role of structural changes in the regulation of uncoating and assembly of alphavirus cores. Virology 222:123- 132.
25. Orvedahl A, MacPherson S, Sumpter R, Jr, Talloczy Z, Zou Z, Levine B. 2010. Autophagy protects against Sindbis virus infection of the central nervous system. Cell Host Microbe 7:115-127.
26. Orvedahl A, Sumpter R, Jr, Xiao G, Ng A, Zou Z, Tang Y, Narimatsu M, Gilpin C, Sun Q, Roth M, Forst CV, Wrana JL, Zhang YE, Luby-Phelps K, Xavier RJ, Xie Y, Levine B. 2011. Image-based genome-wide siRNA screen identifies selective autophagy factors. Nature 480:113-117.
27. Adams SR, Campbell RE, Gross LA, Martin BR, Walkup GK, Yao Y, Llopis J, Tsien RY. 2002. New biarsenical ligands and tetracysteine motifs for protein labeling in vitro and in vivo: synthesis and biological applications. J. Am. Chem. Soc. 124:6063-6076.
28. Hardwick JM, Levine B. 2000. Sindbis virus vector system for functional analysis of apoptosis regulators. Methods Enzymol. 322:492-508.
29. Rice CM, Levis R, Strauss JH, Huang HV. 1987. Production of infectious RNA transcripts from Sindbis virus cDNA clones: Mapping of lethal mutations, rescue of a temperature-sensitive marker, and in vitro mutagenesis to generate defined mutants. J. Virol. 61:3809-3838l9.
30. Pedelacq JD, Cabantous S, Tran T, Terwilliger TC, Waldo GS. 2006. Engineering and characterization of a superfolder green fluorescent protein. Nat. Biotechnol. 24:79-88.
31. Liljeström P, Lusa S, Huylebroeck D, Garoff H. 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.
32. 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.
33. 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.
34. Counihan NA, Rawlinson SM, Lindenbach BD. 2011. Trafficking of hepatitis C virus core protein during virus particle assembly. PLoS Pathog. 7:e1002302. doi:10.1371/journal.ppat.1002302.
35. 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. doi:10.1371/journal .ppat.1000015.
36. Snijder B, Sacher R, Ramo P, Damm EM, Liberali P, Pelkmans L. 2009. Population context determines cell-to-cell variability in endocytosis and virus infection. Nature 461:520-523.
37. 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.
38. Cristea IM, Carroll JW, Rout MP, Rice CM, Chait BT, MacDonald MR. 2006. Tracking and elucidating alphavirus-host protein interactions. J. Biol. Chem. 281:30269-30278.
39. Griffin BA, Adams SR, Tsien RY. 1998. Specific covalent labeling of recombinant protein molecules inside live cells. Science 281:269-272.
40. Rudner L, Nydegger S, Coren LV, Nagashima K, Thali M, Ott DE. 2005. Dynamic fluorescent imaging of human immunodeficiency virus type 1 gag in live cells by biarsenical labeling. J. Virol. 79:4055-4065.
41. Coller KE, Heaton NS, Berger KL, Cooper JD, Saunders JL, Randall G. 2012. Molecular determinants and dynamics of hepatitisCvirus secretion. PLoS Pathog. 8:e1002466. doi:10.1371/journal.ppat.1002466.
42. Das SC, Panda D, Nayak D, Pattnaik AK. 2009. Biarsenical labeling of vesicular stomatitis virus encoding tetracysteine-tagged m protein allows dynamic imaging of m protein and virus uncoating in infected cells. J. Virol. 83:2611-2622.
43. Coombs KM, Brown DT. 1989. Form-determining functions in Sindbis virus nucleocapsids: nucleo somelike organization of the nucleocapsid. J. Virol. 63:883-891.
44. 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.
45. Beitzel BF, Bakken RR, Smith JM, Schmaljohn CS. 2010. Highresolution functional mapping of the venezuelan equine encephalitis virus genome by insertional mutagenesis and massively parallel sequencing. PLoS Pathog. 6:e1001146. doi:10.1371/journal.ppat.1001146.
46. Choi H-K, Tong L, Minor W, Dumas P, Boege U, Rossman MG, Wengler G. 1991. Structure of Sindbis virus core protein reveals a chymotrypsin-like serine proteinase and the organization of the virion. Nature 354:37-43.
47. Salonen A, Ahola T, Kaariainen L. 2005. Viral RNA replication in association with cellular membranes. Curr. Topics Microbiol. Immunol. 285: 139-173.
48. Tourriere H, Chebli K, Zekri L, Courselaud B, Blanchard JM, Bertrand E, Tazi J. 2003. The RasGAP-associated endoribonuclease G3BP assembles stress granules. J. Cell Biol. 160:823-831.
49. McInerney GM, Kedersha NL, Kaufman RJ, Anderson P, Liljestrom P. 2005. Importance of eIF2alpha phosphorylation and stress granule assembly in alphavirus translation regulation. Mol. Biol. Cell 16:3753-3763.
50. Fros JJ, Domeradzka NE, Baggen J, Geertsema C, Flipse J, Vlak JM, Pijlman GP. 2012. Chikungunya Virus nsP3 Blocks Stress Granule Assembly by Recruitment of G3BP into Cytoplasmic Foci. J. Virol. 86: 10873-10879.
51. Frolova E, Gorchakov R, Garmashova N, Atasheva S, Vergara LA, Frolov I. 2006. Formation of nsP3-specific protein complexes during Sindbis virus replication. J. Virol. 80:4122-4134.
52. Panas MD, Varjak M, Lulla A, Er Eng K, Merits A, Karlsson Hedestam GB, McInerney GM. 2012. Sequestration of G3BP coupled with efficient translation inhibits stress granules in Semliki Forest virus infection. Mol. Biol. Cell 23:4701-4712.
53. Cheng RH, Kuhn RJ, Olson NH, Rossman MG, Choi H-K, Smith TJ, Baker TS. 1995. Nucleocapsid and glycoprotein organization in an enveloped virus. Cell 80:621-630.
54. 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.
55. Ormo M, Cubitt AB, Kallio K, Gross LA, Tsien RY, Remington SJ. 1996. Crystal structure of the Aequorea victoria green fluorescent protein. Science 273:1392-1395.
56. 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.
57. Jouvenet N, Bieniasz PD, Simon SM. 2008. Imaging the biogenesis of individual HIV-1 virions in live cells. Nature 454:236-240.
58. Lelek M, Di Nunzio F, Henriques R, Charneau P, Arhel N, Zimmer C. 2012. Superresolution imaging of HIV in infected cells with FlAsH-PALM. Proc. Natl. Acad. Sci. U. S. A. 109:8564-8569.
59. Gaietta G, Deerinck TJ, Adams SR, Bouwer J, Tour O, Laird DW, Sosinsky GE, Tsien RY, Ellisman MH. 2002. Multicolor and electron microscopic imaging of connexin trafficking. Science 296:503-507.
60. Weber F, Wagner V, Rasmussen SB, Hartmann R, Paludan SR. 2006. Double-stranded RNA is produced by positive-strand RNA viruses and DNA viruses but not in detectable amounts by negative-strand RNA viruses. J. Virol. 80:5059-5064.
61. Spuul P, Balistreri G, Hellstrom K, Golubtsov AV, Jokitalo E, Ahola T. 2011. Assembly of alphavirus replication complexes from RNA and protein components in a novel trans-replication system in mammalian cells. J. Virol. 85:4739-4751.
62. Reineke LC, Lloyd RE. 2013. Diversion of stress granules and P-bodies during viral infection. Virology 436:255-267.
63. Valiente-Echeverria F, Melnychuk L, Mouland AJ. 2012. Viral modulation of stress granules. Virus Res. 169:430-437.
64. Beckham CJ, Parker R. 2008. P bodies, stress granules, and viral life cycles. Cell Host Microbe 3:206-212.
65. White JP, Cardenas AM, Marissen WE, Lloyd RE. 2007. Inhibition of cytoplasmic mRNA stress granule formation by a viral proteinase. Cell Host Microbe 2:295-305.
66. Emara MM, Brinton MA. 2007. Interaction of TIA-1/TIAR with West Nile and dengue virus products in infected cells interferes with stress granule formation and processing body assembly. Proc. Natl. Acad. Sci. U. S. A. 104:9041-9046.
67. Foy NJ, Akhrymuk M, Akhrymuk I, Atasheva S, Bopda-Waffo A, Frolov I, Frolova EI. 2013. Hypervariable domains of nsP3 proteins of New World and Old World alphaviruses mediate formation of distinct, virusspecific protein complexes. J. Virol. 87:1997-2010.
68. Ruggieri A, Dazert E, Metz P, Hofmann S, Bergeest JP, Mazur J, Bankhead P, Hiet MS, Kallis S, Alvisi G, Samuel CE, Lohmann V, Kaderali L, Rohr K, Frese M, Stoecklin G, Bartenschlager R. 2012. Dynamic oscillation of translation and stress granule formation mark the cellular response to virus infection. Cell Host Microbe 12:71-85.
69. Cristea IM, Rozjabek H, Molloy KR, Karki S, White LL, Rice CM, Rout MP, Chait BT, MacDonald MR. 2010. Host factors associated with the Sindbis virus RNA-dependent RNA polymerase: role for G3BP1 and G3BP2 in virus replication. J. Virol. 84:6720-6732.