Venezuelan equine encephalitis virus infection of mosquito cells requires acidification as well as mosquito homologs of the endocytic proteins Rab5 and Rab7

Virology

Volumn 369, Issue 1, 2007, Pages 78-91

  Colpitts, Tonya M ^a   Moore, Andrew C ^a   Kolokoltsov, Andrey A ^a   Davey, Robert A ^a  

^a University of Texas Medical Branch School of Medicine   (United States)

Author keywords

Alphavirus; Endocytosis; Mosquito cell; Rab5; Rab7; Virus entry; Virus infection

Indexed keywords

RAB PROTEIN; RAB5 PROTEIN; RAB7 PROTEIN; UNCLASSIFIED DRUG;

ACIDIFICATION; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENCEPHALOMYELITIS; ENDOCYTOSIS; HUMAN; HUMAN CELL; MOSQUITO; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN ANALYSIS;

AMINO ACID SEQUENCE; ANIMALS; CELL LINE; CULICIDAE; ENCEPHALITIS VIRUS, VENEZUELAN EQUINE; ENDOSOMES; GENES, REPORTER; HUMANS; LUCIFERASES; MICROSCOPY, CONFOCAL; MOLECULAR SEQUENCE DATA; RAB GTP-BINDING PROTEINS; RAB5 GTP-BINDING PROTEINS; SEQUENCE ALIGNMENT; VIRUS INTERNALIZATION;

ALPHAVIRUS; MAMMALIA; VENEZUELAN EQUINE ENCEPHALITIS VIRUS;

EID: 35648935496     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2007.07.012     Document Type: Article

References (53)

1. Altschul S.F., Madden T.L., Schaffer A.A., Zhang J., Zhang Z., Miller W., and Lipman D.J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25 17 (1997) 3389-3402
2. Blanchard E., Belouzard S., Goueslain L., Wakita T., Dubuisson J., Wychowski C., and Rouille Y. Hepatitis C virus entry depends on clathrin-mediated endocytosis. J. Virol. 80 14 (2006) 6964-6972
3. Blitzer J.T., and Nusse R. A critical role for endocytosis in Wnt signaling. BMC Cell Biol. 7 (2006) 28
4. Brault A.C., Powers A.M., and Weaver S.C. Vector infection determinants of Venezuelan equine encephalitis virus reside within the E2 envelope glycoprotein. J. Virol. 76 12 (2002) 6387-6392
5. Bucci C., Parton R.G., Mather I.H., Stunnenberg H., Simons K., Hoflack B., and Zerial M. The small GTPase rab5 functions as a regulatory factor in the early endocytic pathway. Cell 70 5 (1992) 715-728
6. Bucci C., Lutcke A., Steele-Mortimer O., Olkkonen V.M., Dupree P., Chiariello M., Bruni C.B., Simons K., and Zerial M. Co-operative regulation of endocytosis by three Rab5 isoforms. FEBS Lett. 366 1 (1995) 65-71
7. Bucci C., Thomsen P., Nicoziani P., McCarthy J., and van Deurs B. Rab7: a key to lysosome biogenesis. Mol. Biol. Cell 11 2 (2000) 467-480
8. Canonico P.G., Kende M., Luscri B.J., and Huggins J.W. In-vivo activity of antivirals against exotic RNA viral infections. J. Antimicrob. Chemother. 14 Suppl. A (1984) 27-41
9. Cassell S., Edwards J., and Brown D.T. Effects of lysosomotropic weak bases on infection of BHK-21 cells by Sindbis virus. J. Virol. 52 3 (1984) 857-864
10. Chen C., and Okayama H. High-efficiency transformation of mammalian cells by plasmid DNA. Mol. Cell. Biol. 7 8 (1987) 2745-2752
11. Chu J.J., and Ng M.L. Infectious entry of West Nile virus occurs through a clathrin-mediated endocytic pathway. J. Virol. 78 19 (2004) 10543-10555
12. Craig F.F., Simmonds A.C., Watmore D., McCapra F., and White M.R. Membrane-permeable luciferin esters for assay of firefly luciferase in live intact cells. Biochem. J. 276 Pt. 3 (1991) 637-641
13. Damke H., Binns D.D., Ueda H., Schmid S.L., and Baba T. Dynamin GTPase domain mutants block endocytic vesicle formation at morphologically distinct stages. Mol. Biol. Cell 12 9 (2001) 2578-2589
14. Feng Y., Press B., and Wandinger-Ness A. Rab 7: an important regulator of late endocytic membrane traffic. J. Cell Biol. 131 6 Pt. 1 (1995) 1435-1452
15. Feng Y., Press B., Chen W., Zimmerman J., and Wandinger-Ness A. Expression and properties of Rab7 in endosome function. Methods Enzymol. 329 (2001) 175-187
16. Galperin E., and Sorkin A. Visualization of Rab5 activity in living cells by FRET microscopy and influence of plasma-membrane-targeted Rab5 on clathrin-dependent endocytosis. J. Cell Sci. 116 Pt. 23 (2003) 4799-4810
17. Glomb-Reinmund S., and Kielian M. The role of low pH and disulfide shuffling in the entry and fusion of Semliki Forest virus and Sindbis virus. Virology 248 2 (1998) 372-381
18. Guha A., Sriram V., Krishnan K.S., and Mayor S. Shibire mutations reveal distinct dynamin-independent and -dependent endocytic pathways in primary cultures of Drosophila hemocytes. J. Cell Sci. 116 Pt. 16 (2003) 3373-3386
19. Gutierrez M.G., Munafo D.B., Beron W., and Colombo M.I. Rab7 is required for the normal progression of the autophagic pathway in mammalian cells. J. Cell Sci. 117 Pt. 13 (2004) 2687-2697
20. Helenius A., Marsh M., and White J. Inhibition of Semliki forest virus penetration by lysosomotropic weak bases. J. Gen. Virol. 58 Pt. 1 (1982) 47-61
21. Hernandez R., Luo T., and Brown D.T. Exposure to low pH is not required for penetration of mosquito cells by Sindbis virus. J. Virol. 75 4 (2001) 2010-2013
22. Holt R.A., Subramanian G.M., Halpern A., Sutton G.G., Charlab R., Nusskern D.R., Wincker P., Clark A.G., Ribeiro J.M., Wides R., Salzberg S.L., Loftus B., Yandell M., Majoros W.H., Rusch D.B., Lai Z., Kraft C.L., Abril J.F., Anthouard V., Arensburger P., Atkinson P.W., Baden H., de Berardinis V., Baldwin D., Benes V., Biedler J., Blass C., Bolanos R., Boscus D., Barnstead M., Cai S., Center A., Chaturverdi K., Christophides G.K., Chrystal M.A., Clamp M., Cravchik A., Curwen V., Dana A., Delcher A., Dew I., Evans C.A., Flanigan M., Grundschober-Freimoser A., Friedli L., Gu Z., Guan P., Guigo R., Hillenmeyer M.E., Hladun S.L., Hogan J.R., Hong Y.S., Hoover J., Jaillon O., Ke Z., Kodira C., Kokoza E., Koutsos A., Letunic I., Levitsky A., Liang Y., Lin J.J., Lobo N.F., Lopez J.R., Malek J.A., McIntosh T.C., Meister S., Miller J., Mobarry C., Mongin E., Murphy S.D., O'Brochta D.A., Pfannkoch C., Qi R., Regier M.A., Remington K., Shao H., Sharakhova M.V., Sitter C.D., Shetty J., Smith T.J., Strong R., Sun J., Thomasova D., Ton L.Q., Topalis P., Tu Z., Unger M.F., Walenz B., Wang A., Wang J., Wang M., Wang X., Woodford K.J., Wortman J.R., Wu M., Yao A., Zdobnov E.M., Zhang H., Zhao Q., Zhao S., Zhu S.C., Zhimulev I., Coluzzi M., della Torre A., Roth C.W., Louis C., Kalush F., Mural R.J., Myers E.W., Adams M.D., Smith H.O., Broder S., Gardner M.J., Fraser C.M., Birney E., Bork P., Brey P.T., Venter J.C., Weissenbach J., Kafatos F.C., Collins F.H., and Hoffman S.L. The genome sequence of the malaria mosquito Anopheles gambiae. Science 298 5591 (2002) 129-149
23. Kahl C.A., Marsh J., Fyffe J., Sanders D.A., and Cornetta K. Human immunodeficiency virus type 1-derived lentivirus vectors pseudotyped with envelope glycoproteins derived from Ross River virus and Semliki Forest virus. J. Virol. 78 3 (2004) 1421-1430
24. Kaufman T.C., Severson D.W., and Robinson G.E. The Anopheles genome and comparative insect genomics. Science 298 5591 (2002) 97-98
25. Kolokoltsov A.A., Weaver S.C., and Davey R.A. Efficient functional pseudotyping of oncoretroviral and lentiviral vectors by Venezuelan equine encephalitis virus envelope proteins. J. Virol. 79 2 (2005) 756-763
26. Kolokoltsov A.A., Fleming E.H., and Davey R.A. Venezuelan equine encephalitis virus entry mechanism requires late endosome formation and resists cell membrane cholesterol depletion. Virology 347 2 (2006) 333-342
27. Li G., Barbieri M.A., Colombo M.I., and Stahl P.D. Structural features of the GTP-binding defective Rab5 mutants required for their inhibitory activity on endocytosis. J. Biol. Chem. 269 20 (1994) 14631-14635
28. Loftus, B.J., 2005. Aedes aegypti Sequencing Project. Broad Institute of Harvard and MIT (http://www.broad.mit.edu) and The Institute for Genomic Research (TIGR) (http://www.tigr.org) In "x", Vol. x.
29. Marsh M., and Helenius A. Virus entry into animal cells. Adv. Virus Res. 36 (1989) 107-151
30. Marsh M., and Helenius A. Virus entry: open sesame. Cell 124 4 (2006) 729-740
31. Marsh M., Kielian M.C., and Helenius A. Semliki forest virus entry and the endocytic pathway. Biochem. Soc. Trans. 12 6 (1984) 981-983
32. Matlin K.S., Reggio H., Helenius A., and Simons K. Pathway of vesicular stomatitis virus entry leading to infection. J. Mol. Biol. 156 3 (1982) 609-631
33. Paessler S., Fayzulin R.Z., Anishchenko M., Greene I.P., Weaver S.C., and Frolov I. Recombinant sindbis/Venezuelan equine encephalitis virus is highly attenuated and immunogenic. J. Virol. 77 17 (2003) 9278-9286
34. Paredes A.M., Ferreira D., Horton M., Saad A., Tsuruta H., Johnston R., Klimstra W., Ryman K., Hernandez R., Chiu W., and Brown D.T. Conformational changes in Sindbis virions resulting from exposure to low pH and interactions with cells suggest that cell penetration may occur at the cell surface in the absence of membrane fusion. Virology 324 2 (2004) 373-386
35. Rauma T., Tuukkanen J., Bergelson J.M., Denning G., and Hautala T. rab5 GTPase regulates adenovirus endocytosis. J. Virol. 73 11 (1999) 9664-9668
36. Russell P.K. Vaccines in civilian defense against bioterrorism. Emerg. Infect. Dis. 5 4 (1999) 531-533
37. Saeed M.F., Kolokoltsov A.A., and Davey R.A. Novel, rapid assay for measuring entry of diverse enveloped viruses, including HIV and rabies. J. Virol. Methods 135 2 (2006) 143-150
38. Satoh A., Tokunaga F., Kawamura S., and Ozaki K. In situ inhibition of vesicle transport and protein processing in the dominant negative Rab1 mutant of Drosophila. J. Cell Sci. 110 Pt. 23 (1997) 2943-2953
39. Satoh A.K., Tokunaga F., and Ozaki K. Rab proteins of Drosophila melanogaster: novel members of the Rab-protein family. FEBS Lett. 404 1 (1997) 65-69
40. Sharma S., Murai F., Miyanohara A., and Friedmann T. Noninfectious virus-like particles produced by Moloney murine leukemia virus-based retrovirus packaging cells deficient in viral envelope become infectious in the presence of lipofection reagents. Proc. Natl. Acad. Sci. U.S.A. 94 20 (1997) 10803-10808
41. Sieczkarski S.B., and Whittaker G.R. Dissecting virus entry via endocytosis. J. Gen. Virol. 83 Pt. 7 (2002) 1535-1545
42. Sieczkarski S.B., and Whittaker G.R. Influenza virus can enter and infect cells in the absence of clathrin-mediated endocytosis. J. Virol. 76 20 (2002) 10455-10464
43. Sieczkarski S.B., and Whittaker G.R. Differential requirements of Rab5 and Rab7 for endocytosis of influenza and other enveloped viruses. Traffic 4 5 (2003) 333-343
44. Stenmark H., Parton R.G., Steele-Mortimer O., Lutcke A., Gruenberg J., and Zerial M. Inhibition of rab5 GTPase activity stimulates membrane fusion in endocytosis. EMBO J. 13 6 (1994) 1287-1296
45. Superti F., Seganti L., Ruggeri F.M., Tinari A., Donelli G., and Orsi N. Entry pathway of vesicular stomatitis virus into different host cells. J. Gen. Virol. 68 Pt. 2 (1987) 387-399
46. Thompson J.D., Higgins D.G., and Gibson T.J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22 22 (1994) 4673-4680
47. Trischler M., Stoorvogel W., and Ullrich O. Biochemical analysis of distinct Rab5- and Rab11-positive endosomes along the transferrin pathway. J. Cell Sci. 112 Pt. 24 (1999) 4773-4783
48. van Dam E.M., and Stoorvogel W. Dynamin-dependent transferrin receptor recycling by endosome-derived clathrin-coated vesicles. Mol. Biol. Cell 13 1 (2002) 169-182
49. Vonderheit A., and Helenius A. Rab7 associates with early endosomes to mediate sorting and transport of Semliki forest virus to late endosomes. PLoS Biol. 3 7 (2005) e233
50. Weaver S.C., Ferro C., Barrera R., Boshell J., and Navarro J.C. Venezuelan equine encephalitis. Annu. Rev. Entomol. 49 (2004) 141-174
51. Wucherpfennig T., Wilsch-Brauninger M., and Gonzalez-Gaitan M. Role of Drosophila Rab5 during endosomal trafficking at the synapse and evoked neurotransmitter release. J. Cell Biol. 161 3 (2003) 609-624
52. Zerial M., and Stenmark H. Rab GTPases in vesicular transport. Curr. Opin. Cell Biol. 5 4 (1993) 613-620
53. Zhao Y.G., and Eggleston P. Comparative analysis of promoters for transient gene expression in cultured mosquito cells. Insect. Mol. Biol. 8 1 (1999) 31-38