Deciphering novel host-herpesvirus interactions by virion proteomics

Frontiers in Microbiology

Volumn 3, Issue MAY, 2012, Pages

  Lippé, Roger ^a  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

EBV HV68; HCMV; Herpes; Host pathogen interactions; HSV; KSHV; PRV; Virus

Indexed keywords

EID: 84867231810     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2012.00181     Document Type: Short Survey

References (108)

1. Antrobus, R., Grant, K., Gangadharan, B., Chittenden, D., Everett, R. D., Zitzmann, N., and Boutell, C. (2009). Proteomic analysis of cells in the early stages of herpes simplex virus type-1 infection reveals widespread changes in the host cell proteome. Proteomics 9, 3913-3927.
2. Ashburner, M., Ball, C. A., Blake, J. A., Botstein, D., Butler, H., Cherry, J. M., Davis, A. P., Dolinski, K., Dwight, S. S., Eppig, J. T., Harris, M. A., Hill, D. P., Issel-Tarver, L., Kasarskis, A., Lewis, S., Matese, J. C., Richardson, J. E.,Ringwald,M.,Rubin,G. M.,and Sherlock, G. (2000). Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat. Genet. 25, 25-29.
3. Avitabile, E., Di Gaeta, S., Torrisi, M. R., Ward, P. L., Roizman, B., and Campadelli-Fiume, G. (1995). Redistribution of microtubules and Golgi apparatus in herpes simplex virus-infected cells and their role in viral exocytosis. J. Virol. 69, 7472-7482.
4. Bartel, S., Doellinger, J., Darsow, K., Bourquain, D., Buchholz, R., Nitsche, A., and Lange, H. A. (2011). Proteome analysis of vaccinia virus IHD-W-infected HEK 293 cells with 2-dimensional gel electrophoresis and MALDI-PSD-TOF MS of on solid phase support N-terminally sulfonated peptides. Virol. J. 8, 380.
5. Bechtel, J. T.,Winant, R. C., and Ganem, D. (2005). Host and viral proteins in the virion of Kaposis sarcomaassociated herpesvirus. J. Virol. 79, 4952-4964.
6. Bernhard, O. K., Diefenbach, R. J., and Cunningham, A. L. (2005). New insights into viral structure and virus-cell interactions through proteomics. Expert Rev. Proteomics 2, 577-588.
7. Bortz, E., Whitelegge, J. P., Jia, Q., Zhou, Z. H., Stewart, J. P., Wu, T. T., and Sun, R. (2003). Identification of proteins associated with murine gammaherpesvirus 68 virions. J. Virol. 77, 13425-13432.
8. Bringhurst, R. M., and Schaffer, P. A. (2006). Cellular stress rather than stage of the cell cycle enhances the replication and plating efficiencies of herpes simplex virus type 1 ICP0viruses. J. Virol. 80, 4528-4537.
9. Brown,C. R.,Nakamura,M. S.,Mosca,J. D., Hayward, G. S., Straus, S. E., and Perera, L. P. (1995). Herpes simplex virus trans-regulatory protein ICP27 stabilizes and binds to 3′ ends of labile mRNA. J.Virol. 69,7187-7195.
10. Bushell, M., and Sarnow, P. (2002). Hijacking the translation apparatus by RNA viruses. J. Cell Biol. 158, 395-399.
11. Cantin, R., Methot, S., and Tremblay, M. J. (2005). Plunder and stowaways: incorporation of cellular proteins by enveloped viruses. J. Virol. 79, 6577-6587.
12. Cepeda,V.,and Fraile-Ramos,A. (2011). A role for the SNARE protein syntaxin 3 in human cytomegalovirus morphogenesis. Cell. Microbiol. 13, 846-858.
13. Chen, I. H., Sciabica, K. S., and Sandri-Goldin, R. M. (2002). ICP27 interacts with the RNA export factor Aly/REF to direct herpes simplex virus type 1 intronless mRNAs to the TAP export pathway. J. Virol. 76, 12877-12889.
14. Chou, W., Ngo, T., and Gershon, P. D. (2012). An overview of the vaccinia virus infectome: a survey of the proteins of the poxvirus-infected cell. J. Virol. 86, 1487-1499.
15. Chua, C. E., Gan, B. Q., and Tang, B. L. (2011). Involvement of members of the Rab family and related small GTPases in autophagosome formation and maturation. Cell.Mol.Life Sci. 68, 3349-3358.
16. Coombs, K. M., Berard, A., Xu, W., Krokhin, O., Meng, X., Cortens, J. P., Kobasa, D., Wilkins, J., and Brown, E. G. (2010). Quantitative proteomic analyses of influenza virus-infected cultured human lung cells. J. Virol. 84, 10888-10906.
17. De Regge, N., Nauwynck, H. J., Geenen, K., Krummenacher, C., Cohen, G. H., Eisenberg, R. J., Mettenleiter, T. C., and Favoreel, H. W. (2006).Alpha-herpesvirus glycoprotein D interaction with sensory neurons triggers formation of varicosities that serve as virus exit sites. J. Cell Biol. 174, 267-275.
18. del Rio, T., Decoste, C. J., and Enquist, L. W. (2005). Actin is a component of the compensation mechanism in pseudorabies virus virions lacking the major tegument protein VP22. J. Virol. 79, 8614-8619.
19. Dohner, K., Wolfstein, A., Prank, U., Echeverri, C., Dujardin, D., Vallee, R., and Sodeik, B. (2002). Function of dynein and dynactin in herpes simplex virus capsid transport. Mol. Biol. Cell 13, 2795-2809.
20. Dry, I., Haig, D. M., Inglis, N. F., Imrie, L., Stewart, J. P., and Russell, G. C. (2008). Proteomic analysis of pathogenic and attenuated alcelaphine herpesvirus 1. J. Virol. 82, 5390-5397.
21. Ellison, K. S., Maranchuk, R. A., Mottet, K. L., and Smiley, J. R. (2005). Control of VP16 translation by the herpes simplex virus type 1 immediateearly protein ICP27. J. Virol. 79, 4120-4131.
22. Emmott,E.,Rodgers,M. A.,Macdonald, A., Mccrory, S., Ajuh, P., and Hiscox, J. A. (2010). Quantitative proteomics using stable isotope labeling with amino acids in cell culture reveals changes in the cytoplasmic, nuclear, and nucleolar proteomes in Vero cells infected with the coronavirus infectious bronchitis virus. Mol. Cell Proteomics 9, 1920-1936.
23. Everett, R. D. (2000). ICP0, a regulator of herpes simplex virus during lytic and latent infection. Bioessays 22, 761-770.
24. Feierbach, B., Piccinotti, S., Bisher, M., Denk, W., and Enquist, L. W. (2006). Alpha-herpesvirus infection induces the formation of nuclear actin filaments. PLoS Pathog. 2, e85. doi:10.1371/journal.ppat.0020085
25. Fontaine-Rodriguez, E. C., and Knipe, D. M. (2008). Herpes simplex virus ICP27 increases translation of a subset of viral late mRNAs. J. Virol. 82, 3538-3545.
26. Forest, T., Barnard, S., and Baines, J. D. (2005). Active intranuclear movement of herpesvirus capsids. Nat. Cell Biol. 7, 429-431.
27. Friedel, C. C., and Haas, J. (2011). Virus-host interactomes and global models of virus-infected cells. Trends Microbiol. 19, 501-508.
28. Goodkin, M. L., Morton, E. R., and Blaho, J. A. (2004). Herpes simplex virus infection and apoptosis. Int. Rev. Immunol. 23, 141-172.
29. Greber, U. F., and Way, M. (2006). A superhighway to virus infection. Cell 124, 741-754.
30. Grunewald, K., Desai, P., Winkler, D., Heymann, J., Belnap, D., Baumeister, W., and Steven, A. (2003). Three-dimensional structure of herpes simplex virus from cryoelectron tomography. Science 302, 1396-1398.
31. Gurer, C., Cimarelli, A., and Luban, J. (2002). specific incorporation of heat shock protein 70 family members into primate lentiviral virions. J. Virol. 76, 4666-4670.
32. Halford,W. P.,and Schaffer,P. A. (2001). ICP0 is required for efficient reactivation of herpes simplex virus type 1 from neuronal latency. J. Virol. 75, 3240-3249.
33. Hancock, M. H., Corcoran, J. A., and Smiley, J. R. (2006). Herpes simplex virus regulatory proteins VP16 and ICP0 counteract an innate intranuclear barrier to viral gene expression. Virology 352, 237-252.
34. Hardwicke, M. A., and Sandri-Goldin, R. M. (1994). The herpes simplex virus regulatory protein ICP27 contributes to the decrease in cellular mRNA levels during infection. J. Virol. 68, 4797-4810.
35. Hardy, W. R., and Sandri-Goldin, R. M. (1994). Herpes simplex virus inhibits host cell splicing, and regulatory protein ICP27 is required for this effect. J. Virol. 68, 7790-7799.
36. Hertel, L. (2011). Herpesviruses and intermediate filaments: close encounters with the third type. Viruses 3, 1015-1040.
37. Hobbs, W. E. II, and DeLuca, N. A. (1999). Perturbation of cell cycle progression and cellular gene expression as a function of herpes simplex virus ICP0. J. Virol. 73, 8245-8255.
38. Huang Da, W., Sherman, B. T., and Lempicki, R. A. (2009). Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4, 44-57.
39. Indran, S. V., and Britt, W. J. (2011). A role for the small GTPase Rab6 in assembly of human cytomegalovirus. J. Virol. 85, 5213-5219.
40. Johannsen, E., Luftig, M., Chase, M. R., Weicksel, S., Cahir-Mcfarland, E., Illanes,D.,Sarracino,D.,and Kieff,E. (2004). Proteins of purified EpsteinBarr virus. Proc. Natl. Acad. Sci. U.S.A. 101, 16286-16291.
41. Kanehisa, M., Goto, S., Furumichi, M., Tanabe, M., and Hirakawa, M. (2010). KEGG for representation and analysis of molecular networks involving diseases and drugs. Nucleic Acids Res. 38, D355-D360.
42. Kattenhorn, L. M., Mills, R., Wagner, M., Lomsadze, A., Makeev, V., Borodovsky, M., Ploegh, H. L., and Kessler, B. M. (2004). Identification of proteins associated with murine cytomegalovirus virions. J. Virol. 78, 11187-11197.
43. Kawaguchi, Y., Van Sant, C., and Roizman,B. (1997). Herpes simplex virus 1 alpha regulatory protein ICP0 interacts with and stabilizes the cell cycle regulator cyclin D3. J. Virol. 71, 7328-7336.
44. Kramer, T., Greco, T. M., Enquist, L. W., and Cristea, I. M. (2011). Proteomic characterization of pseudorabies virus extracellular virions. J. Virol. 85, 6427-6441.
45. Krauss, O., Hollinshead, R., Hollinshead, M., and Smith, G. L. (2002). An investigation of incorporation of cellular antigens into vaccinia virus particles. J. Gen. Virol. 83, 2347-2359.
46. Kubista, H., Edelbauer, H., and Boehm, S. (2004). Evidence for structural and functional diversity among SDS-resistant SNARE complexes in neuroendocrine cells. J. Cell. Sci. 117, 955-966.
47. Lam, Q., Smibert, C. A., Koop, K. E., Lavery, C., Capone, J. P., Weinheimer, S. P., and Smiley, J. R. (1996). Herpes simplex virus VP16 rescues viral mRNA from destruction by the virion host shutoff function. EMBO J. 15, 2575-2581.
48. Larralde, O., Smith, R. W., Wilkie, G. S., Malik, P., Gray, N. K., and Clements, J. B. (2006). Direct stimulation of translation by the multifunctional herpesvirus ICP27 protein. J. Virol. 80, 1588-1591.
49. Lee, G. E., Murray, J. W., Wolkoff, A. W., and Wilson, D. W. (2006). Reconstitution of herpes simplex virus microtubule-dependent trafficking in vitro. J. Virol. 80, 4264-4275.
50. Lietzen, N., Ohman, T., Rintahaka, J., Julkunen, I., Aittokallio, T., Matikainen, S., and Nyman, T. A. (2011). Quantitative subcellular proteome and secretome profiling of influenza A virus-infected human primary macrophages. PLoS Pathog. 7, e1001340. doi:10.1371/journal.ppat.1001340
51. Lindberg, A., and Kreivi, J. P. (2002). Splicing inhibition at the level of spliceosome assembly in the presence of herpes simplex virus protein ICP27. Virology 294, 189-198.
52. Lodish, H., Berk, A., Zipursky, S. L., Matsudaira, P., Baltimore, D., and Darnell, J. (2000). Viruses: Structure, Function, and Uses. Molecular Cell Biology, 4th Edn. (New York: W.H. Freeman and Company), 191-207.
53. Lomonte, P., and Everett, R. D. (1999). Herpes simplex virus type 1 immediate-early protein Vmw110 inhibits progression of cells through mitosis and from G(1) into S phase of the cell cycle. J. Virol. 73, 9456-9467.
54. Loret, S., Guay, G., and Lippe, R. (2008). Comprehensive characterization of extracellular herpes simplex virus type 1 virions. J. Virol. 82, 8605-8618.
55. Loret, S., and Lippe, R. (2012). Biochemical analysis of ICP0, ICP4, UL7 and UL23 incorporated into extracellular herpes simplex type 1 virions. J. Gen. Virol. 93, 624-634.
56. Lu, Q., Bai, J., Zhang, L., Liu, J., Jiang, Z., Michal, J. J., He, Q., and Jiang, P. (2012). Two-dimensional liquid chromatography-tandem mass spectrometry coupled with isobaric tags for relative and absolute quantification (iTRAQ) labeling approach revealed first proteome profiles of pulmonary alveolar macrophages infected with porcine reproductive and respiratory syndrome virus. J. Proteome Res. 11, 2890-2903.
57. Lu, Z., Qin, A., Qian, K., Chen, X., Jin, W., Zhu, Y., and Eltahir, Y. M. (2010). Proteomic analysis of the host response in the bursa of Fabricius of chickens infected with Mareks disease virus. Virus Res. 153, 250-257.
58. Marozin, S., Prank, U., and Sodeik, B. (2004). Herpes simplex virus type 1 infection of polarized epithelial cells requires microtubules and access to receptors present at cell-cell contact sites. J. Gen. Virol. 85, 775-786.
59. Maxwell, K. L., and Frappier, L. (2007). Viral proteomics. Microbiol. Mol. Biol. Rev. 71, 398-411.
60. Mercer, J., Schelhaas, M., and Helenius, A. (2010). Virus entry by endocytosis. Annu. Rev. Biochem. 79,803-833.
61. Michael, K., Klupp, B. G., Mettenleiter, T. C., and Karger, A. (2006). Composition of pseudorabies virus particles lacking tegument protein US3, UL47, or UL49 or envelope glycoprotein E. J. Virol. 80, 1332-1339.
62. Mizuno-Yamasaki, E., Rivera-Molina, F., and Novick, P. (2012). GTPase networks in membrane traffic. Annu. Rev. Biochem. PMID: 22463690. [Epub ahead of print].
63. Moerdyk-Schauwecker, M., Hwang, S. I., and Grdzelishvili, V. Z. (2009). Analysis of virion associated host proteins in vesicular stomatitis virus using a proteomics approach. Virol. J. 6, 166.
64. Munday, D. C., Hiscox, J. A., and Barr, J. N. (2010). Quantitative proteomic analysis of A549 cells infected with human respiratory syncytial virus subgroup B using SILAC coupled to LC-MS/MS. Proteomics 10, 4320-4334.
65. Norrild, B., Lehto, V. P., and Virtanen, I. (1986). Organization of cytoskeleton elements during herpes simplex virus type 1 infection of human fibroblasts: an immunofluorescence study. J. Gen. Virol. 67(Pt 1), 97-105.
66. Ott, D. E. (2008). Cellular proteins detected in HIV-1. Rev. Med. Virol. 18, 159-175.
67. Padula, M. E., Sydnor, M. L., and Wilson, D. W. (2009). Isolation and preliminary characterization of herpes simplex virus 1 primary enveloped virions from the perinuclear space. J. Virol. 83, 4757-4765.
68. Pastorino, B., Boucomont-Chapeaublanc, E., Peyrefitte, C. N., Belghazi, M., Fusai, T., Rogier, C., Tolou, H. J., and Almeras, L. (2009). Identification of cellular proteome modifications in response to West Nile virus infection. Mol. Cell Proteomics 8, 1623-1637.
69. Piluso, D., Bilan, P., and Capone, J. P. (2002). Host cell factor-1 interacts with and antagonizes transactivation by the cell cycle regulatory factor Miz-1. J. Biol. Chem. 277, 46799-46808.
70. Radtke, K., Kieneke, D., Wolfstein, A., Michael, K., Steffen, W., Scholz, T., Karger, A., and Sodeik, B. (2010). Plusand minus-end directed microtubule motors bind simultaneously to herpes simplex virus capsids using different inner tegumentstructures. PLoS Pathog. 6,e1000991. doi:10.1371/journal.ppat.1000991
71. Ramirez-Boo, M., Nunez, E., Jorge, I., Navarro, P., Fernandes, L. T., Segales, J., Garrido, J. J., Vazquez, J., and Moreno, A. (2011). Quantitative proteomics by 2-DE, 16O/18O labelling and linear ion trap mass spectrometry analysis of lymph nodes from piglets inoculated by porcine circovirus type 2. Proteomics 11, 3452-3469.
72. Rassmann, A., Henke, A., Zobawa, M., Carlsohn, M., Saluz, H. P., Grabley, S., Lottspeich, F., and Munder, T. (2006). Proteome alterations in human host cells infected with coxsackievirus B3. J. Gen. Virol. 87, 2631-2638.
73. Rice, S. A., and Knipe, D. M. (1988). Gene-specific transactivation by herpes simplex virus type 1 alpha protein ICP27. J. Virol. 62, 3814-3823.
74. Roberts, K. L., and Baines, J. D. (2011). Actin in herpesvirus infection. Viruses 3, 336-346.
75. Saksena, M. M., Wakisaka, H., Tijono, B., Boadle, R. A., Rixon, F., Takahashi, H., and Cunningham, A. L. (2006). Herpes simplex virus type 1 accumulation, envelopment, and exit in growth cones and varicosities in mid-distal regions of axons. J. Virol. 80, 3592-3606.
76. Sandri-Goldin, R. M., and Mendoza, G. E. (1992). A herpesvirus regulatory protein appears to act posttranscriptionally by affecting mRNA processing. Genes Dev. 6, 848-863.
77. Sarma, N., Agarwal, D., Shiflett, L. A., and Read, G. S. (2008). Small interfering RNAs that deplete the cellular translation factor eIF4H impede mRNA degradation by the virion host shutoff protein of herpes simplex virus. J. Virol. 82, 6600-6609.
78. Schroder, M. (2010). Human DEADbox protein 3 has multiple functions in gene regulation and cell cycle control and is a prime target for viral manipulation. Biochem. Pharmacol. 79, 297-306.
79. Schroder, M. (2011). Viruses and the human DEAD-box helicase DDX3: inhibition or exploitation? Biochem. Soc. Trans. 39, 679-683.
80. Sekulovich, R. E., Leary, K., and Sandri-Goldin, R. M. (1988). The herpes simplex virus type 1 alpha protein ICP27 can act as a trans-repressor or a trans-activator in combination with ICP4 and ICP0. J. Virol. 62, 4510-4522.
81. Shadan, F. F., Cowsert, L. M., and Villarreal, L. P. (1994). n-Butyrate, a cell cycle blocker, inhibits the replication of polyomaviruses and papillomaviruses but not that of adenoviruses and herpesviruses. J. Virol. 68, 4785-4796.
82. Sharma-Walia,N.,Naranatt,P. P.,Krishnan, H. H., Zeng, L., and Chandran, B. (2004). Kaposis sarcomaassociated herpesvirus/human herpesvirus 8 envelope glycoprotein gB induces the integrin-dependent focal adhesion kinase-Srcphosphatidylinositol 3-kinase-rho GTPase signal pathways and cytoskeletal rearrangements. J. Virol. 78, 4207-4223.
83. Shaw, M. L., Stone, K. L., Colangelo, C. M., Gulcicek, E. E., and Palese, P. (2008). Cellular proteins in influenza virus particles. PLoS Pathog. 4, e1000085. doi:10.1371/journal.ppat.1000085
84. Simons, K., and Warren, G. (1984). Semliki forest virus: a probe for membrane traffic in the animal cell. Adv. Protein Chem. 36, 79-132.
85. Simpson-Holley, M., Colgrove, R. C., Nalepa, G., Harper, J. W., and Knipe, D. M. (2005). Identification and functional evaluation of cellular and viral factors involved in the alteration of nuclear architecture during herpes simplex virus 1 infection. J. Virol. 79, 12840-12851.
86. Smith, G. A., Gross, S. P., and Enquist, L. W. (2001). Herpesviruses use bidirectional fast-axonal transport to spread in sensory neurons. Proc. Natl. Acad. Sci. U.S.A. 98, 3466-3470.
87. Smith, I. L., Hardwicke, M. A., and Sandri-Goldin, R. M. (1992). Evidence that the herpes simplex virus immediate early protein ICP27 acts post-transcriptionally during infection to regulate gene expression. Virology 186, 74-86.
88. Sodeik, B., Ebersold, M. W., and Helenius, A. (1997). Microtubulemediated transport of incoming herpes simplex virus 1 capsids to the nucleus. J. Cell Biol. 136, 1007-1021.
89. Soliman, T. M., Sandri-Goldin, R. M., and Silverstein, S. J. (1997). Shuttling of the herpes simplex virus type 1 regulatory protein ICP27 between the nucleus and cytoplasm mediates the expression of late proteins. J. Virol. 71, 9188-9197.
90. Sollner, T. H. (2004). Intracellular and viral membrane fusion: a uniting mechanism. Curr. Opin. Cell Biol. 16, 429-435.
91. Sollner, T. H., and Rothman, J. E. (1996). Molecular machinery mediating vesicle budding, docking and fusion. Experientia 52, 1021-1025.
92. Song, B., Liu, J. J., Yeh, K. C., and Knipe, D. M. (2000). Herpes simplex virus infection blocks events in the G1 phase of the cell cycle. Virology 267, 326-334.
93. Sun, J., Jiang, Y., Shi, Z., Yan, Y., Guo, H., He, F., and Tu, C. (2008). Proteomic alteration of PK-15 cells after infection by classical swine fever virus. J. Proteome Res. 7, 5263-5269.
94. Teodoro, J. G.,and Branton,P. E. (1997). Regulation of apoptosis by viral gene products. J. Virol. 71, 1739-1746.
95. Thanthrige-Don,N.,Abdul-Careem,M. F., Shack, L. A., Burgess, S. C., and Sharif, S. (2009). Analyses of the spleen proteome of chickens infected with Mareks disease virus. Virology 390, 356-367.
96. Tong, A., Wu, L., Lin, Q., Lau, Q. C., Zhao, X., Li, J., Chen, P., Chen, L., Tang, H., Huang, C., and Wei, Y. Q. (2008). Proteomic analysis of cellular protein alterations using a hepatitis B virus-producing cellular model. Proteomics 8, 2012-2023.
97. Varnum, S. M., Streblow, D. N., Monroe, M. E., Smith, P., Auberry, K. J., Pasa-Tolic, L., Wang, D., Camp, D. G. II, Rodland, K., Wiley, S., Britt, W., Shenk, T., Smith, R. D., and Nelson, J. A. (2004). Identification of proteins in human cytomegalovirus (HCMV) particles: the HCMV proteome. J. Virol. 78, 10960-10966.
98. Viswanathan, K., and Fruh, K. (2007). Viral proteomics: global evaluation of viruses and their interaction with the host. Expert Rev. Proteomics 4, 815-829.
99. Wolfstein, A., Nagel, C. H., Radtke, K., Dohner, K., Allan, V. J., and Sodeik, B. (2006). The inner tegument promotes herpes simplex virus capsid motility along microtubules in vitro. Traffic 7, 227-237.
100. Wong, M. L., and Chen, C. H. (1998). Evidence for the internal location of actin in the pseudorabies virion. Virus Res. 56, 191-197.
101. Yang, B., Gonzalez, L. Jr., Prekeris, R., Steegmaier, M., Advani, R. J., and Scheller, R. H. (1999). SNARE interactions are not selective. Implications for membrane fusion specificity. J. Biol. Chem. 274, 5649-5653.
102. Zandi, F., Eslami, N., Soheili, M., Fayaz, A., Gholami, A., and Vaziri, B. (2009). Proteomics analysis of BHK-21 cells infected with a fixed strain of rabies virus. Proteomics 9, 2399-2407.
103. Zenner, H. L., Yoshimura, S., Barr, F. A., and Crump, C. M. (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.
104. Zerial, M., and McBride, H. (2001). Rab proteins as membrane organizers. Nat. Rev. Mol. Cell Biol. 2, 107-117.
105. Zhang, L., Jia, X., Zhang, X., Sun, J., Peng, X., Qi, T., Ma, F., Yin, L., Yao, Y., Qiu, C., and Lu, H. (2010). Proteomic analysis of PBMCs: characterization of potential HIV-associated proteins. Proteome Sci. 8, 12.
106. Zhang, X., Zhou, J., Wu, Y., Zheng, X., Ma, G., Wang, Z., Jin, Y., He, J., and Yan,Y. (2009). Differential proteome analysis of host cells infected with porcine circovirus type 2. J. Proteome Res. 8, 5111-5119.
107. Zheng, J., Sugrue, R. J., and Tang, K. (2011). Mass spectrometry based proteomic studies on viruses and hosts-areview.Anal. Chim. Acta 702, 149-159.
108. Zhu, F. X., Chong, J. M., Wu, L., and Yuan, Y. (2005). Virion proteins of Kaposis sarcoma-associated herpesvirus. J. Virol. 79, 800-811.