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Annual Review of Virology

Volume 1, 2014

The Impact of Mass Spectrometry–Based Proteomics on Fundamental Discoveries in Virology

Abstract

In recent years, mass spectrometry has emerged as a core component of fundamental discoveries in virology. As a consequence of their coevolution, viruses and host cells have established complex, dynamic interactions that function either in promoting virus replication and dissemination or in host defense against invading pathogens. Thus, viral infection triggers an impressive range of proteome changes. Alterations in protein abundances, interactions, posttranslational modifications, subcellular localizations, and secretion are temporally regulated during the progression of an infection. Consequently, understanding viral infection at the molecular level requires versatile approaches that afford both breadth and depth of analysis. Mass spectrometry is uniquely positioned to bridge this experimental dichotomy. Its application to both unbiased systems analyses and targeted, hypothesis-driven studies has accelerated discoveries in viral pathogenesis and host defense. Here, we review the contributions of mass spectrometry–based proteomic approaches to understanding viral morphogenesis, replication, and assembly and to characterizing host responses to infection.

Keyword(s): AP-MS, posttranslational modifications, secretome, viral proteomics, virus-host interactions
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/content/journals/10.1146/annurev-virology-031413-085527
2014-09-29
2024-04-18
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Literature Cited

  1. Milo R. 1.  2013. What is the total number of protein molecules per cell volume? A call to rethink some published values. BioEssays 35:1050–55 [Google Scholar]
  2. Grunewald K, Cyrklaff M. 2.  2006. Structure of complex viruses and virus-infected cells by electron cryo tomography. Curr. Opin. Microbiol. 9:437–42 [Google Scholar]
  3. Kuznetsov YG, McPherson A. 3.  2011. Atomic force microscopy in imaging of viruses and virus-infected cells. Microbiol. Mol. Biol. Rev. 75:268–85 [Google Scholar]
  4. Johannsen E, Luftig M, Chase MR, Weicksel S, Cahir-McFarland E. 4.  et al. 2004. Proteins of purified Epstein–Barr virus. Proc. Natl. Acad. Sci. USA 101:16286–91 [Google Scholar]
  5. Kattenhorn LM, Mills R, Wagner M, Lomsadze A, Makeev V. 5.  et al. 2004. Identification of proteins associated with murine cytomegalovirus virions. J. Virol. 78:11187–97 [Google Scholar]
  6. Kramer T, Greco TM, Enquist LW, Cristea IM. 6.  2011. Proteomic characterization of pseudorabies virus extracellular virions. J. Virol. 85:6427–41 [Google Scholar]
  7. Loret S, Guay G, Lippé R. 7.  2008. Comprehensive characterization of extracellular herpes simplex virus type 1 virions. J. Virol. 82:8605–18 [Google Scholar]
  8. Varnum SM, Streblow DN, Monroe ME, Smith P, Auberry KJ. 8.  et al. 2004. Identification of proteins in human cytomegalovirus (HCMV) particles: the HCMV proteome. J. Virol. 78:10960–66 [Google Scholar]
  9. Vidick S, Leroy B, Palmeira L, Machiels B, Mast J. 9.  et al. 2013. Proteomic characterization of murid herpesvirus 4 extracellular virions. PLoS ONE 8:e83842 [Google Scholar]
  10. Chung CS, Chen CH, Ho MY, Huang CY, Liao CL, Chang W. 10.  2006. Vaccinia virus proteome: identification of proteins in vaccinia virus intracellular mature virion particles. J. Virol. 80:2127–40 [Google Scholar]
  11. Manes NP, Estep RD, Mottaz HM, Moore RJ, Clauss TRW. 11.  et al. 2008. Comparative proteomics of human monkeypox and vaccinia intracellular mature and extracellular enveloped virions. J. Proteome Res. 7:960–68 [Google Scholar]
  12. Yoder JD, Chen TS, Gagnier CR, Vemulapalli S, Maier CS, Hruby DE. 12.  2006. Pox proteomics: mass spectrometry analysis and identification of vaccinia virion proteins. Virol. J. 3:10 [Google Scholar]
  13. Yao X, Freas A, Ramirez J, Demirev PA, Fenselau C. 13.  2001. Proteolytic 18O labeling for comparative proteomics: model studies with two serotypes of adenovirus. Anal. Chem. 73:2836–42 [Google Scholar]
  14. Davison AJ, Davison MD. 14.  1995. Identification of structural proteins of channel catfish virus by mass spectrometry. Virology 206:1035–43 [Google Scholar]
  15. Terrand J, Bruban V, Zhou L, Gong W, El Asmar Z. 15.  et al. 2009. LRP1 controls intracellular cholesterol storage and fatty acid synthesis through modulation of Wnt signaling. J. Biol. Chem. 284:381–88 [Google Scholar]
  16. Spurgers KB, Alefantis T, Peyser BD, Ruthel GT, Bergeron AA. 16.  et al. 2010. Identification of essential filovirion-associated host factors by serial proteomic analysis and RNAi screen. Mol. Cell. Proteomics 9:2690–703 [Google Scholar]
  17. Chertova E, Chertov O, Coren LV, Roser JD, Trubey CM. 17.  et al. 2006. Proteomic and biochemical analysis of purified human immunodeficiency virus type 1 produced from infected monocyte-derived macrophages. J. Virol. 80:9039–52 [Google Scholar]
  18. Linde ME, Colquhoun DR, Ubaida Mohien C, Kole T, Aquino V. 18.  et al. 2013. The conserved set of host proteins incorporated into HIV-1 virions suggests a common egress pathway in multiple cell types. J. Proteome Res. 12:2045–54 [Google Scholar]
  19. Radhakrishnan A, Yeo D, Brown G, Myaing MZ, Iyer LR. 19.  et al. 2010. Protein analysis of purified respiratory syncytial virus particles reveals an important role for heat shock protein 90 in virus particle assembly. Mol. Cell. Proteomics 9:1829–48 [Google Scholar]
  20. Saphire AC, Gallay PA, Bark SJ. 20.  2006. Proteomic analysis of human immunodeficiency virus using liquid chromatography/tandem mass spectrometry effectively distinguishes specific incorporated host proteins. J. Proteome Res. 5:530–38 [Google Scholar]
  21. Shaw ML, Stone KL, Colangelo CM, Gulcicek EE, Palese P. 21.  2008. Cellular proteins in influenza virus particles. PLoS Pathog. 4:e1000085 [Google Scholar]
  22. Stegen C, Yakova Y, Henaff D, Nadjar J, Duron J, Lippé R. 22.  2013. Analysis of virion-incorporated host proteins required for herpes simplex virus type 1 infection through a RNA interference screen. PLoS ONE 8:e53276 [Google Scholar]
  23. Uetrecht C, Barbu IM, Shoemaker GK, van Duijn E, Heck AJR. 23.  2011. Interrogating viral capsid assembly with ion mobility–mass spectrometry. Nat. Chem. 3:126–32 [Google Scholar]
  24. Pease LF III. 24.  2012. Physical analysis of virus particles using electrospray differential mobility analysis. Trends Biotechnol. 30:216–24 [Google Scholar]
  25. Alexander CG, Jürgens MC, Shepherd DA, Freund SMV, Ashcroft AE, Ferguson N. 25.  2013. Thermodynamic origins of protein folding, allostery, and capsid formation in the human hepatitis B virus core protein. Proc. Natl. Acad. Sci. USA 110:E2782–91 [Google Scholar]
  26. Vörös J, Urbanek A, Rautureau GJP, O'Connor M, Fisher HC. 26.  et al. 2014. Large-scale production, structural and biophysical characterizations of the human hepatitis B virus polymerase. J. Virol. 882584–99
  27. Shepherd DA, Holmes K, Rowlands DJ, Stonehouse NJ, Ashcroft AE. 27.  2013. Using ion mobility spectrometry–mass spectrometry to decipher the conformational and assembly characteristics of the hepatitis B capsid protein. Biophys. J. 105:1258–67 [Google Scholar]
  28. Shoemaker GK, van Duijn E, Crawford SE, Uetrecht C, Baclayon M. 28.  et al. 2010. Norwalk virus assembly and stability monitored by mass spectrometry. Mol. Cell. Proteomics 9:1742–51 [Google Scholar]
  29. Snijder J, Uetrecht C, Rose RJ, Sanchez-Eugenia R, Marti GA. 29.  et al. 2013. Probing the biophysical interplay between a viral genome and its capsid. Nat. Chem. 5:502–9Native MS and atomic force microscopy reveal the constraints of Triatoma virus capsid packaging and uncoating. [Google Scholar]
  30. Tuma R, Coward LU, Kirk MC, Barnes S, Prevelige PE Jr. 30.  2001. Hydrogen-deuterium exchange as a probe of folding and assembly in viral capsids. J. Mol. Biol. 306:389–96 [Google Scholar]
  31. Monroe EB, Kang S, Kyere SK, Li R, Prevelige PE Jr. 31.  2010. Hydrogen/deuterium exchange analysis of HIV-1 capsid assembly and maturation. Structure 18:1489–91 [Google Scholar]
  32. Miteva YV, Budayeva HG, Cristea IM. 32.  2013. Proteomics-based methods for discovery, quantification, and validation of protein-protein interactions. Anal. Chem. 85:749–68 [Google Scholar]
  33. Rowles DL, Terhune SS, Cristea IM. 33.  2013. Discovery of host-viral protein complexes during infection. Methods Mol. Biol.106443–70
  34. Fontaine-Rodriguez EC, Taylor TJ, Olesky M, Knipe DM. 34.  2004. Proteomics of herpes simplex virus infected cell protein 27: association with translation initiation factors. Virology 330:487–92 [Google Scholar]
  35. Taylor TJ, Knipe DM. 35.  2004. Proteomics of herpes simplex virus replication compartments: association of cellular DNA replication, repair, recombination, and chromatin remodeling proteins with ICP8. J. Virol. 78:5856–66 [Google Scholar]
  36. Guise AJ, Budayeva HG, Diner BA, Cristea IM. 36.  2013. Histone deacetylases in herpesvirus replication and virus-stimulated host defense. Viruses 5:1607–32 [Google Scholar]
  37. Cristea IM, Williams R, Chait BT, Rout MP. 37.  2005. Fluorescent proteins as proteomic probes. Mol. Cell. Proteomics 4:1933–41 [Google Scholar]
  38. Cristea IM, Carroll JW, Rout MP, Rice CM, Chait BT, MacDonald MR. 38.  2006. Tracking and elucidating Alphavirus-host protein interactions. J. Biol. Chem. 281:30269–78The first temporal AP-MS study of virus-host protein interactions during the progression of an infection. [Google Scholar]
  39. Frolova E, Gorchakov R, Garmashova N, Atasheva S, Vergara LA, Frolov I. 39.  2006. Formation of nsP3-specific protein complexes during Sindbis virus replication. J. Virol. 80:4122–34 [Google Scholar]
  40. Cristea IM, Rozjabek H, Molloy KR, Karki S, White LL, Rice CM. 40.  et al. 2010. Host factors associated with the Sindbis virus RNA-dependent RNA polymerase: role for G3BP1 and G3BP2 in virus replication. J. Virol. 84:6720–32 [Google Scholar]
  41. Moorman NJ, Cristea IM, Terhune SS, Rout MP, Chait BT, Shenk T. 41.  2008. Human cytomegalovirus protein UL38 inhibits host cell stress responses by antagonizing the tuberous sclerosis protein complex. Cell Host Microbe 3:253–62 [Google Scholar]
  42. Moorman NJ, Sharon-Friling R, Shenk T, Cristea IM. 42.  2010. A targeted spatial-temporal proteomics approach implicates multiple cellular trafficking pathways in human cytomegalovirus virion maturation. Mol. Cell. Proteomics 9:851–60 [Google Scholar]
  43. Cristea IM, Moorman NJ, Terhune SS, Cuevas CD, O'Keefe ES. 43.  et al. 2010. Human cytomegalovirus pUL83 stimulates activity of the viral immediate-early promoter through its interaction with the cellular IFI16 protein. J. Virol. 84:7803–14 [Google Scholar]
  44. Terhune SS, Moorman NJ, Cristea IM, Savaryn JP, Cuevas-Bennett C. 44.  et al. 2010. Human cytomegalovirus UL29/28 protein interacts with components of the NuRD complex which promote accumulation of immediate-early RNA. PLoS Pathog. 6:e1000965 [Google Scholar]
  45. Lin AE, Greco TM, Döhner K, Sodeik B, Cristea IM. 45.  2013. A proteomic perspective of inbuilt viral protein regulation: pUL46 tegument protein is targeted for degradation by ICP0 during herpes simplex virus type 1 infection. Mol. Cell. Proteomics 12:3237–52 [Google Scholar]
  46. Kramer T, Greco TM, Taylor MP, Ambrosini AE, Cristea IM, Enquist LW. 46.  2012. Kinesin-3 mediates axonal sorting and directional transport of alphaherpesvirus particles in neurons. Cell Host Microbe 12:806–814 [Google Scholar]
  47. Kratchmarov R, Kramer T, Greco TM, Taylor MP, Ch'ng TH. 47.  et al. 2013. Glycoproteins gE and gI are required for efficient KIF1A-dependent anterograde axonal transport of alphaherpesvirus particles in neurons. J. Virol. 87:9431–40 [Google Scholar]
  48. Youn S, Li T, McCune BT, Edeling MA, Fremont DH. 48.  et al. 2012. Evidence for a genetic and physical interaction between nonstructural proteins NS1 and NS4B that modulates replication of West Nile virus. J. Virol. 86:7360–71 [Google Scholar]
  49. Rigaut G, Shevchenko A, Rutz B, Wilm M, Mann M, Séraphin B. 49.  1999. A generic protein purification method for protein complex characterization and proteome exploration. Nat. Biotechnol. 17:1030–32 [Google Scholar]
  50. Ikura T, Ogryzko VV, Grigoriev M, Groisman R, Wang J. 50.  et al. 2000. Involvement of the TIP60 histone acetylase complex in DNA repair and apoptosis. Cell 102:463–73 [Google Scholar]
  51. Wagenaar TR, Moss B. 51.  2007. Association of vaccinia virus fusion regulatory proteins with the multicomponent entry/fusion complex. J. Virol. 81:6286–93 [Google Scholar]
  52. Tanaka M, Sata T, Kawaguchi Y. 52.  2008. The product of the herpes simplex virus 1 UL7 gene interacts with a mitochondrial protein, adenine nucleotide translocator 2. Virol. J. 5:125 [Google Scholar]
  53. Mayer D, Molawi K, Martínez-Sobrido L, Ghanem A, Thomas S. 53.  et al. 2007. Identification of cellular interaction partners of the influenza virus ribonucleoprotein complex and polymerase complex using proteomic-based approaches. J. Proteome Res. 6:672–82 [Google Scholar]
  54. Yamayoshi S, Noda T, Ebihara H, Goto H, Morikawa Y. 54.  et al. 2008. Ebola virus matrix protein VP40 uses the COPII transport system for its intracellular transport. Cell Host Microbe 3:168–77 [Google Scholar]
  55. Jäger S, Kim DY, Hultquist JF, Shindo K, LaRue RS. 55.  et al. 2012. Vif hijacks CBF-β to degrade APOBEC3G and promote HIV-1 infection. Nature 481:371–75 [Google Scholar]
  56. Naji S, Ambrus G, Cimermančič P, Reyes JR, Johnson JR. 56.  et al. 2012. Host cell interactome of HIV-1 Rev includes RNA helicases involved in multiple facets of virus production. Mol. Cell. Proteomics 11:M111.015313 [Google Scholar]
  57. Chi YH, Semmes OJ, Jeang KT. 57.  2011. A proteomic study of TAR-RNA binding protein (TRBP)-associated factors. Cell Biosci. 1:9 [Google Scholar]
  58. Lee SJ, Shim HY, Hsieh A, Min JY, Jung G. 58.  2009. Hepatitis B virus core interacts with the host cell nucleolar protein, nucleophosmin 1. J. Microbiol. 47:746–52 [Google Scholar]
  59. Mukerji J, Olivieri KC, Misra V, Agopian KA, Gabuzda D. 59.  2012. Proteomic analysis of HIV-1 Nef cellular binding partners reveals a role for exocyst complex proteins in mediating enhancement of intercellular nanotube formation. Retrovirology 9:33 [Google Scholar]
  60. Smirnova EV, Collingwood TS, Bisbal C, Tsygankova OM, Bogush M. 60.  et al. 2008. TULA proteins bind to ABCE-1, a host factor of HIV-1 assembly, and inhibit HIV-1 biogenesis in a UBA-dependent fashion. Virology 372:10–23 [Google Scholar]
  61. Jäger S, Cimermančič P, Gulbahce N, Johnson JR, McGovern KE. 61.  et al. 2012. Global landscape of HIV-human protein complexes. Nature 481:365–70First interactome of all proteins encoded by a viral genome using individually expressed viral proteins. [Google Scholar]
  62. Gordón-Alonso M, Sala-Valdés M, Rocha-Perugini V, Pérez-Hernández D, López-Martín S. 62.  et al. 2012. EWI-2 association with α-actinin regulates T cell immune synapses and HIV viral infection. J. Immunol. 189:689–700 [Google Scholar]
  63. Tran K, Kamil JP, Coen DM, Spector DH. 63.  2010. Inactivation and disassembly of the anaphase-promoting complex during human cytomegalovirus infection is associated with degradation of the APC5 and APC4 subunits and does not require UL97-mediated phosphorylation of Cdh1. J. Virol. 84:10832–43 [Google Scholar]
  64. Chakraborty S, Veettil MV, Bottero V, Chandran B. 64.  2012. Kaposi's sarcoma–associated herpesvirus interacts with EphrinA2 receptor to amplify signaling essential for productive infection. Proc. Natl. Acad. Sci. USA 109:E1163–72Mechanistic insight into macropinocytic entry facilitated by AP-MS of viral entry complexes at 5 min postinfection. [Google Scholar]
  65. Raghu H, Sharma-Walia N, Veettil MV, Sadagopan S, Chandran B. 65.  2009. Kaposi's sarcoma–associated herpesvirus utilizes an actin polymerization–dependent macropinocytic pathway to enter human dermal microvascular endothelial and human umbilical vein endothelial cells. J. Virol. 83:4895–911 [Google Scholar]
  66. Gabaev I, Steinbrück L, Pokoyski C, Pich A, Stanton RJ. 66.  et al. 2011. The human cytomegalovirus UL11 protein interacts with the receptor tyrosine phosphatase CD45, resulting in functional paralysis of T cells. PLoS Pathog. 7:e1002432 [Google Scholar]
  67. Gao Y, Colletti K, Pari GS. 67.  2008. Identification of human cytomegalovirus UL84 virus- and cell-encoded binding partners by using proteomics analysis. J. Virol. 82:96–104 [Google Scholar]
  68. Kagele D, Rossetto CC, Tarrant MT, Pari GS. 68.  2012. Analysis of the interactions of viral and cellular factors with human cytomegalovirus lytic origin of replication, oriLyt. Virology 424:106–14 [Google Scholar]
  69. Lester JT, DeLuca NA. 69.  2011. Herpes simplex virus 1 ICP4 forms complexes with TFIID and mediator in virus-infected cells. J. Virol. 85:5733–44 [Google Scholar]
  70. Raghavendra NK, Shkriabai N, Graham RL, Hess S, Kvaratskhelia M, Wu L. 70.  2010. Identification of host proteins associated with HIV-1 preintegration complexes isolated from infected CD4+ cells. Retrovirology 7:66 [Google Scholar]
  71. Kerur N, Veettil MV, Sharma-Walia N, Bottero V, Sadagopan S. 70a.  et al. 2011. IFI16 acts as a nuclear pathogen sensor to induce the inflammasome in response to Kaposi sarcoma–associated herpesvirus infection. Cell Host Microbe 9:363–75 [Google Scholar]
  72. Li T, Diner BA, Chen J, Cristea IM. 71.  2012. Acetylation modulates cellular distribution and DNA sensing ability of interferon-inducible protein IFI16. Proc. Natl. Acad. Sci. USA 109:10558–63Acetylation modulates the localization of the first viral DNA sensor that functions in the nucleus. [Google Scholar]
  73. Orzalli MH, DeLuca NA, Knipe DM. 72.  2012. Nuclear IFI16 induction of IRF-3 signaling during herpesviral infection and degradation of IFI16 by the viral ICP0 protein. Proc. Natl. Acad. Sci. USA 109:E3008–17 [Google Scholar]
  74. Li T, Chen J, Cristea IM. 73.  2013. Human cytomegalovirus tegument protein pUL83 inhibits IFI16-mediated DNA sensing for immune evasion. Cell Host Microbe 14:591–99Host-mediated phosphorylation of a viral protein during infection inhibits its function in viral immune evasion. [Google Scholar]
  75. Emmott E, Munday D, Bickerton E, Britton P, Rodgers MA. 74.  et al. 2013. The cellular interactome of the coronavirus infectious bronchitis virus nucleocapsid protein and functional implications for virus biology. J. Virol. 87:9486–500 [Google Scholar]
  76. Greninger AL, Knudsen GM, Betegon M, Burlingame AL, DeRisi JL. 75.  2012. The 3A protein from multiple picornaviruses utilizes the Golgi adaptor protein ACBD3 to recruit PI4KIIIβ. J. Virol. 86:3605–16 [Google Scholar]
  77. Lemnitzer F, Raschbichler V, Kolodziejczak D, Israel L, Imhof A. 76.  et al. 2013. Mouse cytomegalovirus egress protein pM50 interacts with cellular endophilin-A2. Cell Microbiol. 15:335–51 [Google Scholar]
  78. Noda T, Sagara H, Suzuki E, Takada A, Kida H, Kawaoka Y. 77.  2002. Ebola virus VP40 drives the formation of virus-like filamentous particles along with GP. J. Virol. 76:4855–65 [Google Scholar]
  79. Vidalain PO, Tangy F. 78.  2010. Virus-host protein interactions in RNA viruses. Microbes Infect. 12:1134–43 [Google Scholar]
  80. Vashist S, Urena L, Chaudhry Y, Goodfellow I. 79.  2012. Identification of RNA-protein interaction networks involved in the norovirus life cycle. J. Virol. 86:11977–90 [Google Scholar]
  81. Galán C, Sola I, Nogales A, Thomas B, Akoulitchev A. 80.  et al. 2009. Host cell proteins interacting with the 3′ end of TGEV coronavirus genome influence virus replication. Virology 391:304–14 [Google Scholar]
  82. Harris D, Zhang Z, Chaubey B, Pandey VN. 81.  2006. Identification of cellular factors associated with the 3′-nontranslated region of the hepatitis C virus genome. Mol. Cell. Proteomics 5:1006–18 [Google Scholar]
  83. Tingting P, Caiyun F, Zhigang Y, Pengyuan Y, Zhenghong Y. 82.  2006. Subproteomic analysis of the cellular proteins associated with the 3′ untranslated region of the hepatitis C virus genome in human liver cells. Biochem. Biophys. Res. Commun. 347:683–91 [Google Scholar]
  84. Upadhyay A, Dixit U, Manvar D, Chaturvedi N, Pandey VN. 83.  2013. Affinity capture and identification of host cell factors associated with hepatitis C virus (+) strand subgenomic RNA. Mol. Cell. Proteomics 12:1539–52A novel peptide nucleic acid–neamine conjugate for in situ capturing of viral RNA–host interactions. [Google Scholar]
  85. Lenarcic EM, Landry DM, Greco TM, Cristea IM, Thompson SR. 84.  2013. Thiouracil cross-linking mass spectrometry: a cell-based method to identify host factors involved in viral amplification. J. Virol. 87:8697–712 [Google Scholar]
  86. Koh GC, Porras P, Aranda B, Hermjakob H, Orchard SE. 85.  2012. Analyzing protein-protein interaction networks. J. Proteome Res. 11:2014–31 [Google Scholar]
  87. Nesvizhskii AI. 86.  2012. Computational and informatics strategies for identification of specific protein interaction partners in affinity purification mass spectrometry experiments. Proteomics 12:1639–55 [Google Scholar]
  88. Sardiu ME, Washburn MP. 87.  2011. Building protein-protein interaction networks with proteomics and informatics tools. J. Biol. Chem. 286:23645–51 [Google Scholar]
  89. Sowa ME, Bennett EJ, Gygi SP, Harper JW. 88.  2009. Defining the human deubiquitinating enzyme interaction landscape. Cell 138:389–403 [Google Scholar]
  90. Sardiu ME, Cai Y, Jin J, Swanson SK, Conaway RC. 89.  et al. 2008. Probabilistic assembly of human protein interaction networks from label-free quantitative proteomics. Proc. Natl. Acad. Sci. USA 105:1454–59 [Google Scholar]
  91. Choi H, Larsen B, Lin ZY, Breitkreutz A, Mellacheruvu D. 90.  et al. 2011. SAINT: probabilistic scoring of affinity purification–mass spectrometry data. Nat. Methods 8:70–73 [Google Scholar]
  92. Tackett AJ, DeGrasse JA, Sekedat MD, Oeffinger M, Rout MP, Chait BT. 91.  2005. I-DIRT, a general method for distinguishing between specific and nonspecific protein interactions. J. Proteome Res. 4:1752–56 [Google Scholar]
  93. Joshi P, Greco TM, Guise AJ, Luo Y, Yu F. 92.  et al. 2013. The functional interactome landscape of the human histone deacetylase family. Mol. Syst. Biol. 9:672Integrated label-free and metabolic labeling approaches measure the relative stability and specificity of protein interactions. [Google Scholar]
  94. Zuberi K, Franz M, Rodriguez H, Montojo J, Lopes CT. 93.  et al. 2013. GeneMANIA prediction server 2013 update. Nucleic Acids Res. 41:W115–22 [Google Scholar]
  95. Franceschini A, Szklarczyk D, Frankild S, Kuhn M, Simonovic M. 94.  et al. 2013. STRING v9.1: protein-protein interaction networks, with increased coverage and integration. Nucleic Acids Res. 41:D808–15 [Google Scholar]
  96. Croft D, Mundo AF, Haw R, Milacic M, Weiser J. 95.  et al. 2014. The Reactome pathway knowledgebase. Nucleic Acids Res. 42:D472–77 [Google Scholar]
  97. Aranda B, Achuthan P, Alam-Faruque Y, Armean I, Bridge A. 96.  et al. 2010. The IntAct molecular interaction database in 2010. Nucleic Acids Res. 38:D525–31 [Google Scholar]
  98. Hulo C, de Castro E, Masson P, Bougueleret L, Bairoch A. 97.  et al. 2011. ViralZone: a knowledge resource to understand virus diversity. Nucleic Acids Res. 39:D576–82 [Google Scholar]
  99. Chatr-aryamontri A, Ceol A, Peluso D, Nardozza A, Panni S. 98.  et al. 2009. VirusMINT: a viral protein interaction database. Nucleic Acids Res. 37:D669–73 [Google Scholar]
  100. Fahey ME, Bennett MJ, Mahon C, Jäger S, Pache L. 99.  et al. 2011. GPS-Prot: a web-based visualization platform for integrating host-pathogen interaction data. BMC Bioinform. 12:298 [Google Scholar]
  101. Gingras AC, Raught B. 100.  2012. Beyond hairballs: the use of quantitative mass spectrometry data to understand protein-protein interactions. FEBS Lett. 586:2723–31 [Google Scholar]
  102. Stern-Ginossar N, Weisburd B, Michalski A, Le VT, Hein MY. 101.  et al. 2012. Decoding human cytomegalovirus. Science 338:1088–93Combination of transcriptomics and proteomics identifies novel viral translation products during HCMV infection. [Google Scholar]
  103. Vogels MW, van Balkom BW, Kaloyanova DV, Batenburg JJ, Heck AJ. 102.  et al. 2011. Identification of host factors involved in coronavirus replication by quantitative proteomics analysis. Proteomics 11:64–80 [Google Scholar]
  104. Santamaría E, Mora MI, Potel C, Fernández-Irigoyen J, Carro-Roldán E. 103.  et al. 2009. Identification of replication-competent HSV-1 Cgal+ strain signaling targets in human hepatoma cells by functional organelle proteomics. Mol. Cell. Proteomics 8:805–15 [Google Scholar]
  105. Emmott E, Wise H, Loucaides EM, Matthews DA, Digard P, Hiscox JA. 104.  2010. Quantitative proteomics using SILAC coupled to LC-MS/MS reveals changes in the nucleolar proteome in influenza A virus–infected cells. J. Proteome Res. 9:5335–45 [Google Scholar]
  106. Lam YW, Evans VC, Heesom KJ, Lamond AI, Matthews DA. 105.  2010. Proteomics analysis of the nucleolus in adenovirus-infected cells. Mol. Cell. Proteomics 9:117–30 [Google Scholar]
  107. Munday DC, Emmott E, Surtees R, Lardeau CH, Wu W. 106.  et al. 2010. Quantitative proteomic analysis of A549 cells infected with human respiratory syncytial virus. Mol. Cell. Proteomics 9:2438–59 [Google Scholar]
  108. Peirce MJ, Wait R, Begum S, Saklatvala J, Cope AP. 107.  2004. Expression profiling of lymphocyte plasma membrane proteins. Mol. Cell. Proteomics 3:56–65 [Google Scholar]
  109. Wollscheid B, Bausch-Fluck D, Henderson C, O'Brien R, Bibel M. 108.  et al. 2009. Mass-spectrometric identification and relative quantification of N-linked cell surface glycoproteins. Nat. Biotechnol. 27:378–86 [Google Scholar]
  110. Berro R, de la Fuente C, Klase Z, Kehn K, Parvin L. 109.  et al. 2007. Identifying the membrane proteome of HIV-1 latently infected cells. J. Biol. Chem. 282:8207–18 [Google Scholar]
  111. Weekes MP, Tan SY, Poole E, Talbot S, Antrobus R. 110.  et al. 2013. Latency-associated degradation of the MRP1 drug transporter during latent human cytomegalovirus infection. Science 340:199–202 [Google Scholar]
  112. Gudleski-O'Regan N, Greco TM, Cristea IM, Shenk T. 111.  2012. Increased expression of LDL receptor–related protein 1 during human cytomegalovirus infection reduces virion cholesterol and infectivity. Cell Host Microbe 12:86–96 [Google Scholar]
  113. Pollock S, Nichita NB, Böhmer A, Radulescu C, Dwek RA, Zitzmann N. 112.  2010. Polyunsaturated liposomes are antiviral against hepatitis B and C viruses and HIV by decreasing cholesterol levels in infected cells. Proc. Natl. Acad. Sci. USA 107:17176–81 [Google Scholar]
  114. Sun X, Whittaker GR. 113.  2003. Role for influenza virus envelope cholesterol in virus entry and infection. J. Virol. 77:12543–51 [Google Scholar]
  115. Campbell SM, Crowe SM, Mak J. 114.  2002. Virion-associated cholesterol is critical for the maintenance of HIV-1 structure and infectivity. AIDS 16:2253–61 [Google Scholar]
  116. Guyader M, Kiyokawa E, Abrami L, Turelli P, Trono D. 115.  2002. Role for human immunodeficiency virus type 1 membrane cholesterol in viral internalization. J. Virol. 76:10356–64 [Google Scholar]
  117. Bonjardim CA, Ferreira PC, Kroon EG. 116.  2009. Interferons: signaling, antiviral and viral evasion. Immunol. Lett. 122:1–11 [Google Scholar]
  118. Pavlou MP, Diamandis EP. 117.  2010. The cancer cell secretome: a good source for discovering biomarkers?. J. Proteomics 73:1896–906 [Google Scholar]
  119. Ciborowski P, Enose Y, Mack A, Fladseth M, Gendelman HE. 118.  2004. Diminished matrix metalloproteinase 9 secretion in human immunodeficiency virus–infected mononuclear phagocytes: modulation of innate immunity and implications for neurological disease. J. Neuroimmunol. 157:11–16 [Google Scholar]
  120. Ciborowski P, Kadiu I, Rozek W, Smith L, Bernhardt K. 119.  et al. 2007. Investigating the human immunodeficiency virus type 1–infected monocyte-derived macrophage secretome. Virology 363:198–209 [Google Scholar]
  121. Lietzén N, Ohman T, Rintahaka J, Julkunen I, Aittokallio T. 120.  et al. 2011. Quantitative subcellular proteome and secretome profiling of influenza A virus–infected human primary macrophages. PLoS Pathog. 7:e1001340 [Google Scholar]
  122. Miettinen JJ, Matikainen S, Nyman TA. 121.  2012. Global secretome characterization of herpes simplex virus 1–infected human primary macrophages. J. Virol. 86:12770–78Multiplexed, quantitative MS analysis of the HSV-1-stimulated macrophage secretome identifies interferon-inducible proteins. [Google Scholar]
  123. Rathinam VA, Jiang Z, Waggoner SN, Sharma S, Cole LE. 122.  et al. 2010. The AIM2 inflammasome is essential for host defense against cytosolic bacteria and DNA viruses. Nat. Immunol. 11:395–402 [Google Scholar]
  124. Johnson KE, Chikoti L, Chandran B. 123.  2013. Herpes simplex virus 1 infection induces activation and subsequent inhibition of the IFI16 and NLRP3 inflammasomes. J. Virol. 87:5005–18 [Google Scholar]
  125. Dumortier J, Streblow DN, Moses AV, Jacobs JM, Kreklywich CN. 124.  et al. 2008. Human cytomegalovirus secretome contains factors that induce angiogenesis and wound healing. J. Virol. 82:6524–35 [Google Scholar]
  126. Vliegen I, Duijvestijn A, Grauls G, Herngreen S, Bruggeman C, Stassen F. 125.  2004. Cytomegalovirus infection aggravates atherogenesis in apoE knockout mice by both local and systemic immune activation. Microbes Infect. 6:17–24 [Google Scholar]
  127. Merigan TC, Renlund DG, Keay S, Bristow MR, Starnes V. 126.  et al. 1992. A controlled trial of ganciclovir to prevent cytomegalovirus disease after heart transplantation. N. Engl. J. Med. 326:1182–86 [Google Scholar]
  128. Vliegen I, Herngreen SB, Grauls GE, Bruggeman CA, Stassen FR. 127.  2005. Mouse cytomegalovirus antigenic immune stimulation is sufficient to aggravate atherosclerosis in hypercholesterolemic mice. Atherosclerosis 181:39–44 [Google Scholar]
  129. Streblow DN, Dumortier J, Moses AV, Orloff SL, Nelson JA. 128.  2008. Mechanisms of cytomegalovirus-accelerated vascular disease: induction of paracrine factors that promote angiogenesis and wound healing. Curr. Top. Microbiol. Immunol. 325:397–415 [Google Scholar]
  130. Bell C, Desjardins M, Thibault P, Radtke K. 129.  2013. Proteomics analysis of herpes simplex virus type 1–infected cells reveals dynamic changes of viral protein expression, ubiquitylation, and phosphorylation. J. Proteome Res. 12:1820–29 [Google Scholar]
  131. Zhao Y, Jensen ON. 130.  2009. Modification-specific proteomics: strategies for characterization of post-translational modifications using enrichment techniques. Proteomics 9:4632–41 [Google Scholar]
  132. Hutchinson EC, Denham EM, Thomas B, Trudgian DC, Hester SS. 131.  et al. 2012. Mapping the phosphoproteome of influenza A and B viruses by mass spectrometry. PLoS Pathog. 8:e1002993 [Google Scholar]
  133. Roby C, Gibson W. 132.  1986. Characterization of phosphoproteins and protein kinase activity of virions, noninfectious enveloped particles, and dense bodies of human cytomegalovirus. J. Virol. 59:714–27 [Google Scholar]
  134. Davido DJ, von Zagorski WF, Lane WS, Schaffer PA. 133.  2005. Phosphorylation site mutations affect herpes simplex virus type 1 ICP0 function. J. Virol. 79:1232–43 [Google Scholar]
  135. Fang CY, von Zagorski WF, Lane WS, Schaffer PA. 134.  2010. Global analysis of modifications of the human BK virus structural proteins by LC-MS/MS. Virology 402:164–76 [Google Scholar]
  136. Bergström Lind S, Artemenko KA, Elfineh L, Zhao Y, Bergquist J, Pettersson U. 135.  2013. Post translational modifications in adenovirus type 2. Virology 447:104–11 [Google Scholar]
  137. Jakobsen MR, Bak RO, Andersen A, Berg RK, Jensen SB. 136.  et al. 2013. IFI16 senses DNA forms of the lentiviral replication cycle and controls HIV-1 replication. Proc. Natl. Acad. Sci. USA 110:E4571–80 [Google Scholar]
  138. Unterholzner L, Keating SE, Baran M, Horan KA, Jensen SB. 137.  et al. 2010. IFI16 is an innate immune sensor for intracellular DNA. Nat. Immunol. 11:997–1004 [Google Scholar]
  139. Choudhary C, Kumar C, Gnad F, Nielsen ML, Rehman M. 138.  et al. 2009. Lysine acetylation targets protein complexes and co-regulates major cellular functions. Science 325:834–40 [Google Scholar]
  140. Halili MA, Andrews MR, Labzin LI, Schroder K, Matthias G. 139.  et al. 2010. Differential effects of selective HDAC inhibitors on macrophage inflammatory responses to the Toll-like receptor 4 agonist LPS. J. Leukoc. Biol. 87:1103–14 [Google Scholar]
  141. Roger T, Lugrin J, Le Roy D, Goy G, Mombelli M. 140.  et al. 2011. Histone deacetylase inhibitors impair innate immune responses to Toll-like receptor agonists and to infection. Blood 117:1205–17 [Google Scholar]
  142. Mombelli M, Lugrin J, Rubino I, Chanson AL, Giddey M. 141.  et al. 2011. Histone deacetylase inhibitors impair antibacterial defenses of macrophages. J. Infect. Dis. 204:1367–74 [Google Scholar]
  143. Hutterer C, Wandinger SK, Wagner S, Müller R, Stamminger T. 142.  et al. 2013. Profiling of the kinome of cytomegalovirus-infected cells reveals the functional importance of host kinases Aurora A, ABL and AMPK. Antivir. Res. 99:139–48 [Google Scholar]
  144. Terry LJ, Vastag L, Rabinowitz JD, Shenk T. 143.  2012. Human kinome profiling identifies a requirement for AMP-activated protein kinase during human cytomegalovirus infection. Proc. Natl. Acad. Sci. USA 109:3071–76 [Google Scholar]
  145. Borodovsky A, Ovaa H, Kolli N, Gan-Erdene T, Wilkinson KD. 144.  et al. 2002. Chemistry-based functional proteomics reveals novel members of the deubiquitinating enzyme family. Chem. Biol. 9:1149–59 [Google Scholar]
  146. Ovaa H, Kessler BM, Rolén U, Galardy PJ, Ploegh HL, Masucci MG. 145.  2004. Activity-based ubiquitin-specific protease (USP) profiling of virus-infected and malignant human cells. Proc. Natl. Acad. Sci. USA 101:2253–58 [Google Scholar]
  147. Picotti P, Aebersold R. 146.  2012. Selected reaction monitoring–based proteomics: workflows, potential, pitfalls and future directions. Nat. Methods 9:555–66 [Google Scholar]
  148. Chavez JD, Cilia M, Weisbrod CR, Ju HJ, Eng JK. 147.  et al. 2012. Cross-linking measurements of the Potato leafroll virus reveal protein interaction topologies required for virion stability, aphid transmission, and virus-plant interactions. J. Proteome Res. 11:2968–81 [Google Scholar]
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The Impact of Mass Spectrometry–Based Proteomics on Fundamental Discoveries in Virology
Annual Review of Virology 1, 581 (2014); https://doi.org/10.1146/annurev-virology-031413-085527
/content/journals/10.1146/annurev-virology-031413-085527
/content/journals/10.1146/annurev-virology-031413-085527
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