Proteomic approaches to uncovering virus-host protein interactions during the progression of viral infection

Expert Review of Proteomics

Volumn 13, Issue 3, 2016, Pages 325-340

  Lum, Krystal K ^a   Cristea, Ileana M ^a  

^a PRINCETON UNIVERSITY   (United States)

Author keywords

AP MS; interactome; IP MS; mass spectrometry; viral proteomics; Virus host interactions

Indexed keywords

EPITOPE; VIRUS PROTEIN; PROTEIN BINDING; PROTEOME; VIRAL PROTEIN;

ANTIBODY AFFINITY; CROSS LINKING; DISEASE COURSE; HUMAN; MASS SPECTROMETRY; NONHUMAN; PROTEIN INTERACTION; PROTEIN ISOLATION; PROTEIN MICROARRAY; PROTEIN PURIFICATION; PROTEOMICS; REVIEW; VIRUS CELL INTERACTION; VIRUS GENE; VIRUS HOST PROTEIN INTERACTION; VIRUS INFECTION; VIRUS REPLICATION; VIRUS STRAIN; ANIMAL; HOST PATHOGEN INTERACTION; METABOLISM; PROCEDURES; VIROLOGY;

ANIMALS; HOST-PATHOGEN INTERACTIONS; HUMANS; PROTEIN BINDING; PROTEOME; PROTEOMICS; VIRAL PROTEINS; VIRUS DISEASES;

EID: 84960415855     PISSN: 14789450     EISSN: 17448387     Source Type: Journal    
DOI: 10.1586/14789450.2016.1147353     Document Type: Review

References (137)

1. Ezkurdia I, Juan D, Rodriguez JM, et al. Multiple evidence strands suggest that there may be as few as 19 000 human protein-coding genes. Hum Mol Genet. 2014; 23 (22): 5866-5878.
2. Milo R. What is the total number of protein molecules per cell volume? A call to rethink some published values. Bioessays. 2013; 35 (12): 1050-1055.
3. Down TA, Hubbard TJP. Computational detection and location of transcription start sites in mammalian genomic DNA. Genome Res. 2002; 12 (3): 458-461.
4. Black DL. Protein diversity from alternative splicing: A challenge for bioinformatics and post-genome biology. Cell. 2000; 103 (3): 367-370.
5. Caceres JF, Kornblihtt AR. Alternative splicing: multiple control mechanisms and involvement in human disease. Trends Genet. 2002; 18 (4): 186-193.
6. Goldstrohm AC, Greenleaf AL, Garcia-Blanco MA. Co-transcriptional splicing of pre-messenger RNAs: considerations for the mechanism of alternative splicing. Gene. 2001; 277 (1-2): 31-47.
7. Graveley BR. Alternative splicing: increasing diversity in the proteomic world. Trend Genet. 2001; 17 (2): 100-107.
8. Gautheret D, Poirot O, Lopez F, et al. Alternate polyadenylation in human mRNAs: A large-scale analysis by EST clustering. Genome Res. 1998; 8 (5): 524-530.
9. Keegan LP, Gallo A, OConnell MA. The many roles of an RNA editor. Nat Rev Genet. 2001; 2 (11): 869-878.
10. Banks RE, Dunn MJ, Hochstrasser DF, et al. Proteomics: new perspectives, new biomedical opportunities. Lancet. 2000; 356 (9243): 1749-1756.
11. Nilsen TW, Graveley BR. Expansion of the eukaryotic proteome by alternative splicing. Nature. 2010; 463 (7280): 457-463.
12. Brett D, Pospisil H, Valcárcel J, et al. Alternative splicing and genome complexity. Nat Genet. 2002; 30 (1): 29-30.
13. Modrek B, Lee C. A genomic view of alternative splicing. Nat Genet. 2002; 30 (1): 13-19.
14. Creasy DM, Cottrell JS. Unimod: protein modifications for mass spectrometry. Proteomics. 2004; 4 (6): 1534-1536.
15. Kalejta RF. Tegument proteins of human cytomegalovirus. Microbiol Mol Biol Rev. 2008; 72 (2): 249-265. table of contents.
16. Philippe N, Legendre M, Doutre G, et al. Pandoraviruses: amoeba viruses with genomes up to 2.5 Mb reaching that of parasitic eukaryotes. Science. 2013; 341 (6143): 281-286.
17. Ojala PM, Sodeik B, Ebersold MW, et al. Herpes simplex virus type 1 entry into host cells: Reconstitution of capsid binding and uncoating at the nuclear pore complex in vitro. Mol Cell Biol. 2000; 20 (13): 4922-4931.
18. Diner BA, Lum KK, Javitt A, et al. Interactions of the antiviral factor interferon gamma-inducible protein 16 (IFI16) mediate immune signaling and herpes simplex virus-1 immunosuppression. Mol Cell Proteomics. 2015; 14 (9): 2341-2356.
19. Orzalli MH, DeLuca NA, Knipe DM. Nuclear IFI16 induction of IRF-3 signaling during herpesviral infection and degradation of IFI16 by the viral ICP0 protein. Proc Natl Acad Sci USA. 2012; 109 (44): E3008-E3017.
20. Garcia-Dorival I, Wu WN, Dowall S, et al. Elucidation of the Ebola virus VP24 cellular interactome and disruption of virus biology through targeted inhibition of host-cell protein function. J Proteome Res. 2014; 13 (11): 5120-5135.
21. Watanabe T, Kawakami E, Shoemaker JE, et al. Influenza virus-host interactome screen as a platform for antiviral drug development. Cell Host Microbe. 2014; 16 (6): 795-805.
22. Cristea IM, Graham D. Virology meets proteomics. Proteomics. 2015; 15 (12): 1941-1942.
23. Miteva YV, Budayeva HG, Cristea IM. Proteomics-based methods for discovery, quantification, and validation of protein-protein interactions. Anal Chem. 2013; 85 (2): 749-768.
24. Cristea IM, Carroll JWN, Rout MP, et al. Tracking and elucidating Alphavirus-host protein interactions. J Biol Chem. 2006; 281 (40): 30269-30278.
25. Cristea IM, Williams R, Chait BT, et al. Fluorescent proteins as proteomic probes. Mol Cell Proteomics. 2005; 4 (12): 1933-1941.
26. Gonzalez-Galarza FF, Lawless C, Hubbard SJ, et al. A critical appraisal of techniques, software packages, and standards for quantitative proteomic analysis. OMICS. 2012; 16 (9): 431-442.
27. Mellacheruvu D, Wright Z, Couzens AL, et al. The CRAPome: a contaminant repository for affinity purification-mass spectrometry data. Nat Methods. 2013; 10 (8): 730-736.
28. Choi H, Larsen B, Lin ZY, et al. SAINT: probabilistic scoring of affinity purification-mass spectrometry data. Nat Methods. 2011; 8 (1): 70-73.
29. Tackett AJ, DeGrasse JA, Sekedat MD, et al. I-DIRT, a general method for distinguishing between specific and nonspecific protein interactions. J Proteome Res. 2005; 4 (5): 1752-1756.
30. Joshi P, Greco TM, Guise AJ, et al. The functional interactome landscape of the human histone deacetylase family. Mol Syst Biol. 2013; 9: 672.
31. Zona L, Lupberger J, Sidahmed-Adrar N, et al. HRas signal transduction promotes hepatitis C virus cell entry by triggering assembly of the host tetraspanin receptor complex. Cell Host Microbe. 2013; 13 (3): 302-313.
32. Gerold G, Meissner F, Bruening J, et al. Quantitative proteomics identifies serum response factor binding protein 1 as a host factor for hepatitis C virus entry. Cell Rep. 2015; 12 (5): 864-878.
33. Ong SE, Blagoev B, Kratchmarova I, et al. Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Mol Cell Proteomics. 2002; 1 (5): 376-386.
34. Weekes MP, Tomasec P, Huttlin EL, et al. Quantitative temporal viromics: an approach to investigate host-pathogen interaction. Cell. 2014; 157 (6): 1460-1472.
35. Taylor TJ, Knipe DM. Proteomics of herpes simplex virus replication compartments: association of cellular DNA replication, repair, recombination, and chromatin remodeling proteins with ICP8. J Virol. 2004; 78 (11): 5856-5866.
36. Fontaine-Rodriguez EC, Taylor TJ, Olesky M, et al. Proteomics of herpes simplex virus infected cell protein 27: association with translation initiation factors. Virology. 2004; 330 (2): 487-492.
37. Cristea IM, Rozjabek H, Molloy KR, et al. Host factors associated with the Sindbis virus RNA-dependent RNA polymerase: role for G3BP1 and G3BP2 in virus replication. J Virol. 2010; 84 (13): 6720-6732.
38. Terhune SS, Moorman NJ, Cristea IM, et al. Human cytomegalovirus UL29/28 protein interacts with components of the NuRD complex which promote accumulation of immediate-early RNA. Plos Pathog. 2010; 6: 6.
39. Reitsma JM, Savaryn JP, Faust K, et al. Antiviral inhibition targeting the HCMV kinase pUL97 requires pUL27-dependent degradation of Tip60 acetyltransferase and cell-cycle arrest. Cell Host Microbe. 2011; 9 (2): 103-114.
40. Lin AE, Greco TM, Döhner K, et al. 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. 2013; 12 (11): 3237-3252.
41. Joubert DA, Blasdell KR, Audsley MD, et al. Bovine ephemeral fever rhabdovirus alpha 1 Protein has viroporin-like properties and binds importin beta 1 and importin 7. J Virol. 2014; 88 (3): 1591-1603.
42. Kramer T, Greco TM, Taylor MP, et al. Kinesin-3 mediates axonal sorting and directional transport of alphaherpesvirus particles in neurons. Cell Host Microbe. 2012; 12 (6): 806-814.
43. Moorman NJ, Sharon-Friling R, Shenk T, et al. A targeted spatial-temporal proteomics approach implicates multiple cellular trafficking pathways in human cytomegalovirus virion maturation. Mol Cell Proteomics. 2010; 9 (5): 851-860.
44. Chng TH, Enquist LW. Neuron-to-cell spread of pseudorabies virus in a compartmented neuronal culture system. J Virol. 2005; 79 (17): 10875-10889.
45. Col E, Caron C, Chable-Bessia C, et al. HIV-1 Tat targets Tip60 to impair the apoptotic cell response to genotoxic stresses. Embo J. 2005; 24 (14): 2634-2645.
46. Jha S, Pol SV, Banerjee NS, et al. Destabilization of TIP60 by human papillomavirus E6 results in attenuation of TIP60-dependent transcriptional regulation and apoptotic pathway. Mol Cell. 2010; 38 (5): 700-711.
47. Cuchet-Lourenco D, Anderson G, Sloan E, et al. The viral ubiquitin ligase ICP0 is neither sufficient nor necessary for degradation of the cellular DNA sensor IFI16 during herpes simplex virus 1 infection. J Virol. 2013; 87 (24): 13422-13432.
48. Cristea IM, Moorman NJ, Terhune SS, et al. Human cytomegalovirus pUL83 stimulates activity of the viral immediate-early promoter through its interaction with the cellular IFI16 protein. J Virol. 2010; 84 (15): 7803-7814.
49. Li T, Chen J, Cristea IM. Human cytomegalovirus tegument protein pUL83 inhibits IFI16-mediated DNA sensing for immune evasion. Cell Host Microbe. 2013; 14 (5): 591-599.
50. Colwill K, Graslund S. A roadmap to generate renewable protein binders to the human proteome. Nat Methods. 2011; 8 (7): 551-558.
51. Chi YH, Semmes OJ, Jeang KT. A proteomic study of TAR-RNA binding protein (TRBP)-associated factors. Cell Biosci. 2011; 1:9.
52. Davis ZH, Verschueren E, Jang GM, et al. Global mapping of herpesvirus-host protein complexes reveals a transcription strategy for late genes. Mol Cell. 2015; 57 (2): 349-360.
53. Germain MA, Chatel-Chaix L, Gagne B, et al. Elucidating novel hepatitis C virus-host interactions using combined mass spectrometry and functional genomics approaches. Mol Cell Proteomics. 2014; 13 (1): 184-203.
54. Jager S, Cimermancic P, Gulbahce N, et al. Global landscape of HIV-human protein complexes. Nature. 2012; 481 (7381): 365-370.
55. Malik-Soni N, Frappier L. Proteomic profiling of EBNA1-host protein interactions in latent and lytic Epstein-Barr virus infections (vol 86, pg 6999, 2012). J Virol. 2015; 89 (17): 9143-9143.
56. Salsman J, Jagannathan M, Paladino P, et al. Proteomic profiling of the human cytomegalovirus UL35 gene products reveals a role for UL35 in the DNA repair response. J Virol. 2012; 86 (2): 806-820.
57. Todorovic B, Nichols AC, Chitilian JM, et al. The human papillomavirus E7 proteins associate with p190RhoGAP and alter its function. J Virol. 2014; 88 (7): 3653-3663.
58. Reid SP, Leung LW, Hartman AL, et al. Ebola virus VP24 binds karyopherin alpha 1 and blocks STAT1 nuclear accumulation. J Virol. 2006; 80 (11): 5156-5167.
59. Li WH, Moore MJ, Vasilieva N, et al. Angiotensin-converting enzyme 2 is a functional receptor for the SARS coronavirus. Nature. 2003; 426 (6965): 450-454.
60. Gallagher TM, Buchmeier MJ. Coronavirus spike proteins in viral entry and pathogenesis. Virology. 2001; 279 (2): 371-374.
61. Holmes KV. SARS-associated coronavirus. New Engl J Med. 2003; 348 (20): 1948-1951.
62. Breslin JJ, Mork I, Smith MK, et al. Human coronavirus 229E: Receptor binding domain and neutralization by soluble receptor at 37 degrees C. J Virol. 2003; 77 (7): 4435-4438.
63. Kubo H, Yamada YK, Taguchi F. Localization of neutralizing epitopes and the receptor-binding site within the amino-terminal 330 amino-acids of the murine coronavirus spike protein. J Virol. 1994; 68 (9): 5403-5410.
64. White EA, Kramer RE, Tan MJA, et al. Comprehensive analysis of host cellular interactions with human papillomavirus E6 proteins identifies new E6 binding partners and reflects viral diversity. J Virol. 2012; 86 (24): 13174-13186.
65. White EA, Sowa ME, Tan MJA, et al. Systematic identification of interactions between host cell proteins and E7 oncoproteins from diverse human papillomaviruses. Proc Natl Acad Sci USA. 2012; 109 (5): E260-E267.
66. Brimer N, Lyons C, Wallberg AE, et al. Cutaneous papillomavirus E6 oncoproteins associate with MAML1 to repress transactivation and NOTCH signaling. Oncogene. 2012; 31 (43): 4639-4646.
67. Chen JJ, Reid CE, Band V, et al. Interaction of papillomavirus E6 oncoproteins with a putative calcium-binding protein. Science. 1995; 269 (5223): 529-531.
68. Nomine Y, Masson M, Charbonnier S, et al. Structural and functional analysis of E6 oncoprotein: insights in the molecular pathways of human papillomavirus-mediated pathogenesis. Mol Cell. 2006; 21 (5): 665-678.
69. Tan MJA, White EA, Sowa ME, et al. Cutaneous-human papillomavirus E6 proteins bind mastermind-like coactivators and repress notch signaling. Proc Natl Acad Sci USA. 2012; 109 (23): E1473-E1480.
70. Rigaut G, Shevchenko A, Rutz B, et al. A generic protein purification method for protein complex characterization and proteome exploration. Nat Biotechnol. 1999; 17 (10): 1030-1032.
71. Holowaty MN, Zeghouf M, Wu H, et al. Protein profiling with Epstein-Barr nuclear antigen-1 reveals an interaction with the herpesvirus-associated ubiquitin-specific protease HAUSP/USP7. J Biol Chem. 2003; 278 (32): 29987-29994.
72. Reisman D, Yates J, Sugden B. A putative origin of replication of plasmids derived from Epstein-Barr virus is composed of 2 cis-acting components. Mol Cell Biol. 1985; 5 (8): 1822-1832.
73. Yates JL, Warren N, Sugden B. Stable replication of plasmids derived from Epstein-Barr virus in various mammalian-cells. Nature. 1985; 313 (6005): 812-815.
74. Boutell C, Sadis S, Rd E. Herpes simplex virus type 1 immediate-early protein ICP0 and its isolated RING finger domain act as ubiquitin E3 ligases in vitro. J Virol. 2002; 76 (2): 841-850.
75. Everett RD, Meredith M, Orr A. The ability of herpes simplex virus type 1 immediate-early protein Vmw110 to bind to a ubiquitin-specific protease contributes to its roles in the activation of gene expression and stimulation of virus replication. J Virol. 1999; 73 (1): 417-426.
76. Everett RD, Meredith M, Orr A, et al. Kathoria M & Parkinson J. A novel ubiquitin-specific protease is dynamically associated with the PML nuclear domain and binds to a herpesvirus regulatory protein. Embo J. 1997; 16 (3): 566-577.
77. Mayer D, Molawi K, Martinez-Sobrido L, et al. Identification of cellular interaction partners of the influenza virus ribonucleoprotein complex and polymerase complex using proteomic-based approaches. J Proteome Res. 2007; 6 (2): 672-682.
78. Yamayoshi S, Noda T, Ebihara H, et al. Ebola virus matrix protein VP40 uses the COPII transport system for its intracellular transport. Cell Host Microbe. 2008; 3 (3): 168-177.
79. Jasenosky LD, Neumann G, Lukashevich I, et al. Ebola virus VP40-induced particle formation and association with the lipid bilayer. J Virol. 2001; 75 (11): 5205-5214.
80. Timmins J, Scianimanico S, Schoehn G, et al. Vesicular release of Ebola virus matrix protein VP40. Virology. 2001; 283 (1): 1-6.
81. Hrecka K, Hao CL, Gierszewska M, et al. Vpx relieves inhibition of HIV-1 infection of macrophages mediated by the SAMHD1 protein. Nature. 2011; 474 (7353): 658-U137.
82. Srivastava S, Swanson SK, Manel N, et al. Lentiviral Vpx accessory factor targets VprBP/DCAF1 substrate adaptor for cullin 4 E3 ubiquitin ligase to enable macrophage infection. Plos Pathog. 2008; 4 (5): e1000059.
83. Bergamaschi A, Ayinde D, David A, et al. The human immunodeficiency virus type 2 Vpx protein usurps the CUL4A-DDB1 DCAF1 ubiquitin ligase to overcome a postentry block in macrophage infection. J Virol. 2009; 83 (10): 4854-4860.
84. Kaul R, Verma SC, Robertson ES. Protein complexes associated with the Kaposis sarcoma-associated herpesvirus-encoded LANA. Virology. 2007; 364 (2): 317-329.
85. Greco TM, Diner BA, Cristea IM. The Impact of Mass Spectrometry-Based Proteomics on Fundamental Discoveries in Virology. Ann Rev Virol. 2014; 1: 581-604.
86. Moorman NJ, Cristea IM, Terhune SS, et al. Human cytomegalovirus protein UL38 inhibits host cell stress responses by antagonizing the tuberous sclerosis protein complex. Cell Host Microbe. 2008; 3 (4): 253-262.
87. Bartel PL, Roecklein JA, SenGupta D, et al. A protein linkage map of Escherichia coli bacteriophage T7. Nat Genet. 1996; 12 (1): 72-77.
88. Calderwood MA, Venkatesan K, Xing L, et al. Epstein-Barr virus and virus human protein interaction maps. Proc Natl Acad Sci USA. 2007; 104 (18): 7606-7611.
89. De Chassey B, Navratil V, Tafforeau L, et al. Hepatitis C virus infection protein network. Mol Syst Biol. 2008; 4: 230.
90. Khadka S, Vangeloff AD, Zhang CY, et al. A physical interaction network of dengue virus and human proteins. Mol Cell Proteomics. 2011; 10: 12.
91. Rozenblatt-Rosen O, Deo RC, Padi M, et al. Interpreting cancer genomes using systematic host network perturbations by tumour virus proteins. Nature. 2012; 487 (7408): 491-495.
92. Pichlmair A, Kandasamy K, Alvisi G, et al. Viral immune modulators perturb the human molecular network by common and unique strategies. Nature. 2012; 487 (7408): 486-490.
93. Bowie AG, Unterholzner L. Viral evasion and subversion of pattern-recognition receptor signalling. Nat Rev Immunol. 2008; 8 (12): 911-922.
94. Finlay BB, McFadden G. Anti-immunology: evasion of the host immune system by bacterial and viral pathogens. Cell. 2006; 124 (4): 767-782.
95. Miernyk JA, Thelen JJ. Biochemical approaches for discovering protein-protein interactions. Plant J. 2008; 53 (4): 597-609.
96. Spirin AS, Belitsin N, Lerman MI. Use of formaldehyde fixation for studies of ribonucleoprotein particles by caesium chloride density-gradient centrifugation. J Mol Biol. 1965; 14 (2): 611.
97. Singh P, Panchaud A, Goodlett DR. Chemical cross-linking and mass spectrometry as a low-resolution protein structure determination technique. Anal Chem. 2010; 82 (7): 2636-2642.
98. Sutherland BW, Toews J, Kast J. Utility of formaldehyde cross-linking and mass spectrometry in the study of protein-protein interactions. J Mass Spectrom. 2008; 43 (6): 699-715.
99. Tang XT, Bruce JE. A new cross-linking strategy: protein interaction reporter (PIR) technology for protein-protein interaction studies. Mol Biosyst. 2010; 6 (6): 939-947.
100. Chavez JD, Cilia M, Weisbrod CR, et al. 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. 2012; 11 (5): 2968-2981.
101. Anderson GA, Tolic N, Tang XT, et al. Informatics strategies for large-scale novel cross-linking analysis. J Proteome Res. 2007; 6 (9): 3412-3421.
102. Cy F, Uetrecht C, Kang SY, et al. A docking model based on mass spectrometric and biochemical data describes phage packaging motor incorporation. Mol Cell Proteomics. 2010; 9 (8): 1764-1773.
103. Kang S, Hawkridge AM, Johnson KL, et al. Identification of subunit-subunit interactions in bacteriophage P22 procapsids by chemical cross-linking and mass spectrometry. J Proteome Res. 2006; 5 (2): 370-377.
104. Yu XB, Bian XF, Throop A, et al. Exploration of panviral proteome: high-throughput cloning and functional implications in virus-host interactions. Theranostics. 2014; 4 (8): 808-822.
105. Lueking A, Horn M, Eickhoff H, et al. Protein microarrays for gene expression and antibody screening. Anal Biochem. 1999; 270 (1): 103-111.
106. MacBeath G, Schreiber SL. Printing proteins as microarrays for high-throughput function determination. Science. 2000; 289 (5485): 1760-1763.
107. Newman JRS, Keating AE. Comprehensive identification of human bZIP interactions with coiled-coil arrays. Science. 2003; 300 (5628): 2097-2101.
108. Zhu H, Bilgin M, Bangham R, et al. Global analysis of protein activities using proteome chips. Science. 2001; 293 (5537): 2101-2105.
109. Ramachandran N, Hainsworth E, Bhullar B, et al. Self-assembling protein microarrays. Science. 2004; 305 (5680): 86-90.
110. Ramachandran N, Raphael JV, Hainsworth E, et al. Next-generation high-density self-assembling functional protein arrays. Nat Methods. 2008; 5 (6): 535-538.
111. Bian X, Wiktor P, Kahn P, et al. Antiviral antibody profiling by high-density protein arrays. Proteomics. 2015; 15 (12): 2136-2145.
112. Ceroni A, Sibani S, Baiker A, et al. Systematic analysis of the IgG antibody immune response against varicella zoster virus (VZV) using a self-assembled protein microarray. Mol Biosyst. 2010; 6 (9): 1604-1610.
113. Tsai Y-C, Greco TM, Boonmee A, et al. Functional proteomics establishes the interaction of SIRT7 with chromatin remodeling complexes and expands its role in regulation of RNA polymerase I transcription. Mol Cell Proteomics. 2012; 11 (5): 60-76.
114. Dunham SM, Pudavar HE, Prasad PN, et al. Cellular signaling and protein-protein interactions studied using fluorescence recovery after photobleaching. J Phys Chem B. 2004; 108 (29): 10540-10546.
115. Piston DW, Kremers G-J. Fluorescent protein FRET: the good, the bad and the ugly. Trends Biochem Sci. 2007; 32 (9): 407-414.
116. Masi A, Cicchi R, Carloni A, et al. Optical methods in the study of protein-protein interactions. Adv Exp Med Biol. 2010; 674: 33-42.
117. Helbig KJ, Eyre NS, Yip E, et al. The antiviral protein viperin inhibits hepatitis c virus replication via interaction with nonstructural protein 5A. Hepatology. 2011; 54 (5): 1506-1517.
118. Fredriksson S, Gullberg M, Jarvius J, et al. Protein detection using proximity-dependent DNA ligation assays. Nat Biotechnol. 2002; 20 (5): 473-477.
119. Dutta D, Dutta S, Veettil MV, et al. BRCA1 regulates IFI16 mediated nuclear innate sensing of herpes viral DNA and subsequent induction of the innate inflammasome and interferon-beta responses. Plos Pathog. 2015; 11: 6.
120. Johnson KE, Bottero V, Flaherty S, et al. IFI16 restricts HSV-1 replication by accumulating on the HSV-1 genome, repressing HSV-1 gene expression, and directly or indirectly modulating histone modifications. Plos Pathog. 2014; 10: 11.
121. De Chassey B, Meyniel-Schicklin L, Vonderscher J, et al. Virus-host interactomics: new insights and opportunities for antiviral drug discovery. Genome Med. 2014; 6:115.
122. Bateman A, Martin MJ, ODonovan C, et al. UniProt: a hub for protein information. Nucleic Acids Res. 2015; 43 (D1): D204-D212.
123. Calderone A, Licata L, Cesareni G. VirusMentha: a new resource for virus-host protein interactions. Nucleic Acids Res. 2015; 43 (D1): D588-D592.
124. Guirimand T, Delmotte S, Navratil V. VirHostNet 2.0: surfing on the web of virus/host molecular interactions data. Nucleic Acids Res. 2015; 43 (D1): D583-D587.
125. Navratil V, De Chassey B, Meyniel L, et al. VirHostNet: a knowledge base for the management and the analysis of proteome-wide virus-host interaction networks. Nucleic Acids Res. 2009; 37: D661-D668.
126. Orchard S, Ammari M, Aranda B, et al. The MIntAct project-IntAct as a common curation platform for 11 molecular interaction databases. Nucleic Acids Res. 2014; 42 (D1): D358-D363.
127. Salwinski L, Miller CS, Smith AJ, et al. The database of Interacting Proteins: 2004 update. Nucleic Acids Res. 2004; 32: D449-D451.
128. Serva S, Nagy PD. Proteomics analysis of the tombusvirus replicase: Hsp70 molecular chaperone is associated with the replicase and enhances viral RNA replication. J Virol. 2006; 80 (5): 2162-2169.
129. Nagy PD, Pogany J, Lin J-Y. How yeast can be used as a genetic platform to explore virus-host interactions: from omics to functional studies. Trends Microbiol. 2014; 22 (6): 309-316.
130. Li ZH, Barajas D, Panavas T, et al. Cdc34p ubiquitin-conjugating enzyme is a component of the tombusvirus replicase complex and ubiquitinates p33 replication protein. J Virol. 2008; 82 (14): 6911-6926.
131. Mendu V, Chiu MH, Barajas D, et al. Cpr1 cyclophilin and Ess1 parvulin prolyl isomerases interact with the tombusvirus replication protein and inhibit viral replication in yeast model host. Virology. 2010; 406 (2): 342-351.
132. MacLean B, Tomazela DM, Shulman N, et al. Skyline: an open source document editor for creating and analyzing targeted proteomics experiments. Bioinformatics. 2010; 26 (7): 966-968.
133. Picotti P, Bodenmiller B, Mueller LN, et al. Full dynamic range proteome analysis of S. cerevisiae by targeted proteomics. Cell. 2009; 138 (4): 795-806.
134. Prakash A, Tomazela DM, Frewen B, et al. Expediting the development of targeted SRM assays: using data from shotgun proteomics to automate method development. J Proteome Res. 2009; 8 (6): 2733-2739.
135. Cilia M, Peter KA, Bereman MS, et al. Discovery and targeted LC-MS/MS of purified polerovirus reveals differences in the virus-host interactome associated with altered aphid transmission. Plos One. 2012; 7: 10.
136. Jessani N, Cravatt BF. The development and application of methods for activity-based protein profiling. Curr Opin Chem Biol. 2004; 8 (1): 54-59.
137. Speers AE, Cravatt BF. Chemical strategies for activity-based proteomics. Chembiochem. 2004; 5 (1): 41-47.