Identifying host factors associated with DNA replicated during virus infection

Molecular and Cellular Proteomics

Volumn 16, Issue 12, 2017, Pages 2079-2097

  Reyes, Emigdio D ^a,b   Kulej, Katarzyna ^a,b   Pancholi, Neha J ^a,b   Akhtar, Lisa N ^b   Avgousti, Daphne C ^a,b   Kim, Eui Tae ^b   Bricker, Daniel K ^a,b   Spruce, Lynn A ^b   Koniski, Sarah A ^b   Seeholzer, Steven H ^b   Isaacs, Stuart N ^a   Garcia, Benjamin A ^a   Weitzman, Matthew D ^a,b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HOST FACTOR; VIRAL PROTEIN; PROTEOME;

ADENOVIRIDAE; ARTICLE; DNA REPLICATION; FEMALE; HUMAN; HUMAN CELL; NONHUMAN; NUCLEOLUS; PRIORITY JOURNAL; PROTEIN ISOLATION; VIRUS CELL INTERACTION; VIRUS GENOME; VIRUS INFECTION; VIRUS REPLICATION; A-549 CELL LINE; COMPARATIVE STUDY; DEPENDOPARVOVIRUS; HELA CELL LINE; HOST PATHOGEN INTERACTION; METABOLISM; PHYSIOLOGY; PROCEDURES; PROTEIN ANALYSIS; PROTEOMICS; SIMPLEXVIRUS; TUMOR CELL LINE; VACCINIA VIRUS;

A549 CELLS; CELL LINE, TUMOR; DEPENDOVIRUS; DNA REPLICATION; GENOME, VIRAL; HELA CELLS; HOST-PATHOGEN INTERACTIONS; HUMANS; PROTEIN INTERACTION MAPS; PROTEOME; PROTEOMICS; SIMPLEXVIRUS; VACCINIA VIRUS; VIRAL PROTEINS; VIRUS DISEASES; VIRUS REPLICATION;

EID: 85038814950     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M117.067116     Document Type: Article

References (94)

1. Goebel, S. J., Johnson, G. P., Perkus, M. E., Davis, S. W., Winslow, J. P., Paoletti, E. (1990) The complete DNA sequence of vaccinia virus. Virology 179, 247-266, 517-563
2. Moss, B. (2013) Poxvirus DNA replication. Cold Spring Harb. Perspect. Biol. 5, a010199
3. Boyle, K. A., Greseth, M. D., Traktman, P. (2015) Genetic confirmation that the H5 protein is required for vaccinia virus DNA replication. J. Virol. 89, 6312-6327
4. Challberg, M. D., Kelly, T. J. (1989) Animal virus DNA replication. Annu. Rev. Biochem. 58, 671-717
5. Challberg, M. D. (1986) A method for identifying the viral genes required for herpesvirus DNA replication. Proc. Natl. Acad. Sci. U.S.A. 83, 9094-9098
6. Schmid, M., Speiseder, T., Dobner, T., Gonzalez, R. A. (2014) DNA virus replication compartments. J. Virol. 88, 1404-1420
7. Puvion-Dutilleul, F., Puvion, E. (1990) Replicating single-stranded adenovirus type 5 DNA molecules accumulate within well-delimited intranuclear areas of lytically infected HeLa cells. Eur. J. Cell Biol. 52, 379-388
8. Quinlan, M. P., Chen, L. B., Knipe, D. M. (1984) The intranuclear location of a herpes simplex virus DNA-binding protein is determined by the status of viral DNA replication. Cell 36, 857-868
9. Tolonen, N., Doglio, L., Schleich, S., Krijnse Locker, J. (2001) Vaccinia virus DNA replication occurs in endoplasmic reticulum-enclosed cytoplasmic mini-nuclei. Mol. Biol. Cell 12, 2031-2046
10. Taylor, T. J., Knipe, D. M. (2004) Proteomics of herpes simplex virus replication compartments: Association of cellular DNA replication, repair, recombination, chromatin remodeling proteins with ICP8. J. Virol. 78, 5856-5866
11. Wilkinson, D. E., Weller, S. K. (2004) Recruitment of cellular recombination and repair proteins to sites of herpes simplex virus type 1 DNA replication is dependent on the composition of viral proteins within prereplicative sites and correlates with the induction of the DNA damage response. J. Virol. 78, 4783-4796
12. Ebert, S. N., Subramanian, D., Shtrom, S. S., Chung, I. K., Parris, D. S., Muller, M. T. (1994) Association between the p170 form of human topoisomerase II and progeny viral DNA in cells infected with herpes simplex virus type 1. J. Virol. 68, 1010-1020
13. Katsafanas, G. C., Moss, B. (2007) Colocalization of transcription and translation within cytoplasmic poxvirus factories coordinates viral expression and subjugates host functions. Cell Host Microbe 2, 221-228
14. Oh, J., Broyles, S. S. (2005) Host cell nuclear proteins are recruited to cytoplasmic vaccinia virus replication complexes. J. Virol. 79, 12852-12860
15. Lin, Y.-C. J., Li, J., Irwin, C. R., Jenkins, H., DeLange, L., Evans, D. H. (2008) Vaccinia virus DNA ligase recruits cellular topoisomerase II to sites of viral replication and assembly. J. Virol. 82, 5922-5932
16. Paran, N., De Silva, F. S., Senkevich, T. G., Moss, B. (2009) Cellular DNA ligase I is recruited to cytoplasmic vaccinia virus factories and masks the role of the vaccinia ligase in viral DNA replication. Cell Host Microbe 6, 563-569
17. de Jong, R. N., van der Vliet, P. C. (1999) Mechanism of DNA replication in eukaryotic cells: Cellular host factors stimulating adenovirus DNA replication. Gene 236, 1-12
18. Sirbu, B. M., McDonald, W. H., Dungrawala, H., Badu-Nkansah, A., Kavanaugh, G. M., Chen, Y., Tabb, D. L., Cortez, D. (2013) Identification of proteins at active, stalled, collapsed replication forks using isolation of proteins on nascent DNA (iPOND) coupled with mass spectrometry. J. Biol. Chem. 288, 31458-31467
19. Lopez-Contreras, A. J., Ruppen, I., Nieto-Soler, M., Murga, M., Rodriguez-Acebes, S., Remeseiro, S., Rodrigo-Perez, S., Rojas, A. M., Mendez, J., Muñ oz, J., Fernandez-Capetillo, O. (2013) A proteomic characterization of factors enriched at nascent DNA molecules. Cell Rep. 3, 1105-1116
20. Alabert, C., Bukowski-Wills, J.-C., Lee, S.-B., Kustatscher, G., Nakamura, K., de Lima Alves, F., Menard, P., Mejlvang, J., Rappsilber, J., Groth, A. (2014) Nascent chromatin capture proteomics determines chromatin dynamics during DNA replication and identifies unknown fork components. Nat. Cell Biol. 16, 281-293
21. Sirbu, B. M., Couch, F. B., Feigerle, J. T., Bhaskara, S., Hiebert, S. W., Cortez, D. (2011) Analysis of protein dynamics at active, stalled, collapsed replication forks. Genes Dev. 25, 1320-1327
22. Sirbu, B. M., Couch, F. B., Cortez, D. (2012) Monitoring the spatiotemporal dynamics of proteins at replication forks and in assembled chromatin using isolation of proteins on nascent DNA. Nat. Protoc. 7, 594-605
23. Wang, I.-H., Suomalainen, M., Andriasyan, V., Kilcher, S., Mercer, J., Neef, A., Luedtke, N. W., Greber, U. F. (2013) Tracking viral genomes in host cells at single-molecule resolution. Cell Host Microbe 14, 468-480
24. Dembowski, J. A., DeLuca, N. A. (2015) Selective recruitment of nuclear factors to productively replicating herpes simplex virus genomes. PLoS Pathog. 11, e1004939
25. Dungrawala, H., Rose, K. L., Bhat, K. P., Mohni, K. N., Glick, G. G., Couch, F. B., Cortez, D. (2015) The replication checkpoint prevents two types of fork collapse without regulating replisome stability. Mol. Cell 59, 998-1010
26. Carson, C. T., Schwartz, R. A., Stracker, T. H., Lilley, C. E., Lee, D. V., Weitzman, M. D. (2003) The Mre11 complex is required for ATM activation and the G2/M checkpoint. EMBO J. 22, 6610-6620
27. Kim, Y., Lach, F. P., Desetty, R., Hanenberg, H., Auerbach, A. D., Smogorzewska, A. (2011) Mutations of the SLX4 gene in Fanconi anemia. Nat. Genet. 43, 142-146
28. Bridge, E., Ketner, G. (1989) Redundant control of adenovirus late gene expression by early region 4. J. Virol. 63, 631-638
29. Bridge, E., Ketner, G. (1990) Interaction of adenoviral E4 and E1b products in late gene expression. Virology 174, 345-353
30. Stracker, T. H., Carson, C. T., Weitzman, M. D. (2002) Adenovirus oncoproteins inactivate the Mre11-Rad50-NBS1 DNA repair complex. Nature 418, 348-352
31. Cox, J., Mann, M. (2008) MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol. 26, 1367-1372
32. Cox, J., Neuhauser, N., Michalski, A., Scheltema, R. A., Olsen, J. V., Mann, M. (2011) Andromeda: A peptide search engine integrated into the MaxQuant environment. J. Proteome Res. 10, 1794-1805
33. Schwanhä usser, B., Busse, D., Li, N., Dittmar, G., Schuchhardt, J., Wolf, J., Chen, W., Selbach, M. (2011) Global quantification of mammalian gene expression control. Nature 473, 337-342
34. Pombo, A., Ferreira, J., Bridge, E., Carmo-Fonseca, M. (1994) Adenovirus replication and transcription sites are spatially separated in the nucleus of infected cells. EMBO J. 13, 5075-5085
35. Hancock, M. H., Corcoran, J. A., 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
36. Lin, Y.-C. J., Evans, D. H. (2010) Vaccinia virus particles mix inefficiently, in a way that would restrict viral recombination, in coinfected cells. J. Virol. 84, 2432-2443
37. de Bruyn Kops, A., Knipe, D. M. (1988) Formation of DNA replication structures in herpes virus-infected cells requires a viral DNA binding protein. Cell 55, 857-868
38. Nakamura, H., Morita, T., Sato, C. (1986) Structural organizations of replicon domains during DNA synthetic phase in the mammalian nucleus. Exp. Cell Res. 165, 291-297
39. Leonhardt, H., Rahn, H. P., Weinzierl, P., Sporbert, A., Cremer, T., Zink, D., Cardoso, M. C. (2000) Dynamics of DNA replication factories in living cells. J. Cell Biol. 149, 271-280
40. Halbert, D. N., Cutt, J. R., Shenk, T. (1985) Adenovirus early region 4 encodes functions required for efficient DNA replication, late gene expression, host cell shutoff. J. Virol. 56, 250-257
41. Joklik, W. K., Becker, Y. (1964) The replication and coating of vaccinia DNA. J. Mol. Biol. 10, 452-474
42. Hoeben, R. C., Uil, T. G. (2013) Adenovirus DNA replication. Cold Spring Harb. Perspect. Biol. 5, a013003
43. Weller, S. K., Coen, D. M. (2012) Herpes simplex viruses: Mechanisms of DNA replication. Cold Spring Harb. Perspect. Biol. 4:a013011,
44. Weitzman, M. D., Lilley, C. E., Chaurushiya, M. S. (2010) Genomes in conflict: Maintaining genome integrity during virus infection. Annu. Rev. Microbiol. 64, 61-81
45. Luftig, M. A. (2014) Viruses and the DNA damage response: Activation and antagonism. Annu. Rev. Virol. 1, 605-625
46. Turnell, A. S., Grand, R. J. (2012) DNA viruses and the cellular DNAdamage response. J. Gen. Virol. 93, 2076-2097
47. Orazio, N. I., Naeger, C. M., Karlseder, J., Weitzman, M. D. (2011) The adenovirus E1b55K/E4orf6 complex induces degradation of the Bloom helicase during infection. J. Virol. 85, 1887-1892
48. Evans, J. D., Hearing, P. (2005) Relocalization of the Mre11-Rad50-Nbs1 complex by the adenovirus E4 ORF3 protein is required for viral replication. J. Virol. 79, 6207-6215
49. Mathew, S. S., Bridge, E. (2007) The cellular Mre11 protein interferes with adenovirus E4 mutant DNA replication. Virology 365, 346-355
50. Lilley, C. E., Carson, C. T., Muotri, A. R., Gage, F. H., Weitzman, M. D. (2005) DNA repair proteins affect the lifecycle of herpes simplex virus 1. Proc. Natl. Acad. Sci. U.S.A. 102, 5844-5849
51. Weitzman, M. D., Ornelles, D. A. (2005) Inactivating intracellular antiviral responses during adenovirus infection. Oncogene 24, 7686-7696
52. Doucas, V., Ishov, A. M., Romo, A., Juguilon, H., Weitzman, M. D., Evans, R. M., Maul, G. G. (1996) Adenovirus replication is coupled with the dynamic properties of the PML nuclear structure. Genes Dev. 10, 196-207
53. Schreiner, S., Wimmer, P., Dobner, T. (2012) Adenovirus degradation of cellular proteins. Future Microbiol. 7, 211-225
54. Schwartz, R. A., Lakdawala, S. S., Eshleman, H. D., Russell, M. R., Carson, C. T., Weitzman, M. D. (2008) Distinct requirements of adenovirus E1b55K protein for degradation of cellular substrates. J. Virol. 82, 9043-9055
55. Roy, A. L. (2012) Biochemistry and biology of the inducible multifunctional transcription factor TFII-I: 10years later. Gene 492, 32-41
56. Shepard, R. N., Ornelles, D. A. (2003) E4orf3 is necessary for enhanced S-phase replication of cell cycle-restricted subgroup C adenoviruses. J. Virol. 77, 8593-8595
57. Huang, M. M., Hearing, P. (1989) Adenovirus early region 4 encodes two gene products with redundant effects in lytic infection. J. Virol. 63, 2605-2615
58. Carson, C. T., Orazio, N. I., Lee, D. V., Suh, J., Bekker-Jensen, S., Araujo, F. D., Lakdawala, S. S., Lilley, C. E., Bartek, J., Lukas, J., Weitzman, M. D. (2009) Mislocalization of the MRN complex prevents ATR signaling during adenovirus infection. EMBO J. 28, 652-662
59. Sloan, K. E., Bohnsack, M. T., Schneider, C., Watkins, N. J. (2014) The roles of SSU processome components and surveillance factors in the initial processing of human ribosomal RNA. RNA 20, 540-550
60. Lafontaine, D. L. J. (2015) Noncoding RNAs in eukaryotic ribosome biogenesis and function. Nat. Struct. Mol. Biol. 22, 11-19
61. Phipps, K. R., Charette, J. M., Baserga, S. J. (2011) The small subunit processome in ribosome biogenesis-progress and prospects. RNA 2, 1-21
62. Hayano, T., Yanagida, M., Yamauchi, Y., Shinkawa, T., Isobe, T., Takahashi, N. (2003) Proteomic analysis of human Nop56p-associated pre-ribosomal ribonucleoprotein complexes. Possible link between Nop56p and the nucleolar protein treacle responsible for Treacher Collins syndrome. J. Biol. Chem. 278, 34309-34319
63. Lin, C.-I., Yeh, N.-H. (2009) Treacle recruits RNA polymerase I complex to the nucleolus that is independent of UBF. Biochem. Biophys. Res. Commun. 386, 396-401
64. Ciccia, A., Huang, J.-W., Izhar, L., Sowa, M. E., Harper, J. W., Elledge, S. J. (2014) Treacher Collins syndrome TCOF1 protein cooperates with NBS1 in the DNA damage response. Proc. Natl. Acad. Sci. U.S.A. 111, 18631-18636
65. Werner, A., Iwasaki, S., McGourty, C. A., Medina-Ruiz, S., Teerikorpi, N., Fedrigo, I., Ingolia, N. T., Rape, M. (2015) Cell-fate determination by ubiquitin-dependent regulation of translation. Nature 525, 523-527
66. Hidalgo, P., Anzures, L., Herná ndez-Mendoza, A., Guerrero, A., Wood, C. D., Valdé s, M., Dobner, T., Gonzalez, R. A. (2016) Morphological, biochemical, functional study of viral replication compartments isolated from adenovirus-infected cells. J. Virol. 90, 3411-3427
67. Lenarcic, E. M., Landry, D. M., Greco, T. M., Cristea, I. M., Thompson, S. R. (2013) Thiouracil cross-linking mass spectrometry: A cell-based method to identify host factors involved in viral amplification. J. Virol. 87, 8697-8712
68. Sugimoto, A., Kanda, T., Yamashita, Y., Murata, T., Saito, S., Kawashima, D., Isomura, H., Nishiyama, Y., Tsurumi, T. (2011) Spatiotemporally different DNA repair systems participate in Epstein-Barr virus genome maturation. J. Virol. 85, 6127-6135
69. Mercer, J., Snijder, B., Sacher, R., Burkard, C., Bleck, C. K. E., Stahlberg, H., Pelkmans, L., Helenius, A. (2012) RNAi screening reveals proteasome-A nd Cullin3-dependent stages in vaccinia virus infection. Cell Rep. 2, 1036-1047
70. Sivan, G., Martin, S. E., Myers, T. G., Buehler, E., Szymczyk, K. H., Ormanoglu, P., Moss, B. (2013) Human genome-wide RNAi screen reveals a role for nuclear pore proteins in poxvirus morphogenesis. Proc. Natl. Acad. Sci. U.S.A. 110, 3519-3524
71. Cassimeris, L., Skibbens, R. V. (2003) Regulated assembly of the mitotic spindle: A perspective from two ends. Curr. Issues Mol. Biol. 5, 99-112
72. Booth, D. G., Hood, F. E., Prior, I. A., Royle, S. J. (2011) A TACC3/ch-TOG/clathrin complex stabilises kinetochore fibres by inter-microtubule bridging. EMBO J. 30, 906-919
73. Chini, C. C. S., Chen, J. (2003) Human claspin is required for replication checkpoint control. J. Biol. Chem. 278, 30057-30062
74. Lin, S.-Y., Li, K., Stewart, G. S., Elledge, S. J. (2004) Human Claspin works with BRCA1 to both positively and negatively regulate cell proliferation. Proc. Natl. Acad. Sci. U.S.A. 101, 6484-6489
75. Zhang, Y., Hunter, T. (2014) Roles of Chk1 in cell biology and cancer therapy. Int. J. Cancer 134, 1013-1023
76. Lakdawala, S. S., Schwartz, R. A., Ferenchak, K., Carson, C. T., McSharry, B. P., Wilkinson, G. W., Weitzman, M. D. (2008) Differential requirements of the C terminus of Nbs1 in suppressing adenovirus DNA replication and promoting concatemer formation. J. Virol. 82, 8362-8372
77. Kottemann, M. C., Smogorzewska, A. (2013) Fanconi anaemia and the repair of Watson and Crick DNA crosslinks. Nature 493, 356-363
78. Andersen, S. L., Bergstralh, D. T., Kohl, K. P., LaRocque, J. R., Moore, C. B., Sekelsky, J. (2009) Drosophila MUS312 and the vertebrate ortholog BTBD12 interact with DNA structure-specific endonucleases in DNA repair and recombination. Mol. Cell 35, 128-135
79. Fekairi, S., Scaglione, S., Chahwan, C., Taylor, E. R., Tissier, A., Coulon, S., Dong, M.-Q., Ruse, C., Yates, J. R., Russell, P., Fuchs, R. P., McGowan, C. H., Gaillard, P.-H. L. (2009) Human SLX4 is a Holliday junction resolvase subunit that binds multiple DNA repair/recombination endonucleases. Cell 138, 78-89
80. Muñ oz, I. M., Hain, K., Dé clais, A.-C., Gardiner, M., Toh, G. W., Sanchez-Pulido, L., Heuckmann, J. M., Toth, R., Macartney, T., Eppink, B., Kanaar, R., Ponting, C. P., Lilley, D. M. J., Rouse, J. (2009) Coordination of structure-specific nucleases by human SLX4/BTBD12 is required for DNA repair. Mol. Cell 35, 116-127
81. Saito, T. T., Youds, J. L., Boulton, S. J., Colaiá covo, M. P. (2009) Caenorhabditis elegans HIM-18/SLX-4 interacts with SLX-1 and XPF-1 and maintains genomic integrity in the germline by processing recombination intermediates. PLoS Genet. 5, e1000735
82. Svendsen, J. M., Smogorzewska, A., Sowa, M. E., O'Connell, B. C., Gygi, S. P., Elledge, S. J., Harper, J. W. (2009) Mammalian BTBD12/SLX4 assembles a Holliday junction resolvase and is required for DNA repair. Cell 138, 63-77
83. Guervilly, J.-H., Takedachi, A., Naim, V., Scaglione, S., Chawhan, C., Lovera, Y., Despras, E., Kuraoka, I., Kannouche, P., Rosselli, F., Gaillard, P.-H. L. (2015) The SLX4 complex is a SUMO E3 ligase that impacts on replication stress outcome and genome stability. Mol. Cell 57, 123-137
84. Nielsen, C. F., Huttner, D., Bizard, A. H., Hirano, S., Li, T.-N., Palmai-Pallag, T., Bjerregaard, V. A., Liu, Y., Nigg, E. A., Wang, L. H.-C., Hickson, I. D. (2015) PICH promotes sister chromatid disjunction and co-operates with topoisomerase II in mitosis. Nat. Commun. 6, 8962
85. Okuwaki, M., Matsumoto, K., Tsujimoto, M., Nagata, K. (2001) Function of nucleophosmin/B23, a nucleolar acidic protein, as a histone chaperone. FEBS Letters 506, 272-276
86. Lawrence, F. J. (2006) Nucleolar protein upstream binding factor is sequestered into adenovirus DNA replication centres during infection without affecting RNA polymerase I location or ablating rRNA synthesis. J. Cell Sci. 119, 2621-2631
87. Hindley, C. E., Davidson, A. D., Matthews, D. A. (2007) Relationship between adenovirus DNA replication proteins and nucleolar proteins B23.1 and B23.2. J. Gen. Virol. 88, 3244-3248
88. Lam, Y. W., Evans, V. C., Heesom, K. J., Lamond, A. I., Matthews, D. A. (2010) Proteomics analysis of the nucleolus in adenovirus-infected cells. Mol. Cell. Proteomics 9, 117-130
89. Maden, B. E. (1990) The numerous modified nucleotides in eukaryotic ribosomal RNA. Prog. Nucleic Acids Res. Mol. Biol. 39, 241-303
90. Sohn, S.-Y., Bridges, R. G., Hearing, P. (2015) Proteomic analysis of ubiquitin-like posttranslational modifications induced by the adenovirus E4-ORF3 protein. J. Virol. 89, 1744-1755
91. Wright, J., Atwan, Z., Morris, S. J., Leppard, K. N. (2015) The human adenovirus type 5 L4 promoter is negatively regulated by TFII-I and L4-33K. J. Virol. 89, 7053-7063
92. Bridges, R. G., Sohn, S.-Y., Wright, J., Leppard, K. N., Hearing, P. (2016) The adenovirus E4-ORF3 protein stimulates SUMOylation of general transcription factor TFII-I to direct proteasomal degradation. mBio 7, e02184-15-10
93. Peñ a-Herná ndez, R., Marques, M., Hilmi, K., Zhao, T., Saad, A., Alaoui-Jamali, M. A., del Rincon, S. V., Ashworth, T., Roy, A. L., Emerson, B. M., Witcher, M. (2015) Genome-wide targeting of the epigenetic regulatory protein CTCF to gene promoters by the transcription factor TFII-I. Proc. Natl. Acad. Sci. U.S.A. 112, E677-E86
94. Pentland, I., Parish, J. L. (2015) Targeting CTCF to control virus gene expression: A common theme amongst diverse DNA viruses. Viruses 7, 3574-3585