What's the damage? The impact of pathogens on pathways that maintain host genome integrity

Cell Host and Microbe

Volumn 15, Issue 3, 2014, Pages 283-294

  Weitzman, Matthew D ^a,b   Weitzman, Jonathan B ^c  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^c UNIVERSITÉ PARIS DESCARTES   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL INFECTION; BACTERIUM; CARCINOGENESIS; CELL METABOLISM; CELL STRUCTURE; DNA DAMAGE; DNA REPAIR; GENOME; HUMAN; INFLAMMATION; NONHUMAN; ONCOGENE; PARASITE; PARASITOSIS; PATHOGENESIS; PRIORITY JOURNAL; REVIEW; SOMATIC MUTATION; VIRUS; VIRUS INFECTION;

APOPTOSIS; BACTERIAL INFECTIONS; DNA DAMAGE; DNA REPAIR; GENOMIC INSTABILITY; HOST-PATHOGEN INTERACTIONS; MUTATION; NEOPLASMS; PARASITIC DISEASES; VIRUS DISEASES;

EID: 84896064537     PISSN: 19313128     EISSN: 19346069     Source Type: Journal    
DOI: 10.1016/j.chom.2014.02.010     Document Type: Review

References (122)

1. Alaoui-El-Azher, M., Mans, J.J., Baker, H.V., Chen, C., Progulske-Fox, A., Lamont, R.J., and Handfield, M. (2010). Role of the ATM-checkpoint kinase 2 pathway in CDT-mediated apoptosis of gingival epithelial cells. PLoS ONE 5, e11714.
2. Araujo, F.D., Stracker, T.H., Carson, C.T., Lee, D.V., and Weitzman, M.D. (2005). Adenovirus type 5 E4orf3 protein targets the Mre11 complex to cytoplasmic aggresomes. J. Virol. 79, 11382-11391. (Pubitemid 41170679)
3. Arthur, J.C., Perez-Chanona, E., Mühlbauer, M., Tomkovich, S., Uronis, J.M., Fan, T.J., Campbell, B.J., Abujamel, T., Dogan, B., Rogers, A.B., et al. (2012). Intestinal inflammation targets cancer-inducing activity of the microbiota. Science 338, 120-123.
4. Bekerman, E., Jeon, D., Ardolino, M., and Coscoy, L. (2013). A role for host activation-induced cytidine deaminase in innate immune defense against KSHV. PLoS Pathog. 9, e1003748.
5. Belgnaoui, S.M., Fryrear, K.A., Nyalwidhe, J.O., Guo, X., and Semmes, O.J. (2010). The viral oncoprotein tax sequesters DNA damage response factors by tethering MDC1 to chromatin. J. Biol. Chem. 285, 32897-32905.
6. Benamrouz, S., Conseil, V., Creusy, C., Calderon, E., Dei-Cas, E., and Certad, G. (2012). Parasites and malignancies, a review, with emphasis on digestive cancer induced by Cryptosporidium parvum (Alveolata: Apicomplexa). Parasite 19, 101-115.
7. Bierne, H., Hamon, M., and Cossart, P. (2012). Epigenetics and bacterial infections. Cold Spring Harb Perspect Med 2, a010272.
8. Blackford, A.N., Patel, R.N., Forrester, N.A., Theil, K., Groitl, P., Stewart, G.S., Taylor, A.M., Morgan, I.M., Dobner, T., Grand, R.J., and Turnell, A.S. (2010). Adenovirus 12 E4orf6 inhibits ATR activation by promoting TOPBP1 degradation. Proc. Natl. Acad. Sci. USA 107, 12251-12256.
9. Bougdour, A., Durandau, E., Brenier-Pinchart, M.P., Ortet, P., Barakat, M., Kieffer, S., Curt-Varesano, A., Curt-Bertini, R.L., Bastien, O., Coute, Y., et al. (2013). Host cell subversion by Toxoplasma GRA16, an exported dense granule protein that targets the host cell nucleus and alters gene expression. Cell Host Microbe 13, 489-500.
10. Bouvard, V., Baan, R.A., Grosse, Y., Lauby-Secretan, B., El Ghissassi, F., Benbrahim-Tallaa, L., Guha, N., and Straif, K.; WHO International Agency for Research on Cancer Monograph Working Group (2012). Carcinogenicity of malaria and of some polyomaviruses. Lancet Oncol. 13, 339-340.
11. Boxus, M., Twizere, J.C., Legros, S., Dewulf, J.F., Kettmann, R., and Willems, L. (2008). The HTLV-1 Tax interactome. Retrovirology 5, 76.
12. Boyer, J., Rohleder, K., and Ketner, G. (1999). Adenovirus E4 34k and E4 11k inhibit double strand break repair and are physically associated with the cellular DNA-dependent protein kinase. Virology 263, 307-312. (Pubitemid 29521523)
13. Burns, M.B., Lackey, L., Carpenter, M.A., Rathore, A., Land, A.M., Leonard, B., Refsland, E.W., Kotandeniya, D., Tretyakova, N., Nikas, J.B., et al. (2013). APOBEC3B is an enzymatic source of mutation in breast cancer. Nature 494, 366-370.
14. Carson, C.T., Schwartz, R.A., Stracker, T.H., Lilley, C.E., Lee, D.V., and Weitzman, M.D. (2003). The Mre11 complex is required for ATM activation and the G2/M checkpoint. EMBO J. 22, 6610-6620. (Pubitemid 38009607)
15. 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., and Weitzman, M.D. (2009). Mislocalization of the MRN complex prevents ATR signaling during adenovirus infection. EMBO J. 28, 652-662.
16. Certad, G., Creusy, C., Guyot, K., Mouray, A., Chassat, T., Delaire, B., Pinon, A., Sitja-Bobadilla, A., Alvarez-Pellitero, P., Praet, M., et al. (2010). Fulminant cryptosporidiosis associated with digestive adenocarcinoma in SCID mice infected with Cryptosporidium parvum TUM1 strain. Int. J. Parasitol. 40, 1469-1475.
17. Chaussepied, M., and Langsley, G. (1996). Theileria transformation of bovine leukocytes: a parasite model for the study of lymphoproliferation. Res. Immunol. 147, 127-138. (Pubitemid 26227519)
18. Choudhuri, T., Verma, S.C., Lan, K., Murakami, M., and Robertson, E.S. (2007). The ATM/ATR signaling effector Chk2 is targeted by Epstein-Barr virus nuclear antigen 3C to release the G2/M cell cycle block. J. Virol. 81, 6718-6730. (Pubitemid 46878076)
19. Chumduri, C., Gurumurthy, R.K., Zadora, P.K., Mi, Y., and Meyer, T.F. (2013). Chlamydia infection promotes host DNA damage and proliferation but impairs the DNA damage response. Cell Host Microbe 13, 746-758.
20. Ciccia, A., and Elledge, S.J. (2010). The DNA damage response: making it safe to play with knives. Mol. Cell 40, 179-204.
21. Cock-Rada, A.M., Medjkane, S., Janski, N., Yousfi, N., Perichon, M., Chaussepied, M., Chluba, J., Langsley, G., and Weitzman, J.B. (2012). SMYD3 promotes cancer invasion by epigenetic upregulation of the metalloproteinase MMP-9. Cancer Res. 72, 810-820.
22. Cuevas-Ramos, G., Petit, C.R., Marcq, I., Boury, M., Oswald, E., and Nougayrède, J.P. (2010). Escherichia coli induces DNA damage in vivo and triggers genomic instability in mammalian cells. Proc. Natl. Acad. Sci. USA 107, 11537-11542.
23. de Martel, C., Ferlay, J., Franceschi, S., Vignat, J., Bray, F., Forman, D., and Plummer, M. (2012). Global burden of cancers attributable to infections in 2008: a review and synthetic analysis. Lancet Oncol. 13, 607-615.
24. Demogines, A., East, A.M., Lee, J.H., Grossman, S.R., Sabeti, P.C., Paull, T.T., and Sawyer, S.L. (2010). Ancient and recent adaptive evolution of primate nonhomologous end joining genes. PLoS Genet. 6, e1001169.
25. Durkin, S.S., Guo, X., Fryrear, K.A., Mihaylova, V.T., Gupta, S.K., Belgnaoui, S.M., Haoudi, A., Kupfer, G.M., and Semmes, O.J. (2008). HTLV-1 Tax oncoprotein subverts the cellular DNA damage response via binding to DNA-dependent protein kinase. J. Biol. Chem. 283, 36311-36320.
26. Elwell, C.A., and Dreyfus, L.A. (2000). DNase I homologous residues in CdtB are critical for cytolethal distending toxin-mediated cell cycle arrest. Mol. Microbiol. 37, 952-963. (Pubitemid 30618154)
27. Endo, Y., Marusawa, H., Kinoshita, K., Morisawa, T., Sakurai, T., Okazaki, I.M., Watashi, K., Shimotohno, K., Honjo, T., and Chiba, T. (2007). Expression of activation-induced cytidine deaminase in human hepatocytes via NF-kappaB signaling. Oncogene 26, 5587-5595. (Pubitemid 47267836)
28. Everett, R.D., Rechter, S., Papior, P., Tavalai, N., Stamminger, T., and Orr, A. (2006). PML contributes to a cellular mechanism of repression of herpes simplex virus type 1 infection that is inactivated by ICP0. J. Virol. 80, 7995-8005. (Pubitemid 44182300)
29. Fedor, Y., Vignard, J., Nicolau-Travers, M.L., Boutet-Robinet, E., Watrin, C., Salles, B., and Mirey, G. (2013). From single-strand breaks to double-strand breaks during S-phase: a new mode of action of the Escherichia coli Cytolethal Distending Toxin. Cell. Microbiol. 15, 1-15.
30. Feng, H., Shuda, M., Chang, Y., and Moore, P.S. (2008). Clonal integration of a polyomavirus in human Merkel cell carcinoma. Science 319, 1096-1100. (Pubitemid 351300792)
31. Fonseca, G.J., Thillainadesan, G., Yousef, A.F., Ablack, J.N., Mossman, K.L., Torchia, J., and Mymryk, J.S. (2012). Adenovirus evasion of interferon-mediated innate immunity by direct antagonismof a cellular histone posttranslational modification. Cell Host Microbe 11, 597-606.
32. Fradet-Turcotte, A., Bergeron-Labrecque, F., Moody, C.A., Lehoux, M., Laimins, L.A., and Archambault, J. (2011). Nuclear accumulation of the papillomavirus E1 helicase blocks S-phase progression and triggers an ATM-dependent DNA damage response. J. Virol. 85, 8996-9012.
33. Friedberg, E.C., Walker, G.C., Siede, W., Wood, R.D., Schultz, R.A., and Ellenberger, T. (2006). DNA Repair and Mutagenesis, Second Edition. (New York: ASM Press).
34. Frisan, T., Cortes-Bratti, X., Chaves-Olarte, E., Stenerlöw, B., and Thelestam, M. (2003). The Haemophilus ducreyi cytolethal distending toxin induces DNA double-strand breaks and promotes ATM-dependent activation of RhoA. Cell. Microbiol. 5, 695-707. (Pubitemid 37185046)
35. Ge, Z., Rogers, A.B., Feng, Y., Lee, A., Xu, S., Taylor, N.S., and Fox, J.G. (2007). Bacterial cytolethal distending toxin promotes the development of dysplasia in a model of microbially induced hepatocarcinogenesis. Cell. Microbiol. 9, 2070-2080. (Pubitemid 47087096)
36. Gillespie, K.A., Mehta, K.P., Laimins, L.A., and Moody, C.A. (2012). Human papillomaviruses recruit cellular DNA repair and homologous recombination factors to viral replication centers. J. Virol. 86, 9520-9526.
37. Gruhne, B., Sompallae, R., Marescotti, D., Kamranvar, S.A., Gastaldello, S., and Masucci, M.G. (2009). The Epstein-Barr virus nuclear antigen-1 promotes genomic instability via induction of reactive oxygen species. Proc. Natl. Acad. Sci. USA 106, 2313-2318.
38. Guerra, L., Guidi, R., and Frisan, T. (2011). Do bacterial genotoxins contribute to chronic inflammation, genomic instability and tumor progression? FEBS J. 278, 4577-4588.
39. Guidi, R., Guerra, L., Levi, L., Stenerlöw, B., Fox, J.G., Josenhans, C., Masucci, M.G., and Frisan, T. (2013). Chronic exposure to the cytolethal distending toxins of Gram-negative bacteria promotes genomic instability and altered DNA damage response. Cell. Microbiol. 15, 98-113.
40. Guidoboni, M., Ferreri, A.J., Ponzoni, M., Doglioni, C., and Dolcetti, R. (2006). Infectious agents in mucosa-associated lymphoid tissue-type lymphomas: pathogenic role and therapeutic perspectives. Clin. Lymphoma Myeloma 6, 289-300.
41. Haller, D., Mackiewicz, M., Gerber, S., Beyer, D., Kullmann, B., Schneider, I., Ahmed, J.S., and Seitzer, U. (2010). Cytoplasmic sequestration of p53 promotes survival in leukocytes transformed by Theileria. Oncogene 29, 3079-3086.
42. Hanahan, D., and Weinberg, R.A. (2011). Hallmarks of cancer: the next generation. Cell 144, 646-674.
43. Hatakeyama, M. (2014). Helicobacter pylori CagA and Gastric Cancer: A Paradigm for Hit-and-Run Carcinogenesis. Cell Host Microbe 15, this issue, 306-316.
44. Hayashida, K., Kajino, K., Hattori, M., Wallace, M., Morrison, I., Greene, M.I., and Sugimoto, C. (2013). MDM2 regulates a novel form of incomplete neoplastic transformation of Theileria parva infected lymphocytes. Exp. Mol. Pathol. 94, 228-238.
45. Howley, P.M., and Livingston, D.M. (2009). Small DNA tumor viruses: large contributors to biomedical sciences. Virology 384, 256-259.
46. Jackson, S.P., and Durocher, D. (2013). Regulation of DNA damage responses by ubiquitin and SUMO. Mol. Cell 49, 795-807.
47. Jang, S.H., Lim, J.W., Morio, T., and Kim, H. (2012). Lycopene inhibits Helicobacter pylori-induced ATM/ATR-dependent DNA damage response in gastric epithelial AGS cells. Free Radic. Biol. Med. 52, 607-615.
48. Jha, H.C., Upadhyay, S.K., A J Prasad, M., Lu, J., Cai, Q., Saha, A., and Robertson, E.S. (2013). H2AX phosphorylation is important for LANA-mediated Kaposi's sarcoma-associated herpesvirus episome persistence. J. Virol. 87, 5255-5269.
49. Jinadasa, R.N., Bloom, S.E., Weiss, R.S., and Duhamel, G.E. (2011). Cytolethal distending toxin: a conserved bacterial genotoxin that blocks cell cycle progression, leading to apoptosis of a broad range of mammalian cell lineages. Microbiology 157, 1851-1875.
50. Kadaja, M., Isok-Paas, H., Laos, T., Ustav, E., and Ustav, M. (2009). Mechanism of genomic instability in cells infected with the high-risk human papillo-maviruses. PLoS Pathog. 5, e1000397.
51. Karen, K.A., and Hearing, P. (2011). Adenovirus core protein VII protects the viral genome from a DNA damage response at early times after infection. J. Virol. 85, 4135-4142.
52. Kerur, N., Veettil, M.V., Sharma-Walia, N., Bottero, V., Sadagopan, S., Otageri, P., and Chandran, B. (2011). IFI16 acts as a nuclear pathogen sensor to induce the inflammasome in response to Kaposi Sarcoma-associated herpesvirus infection. Cell Host Microbe 9, 363-375.
53. Kim, J.H., Kim, W.S., and Park, C. (2013). Epstein-Barr virus latent membrane protein 1 increases genomic instability through Egr-1-mediated up-regulation of activation-induced cytidine deaminase in B-cell lymphoma. Leuk. Lymphoma 54, 2035-2040.
54. Kinjo, T., Ham-Terhune, J., Peloponese, J.M., Jr., and Jeang, K.T. (2010). Induction of reactive oxygen species by human T-cell leukemia virus type 1 tax correlates with DNA damage and expression of cellular senescence marker. J. Virol. 84, 5431-5437.
55. Kondo, T., Kobayashi, J., Saitoh, T., Maruyama, K., Ishii, K.J., Barber, G.N., Komatsu, K., Akira, S., and Kawai, T. (2013). DNA damage sensor MRE11 recognizes cytosolic double-stranded DNA and induces type I interferon by regulating STING trafficking. Proc. Natl. Acad. Sci. USA 110, 2969-2974.
56. Koopal, S., Furuhjelm, J.H., Järviluoma, A., Jäämaa, S., Pyakurel, P., Pussinen, C., Wirzenius, M., Biberfeld, P., Alitalo, K., Laiho, M., and Ojala, P.M. (2007). Viral oncogene-induced DNA damage response is activated in Kaposi sarcoma tumorigenesis. PLoS Pathog. 3, 1348-1360. (Pubitemid 47510286)
57. Landry, S., Narvaiza, I., Linfesty, D.C., and Weitzman, M.D. (2011). APOBEC3A can activate the DNA damage response and cause cell-cycle arrest. EMBO Rep. 12, 444-450.
58. Leidal, A.M., Cyr, D.P., Hill, R.J., Lee, P.W., and McCormick, C. (2012a). Subversion of autophagy by Kaposi's sarcoma-associated herpesvirus impairs oncogene-induced senescence. Cell Host Microbe 11, 167-180.
59. Leidal, A.M., Pringle, E.S., and McCormick, C. (2012b). Evasion of oncogene-induced senescence by gammaherpesviruses. Curr Opin Virol 2, 748-754.
60. Lengauer, C., Kinzler, K.W., and Vogelstein, B. (1998). Genetic instabilities in human cancers. Nature 396, 643-649. (Pubitemid 29003936)
61. Li, R., Zhu, J., Xie, Z., Liao, G., Liu, J., Chen, M.R., Hu, S., Woodard, C., Lin, J., Taverna, S.D., et al. (2011). Conserved herpesvirus kinases target the DNA damage response pathway and TIP60 histone acetyltransferase to promote virus replication. Cell Host Microbe 10, 390-400.
62. Li, J., Wang, X., Diaz, J., Tsang, S.H., Buck, C.B., and You, J. (2013a). Merkel cell polyomavirus large T antigen disrupts host genomic integrity and inhibits cellular proliferation. J. Virol. 87, 9173-9188.
63. Li, T., Chen, J., and Cristea, I.M. (2013b). Human cytomegalovirus tegument protein pUL83 inhibits IFI16-mediated DNA sensing for immune evasion. Cell Host Microbe 14, 591-599.
64. Lilley, C.E., Carson, C.T., Muotri, A.R., Gage, F.H., and Weitzman, M.D. (2005). DNA repair proteins affect the lifecycle of herpes simplex virus 1. Proc. Natl. Acad. Sci. USA 102, 5844-5849. (Pubitemid 40559647)
65. Lilley, C.E., Chaurushiya, M.S., Boutell, C., Landry, S., Suh, J., Panier, S., Everett, R.D., Stewart, G.S., Durocher, D., and Weitzman, M.D. (2010). A viral E3 ligase targets RNF8 and RNF168 to control histone ubiquitination and DNA damage responses. EMBO J. 29, 943-955.
66. Lilley, C.E., Chaurushiya, M.S., Boutell, C., Everett, R.D., and Weitzman, M.D. (2011). The intrinsic antiviral defense to incoming HSV-1 genomes includes specific DNA repair proteins and is counteracted by the viral protein ICP0. PLoS Pathog. 7, e1002084.
67. Liu, Y., Shevchenko, A., Shevchenko, A., and Berk, A.J. (2005). Adenovirus exploits the cellular aggresome response to accelerate inactivation of the MRN complex. J. Virol. 79, 14004-14016. (Pubitemid 41552699)
68. Lizundia, R., Chaussepied, M., Huerre, M., Werling, D., Di Santo, J.P., and Langsley, G. (2006). c-Jun NH2-terminal kinase/c-Jun signaling promotes survival and metastasis of B lymphocytes transformed by Theileria. Cancer Res. 66, 6105-6110.
69. Machado, A.M., Figueiredo, C., Seruca, R., and Rasmussen, L.J. (2010). Helicobacter pylori infection generates genetic instability in gastric cells. Biochim. Biophys. Acta 1806, 58-65.
70. Maréchal, A., and Zou, L. (2013). DNA damage sensing by the ATM and ATR kinases. Cold Spring Harb. Perspect. Biol. 5, 5.
71. Marsolier, J., Pineau, S., Medjkane, S., Perichon, M., Yin, Q., Flemington, E., Weitzman, M.D., and Weitzman, J.B. (2013). OncomiR addiction is generated by a miR-155 feedback loop in Theileria-transformed leukocytes. PLoS Pathog. 9, e1003222.
72. Matsumoto, Y., Marusawa, H., Kinoshita, K., Endo, Y., Kou, T., Morisawa, T., Azuma, T., Okazaki, I.M., Honjo, T., and Chiba, T. (2007). Helicobacter pylori infection triggers aberrant expression of activation-induced cytidine deaminase in gastric epithelium. Nat. Med. 13, 470-476. (Pubitemid 46559833)
73. McFadden, K., and Luftig, M.A. (2013). Interplay between DNA tumor viruses and the host DNA damage response. Curr. Top. Microbiol. Immunol. 371, 229-257.
74. Medjkane, S., Perichon, M., Marsolier, J., Dairou, J., and Weitzman, J.B. (2013). Theileria induces oxidative stress and HIF1α activation that are essential for host leukocyte transformation. Oncogene. Published online May 13, 2013. http://dx.doi.org/10.1038/onc.2013.134.
75. Mesri, E.A., Feitelson, M., and Munger, K. (2014). Human Viral Oncogenesis: A Cancer Hallmarks Analysis. Cell Host Microbe 15, this issue, 266-282.
76. Moody, C.A., and Laimins, L.A. (2009). Human papillomaviruses activate the ATM DNA damage pathway for viral genome amplification upon differentiation. PLoS Pathog. 5, e1000605.
77. Moody, C.A., and Laimins, L.A. (2010). Human papillomavirus oncoproteins: pathways to transformation. Nat. Rev. Cancer 10, 550-560.
78. Moore, P.S., and Chang, Y. (2010). Why do viruses cause cancer? Highlights of the first century of human tumour virology. Nat. Rev. Cancer 10, 878-889.
79. Nesić, D., Hsu, Y., and Stebbins, C.E. (2004). Assembly and function of a bacterial genotoxin. Nature 429, 429-433. (Pubitemid 38715135)
80. Nikitin, P.A., and Luftig, M.A. (2012). The DNA damage response in viral-induced cellular transformation. Br. J. Cancer 106, 429-435.
81. Nikitin, P.A., Yan, C.M., Forte, E., Bocedi, A., Tourigny, J.P., White, R.E., Allday, M.J., Patel, A., Dave, S.S., Kim, W., et al. (2010). An ATM/Chk2-mediated DNA damage-responsive signaling pathway suppresses Epstein-Barr virus transformation of primary human B cells. Cell Host Microbe 8, 510-522.
82. Niller, H.H., Wolf, H., and Minarovits, J. (2011). Viral hit and run-oncogenesis: genetic and epigenetic scenarios. Cancer Lett. 305, 200-217.
83. Norman, J.M., Mashiba, M., McNamara, L.A., Onafuwa-Nuga, A., Chiari-Fort, E., Shen, W., and Collins, K.L. (2011). The antiviral factor APOBEC3G enhances the recognition of HIV-infected primary T cells by natural killer cells. Nat. Immunol. 12, 975-983.
84. Nougayrède, J.P., Homburg, S., Taieb, F., Boury, M., Brzuszkiewicz, E., Gottschalk, G., Buchrieser, C., Hacker, J., Dobrindt, U., and Oswald, E. (2006). Escherichia coli induces DNA double-strand breaks in eukaryotic cells. Science 313, 848-851.
85. Okazaki, I.M., Hiai, H., Kakazu, N., Yamada, S., Muramatsu, M., Kinoshita, K., and Honjo, T. (2003). Constitutive expression of AID leads to tumorigenesis. J. Exp. Med. 197, 1173-1181. (Pubitemid 36570072)
86. Okazaki, I.M., Kotani, A., and Honjo, T. (2007). Role of AID in tumorigenesis. Adv. Immunol. 94, 245-273. (Pubitemid 46856613)
87. Ou, H.D., Kwiatkowski, W., Deerinck, T.J., Noske, A., Blain, K.Y., Land, H.S., Soria, C., Powers, C.J., May, A.P., Shu, X., et al. (2012). A structural basis for the assembly and functions of a viral polymer that inactivates multiple tumor suppressors. Cell 151, 304-319.
88. Ouchi, M., and Ouchi, T. (2008). Role of IFI16 in DNA damage and checkpoint. Front. Biosci. 13, 236-239. (Pubitemid 351594774)
89. Pavri, R., and Nussenzweig, M.C. (2011). AID targeting in antibody diversity. Adv. Immunol. 110, 1-26.
90. Petersen-Mahrt, S.K., Coker, H.A., and Pauklin, S. (2009). DNA deaminases: AIDing hormones in immunity and cancer. J. Mol. Med. 87, 893-897.
91. Polo, S.E., and Jackson, S.P. (2011). Dynamics of DNA damage response proteins at DNA breaks: a focus on protein modifications. Genes Dev. 25, 409-433.
92. Price, B.D., and D'Andrea, A.D. (2013). Chromatin remodeling at DNA double-strand breaks. Cell 152, 1344-1354.
93. Ramadan, E., Ward, M., Guo, X., Durkin, S.S., Sawyer, A., Vilela, M., Osgood, C., Pothen, A., and Semmes, O.J. (2008). Physical and in silico approaches identify DNA-PK in a Tax DNA-damage response interactome. Retrovirology 5, 92.
94. Refsland, E.W., and Harris, R.S. (2013). The APOBEC3 family of retroelement restriction factors. Curr. Top. Microbiol. Immunol. 371, 1-27.
95. Reinhardt, H.C., and Yaffe, M.B. (2013). Phospho-Ser/Thr-binding domains: navigating the cell cycle and DNA damage response. Nat. Rev. Mol. Cell Biol. 14, 563-580.
96. Robbiani, D.F., and Nussenzweig, M.C. (2013). Chromosome translocation, B cell lymphoma, and activation-induced cytidine deaminase. Annu. Rev. Pathol. 8, 79-103.
97. Rolando, M., Sanulli, S., Rusniok, C., Gomez-Valero, L., Bertholet, C., Sahr, T., Margueron, R., and Buchrieser, C. (2013). Legionella pneumophila effector RomA uniquely modifies host chromatin to repress gene expression and promote intracellular bacterial replication. Cell Host Microbe 13, 395-405.
98. Sakakibara, N., Mitra, R., and McBride, A.A. (2011). The papillomavirus E1 helicase activates a cellular DNA damage response in viral replication foci. J. Virol. 85, 8981-8995.
99. Samaras, V., Rafailidis, P.I., Mourtzoukou, E.G., Peppas, G., and Falagas, M.E. (2010). Chronic bacterial and parasitic infections and cancer: a review. J. Infect. Dev. Ctries. 4, 267-281.
100. Schmid, M., Speiseder, T., Dobner, T., and Gonzalez, R.A. (2014). DNA virus replication compartments. J. Virol. 88, 1404-1420.
101. Sears, C.L., and Garrett, W.S. (2014). Microbes, Microbiota, and Colon Cancer. Cell Host Microbe 15, this issue, 317-328.
102. Shi, Y., Dodson, G.E., Shaikh, S., Rundell, K., and Tibbetts, R.S. (2005). Ataxia-telangiectasia-mutated (ATM) is a T-antigen kinase that controls SV40 viral replication in vivo. J. Biol. Chem. 280, 40195-40200. (Pubitemid 41779156)
103. Shiels, B., Langsley, G., Weir, W., Pain, A., McKellar, S., and Dobbelaere, D. (2006). Alteration of host cell phenotype by Theileria annulata and Theileria parva: mining for manipulators in the parasite genomes. Int. J. Parasitol. 36, 9-21. (Pubitemid 43049693)
104. Shimizu, T., Marusawa, H., Endo, Y., and Chiba, T. (2012). Inflammation-mediated genomic instability: roles of activation-induced cytidine deaminase in carcinogenesis. Cancer Sci. 103, 1201-1206.
105. Stracker, T.H., Carson, C.T., and Weitzman, M.D. (2002). Adenovirus oncoproteins inactivate the Mre11-Rad50-NBS1 DNA repair complex. Nature 418, 348-352. (Pubitemid 34790688)
106. Suspène, R., Aynaud, M.M., Guétard, D., Henry, M., Eckhoff, G., Marchio, A., Pineau, P., Dejean, A., Vartanian, J.P., and Wain-Hobson, S. (2011). Somatic hypermutation of human mitochondrial and nuclear DNA by APOBEC3 cytidine deaminases, a pathway for DNA catabolism. Proc. Natl. Acad. Sci. USA 108, 4858-4863.
107. Sutcliffe, S. (2010). Sexually transmitted infections and risk of prostate cancer: review of historical and emerging hypotheses. Future Oncol. 6, 1289-1311.
108. Tang, K.W., Alaei-Mahabadi, B., Samuelsson, T., Lindh, M., and Larsson, E. (2013). The landscape of viral expression and host gene fusion and adaptation in human cancer. Nat Commun 4, 2513.
109. Tarakanova, V.L., Leung-Pineda, V., Hwang, S., Yang, C.W., Matatall, K., Basson, M., Sun, R., Piwnica-Worms, H., Sleckman, B.P., and Virgin, H.W., 4th. (2007). Gamma-herpesvirus kinase actively initiates a DNA damage response by inducing phosphorylation of H2AX to foster viral replication. Cell Host Microbe 1, 275-286. (Pubitemid 46865610)
110. Tian, Y., Yang, W., Song, J., Wu, Y., and Ni, B. (2013). Hepatitis B virus X protein-induced aberrant epigenetic modifications contributing to human hepatocellular carcinoma pathogenesis. Mol. Cell. Biol. 33, 2810-2816.
111. Toller, I.M., Neelsen, K.J., Steger, M., Hartung, M.L., Hottiger, M.O., Stucki, M., Kalali, B., Gerhard, M., Sartori, A.A., Lopes, M., and Müller, A. (2011). Carcinogenic bacterial pathogen Helicobacter pylori triggers DNA doublestrand breaks and a DNA damage response in its host cells. Proc. Natl. Acad. Sci. USA 108, 14944-14949.
112. Touati, E. (2010). When bacteria become mutagenic and carcinogenic: lessons from H. pylori. Mutat. Res. 703, 66-70.
113. Turnell, A.S., and Grand, R.J. (2012). DNA viruses and the cellular DNA-damage response. J. Gen. Virol. 93, 2076-2097.
114. Vogelmann, R., and Amieva, M.R. (2007). The role of bacterial pathogens in cancer. Curr. Opin. Microbiol. 10, 76-81. (Pubitemid 46223641)
115. Wallace, N.A., and Galloway, D.A. (2014). Manipulation of cellular DNA damage repair machinery facilitates propagation of human papillomaviruses. Semin. Cancer Biol. Published online January 8, 2014. http://dx.doi.org/10.1016/ j.semcancer.2013.12.003.
116. Weitzman, M.D., Lilley, C.E., and Chaurushiya, M.S. (2010). Genomes in conflict: maintaining genome integrity during virus infection. Annu. Rev. Microbiol. 64, 61-81.
117. Wilkinson, D.E., and 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. (Pubitemid 38501099)
118. Yang, X., He, Z., Xin, B., and Cao, L. (2000). LMP1 of Epstein-Barr virus suppresses cellular senescence associated with the inhibition of p16INK4a expression. Oncogene 19, 2002-2013. (Pubitemid 30229413)
119. Zackular, J.P., Baxter, N.T., Iverson, K.D., Sadler, W.D., Petrosino, J.F., Chen, G.Y., and Schloss, P.D. (2013). The gut microbiome modulates colon tumorigenesis. MBio 4, e00692-e13.
120. Zhang, X., Li, Q., Hu, P., Cheng, H., and Huang, G. (2002). Two case reports of pituitary adenoma associated with Toxoplasma gondii infection. J. Clin. Pathol. 55, 965-966. (Pubitemid 35454503)
121. Zhao, X., Madden-Fuentes, R.J., Lou, B.X., Pipas, J.M., Gerhardt, J., Rigell, C.J., and Fanning, E. (2008). Ataxia telangiectasia-mutated damagesignaling kinase- and proteasome-dependent destruction of Mre11-Rad50-Nbs1 subunits in Simian virus 40-infected primate cells. J. Virol. 82, 5316-5328. (Pubitemid 351705239)
122. Zur Hausen, H. (2009). The search for infectious causes of human cancers: where and why. Virology 392, 1-10.