Human APOBEC3A Isoforms Translocate to the Nucleus and Induce DNA Double Strand Breaks Leading to Cell Stress and Death

PLoS ONE

Volumn 8, Issue 8, 2013, Pages

  Mussil, Bianka ^a   Suspène, Rodolphe ^a   Aynaud, Marie Ming ^a   Gauvrit, Anne ^a   Vartanian, Jean Pierre ^a   Wain Hobson, Simon ^a  

^a INSTITUT PASTEUR   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; CD4 ANTIGEN; CHECKPOINT KINASE 2; CYTIDINE DEAMINASE; CYTOSINE; DOUBLE STRANDED DNA; GENOMIC DNA; HISTONE H2AX; INTERLEUKIN 2; ISOPROTEIN; PROTEIN APOBEC3A; THYMINE; UNCLASSIFIED DRUG; AICDA (ACTIVATION-INDUCED CYTIDINE DEAMINASE); APOBEC3A PROTEIN, HUMAN; H2AFX PROTEIN, HUMAN; HISTONE; PROTEIN; URACIL DNA GLYCOSIDASE;

ANIMAL CELL; APOPTOSIS; ARTICLE; CD4+ T LYMPHOCYTE; CELL CYCLE ARREST; CELL CYCLE G1 PHASE; CELL DEATH; CELL LINE; CELL NUCLEUS; CELL STRESS; CHRONIC INFLAMMATION; DOUBLE STRANDED DNA BREAK; HUMAN; HUMAN CELL; NEOPLASM; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; T LYMPHOCYTE ACTIVATION; CELL CYCLE CHECKPOINT; GENETICS; HELA CELL LINE; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; MOLECULAR GENETICS; PHYSIOLOGICAL STRESS; RNA EDITING; SIGNAL TRANSDUCTION;

BASE SEQUENCE; CD4-POSITIVE T-LYMPHOCYTES; CELL CYCLE CHECKPOINTS; CELL DEATH; CELL NUCLEUS; CYTIDINE DEAMINASE; DNA BREAKS, DOUBLE-STRANDED; HELA CELLS; HISTONES; HUMANS; LYMPHOCYTE ACTIVATION; MOLECULAR SEQUENCE DATA; PROTEIN ISOFORMS; PROTEIN TRANSPORT; PROTEINS; RNA EDITING; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL; URACIL-DNA GLYCOSIDASE;

EID: 84882593001     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0073641     Document Type: Article

References (121)

1. Jarmuz A, Chester A, Bayliss J, Gisbourne J, Dunham I, et al. (2002) An anthropoid-specific locus of orphan C to U RNA-editing enzymes on chromosome 22. Genomics 79: 285-296. doi:10.1006/geno.2002.6718. PubMed: 11863358.
2. Petersen-Mahrt SK, Harris RS, Neuberger MS, (2002) AID mutates E. coli suggesting a DNA deamination mechanism for antibody diversification. Nature 418: 99-103. doi:10.1038/nj6896-99a. PubMed: 12097915.
3. Delker RK, Fugmann SD, Papavasiliou FN, (2009) A coming-of-age story: activation-induced cytidine deaminase turns 10. Nat Immunol 10: 1147-1153. doi:10.1038/ni.1799. PubMed: 19841648.
4. Di Noia JM, Neuberger MS, (2007) Molecular mechanisms of antibody somatic hypermutation. Annu Rev Biochem 76: 1-22. doi:10.1146/annurev.biochem.76.061705.090740. PubMed: 17328676.
5. Liu M, Duke JL, Richter DJ, Vinuesa CG, Goodnow CC, et al. (2008) Two levels of protection for the B cell genome during somatic hypermutation. Nature 451: 841-845. doi:10.1038/nature06547. PubMed: 18273020.
6. Liu M, Schatz DG, (2009) Balancing AID and DNA repair during somatic hypermutation. Trends Immunol 30: 173-181. doi:10.1016/j.it.2009.01.007. PubMed: 19303358.
7. Adams JM, Harris AW, Strasser A, Ogilvy S, Cory S, (1999) Transgenic models of lymphoid neoplasia and development of a pan-hematopoietic vector. Oncogene 18: 5268-5277. doi:10.1038/sj.onc.1202997. PubMed: 10498879.
8. Kovalchuk AL, Kim JS, Park SS, Coleman AE, Ward JM, et al. (2002) IL-6 transgenic mouse model for extraosseous plasmacytoma. Proc Natl Acad Sci U S A 99: 1509-1514. doi:10.1073/pnas.022643999. PubMed: 11805288.
9. Okazaki IM, Hiai H, Kakazu N, Yamada S, Muramatsu M, et al. (2003) Constitutive expression of AID leads to tumorigenesis. J Exp Med 197: 1173-1181. doi:10.1084/jem.20030275. PubMed: 12732658.
10. Okazaki IM, Kotani A, Honjo T, (2007) Role of AID in tumorigenesis. Adv Immunol 94: 245-273. doi:10.1016/S0065-2776(06)94008-5. PubMed: 17560277.
11. Ramiro AR, Jankovic M, Callen E, Difilippantonio S, Chen HT, et al. (2006) Role of genomic instability and p53 in AID-induced c-myc-Igh translocations. Nature 440: 105-109. doi:10.1038/nature04495. PubMed: 16400328.
12. Ramiro AR, Jankovic M, Eisenreich T, Difilippantonio S, Chen-Kiang S, et al. (2004) AID is required for c-myc/IgH chromosome translocations in vivo. Cell 118: 431-438. doi:10.1016/j.cell.2004.08.006. PubMed: 15315756.
13. Robbiani DF, Bothmer A, Callen E, Reina-San-Martin B, Dorsett Y,et al (2008) AID is required for the chromosomal breaks in c-myc that lead to c-myc/IgH translocations. Cell 135: 1028-1038. doi:10.1016/j.cell.2008.09.062. PubMed: 19070574.
14. Conticello SG, Thomas CJ, Petersen-Mahrt SK, Neuberger MS, (2005) Evolution of the AID/APOBEC family of polynucleotide (deoxy)cytidine deaminases. Mol Biol Evol 22: 367-377. PubMed: 15496550.
15. Bishop KN, Holmes RK, Sheehy AM, Davidson NO, Cho SJ, et al. (2004) Cytidine deamination of retroviral DNA by diverse APOBEC proteins. Curr Biol 14: 1392-1396. doi:10.1016/j.cub.2004.06.057. PubMed: 15296758.
16. Chiu YL, Greene WC, (2008) The APOBEC3 cytidine deaminases: an innate defensive network opposing exogenous retroviruses and endogenous retroelements. Annu Rev Immunol 26: 317-353. doi:10.1146/annurev.immunol.26.021607.090350. PubMed: 18304004.
17. Neil S, Bieniasz P, (2009) Human immunodeficiency virus, restriction factors, and interferon. J Interferon Cytokine Res 29: 569-580. doi:10.1089/jir.2009.0077. PubMed: 19694548.
18. Okeoma CM, Low A, Bailis W, Fan HY, Peterlin BM, et al. (2009) Induction of APOBEC3 in vivo causes increased restriction of retrovirus infection. J Virol 83: 3486-3495. doi:10.1128/JVI.02347-08. PubMed: 19153238.
19. Ooms M, Krikoni A, Kress AK, Simon V, Münk C, (2012) APOBEC3A, APOBEC3B, and APOBEC3H haplotype 2 restrict human T-lymphotropic virus type 1. J Virol 86: 6097-6108. doi:10.1128/JVI.06570-11. PubMed: 22457529.
20. Pillai SK, Abdel-Mohsen M, Guatelli J, Skasko M, Monto A, et al. (2012) Role of retroviral restriction factors in the interferon-alpha-mediated suppression of HIV-1 in vivo. Proc Natl Acad Sci U S A 109: 3035-3040. doi:10.1073/pnas.1111573109. PubMed: 22315404.
21. Sanchez-Martinez S, Aloia AL, Harvin D, Mirro J, Gorelick RJ, et al. (2012) Studies on the restriction of murine leukemia viruses by mouse APOBEC3. PLOS ONE 7: e38190. doi:10.1371/journal.pone.0038190. PubMed: 22666481.
22. Harris RS, Liddament MT, (2004) Retroviral restriction by APOBEC proteins. Nat Rev Immunol 4: 868-877. doi:10.1038/nri1489. PubMed: 15516966.
23. Lecossier D, Bouchonnet F, Clavel F, Hance AJ, (2003) Hypermutation of HIV-1 DNA in the absence of the Vif protein. Science 300: 1112. doi:10.1126/science.1083338. PubMed: 12750511.
24. Liddament MT, Brown WL, Schumacher AJ, Harris RS, (2004) APOBEC3F properties and hypermutation preferences indicate activity against HIV-1 in vivo. Curr Biol 14: 1385-1391. doi:10.1016/j.cub.2004.06.050. PubMed: 15296757.
25. Mangeat B, Turelli P, Caron G, Friedli M, Perrin L, et al. (2003) Broad antiretroviral defence by human APOBEC3G through lethal editing of nascent reverse transcripts. Nature 424: 99-103. doi:10.1038/nature01709. PubMed: 12808466.
26. Sheehy AM, Gaddis NC, Choi JD, Malim MH, (2002) Isolation of a human gene that inhibits HIV-1 infection and is suppressed by the viral Vif protein. Nature 418: 646-650. doi:10.1038/nature00939. PubMed: 12167863.
27. Zhang H, Yang B, Pomerantz RJ, Zhang C, Arunachalam SC, et al. (2003) The cytidine deaminase CEM15 induces hypermutation in newly synthesized HIV-1 DNA. Nature 424: 94-98. doi:10.1038/nature01707. PubMed: 12808465.
28. Suspène R, Guétard D, Henry M, Sommer P, Wain-Hobson S, et al. (2005) Extensive editing of both hepatitis B virus DNA strands by APOBEC3 cytidine deaminases in vitro and in vivo. Proc Natl Acad Sci U S A 102: 8321-8326. doi:10.1073/pnas.0408223102. PubMed: 15919829.
29. Vartanian JP, Henry M, Marchio A, Suspène R, Aynaud MM, et al. (2010) Massive APOBEC3 editing of hepatitis B viral DNA in cirrhosis. PLOS Pathog 6: e1000928. PubMed: 20523896.
30. Vartanian JP, Guétard D, Henry M, Wain-Hobson S, (2008) Evidence for editing of human papillomavirus DNA by APOBEC3 in benign and precancerous lesions. Science 320: 230-233. doi:10.1126/science.1153201. PubMed: 18403710.
31. Suspène R, Aynaud MM, Koch S, Pasdeloup D, Labetoulle M, et al. (2011) Genetic editing of herpes simplex virus 1 and Epstein-Barr herpesvirus genomes by human APOBEC3 cytidine deaminases in culture and in vivo. J Virol 85: 7594-7602. doi:10.1128/JVI.00290-11. PubMed: 21632763.
32. Argyris EG, Acheampong E, Wang F, Huang J, Chen K, et al. (2007) The interferon-induced expression of APOBEC3G in human blood-brain barrier exerts a potent intrinsic immunity to block HIV-1 entry to central nervous system. Virology 367: 440-451. doi:10.1016/j.virol.2007.06.010. PubMed: 17631933.
33. Bonvin M, Achermann F, Greeve I, Stroka D, Keogh A, et al. (2006) Interferon-inducible expression of APOBEC3 editing enzymes in human hepatocytes and inhibition of hepatitis B virus replication. Hepatology 43: 1364-1374. doi:10.1002/hep.21187. PubMed: 16729314.
34. Koning FA, Newman EN, Kim EY, Kunstman KJ, Wolinsky SM, et al. (2009) Defining APOBEC3 expression patterns in human tissues and hematopoietic cell subsets. J Virol 83: 9474-9485. doi:10.1128/JVI.01089-09. PubMed: 19587057.
35. Refsland EW, Stenglein MD, Shindo K, Albin JS, Brown WL, et al. (2010) Quantitative profiling of the full APOBEC3 mRNA repertoire in lymphocytes and tissues: implications for HIV-1 restriction. Nucleic Acids Res 38: 4274-4284. doi:10.1093/nar/gkq174. PubMed: 20308164.
36. Stenglein MD, Burns MB, Li M, Lengyel J, Harris RS, (2010) APOBEC3 proteins mediate the clearance of foreign DNA from human cells. Nat Struct Mol Biol 17: 222-229. doi:10.1038/nsmb.1744. PubMed: 20062055.
37. Tanaka Y, Marusawa H, Seno H, Matsumoto Y, Ueda Y, et al. (2006) Anti-viral protein APOBEC3G is induced by interferon-alpha stimulation in human hepatocytes. Biochem Biophys Res Commun 341: 314-319. doi:10.1016/j.bbrc.2005.12.192. PubMed: 16426578.
38. Turelli P, Liagre-Quazzola A, Mangeat B, Verp S, Jost S, et al. (2008) APOBEC3-independent interferon-induced viral clearance in hepatitis B virus transgenic mice. J Virol 82: 6585-6590. doi:10.1128/JVI.00216-08. PubMed: 18434399.
39. Wang FX, Huang J, Zhang H, Ma X, Zhang H, (2008) APOBEC3G upregulation by alpha interferon restricts human immunodeficiency virus type 1 infection in human peripheral plasmacytoid dendritic cells. J Gen Virol 89: 722-730. doi:10.1099/vir.0.83530-0. PubMed: 18272764.
40. Suspène R, Aynaud MM, Guétard D, Henry M, Eckhoff G, et al. (2011) Somatic hypermutation of human mitochondrial and nuclear DNA by APOBEC3 cytidine deaminases, a pathway for DNA catabolism. Proc Natl Acad Sci U S A 108: 4858-4863. doi:10.1073/pnas.1009687108. PubMed: 21368204.
41. Burns MB, Lackey L, Carpenter MA, Rathore A, Land AM, et al. (2013) APOBEC3B is an enzymatic source of mutation in breast cancer. Nature 494: 366-370. doi:10.1038/nature11881. PubMed: 23389445.
42. Shinohara M, Io K, Shindo K, Matsui M, Sakamoto T, et al. (2012) APOBEC3B can impair genomic stability by inducing base substitutions in genomic DNA in human cells. Sci Rep 2: 806.
43. Taylor BJ, Nik-Zainal S, Wu YL, Stebbings LA, Raine K, et al. (2013) DNA deaminases induce break-associated mutation showers with implication of APOBEC3B and 3A in breast cancer kataegis. Elife 2: e00534. doi:10.7554/eLife.00534. PubMed: 23599896.
44. Komatsu A, Nagasaki K, Fujimori M, Amano J, Miki Y, (2008) Identification of novel deletion polymorphisms in breast cancer. Int J Oncol 33: 261-270. PubMed: 18636146.
45. Zhang T, Cai J, Chang J, Yu D, Wu C, et al. (2013) Evidence of associations of APOBEC3B gene deletion with susceptibility to persistent HBV infection and hepatocellular carcinoma. Hum Mol Genet 22: 1262-1269. doi:10.1093/hmg/dds513. PubMed: 23213177.
46. Landry S, Narvaiza I, Linfesty DC, Weitzman MD, (2011) APOBEC3A can activate the DNA damage response and cause cell-cycle arrest. EMBO Rep 12: 444-450. doi:10.1038/embor.2011.46. PubMed: 21460793.
47. Love RP, Xu H, Chelico L, (2012) Biochemical analysis of hypermutation by the deoxycytidine deaminase APOBEC3A. J Biol Chem 287: 30812-30822. doi:10.1074/jbc.M112.393181. PubMed: 22822074.
48. Yang N, Galick H, Wallace SS, (2004) Attempted base excision repair of ionizing radiation damage in human lymphoblastoid cells produces lethal and mutagenic double strand breaks. DNA Repair 3: 1323-1334. doi:10.1016/j.dnarep.2004.04.014. PubMed: 15336627.
49. Cann KL, Hicks GG, (2007) Regulation of the cellular DNA double-strand break response. Biochem Cell Biol 85: 663-674. doi:10.1139/O07-135. PubMed: 18059525.
50. Fernandez-Capetillo O, Chen HT, Celeste A, Ward I, Romanienko PJ, et al. (2002) DNA damage-induced G2-M checkpoint activation by histone H2AX and 53BP1. Nat Cell Biol 4: 993-997. doi:10.1038/ncb884. PubMed: 12447390.
51. Karlsson KH, Stenerlöw B, (2004) Focus formation of DNA repair proteins in normal and repair-deficient cells irradiated with high-LET ions. Radiat Res 161: 517-527. doi:10.1667/RR3171. PubMed: 15161372.
52. Kurz EU, Lees-Miller SP, (2004) DNA damage-induced activation of ATM and ATM-dependent signaling pathways. DNA Repair 3: 889-900. doi:10.1016/j.dnarep.2004.03.029. PubMed: 15279774.
53. Leatherbarrow EL, Harper JV, Cucinotta FA, O'Neill P, (2006) Induction and quantification of gamma-H2AX foci following low and high LET-irradiation. Int J Radiat Biol 82: 111-118. doi:10.1080/09553000600599783. PubMed: 16546909.
54. Lees-Miller SP, Sakaguchi K, Ullrich SJ, Appella E, Anderson CW, (1992) Human DNA-activated protein kinase phosphorylates serines 15 and 37 in the amino-terminal transactivation domain of human p53. Mol Cell Biol 12: 5041-5049. PubMed: 1406679.
55. Bonner WM, Redon CE, Dickey JS, Nakamura AJ, Sedelnikova OA, et al. (2008) GammaH2AX and cancer. Nat Rev Cancer 8: 957-967. doi:10.1038/nrc2523. PubMed: 19005492.
56. Khanna KK, Jackson SP, (2001) DNA double-strand breaks: signaling, repair and the cancer connection. Nat Genet 27: 247-254. doi:10.1038/85798. PubMed: 11242102.
57. Kaina B, (2003) DNA damage-triggered apoptosis: critical role of DNA repair, double-strand breaks, cell proliferation and signaling. Biochem Pharmacol 66: 1547-1554. doi:10.1016/S0006-2952(03)00510-0. PubMed: 14555233.
58. Suspène R, Henry M, Guillot S, Wain-Hobson S, Vartanian JP, (2005) Recovery of APOBEC3-edited human immunodeficiency virus G->A hypermutants by differential DNA denaturation PCR. J Gen Virol 86: 125-129. doi:10.1099/vir.0.80426-0. PubMed: 15604439.
59. Zuba-Surma EK, Kucia M, Abdel-Latif A, Lillard JW Jr., Ratajczak MZ, (2007) The ImageStream System: a key step to a new era in imaging. Folia Histochem Cytobiol 45: 279-290. PubMed: 18165167.
60. Bossy-Wetzel E, Green DR, (2000) Detection of apoptosis by annexin V labeling. Methods Enzymol 322: 15-18. doi:10.1016/S0076-6879(00)22004-1. PubMed: 10914001.
61. Thielen BK, McNevin JP, McElrath MJ, Hunt BV, Klein KC, et al. (2010) Innate immune signaling induces high levels of TC-specific deaminase activity in primary monocyte-derived cells through expression of APOBEC3A isoforms. J Biol Chem 285: 27753-27766. doi:10.1074/jbc.M110.102822. PubMed: 20615867.
62. Rogakou EP, Pilch DR, Orr AH, Ivanova VS, Bonner WM, (1998) DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J Biol Chem 273: 5858-5868. doi:10.1074/jbc.273.10.5858. PubMed: 9488723.
63. Tanaka T, Halicka HD, Traganos F, Seiter K, Darzynkiewicz Z, (2007) Induction of ATM activation, histone H2AX phosphorylation and apoptosis by etoposide: relation to cell cycle phase. Cell Cycle 6: 371-376. doi:10.4161/cc.6.3.3835. PubMed: 17297310.
64. Henry M, Guétard D, Suspène R, Rusniok C, Wain-Hobson S, et al. (2009) Genetic editing of HBV DNA by monodomain human APOBEC3 cytidine deaminases and the recombinant nature of APOBEC3G. PLOS ONE 4: e4277. doi:10.1371/journal.pone.0004277. PubMed: 19169351.
65. Petit V, Vartanian JP, Wain-Hobson S, (2009) Powerful mutators lurking in the genome. Philos Trans R Soc Lond B Biol Sci 364: 705-715. doi:10.1098/rstb.2008.0272. PubMed: 19042181.
66. Wang Z, Mosbaugh DW, (1988) Uracil-DNA glycosylase inhibitor of bacteriophage PBS2: cloning and effects of expression of the inhibitor gene in Escherichia coli. J Bacteriol 170: 1082-1091. PubMed: 2963806.
67. Berger G, Durand S, Fargier G, Nguyen XN, Cordeil S, et al. (2011) APOBEC3A is a specific inhibitor of the early phases of HIV-1 infection in myeloid cells. PLOS Pathog 7: e1002221. PubMed: 21966267.
68. Peng G, Greenwell-Wild T, Nares S, Jin W, Lei KJ, et al. (2007) Myeloid differentiation and susceptibility to HIV-1 are linked to APOBEC3 expression. Blood 110: 393-400. doi:10.1182/blood-2006-10-051763. PubMed: 17371941.
69. Ahn JY, Schwarz JK, Piwnica-Worms H, Canman CE, (2000) Threonine 68 phosphorylation by ataxia telangiectasia mutated is required for efficient activation of Chk2 in response to ionizing radiation. Cancer Res 60: 5934-5936. PubMed: 11085506.
70. Kastan MB, Lim DS, (2000) The many substrates and functions of ATM. Nat Rev Mol Cell Biol 1: 179-186. doi:10.1038/35043058. PubMed: 11252893.
71. Matsuoka S, Rotman G, Ogawa A, Shiloh Y, Tamai K, et al. (2000) Ataxia telangiectasia-mutated phosphorylates Chk2 in vivo and in vitro. Proc Natl Acad Sci U S A 97: 10389-10394. doi:10.1073/pnas.190030497. PubMed: 10973490.
72. Melchionna R, Chen XB, Blasina A, McGowan CH, (2000) Threonine 68 is required for radiation-induced phosphorylation and activation of Cds1. Nat Cell Biol 2: 762-765. doi:10.1038/35036406. PubMed: 11025670.
73. Chehab NH, Malikzay A, Appel M, Halazonetis TD, (2000) Chk2/hCds1 functions as a DNA damage checkpoint in G(1) by stabilizing p53. Genes Dev 14: 278-288. PubMed: 10673500.
74. Satoh MS, Lindahl T, (1992) Role of poly(ADP-ribose) formation in DNA repair. Nature 356: 356-358. doi:10.1038/356356a0. PubMed: 1549180.
75. Cohen GM, (1997) Caspases: the executioners of apoptosis. Biochem J 326(1):: 1-16. PubMed: 9337844.
76. Lazebnik YA, Kaufmann SH, Desnoyers S, Poirier GG, Earnshaw WC, (1994) Cleavage of poly(ADP-ribose) polymerase by a proteinase with properties like ICE. Nature 371: 346-347. doi:10.1038/371346a0. PubMed: 8090205.
77. Nicholson DW, Ali A, Thornberry NA, Vaillancourt JP, Ding CK, et al. (1995) Identification and inhibition of the ICE/CED-3 protease necessary for mammalian apoptosis. Nature 376: 37-43. doi:10.1038/376037a0. PubMed: 7596430.
78. Tewari M, Quan LT, O'Rourke K, Desnoyers S, Zeng Z, et al. (1995) Yama/CPP32 beta, a mammalian homolog of CED-3, is a CrmA-inhibitable protease that cleaves the death substrate poly(ADP-ribose) polymerase. Cell 81: 801-809. doi:10.1016/0092-8674(95)90541-3. PubMed: 7774019.
79. Oliver FJ, de la Rubia G, Rolli V, Ruiz-Ruiz MC, de Murcia G, et al. (1998) Importance of poly(ADP-ribose) polymerase and its cleavage in apoptosis. Lesson from an uncleavable mutant. J Biol Chem 273: 33533-33539. doi:10.1074/jbc.273.50.33533. PubMed: 9837934.
80. Koopman G, Reutelingsperger CP, Kuijten GA, Keehnen RM, Pals ST, et al. (1994) Annexin V for flow cytometric detection of phosphatidylserine expression on B cells undergoing apoptosis. Blood 84: 1415-1420. PubMed: 8068938.
81. Martin SJ, Reutelingsperger CP, McGahon AJ, Rader JA, van Schie RC, et al. (1995) Early redistribution of plasma membrane phosphatidylserine is a general feature of apoptosis regardless of the initiating stimulus: inhibition by overexpression of Bcl-2 and Abl. J Exp Med 182: 1545-1556. doi:10.1084/jem.182.5.1545. PubMed: 7595224.
82. Delebecque F, Suspène R, Calattini S, Casartelli N, Saïb A, et al. (2006) Restriction of foamy viruses by APOBEC cytidine deaminases. J Virol 80: 605-614. doi:10.1128/JVI.80.2.605-614.2006. PubMed: 16378963.
83. Mahieux R, Suspène R, Delebecque F, Henry M, Schwartz O, et al. (2005) Extensive editing of a small fraction of human T-cell leukemia virus type 1 genomes by four APOBEC3 cytidine deaminases. J Gen Virol 86: 2489-2494. doi:10.1099/vir.0.80973-0. PubMed: 16099907.
84. Henry M, Terzian C, Peeters M, Wain-Hobson S, Vartanian JP, (2012) Evolution of the primate APOBEC3A cytidine deaminase gene and identification of related coding regions. PLOS ONE 7: e30036. doi:10.1371/journal.pone.0030036. PubMed: 22272271.
85. Bennett P, Ishchenko AA, Laval J, Paap B, Sutherland BM, (2008) Endogenous DNA damage clusters in human hematopoietic stem and progenitor cells. Free Radic Biol Med 45: 1352-1359. doi:10.1016/j.freeradbiomed.2008.08.007. PubMed: 18775489.
86. Garrod KR, Moreau HD, Garcia Z, Lemaitre F, Bouvier I, et al. (2012) Dissecting T cell contraction in vivo using a genetically encoded reporter of apoptosis. Cell Rep 2: 1-10. doi:10.1016/j.celrep.2012.05.015. PubMed: 22840390.
87. Lengauer C, Kinzler KW, Vogelstein B, (1998) Genetic instabilities in human cancers. Nature 396: 643-649. doi:10.1038/25292. PubMed: 9872311.
88. Nakamura AJ, Redon CE, Sedelnikova OA, (2009) Where did they come from? The origin of endogenous gamma-H2AX foci in tumor cells. Cell Cycle 8: 2324. doi:10.4161/cc.8.15.9311.
89. Sedelnikova OA, Bonner WM, (2006) GammaH2AX in cancer cells: a potential biomarker for cancer diagnostics, prediction and recurrence. Cell Cycle 5: 2909-2913. doi:10.4161/cc.5.24.3569. PubMed: 17172873.
90. Stratton MR, Campbell PJ, Futreal PA, (2009) The cancer genome. Nature 458: 719-724. doi:10.1038/nature07943. PubMed: 19360079.
91. Warters RL, Adamson PJ, Pond CD, Leachman SA, (2005) Melanoma cells express elevated levels of phosphorylated histone H2AX foci. J Invest Dermatol 124: 807-817. doi:10.1111/j.0022-202X.2005.23674.x. PubMed: 15816840.
92. Yu T, MacPhail SH, Banáth JP, Klokov D, Olive PL, (2006) Endogenous expression of phosphorylated histone H2AX in tumors in relation to DNA double-strand breaks and genomic instability. DNA Repair 5: 935-946. doi:10.1016/j.dnarep.2006.05.040. PubMed: 16814620.
93. Gorgoulis VG, Vassiliou LV, Karakaidos P, Zacharatos P, Kotsinas A, et al. (2005) Activation of the DNA damage checkpoint and genomic instability in human precancerous lesions. Nature 434: 907-913. doi:10.1038/nature03485. PubMed: 15829965.
94. Schumacher B, Garinis GA, Hoeijmakers JH, (2008) Age to survive: DNA damage and aging. Trends Genet 24: 77-85. doi:10.1016/j.tig.2007.11.004. PubMed: 18192065.
95. Gorbunova V, Seluanov A, Mao Z, Hine C, (2007) Changes in DNA repair during aging. Nucleic Acids Res 35: 7466-7474. doi:10.1093/nar/gkm756. PubMed: 17913742.
96. Imam SZ, Karahalil B, Hogue BA, Souza-Pinto NC, Bohr VA, (2006) Mitochondrial and nuclear DNA-repair capacity of various brain regions in mouse is altered in an age-dependent manner. Neurobiol Aging 27: 1129-1136. doi:10.1016/j.neurobiolaging.2005.06.002. PubMed: 16005114.
97. Katyal S, McKinnon PJ, (2008) DNA strand breaks, neurodegeneration and aging in the brain. Mech Ageing Dev 129: 483-491. doi:10.1016/j.mad.2008.03.008. PubMed: 18455751.
98. Wilson DM 3rd, Bohr VA, (2007) The mechanics of base excision repair, and its relationship to aging and disease. DNA Repair 6: 544-559. doi:10.1016/j.dnarep.2006.10.017. PubMed: 17112792.
99. Nakamura AJ, Chiang YJ, Hathcock KS, Horikawa I, Sedelnikova OA, et al. (2008) Both telomeric and non-telomeric DNA damage are determinants of mammalian cellular senescence. Epigenetics Chromatin 1: 6. doi:10.1186/1756-8935-1-6. PubMed: 19014415.
100. Sedelnikova OA, Horikawa I, Redon C, Nakamura A, Zimonjic DB, et al. (2008) Delayed kinetics of DNA double-strand break processing in normal and pathological aging. Aging Cell 7: 89-100. doi:10.1111/j.1474-9726.2007.00354.x. PubMed: 18005250.
101. Sedelnikova OA, Horikawa I, Zimonjic DB, Popescu NC, Bonner WM, et al. (2004) Senescing human cells and ageing mice accumulate DNA lesions with unrepairable double-strand breaks. Nat Cell Biol 6: 168-170. doi:10.1038/ncb1095. PubMed: 14755273.
102. Bohr VA, (2005) Deficient DNA repair in the human progeroid disorder, Werner syndrome. Mutat Res 577: 252-259. doi:10.1016/j.mrfmmm.2005.03.021. PubMed: 15916783.
103. Gorbunova V, Seluanov A, (2005) Making ends meet in old age: DSB repair and aging. Mech Ageing Dev 126: 621-628. doi:10.1016/j.mad.2005.02.008. PubMed: 15888314.
104. Campisi J, d'Adda di Fagagna F, (2007) Cellular senescence: when bad things happen to good cells. Nat Rev Mol Cell Biol 8: 729-740. doi:10.1038/nrg2208. PubMed: 17667954.
105. d'Adda di Fagagna F, (2008) Living on a break: cellular senescence as a DNA-damage response. Nat Rev Cancer 8: 512-522. doi:10.1038/nri2318. PubMed: 18574463.
106. Deniaud E, Baguet J, Mathieu AL, Pagès G, Marvel J, et al. (2006) Overexpression of Sp1 transcription factor induces apoptosis. Oncogene 25: 7096-7105. doi:10.1038/sj.onc.1209696. PubMed: 16715126.
107. Zhang P, Chen J, Liang Y, (2010) DNA binding, cytotoxicity, and apoptotic-inducing activity of ruthenium(II) polypyridyl complex. Acta Biochim Biophys Sin 42: 440-449. doi:10.1093/abbs/gmq040. PubMed: 20705582.
108. Chiang SY, Welch J, Rauscher FJ 3rd, Beerman TA, (1994) Effects of minor groove binding drugs on the interaction of TATA box binding protein and TFIIA with DNA. Biochemistry 33: 7033-7040. doi:10.1021/bi00189a003. PubMed: 7516181.
109. Zhang X, Chen J, Davis B, Kiechle F, (1999) Hoechst 33342 induces apoptosis in HL-60 cells and inhibits topoisomerase I in vivo. Arch Pathol Lab Med 123: 921-927. PubMed: 10506445.
110. Zhang X, Kiechle FL, (1997) Hoechst 33342-induced apoptosis in BC3H-1 myocytes. Ann Clin Lab Sci 27: 260-275. PubMed: 9210971.
111. Zhang X, Kiechle FL, (1998) Hoechst 33342 induces apoptosis and alters tata box binding protein/DNA complexes in nuclei from BC3H-1 myocytes. Biochem Biophys Res Commun 248: 18-21. doi:10.1006/bbrc.1998.8906. PubMed: 9675078.
112. Stephens PJ, Greenman CD, Fu B, Yang F, Bignell GR, et al. (2011) Massive genomic rearrangement acquired in a single catastrophic event during cancer development. Cell 144: 27-40. doi:10.1016/j.cell.2010.11.055. PubMed: 21215367.
113. Nik-Zainal S, Alexandrov LB, Wedge DC, Van Loo P, Greenman CD, et al. (2012) Mutational processes molding the genomes of 21 breast cancers. Cell 149: 979-993. doi:10.1016/j.cell.2012.04.024. PubMed: 22608084.
114. Carpenter MA, Li M, Rathore A, Lackey L, Law EK, et al. (2012) Methylcytosine and Normal Cytosine Deamination by the Foreign DNA Restriction Enzyme APOBEC3A. J Biol Chem 287: 34801-34808. doi:10.1074/jbc.M112.385161. PubMed: 22896697.
115. Suspène R, Aynaud MM, Vartanian JP, Wain-Hobson S, (2013) Efficient deamination of 5-methylcytidine and 5-substituted cytidine residues in DNA by human APOBEC3A cytidine deaminase. In press. PubMed: 23840298.
116. Wijesinghe P, Bhagwat AS, (2012) Efficient deamination of 5-methylcytosines in DNA by human APOBEC3A, but not by AID or APOBEC3G. Nucleic Acids Res 40: 9206-9217. doi:10.1093/nar/gks685. PubMed: 22798497.
117. Coker HA, Petersen-Mahrt SK, (2007) The nuclear DNA deaminase AID functions distributively whereas cytoplasmic APOBEC3G has a processive mode of action. DNA Repair 6: 235-243. doi:10.1016/j.dnarep.2006.10.001. PubMed: 17161027.
118. Biebricher CK, Eigen M, (2005) The error threshold. Virus Res 107: 117-127. doi:10.1016/j.virusres.2004.11.002. PubMed: 15649558.
119. Crotty S, Cameron CE, Andino R, (2001) RNA virus error catastrophe: direct molecular test by using ribavirin. Proc Natl Acad Sci U S A 98: 6895-6900. doi:10.1073/pnas.111085598. PubMed: 11371613.
120. Holmes EC, (2003) Error thresholds and the constraints to RNA virus evolution. Trends Microbiol 11: 543-546. doi:10.1016/j.tim.2003.10.006. PubMed: 14659685.
121. Aynaud MM, Suspène R, Vidalain PO, Mussil B, Guétard D, et al. (2012) Human Tribbles 3 protects nuclear DNA from cytidine deamination by APOBEC3A. J Biol Chem 287: 39182-39192. doi:10.1074/jbc.M112.372722. PubMed: 22977230.