What mechanisms/processes underlie radiation-induced genomic instability?

Cellular and Molecular Life Sciences

Volumn 69, Issue 20, 2012, Pages 3351-3360

  Karotki, Andrei V ^a   Baverstock, Keith ^b  

^a INTERNATIONAL AGENCY FOR RESEARCH ON CANCER   (France)

^b UNIVERSITY OF EASTERN FINLAND   (Finland)

Author keywords

Cell regulation; Centrosome; Chromosomal damage; DNA methylation; Epigenetic processes; Extracellular matrix; Genomic instability; High dimensional complex system; Information; Ionising radiation; Non targeted effects; Reactive oxygen species; Self organisation

Indexed keywords

DNA; REACTIVE OXYGEN METABOLITE; TELOMERASE; TRANSFORMING GROWTH FACTOR BETA; UNTRANSLATED RNA;

ALPHA RADIATION; ARTICLE; BYSTANDER EFFECT; CELL CLONE; CELL DIVISION; CENTROSOME; CHROMATIN; CHROMOSOME ABERRATION; DNA DAMAGE; DNA METHYLATION; DNA SEQUENCE; EXTRACELLULAR MATRIX; GENE MUTATION; GENETIC PARAMETERS; GENOMIC INSTABILITY; HETEROZYGOSITY LOSS; HUMAN; INFLAMMATION; INHERITANCE; INTRACELLULAR SIGNALING; IONIZING RADIATION; IRRADIATION; MICROENVIRONMENT; MITOCHONDRION; MITOSIS SPINDLE; NONHUMAN; OXIDATIVE STRESS; PROGENY; RADIATION HAZARD; RADIATION INDUCED GENOMIC INSTABILITY; TELOMERE; TRANSCRIPTION INITIATION;

ANIMALS; DNA DAMAGE; GENOMIC INSTABILITY; HUMANS; RADIATION INJURIES;

EID: 84867577104     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-012-1148-5     Document Type: Article

References (99)

1. Kadhim MA, Macdonald DA, Goodhead DT, Lorimore SA, Marsden SJ, Wright EG (1992) Transmission of chromosomal instability after plutonium alpha-particle irradiation. Nature 355:738-740
2. Morgan WF (2003) Non-targeted and delayed effects of exposure to ionizing radiation: II. Radiation-induced genomic instability and bystander effects in vivo, clastogenic factors and transgenerational effects. Radiat Res 159:581-596
3. Morgan WF (2003) Non-targeted and delayed effects of exposure to ionizing radiation: I. Radiation-induced genomic instability and bystander effects in vitro. Radiat Res 159:567-580
4. Coen N, Mothersill C, Kadhim M, Wright EG (2001) Heavy metals of relevance to human health induce genomic instability. J Pathol 195:293-299
5. Baverstock K (2000) Radiation-induced genomic instability: A paradigm-breaking phenomenon and its relevance to environmentally induced cancer. Mutat Res 454:89-109
6. Goodhead DT (2006) Energy deposition stochastics and track structure: What about the target? Radiat Prot Dosimetry 122:3-15
7. Baverstock K, Belyakov OV (2005) Classical radiation biology, the bystander effect and paradigms: A reply. Hum Exp Toxicol 24:537-542
8. Watson GE, Pocock DA, Papworth D, Lorimore SA, Wright EG (2001) In vivo chromosomal instability and transmissible aberrations in the progeny of haemopoietic stem cells induced by high-and low-LET radiations. Int J Radiat Biol 77:409-417
9. Huumonen K, Immonen HK, Baverstock K, Hiltunen M, Korkalainen M, Lahtinen T, Parviainen J, Viluksela M, Wong G, Naarala J, Juutilainen J (2012) Radiation-induced genomic instability in Caenorhabditis elegans. Mutat Res 748:36-41
10. Schiestl RH, Aubrecht J, Khogali F, Carls N (1997) Carcinogens induce reversion of the mouse pink-eyed unstable mutation. Proc Natl Acad Sci USA 94:4576-4581
11. Dubrova YE, Nesterov VN, Krouchinsky NG, Ostapenko VA, Neumann R, Neil DL, Jeffreys AJ (1996) Human minisatellite mutation rate after the Chernobyl accident. Nature 380:683-686
12. Dubrova YE, Nesterov VN, Krouchinsky NG, Ostapenko VA, Vergnaud G, Giraudeau F, Buard J, Jeffreys AJ (1997) Further evidence for elevated human minisatellite mutation rate in Belarus eight years after the Chernobyl accident. Mutat Res 381:267-278
13. Dubrova YE, Bersimbaev RI, Djansugurova LB, Tankimanova MK, Mamyrbaeva ZZ, Mustonen R, Lindholm C, Hulten M, Salomaa S (2002) Nuclear weapons tests and human germline mutation rate. Science 295:1037
14. Dubrova YE, Grant G, Chumak AA, Stezhka VA, Karakasian AN (2002) Elevated minisatellite mutation rate in the post-chernobyl families from Ukraine. Am J Hum Genet 71:801-809
15. Barber R, Plumb MA, Boulton E, Roux I, Dubrova YE (2002) Elevated mutation rates in the germ line of first-and secondgeneration offspring of irradiated male mice. Proc Natl Acad Sci USA 99:6877-6882
16. Barber RC, Hardwick RJ, Shanks ME, Glen CD, Mughal SK, Voutounou M, Dubrova YE (2009) The effects of in utero irradiation on mutation induction and transgenerational instability in mice. Mutat Res 664:6-12
17. Barber RC, Hickenbotham P, Hatch T, Kelly D, Topchiy N, Almeida GM, Jones GD, Johnson GE, Parry JM, Rothkamm K, Dubrova YE (2006) Radiation-induced transgenerational alterations in genome stability and DNA damage. Oncogene 25:7336-7342
18. Chang WP, Little JB (1992) Persistently elevated frequency of spontaneous mutations in progeny of CHO clones surviving X-irradiation: Association with delayed reproductive death phenotype. Mutat Res 270:191-199
19. Little JB, Nagasawa H, Pfenning T, Vetrovs H (1997) Radiation-induced genomic instability: Delayed mutagenic and cytogenetic effects of X rays and alpha particles. Radiat Res 148:299-307
20. Grosovsky AJ, Parks KK, Giver CR, Nelson SL (1996) Clonal analysis of delayed karyotypic abnormalities and gene mutations in radiation-induced genetic instability. Mol Cell Biol 16:6252-6262
21. Dubrova YE, Hickenbotham P, Glen CD, Monger K, Wong HP, Barber RC (2008) Paternal exposure to ethylnitrosourea results in transgenerational genomic instability in mice. Environ Mol Mutag 49:308-311
22. Vilarino-Guell C, Smith AG, Dubrova YE (2003) Germline mutation induction at mouse repeat DNA loci by chemical mutagens. Mutat Res 526:63-73
23. Cuevas-Ramos G, Petit CR, Marcq I, Boury M, Oswald E, Nougayrede JP (2010) Escherichia coli induces DNA damage in vivo and triggers genomic instability in mammalian cells. Proc Natl Acad Sci USA 107:1153-11542
24. Koturbash I, Thomas JE, Kovalchuk O, Kovalchuk I (2009) Heatkilled bacteria induce genome instability in mouse small intestine, liver and spleen tissues. Cell Cycle 8:1935-1939
25. Brennan RJ, Schiestl RH (2001) Persistent genomic instability in the yeast Saccharomyces cerevisiae induced by ionizing radiation and DNA-damaging agents. Radiat Res 155:768-777
26. Niwa O (2003) Induced genomic instability in irradiated germ cells and in the offspring; reconciling discrepancies among the human and animal studies. Oncogene 22:7078-7086
27. Barcellos-Hoff MH, Brooks AL (2001) Extracellular signaling through the microenvironment: A hypothesis relating carcinogenesis, bystander effects, and genomic instability. Radiat Res 156:618-627
28. Bissell MJ, Hall HG, Parry G (1982) How does the extracellular matrix direct gene expression? J Theor Biol 99:31-68
29. Bissell MJ, Barcellos-Hoff MH (1987) The influence of extracellular matrix on gene expression: Is structure the message? J Cell Sci Suppl 8:327-343
30. Gordon MY, Dowding CR, Riley GP, Goldman JM, Greaves MF (1987) Altered adhesive interactions with marrow stroma of haematopoietic progenitor cells in chronic myeloid leukaemia. Nature 328:342-344
31. Lochter A, Galosy S, Muschler J, Freedman N, Werb Z, Bissell MJ (1997) Matrix metalloproteinase stromelysin-1 triggers a cascade of molecular alterations that leads to stable epithelial-tomesenchymal conversion and a premalignant phenotype in mammary epithelial cells. J Cell Biol 139:1861-1872
32. Whetton AD, Graham GJ (1999) Homing and mobilization in the stem cell niche. Trends Cell Biol 9:233-238
33. Soto AM, Sonnenschein C (2004) The somatic mutation theory of cancer: Growing problems with the paradigm? Bioessays 26:1097-1107
34. Wiseman BS, Werb Z (2002) Stromal effects on mammary gland development and breast cancer. Science 296:1046-1049
35. Barcellos-Hoff MH (1993) Radiation-induced transforming growth factor beta and subsequent extracellular matrix reorganization in murine mammary gland. Cancer Res 53:3880-3886
36. Massague J, Blain SW, Lo RS (2000) TGFbeta signaling in growth control, cancer, and heritable disorders. Cell 103:295-309
37. Roberts AB, Flanders KC, Kondaiah P, Thompson NL, Van Obberghen-Schilling E, Wakefield L, Rossi P, De CB, Heine U, Sporn MB (1988) Transforming growth factor beta: Biochemistry and roles in embryogenesis, tissue repair and remodeling, and carcinogenesis. Recent Prog Horm Res 44:157-197
38. Ehrhart EJ, Segarini P, Tsang ML, Carroll AG, Barcellos-Hoff MH (1997) Latent transforming growth factor beta1 activation in situ: Quantitative and functional evidence after low-dose gammairradiation. FASEB J 11:991-1002
39. Barcellos-Hoff MH, Nguyen DH (2009) Radiation carcinogenesis in context: How do irradiated tissues become tumors? Health Phys 97:446-457
40. Spencer VA, Xu R, Bissell MJ (2010) Gene expression in the third dimension: The ECM-nucleus connection. J Mammary Gland Biol Neoplasia 15:65-71
41. Maxwell CA, Fleisch MC, Costes SV, Erickson AC, Boissiere A, Gupta R, Ravani SA, Parvin B, Barcellos-Hoff MH (2008) Targeted and nontargeted effects of ionizing radiation that impact genomic instability. Cancer Res 68:8304-8311
42. Bornens M, Azimzadeh J (2007) Origin and evolution of the centrosome. In: Jekely G (ed) Eukaryotic membranes and cytoskeleton origins and evolution. Springer, New York
43. Sluder G, Nordberg JJ (2004) The good, the bad and the ugly: The practical consequences of centrosome amplification. Curr Opin Cell Biol 16:49-54
44. Karsenti E (2008) Self-organization in cell biology: A brief history. Nat Rev Mol Cell Biol 9:255-262
45. La Terra S, English CN, Hergert P, Mcewen BF, Sluder G, Khodjakov A (2005) The de novo centriole assembly pathway in HeLa cells: Cell cycle progression and centriole assembly/maturation. J Cell Biol 168:713-722
46. Uetake Y, Loncarek J, Nordberg JJ, English CN, La Terra S, Khodjakov A, Sluder G (2007) Cell cycle progression and de novo centriole assembly after centrosomal removal in untransformed human cells. J Cell Biol 176:173-182
47. Lorimore SA, Coates PJ, Wright EG (2003) Radiation-induced genomic instability and bystander effects: Inter-related nontargeted effects of exposure to ionizing radiation. Oncogene 22:7058-7069
48. Barcellos-Hoff MH, Park C, Wright EG (2005) Radiation and the microenvironment-tumorigenesis and therapy. Nat Rev Cancer 5:867-875
49. Coussens LM, Werb Z (2002) Inflammation and cancer. Nature 420:860-867
50. Clutton SM, Townsend KM, Walker C, Ansell JD, Wright EG (1996) Radiation-induced genomic instability and persisting oxidative stress in primary bone marrow cultures. Carcinogenesis 17:1633-1639
51. Limoli CL, Hartmann A, Shephard L, Yang CR, Boothman DA, Bartholomew J, Morgan WF (1998) Apoptosis, reproductive failure, and oxidative stress in Chinese hamster ovary cells with compromised genomic integrity. Cancer Res 58:3712-3718
52. Limoli CL, Kaplan MI, Giedzinski E, Morgan WF (2001) Attenuation of radiation-induced genomic instability by free radical scavengers and cellular proliferation. Free Radic Biol Med 31:10-19
53. Limoli CL, Giedzinski E, Morgan WF, Swarts SG, Jones GD, Hyun W (2003) Persistent oxidative stress in chromosomally unstable cells. Cancer Res 63:3107-3111
54. Wright EG (2010) Manifestations and mechanisms of non-targeted effects of ionizing radiation. Mutat Res 687:28-33
55. Samper E, Nicholls DG, Melov S (2003) Mitochondrial oxidative stress causes chromosomal instability of mouse embryonic fibroblasts. Aging Cell 2:277-285
56. Kim GJ, Fiskum GM, Morgan WF (2006) A role for mitochondrial dysfunction in perpetuating radiation-induced genomic instability. Cancer Res 66:10377-10383
57. Kim GJ, Chandrasekaran K, Morgan WF (2006) Mitochondrial dysfunction, persistently elevated levels of reactive oxygen species and radiation-induced genomic instability: A review. Mutagenesis 21:361-367
58. Zyuzikov NA, Coates PJ, Parry JM, Lorimore SA, Wright EG (2012) Lack of nontargeted effects in murine bone marrow after low-dose in vivo X irradiation. Radiat Res 175:322-327
59. Mukherjee D, Coates PJ, Lorimore SA, Wright EG (2012) The in vivo expression of radiation-induced chromosomal instability has an inflammatory mechanism. Radiat Res 177:18-24
60. Ayouaz A, Raynaud C, Heride C, Revaud D, Sabatier L (2008) Telomeres: Hallmarks of radiosensitivity. Biochimie 90:60-72
61. Raynaud CM, Sabatier L, Philipot O, Olaussen KA, Soria JC (2008) Telomere length, telomeric proteins and genomic instability during the multistep carcinogenic process. Crit Rev Oncol Hematol 66:99-117
62. Murnane JP (2006) Telomeres and chromosome instability. DNA Repair 5:1082-1092
63. Ju Z, Rudolph KL (2006) Telomeres and telomerase in stem cells during aging and disease. Genome Dyn 1:84-103
64. Osterhage JL, Friedman KL (2009) Chromosome end maintenance by telomerase. J Biol Chem 284:16061-16065
65. Aypar U, Morgan WF, Baulch JE (2010) Radiation-induced genomic instability: Are epigenetic mechanisms the missing link? Int J Radiat Biol 87:179-191
66. Ilnytskyy Y, Kovalchuk O (2011) Non-targeted radiation effects-an epigenetic connection. Mutat Res 714:113-125
67. Rugo RE, Mutamba JT, Mohan KN, Yee T, Chaillet JR, Greenberger JS, Engelward BP (2011) Methyltransferases mediate cell memory of a genotoxic insult. Oncogene 30:751-756
68. Dubrova YE (2006) Genomic instability in the offspring of irradiated parents: Facts and interpretations. Russ J Genet 42:1116-1126
69. Baulch JE, Raabe OG (2005) Gamma irradiation of type B spermatogonia leads to heritable genomic instability in four generations of mice. Mutagenesis 20:337-343
70. Baulch JE, Raabe OG, Wiley LM (2001) Heritable effects of paternal irradiation in mice on signaling protein kinase activities in F3 offspring. Mutagenesis 16:17-23
71. Koturbash I, Rugo RE, Hendricks CA, Loree J, Thibault B, Kutanzi K, Pogribny I, Yanch JC, Engelward BP, Kovalchuk O (2006) Irradiation induces DNA damage and modulates epigenetic effectors in distant bystander tissue in vivo. Oncogene 25:4267-4275
72. Kovalchuk O, Baulch JE (2008) Epigenetic changes and nontargeted radiation effects-is there a link? Environ Mol Mutag 49:16-25
73. Jaenisch R, Bird A (2003) Epigenetic regulation of gene expression: How the genome integrates intrinsic and environmental signals. Nat Genet 33(Suppl):245-254
74. Krawetz SA (2005) Paternal contribution: New insights and future challenges. Nat Rev Genet 6:633-642
75. Rousseaux S, Caron C, Govin J, Lestrat C, Faure AK, Khochbin S (2005) Establishment of male-specific epigenetic information. Gene 345:139-153
76. Santos F, Dean W (2004) Epigenetic reprogramming during early development in mammals. Reproduction 127:643-651
77. Huang S (2009) Reprogramming cell fates: Reconciling rarity with robustness. BioEssays 31:546-560
78. Deal RB, Henikoff JG, Henikoff S (2010) Genome-wide kinetics of nucleosome turnover determined by metabolic labeling of histones. Science 328:1161-1164
79. Cremer T, Cremer C (2001) Chromosome territories, nuclear architecture and gene regulation in mammalian cells. Nat Rev Genet 2:292-301
80. Cremer M, Von Hase J, Volm T, Brero A, Kreth G, Walter J, Fischer C, Solovei I, Cremer C, Cremer T (2001) Non-random radial higher-order chromatin arrangements in nuclei of diploid human cells. Chromosome Res 9:541-567
81. Chen K, Rajewsky N (2007) The evolution of gene regulation by transcription factors and microRNAs. Nat Rev Genet 8:93-103
82. Yus E, Maier T, Michalodimitrakis K, Van Noort V, Yamada T, Chen WH, Wodke JA, Guell M, Martinez S, Bourgeois R, Kuhner S, Raineri E, Letunic I, Kalinina OV, Rode M, Herrmann R, Gutierrez-Gallego R, Russell RB, Gavin AC, Bork P, Serrano L (2009) Impact of genome reduction on bacterial metabolism and its regulation. Science 326:1263-1268
83. O'Neill JS, Van Ooijen G, Dixon LE, Troein C, Corellou F, Bouget FY, Reddy AB, Millar AJ (2011) Circadian rhythms persist without transcription in a eukaryote. Nature 469:554-558
84. Baverstock K (2010) Why do we need a new paradigm in radiobiology? Mutat Res 687:3-6
85. Baverstock K, Rönkkö M (2008) Epigenetic regulation of the mammalian cell. PLoS ONE 3:e2290
86. Karsenti E, Nedelec F, Surrey T (2006) Modelling microtubule patterns. Nat Cell Biol 8:1204-1211
87. Nicolis, G. and Prigogine, I. (1989) Exploring complexity: An introduction W.H. Freeman New York
88. Baverstock K (2011) A comparison of two cell regulatory models entailing high dimensional attractors representing phenotype. Prog Biophys Mol Biol 106:443-449
89. Falt S, Holmberg K, Lambert B, Wennberg A (2003) Long-term global gene expression patterns in irradiated human lymphocytes. Carcinogenesis 24:1823-1845
90. Eichler EE, Flint J, Gibson G, Kong A, Leal SM, Moore JH, Nadeau JH (2010) Missing heritability and strategies for finding the underlying causes of complex disease. Nat Rev Genet 11:446-450
91. Manolio TA, Collins FS, Cox NJ, Goldstein DB, Hindorff LA, Hunter DJ, Mccarthy MI, Ramos EM, Cardon LR, Chakravarti A, Cho JH, Guttmacher AE, Kong A, Kruglyak L, Mardis E, Rotimi CN, Slatkin M, Valle D, Whittemore AS, Boehnke M, Clark AG, Eichler EE, Gibson G, Haines JL, Mackay TF, Mccarroll SA, Visscher PM (2009) Finding the missing heritability of complex diseases. Nature 461:747-753
92. Mitchell KJ (2011) The miswired brain: Making connections from neurodevelopment to psychopathology. BMC Biol 9:23
93. Barrick JE, Yu DS, Yoon SH, Jeong H, Oh TK, Schneider D, Lenski RE, Kim JF (2009) Genome evolution and adaptation in a long-term experiment with Escherichia coli. Nature 461:1243-1247
94. Nakajima M, Imai K, Ito H, Nishiwaki T, Murayama Y, Iwasaki H, Oyama T, Kondo T (2005) Reconstitution of circadian oscillation of cyanobacterial KaiC phosphorylation in vitro. Science 308:414-415
95. O'neill JS, Reddy AB (2011) Circadian clocks in human red blood cells. Nature 469:498-503
96. Kashiwagi A, Urabe I, Kaneko K, Yomo T (2006) Adaptive response of a gene network to environmental changes by fitnessinduced attractor selection. PLoS ONE 1:e49
97. Crowther JA (1924) Some considerations relative to the actions of X-rays on tissue cells. Proc Roy Soc Series B 96:2007-2211
98. Timoféeff-Ressovsky NW, Zimmer KG, Delbrück M (1935)Über die Natur der Genmutation und der Genstruktur. Nachrichten der Biologischen Gesellschaft für Wissenschaft, Göttingen 1:189-241
99. Noble D (2010) Biophysics and systems biology. Philos Transact A Math Phys Eng Sci 368:1125-1139