Epigenetics in radiation biology: A new research frontier

Frontiers in Genetics

Volumn 4, Issue APR, 2013, Pages

  Merrifield, Matt ^a   Kovalchuk, Olga ^a  

^a UNIVERSITY OF LETHBRIDGE   (Canada)

Author keywords

Bystander effects; DNA methylation; Epigenetics; Genome instability; Histones; Radiation; Small rnas; Transgeneration effects

Indexed keywords

EID: 84876163688     PISSN: None     EISSN: 16648021     Source Type: Journal    
DOI: 10.3389/fgene.2013.00040     Document Type: Review

References (233)

1. Amundson, S. A., and Fornace, A. J. Jr. (2003). Monitoring human radiation exposure by gene expression profiling: possibilities and pitfalls. Health Phys. 85, 36-42.
2. Anway, M. D., Rekow, S. S., and Skinner, M. K. (2008). Comparative anti-androgenic actions of vinclozolin and flutamide on transgenerational adult onset disease and spermatogenesis. Reprod. Toxicol 26,100-106.
3. Aqeilan, R. I., Calin, G. A., and Croce, C. M. (2010). miR-15a and miR-16-1 in cancer: discovery, function and future perspectives. Cell Death Differ. 17,215-220.
4. Aravin, A. A., and Bourc'his, D. (2008). Small RNA guides for de novo DNA methylation in mammalian germ cells. Genes Dev. 22, 970-975.
5. Aravin, A. A., and Hannon, G. J. (2008). Small RNA silencing pathways in germ and stem cells. Cold Spring Harb. Symp. Quant. Biol. 73, 283-290.
6. Aravin, A. A., Hannon, G. J., and Bren-necke, J. (2007a). The Piwi-piRNA pathway provides an adaptive defense in the transposon arms race. Science 318,761-764.
7. Aravin, A. A., Sachidanandam, R., Girard, A., Fejes-Toth, K., and Hannon, G. J. (2007b). Developmentally regulated piRNA clusters implicate MILI in transposon control. Science 316,744-747.
8. Aravin, A. A., Lagos-Quintana, M., Yalcin, A., Zavolan, M., Marks, D., Snyder, B., et al. (2003). The small RNA profile during Drosophila melanogaster development. Dev. Cell 5,337-350.
9. Aravin, A. A., Sachidanandam, R., Bourc'his, D., Schaefer, C., Pezic, D., Toth, K. F., et al. (2008). A piRNA pathway primed by individual transposons is linked to de novo DNA methylation in mice. Mol. Cell 31, 785-799.
10. Aravin, A., Gaidatzis, D., Pfeffer, S., Lagos-Quintana, M., Landgraf, P., Iovino, N., et al. (2006). A novel class of small RNAs bind to MILI protein in mouse testes. Nature 442, 203-207.
11. Azzam, E. I., de Toledo, S. M., and Little, J. B. (2003a). Expression of CONNEXIN43 is highly sensitive to ionizing radiation and other environmental stresses. Cancer Res. 63,7128-7135.
12. Azzam, E. I., de Toledo, S. M., and Little, J. B. (2003b). Oxidative metabolism, gap junctions and the ionizingradiation-inducedbystander effect. Oncogene 22, 7050-7057.
13. Balonov, M. I. (2007). The Chernobyl Forum: major findings and recommendations. J. Environ. Radioact. 96, 6-12.
14. Barber, R. C., and Dubrova, Y. E. (2006). The offspring of irradiated parents, are they stable? Mutat. Res. 598, 50-60.
15. Barber, R. C., Hickenbotham, P., Hatch, T., Kelly, D., Topchiy, N., Almeida, G. M., et al. (2006). Radiation-induced transgenerational alterations in genome stability and DNA damage. Oncogene 25, 7336-7342.
16. Barber, R., Plumb, M. A., Boulton, E., Roux, I., and Dubrova, Y. E. (2002). Elevated mutation rates in the germ line of firstand second-generation offspring of irradiated male mice. Proc. Natl. Acad. Sci. U.S.A. 99, 6877-6882.
17. Barcellos-Hoff, M. H. (2005). Integrative radiation carcinogenesis: interactions between cell and tissue responses to DNA damage. Semin. Cancer Biol. 15, 138-148.
18. Baylin, S. B. (2005). DNA methylation and gene silencing in cancer. Nat. Clin. Pract. Oncol. 2(Suppl. 1), S4-S11.
19. Baylin, S. B., and Ohm, J. E. (2006). Epi-genetic gene silencing in cancer - a mechanism for early oncogenic pathway addiction? Nat. Rev. Cancer 6, 107-116.
20. Belyakov, O. V., Mitchell, S. A., Parikh, D., Randers-Pehrson, G., Marino, S. A., Amundson, S. A., et al. (2005). Biological effects in unirradiated human tissue induced by radiation damage up to 1 mm away. Proc. Natl. Acad. Sci. U.S.A. 102, 14203-14208.
21. Bernstein, E., and Allis, C. D. (2005). RNA meets chromatin. GenesDev. 19, 1635-1655.
22. Bishayee, A., Hill, H. Z., Stein, D., Rao, D. V., and Howell, R. W. (2001). Free radical-initiated and gap junction-mediated bystander effect due to nonuniform distribution of incorporated radioactivity in a three-dimensional tissue culture model. Radiat. Res. 155, 335-344.
23. Bois, P., Williamson, J., Brown, J., Dubrova, Y. E., and Jeffreys, A. J. (1998). A novel unstable mouse VNTR family expanded from SINE B1 elements. Genomics 49, 122-128.
24. Brenner, D. J., and Hall, E. J. (2004). Risk of cancer from diagnostic X-rays. Lancet 363, 2192-2193.
25. Brooks, A. L. (2004). Evidence for 'bystander effects' in vivo. Hum. Exp. Toxicol. 23, 67-70.
26. Brooks, A. L., Retherford, J. C., and McClellan, R. O. (1974). Effect of 239PuO2 particle number and size on the frequency and distribution of chromosome aberrations in the liver of the Chinese hamster. Radiat. Res. 59, 693-709.
27. Burruel, V. R., Raabe, O. G., and Wiley, L.M. (1997). In vitro fertilization rate of mouse oocytes with spermatozoa from the F1 offspring of males irradiated with 1.0 Gy 137Cs gamma-rays. Mutat. Res. 381,59-66.
28. Carmell, M. A., Girard, A., van de Kant, H. J., Bourc'his, D., Bestor, T. H., de Rooij, D. G., et al. (2007). MIWI2 is essential for spermatogenesis and repression of transposons in the mouse male germline. Dev. Cell 12,503-514.
29. Carmichael, A., Sami, A. S., and Dixon, J. M. (2003). Breast cancer risk among the survivors of atomic bomb and patients exposed to therapeutic ionising radiation. Eur. J. Surg. Oncol. 29,475-479.
30. Chang, T. C., and Mendell, J. T. (2007). microRNAs in vertebrate physiology and human disease. Annu. Rev. Genomics Hum. Genet. 8,215-239.
31. Chen, P. Y., and Meister, G. (2005). microRNA-guided posttran-scriptional gene regulation. Biol. Chem. 386, 1205-1218.
32. Cheng, K. C., and Loeb, L. A. (1993). Genomic instability and tumor progression: mechanistic considerations. Adv. Cancer Res. 60, 121-156.
33. Cheung, P., and Lau, P. (2005). Epi-genetic regulation by histone methylation and histone variants. Mol. Endocrinol. 19, 563-573.
34. Criswell, T., Leskov, K., Miyamoto, S., Luo, G., and Boothman, D. A. (2003). Transcription factors activated in mammalian cells after clinically relevant doses of ionizing radiation. Oncogene 22, 5813-5827.
35. Deng, W., and Lin, H. (2002). miwi, a murine homolog of piwi, encodes a cytoplasmic protein essential for spermatogenesis. Dev. Cell 2, 819-830.
36. De Potter, P., Levecq, L., Godfraind, C., and Renard, L. (2006). Primary orbital melanoma treated with iodine-125 plaque radiotherapy. Am. I Ophthalmol. 142, 864-866.
37. Dickinson, H. O., and Parker, L. (2002). Leukaemia and non-Hodgkin's lym-phoma in children of Sellafield male radiation workers. Int. J. Cancer 101, 100.
38. Doench, J. G., and Sharp, P. A. (2004). Specificity of microRNA target selection in translational repression. Genes Dev. 18,504-511.
39. Doody, M. M., Lonstein, J. E., Stovall, M., Hacker, D. G., Luckyanov, N., and Land, C. E. (2000). Breast cancer mortality after diagnostic radiography: findings from the U.S. Scoliosis Cohort Study. Spine 25, 2052-2063.
40. Dubrova, Y. E. (2003a). Long-term genetic effects of radiation exposure. Mutat. Res. 544, 433-439.
41. Dubrova, Y. E. (2003b). Radiation-induced transgenerational instability. Oncogene 22, 7087-7093.
42. Dubrova, Y. E. (2003c). Monitoring of radiation-induced germline mutation in humans. SwissMed. Wkly 133, 474-478.
43. Dubrova, Y. E., Bersimbaev, R. I., Djan-sugurova, L. B., Tankimanova, M. K., Mamyrbaeva, Z., Mustonen, R., et al. (2002a). Nuclear weapons tests and human germline mutation rate. Science 295,1037.
44. Dubrova, Y. E., Grant, G., Chumak, A. A., Stezhka, V. A., and Karakasian, A. N. (2002b). Elevated minisatellite mutation rate in the post-chernobyl families from ukraine. Am. J. Hum. Genet 71, 801-809.
45. Dubrova, Y. E., Hickenbotham, P., Glen, C. D., Monger, K., Wong, H. P., and Barber, R. C. (2008). Paternal exposure to ethylnitrosourea results in transgenerational genomic instability in mice. Environ. Mol. Mutagen. 49,308-311.
46. Dubrova, Y. E., Nesterov, V. N., Krouchinsky, N. G., Ostapenko, V. A., Neumann, R., Neil, D. L., et al. (1996). Human minisatellite mutation rate after the Chernobyl accident. Nature, 380,683-686.
47. Ehrlich, M. (2002).DNAmethylationin cancer: too much, but also too little. Oncogene 21, 5400-5413.
48. Emerit, I., Levy, A., Cernjavski, L., Arutyunyan, R., Oganesyan, N., Pogosian, A., et al. (1994). Transferable clastogenic activity in plasma from persons exposed as salvage personnel of the Chernobyl reactor. J. Cancer Res. Clin. Oncol. 120, 558-561.
49. Emerit, I., Oganesian, N., Sarkisian, T., Arutyunyan, R., Pogosian, A., Asrian, K., et al. (1995). Clastogenic factors in the plasma of Chernobyl accident recovery workers: anticlasto-genic effect of Ginkgo biloba extract. Radiat. Res. 144, 198-205.
50. Erven, K., and Van Limbergen, E. (2007). Regional lymph node irradiation in breast cancer. Future Oncol. 3,343-352.
51. Fabbri, M., Ivan, M., Cimmino, A., Negrini, M., and Calin, G. A. (2007). Regulatory mechanisms of microR-NAs involvement in cancer. Expert Opin. Biol. Ther. 7, 1009-1019.
52. Facoetti, A., Ballarini, F., Cherubini, R., Gerardi, S., Nano, R., Ottolenghi, A., et al. (2006). Gamma ray-induced bystander effect in tumour glioblas-toma cells: a specific study on cell survival, cytokine release and cytokine receptors. Radiat. Prot. Dosimetry 122,271-274.
53. Fei, P., and El-Deiry, W. S. (2003). P53 and radiation responses. Oncogene 22,5774-5783.
54. Feinberg, A. P. (2004). The epigenetics of cancer etiology. Semin. Cancer Biol. 14, 427-432.
55. Feinberg, A. P., and Vogelstein, B. (1983). Hypomethylation distinguishes genes of some human cancers from their normal counterparts. Nature 301, 89-92.
56. Feinendegen, L. E. (2005). Evidence for beneficial low level radiation effects and radiation hormesis. Br. J. Radiol. 78, 3-7.
57. Filkowski, J. N., Ilnytskyy, Y., Tamminga, J., Koturbash, I., Golubov, A., Bagnyukova, T., et al. (2010). Hypomethylation and genome instability in the germline of exposed parents and their progeny is associated with altered miRNA expression. Carcinogenesis 31,1110-1115.
58. Flatau, E., Bogenmann, E., and Jones, P. A. (1983). Variable 5-methylcytosine levels in human tumor cell lines and fresh pediatric tumor explants. Cancer Res. 43, 4901-4905.
59. Folkard, M., Vojnovic, B., Prise, K. M., Bowey, A. G., Locke, R. J., Schettino, G., et al. (1997). A charged-particle microbeam: I. Development of an experimental system for targeting cells individually with counted particles. Int. J. Radiat. Biol. 72, 375-385.
60. Folley, J. H., Borges, W., and Yamawaki, T. (1952). Incidence of leukemia in survivors of the atomic bomb in Hiroshima and Nagasaki, Japan. Am. J.Med. 13,311-321.
61. Fraga, M. F., Ballestar, E., Villar-Garea, A., Boix-Chornet, M., Espada, J., Schotta, G., et al. (2005). Loss of acetylation at Lys16 and trimethylation at Lys20 of histone H4 is a common hallmark of human cancer. Nat. Genet. 37,391-400.
62. Frankenberg-Schwager, M. (1990). Induction, repair and biological relevance of radiation-induced DNA lesions in eukaryotic cells. Radiat. Environ. Biophys. 29, 273-292.
63. Freeman, S. M., Abboud, C. N., Whartenby, K. A., Packman, C. H., Koeplin, D. S., Moolten, F. L., et al. (1993). The"bystander effect": tumor regression when a fraction of the tumor mass is genetically modified. Cancer Res. 53, 5274-5283.
64. Gama-Sosa, M. A., Slagel, V A., Trewyn, R. W., Oxenhandler, R., Kuo, K. C., Gehrke, C. W., et al. (1983). The 5-methylcytosine content of DNA from human tumors. Nucleic Acids Res. 11, 6883-6894.
65. Gardner, M. J., Snee, M. P., Hall, A. J., Powell, C. A., Downes, S., and Terrell, J. D. (1990). Results of case-control study of leukaemia and lymphoma among young people near Sellafield nuclear plant in West Cumbria. BMJ 300,423-429.
66. Gibbs, M., Collick, A., Kelly, R. G., and Jeffreys, A. J. (1993). A tetranucleotide repeat mouse minisatellite displaying substantial somatic instability during early preimplantation development. Genomics 17, 121-128.
67. Girard, A., Sachidanandam, R., Hannon, G. J., and Carmell, M. A. (2006). A germline-specific class of small RNAs binds mammalian Piwi proteins. Nature 442, 199-202.
68. Glen, C. D., Smith, A. G., and Dubrova, Y. E. (2008). Single-molecule PCR analysis of germ line mutation induction by anticancer drugs in mice. Cancer Res. 68, 3630-3636.
69. Gluzman, D., Imamura, N., Sklyarenko, L., Nadgornaya, V., Zavelevich, M., and Machilo, V (2005). Malignant diseases of hematopoietic and lymphoid tissues in Chernobyl clean-up workers. Hematol. J. 5, 565-571.
70. Goh, K., and Sumner, H. (1968). Breaks in normal human chromosomes: are they induced by a transferable substance in the plasma of persons exposed to total-body irradiation? Radiat. Res. 35,171-181.
71. Goldberg, Z. (2003). Clinical implications of radiation-induced genomic instability. Oncogene 22, 7011-7017.
72. Goldberg, Z., and Lehnert, B. E. (2002). Radiation-induced effects in unirradiated cells: areviewand implications in cancer. Int. J. Oncol. 21, 337-349.
73. Goll, M. G., and Bestor, T. H. (2005). Eukaryotic cytosine methyl-transferases. Annu. Rev. Biochem. 74, 481-514.
74. Goodhead, D. T. (1994). Initial events in the cellular effects of ionizing radiations: clustered damage in DNA. Int. J. Radiat. Biol. 65, 7-17.
75. Gramegna, A. (1909). Un cas d'acromegalie traitè pour la radioterapie. Rev. Neurol. 17, 15-17.
76. Greenbaum, M. P., Ma, L., and Matzuk, M. M. (2007). Conversion of mid-bodies into germ cell intercellular bridges. Dev. Biol. 305, 389-396.
77. Grivna, S. T., Pyhtila, B., and Lin, H. (2006). MIWI associates with translational machinery and PIWI-interacting RNAs (piRNAs) in regulating spermatogenesis. Proc. Natl. Acad. Sci. U.S.A. 103, 13415-13420.
78. Hall, E. J. (2002). Lessons we have learned from our children: cancer risks from diagnostic radiology. Pediatr. Radiol. 32, 700-706.
79. Hall, E. J. (2003). The bystander effect. Health Phys. 85,31-35.
80. Hartig, J. V., Tomari, Y., and Forstemann, K. (2007). piRNAs - the ancient hunters of genome invaders. Genes Dev. 21, 1707-1713.
81. He, S., Dunn, K. L., Espino, P. S., Drobic, B., Li, L., Yu, J., et al. (2008). Chromatin organization and nuclear microenvironments in cancer cells. J. Cell. Biochem. 104,2004-2015.
82. Hendrich, B., and Tweedie, S. (2003). The methyl-CpG binding domain and the evolving role of DNA methylation in animals. Trends Genet. 19, 269-277.
83. Hermo, L., Pelletier, R. M., Cyr, D. G., and Smith, C. E. (2010). Surfing the wave, cycle, life history, and genes/proteins expressed by testicular germ cells. Part 1: background to spermatogenesis, spermatogonia, and spermatocytes. Microsc. Res. Tech. 73,241-278.
84. Hess, R. A., Schaeffer, D. J., Eroschenko, V P., and Keen, J. E. (1990). Frequency of the stages in the cycle of the seminiferous epithelium in the rat. Biol. Reprod. 43,517-524.
85. Hildreth, N. G., Shore, R. E., and Dvoretsky, P. M. (1989). The risk of breast cancer after irradiation of the thymus in infancy. N Engl. J. Med. 321, 1281-1284.
86. Hollowell, J. G. Jr., and Littlefield, L. G. (1968). Chromosome damage induced by plasma of x-rayed patients: an indirect effect of x-ray. Proc. Soc. Exp. Biol. Med 129, 240-244.
87. Holstein, A. F., Schulze, W., and Davidoff, M. (2003). Understanding spermatogenesis is a prerequisite for treatment. Reprod. Biol. Endocrinol. 1, 107.
88. Hoyes, K. P., Lord, B. I., McCann, C., Hendry, J. H., and Morris, I. D. (2001). Transgenerational effects of preconception paternal contamination with (55)Fe. Radiat Res, 156(Pt 1), 488-494.
89. Huang, L., Snyder, A. R., and Morgan, W. F. (2003). Radiation-induced genomic instability and its implications for radiation carcinogenesis. Oncogene 22, 5848-5854.
90. Hunter, N. (2008). The RecQ DNA heli-cases: jacks-of-all-trades or master-tradesmen? Cell Res. 18,328-330.
91. Hutvagner, G., and Zamore, P. D. (2002). A microRNA in a multiple-turnover RNAi enzyme complex. Science 297,2056-2060.
92. Hwang, H. W., and Mendell, J. T. (2006). MicroRNAs in cell proliferation, cell death, and tumorigenesis. Br. I Cancer 94, 776-780.
93. Iliakis, G., Wang, Y., Guan, J., and Wang, H. (2003). DNA damage checkpoint control in cells exposed to ionizing radiation. Oncogene 22, 5834-5847.
94. Ilnytskyy, Y., and Kovalchuk, O. (2011). Non-targeted radiation effects-an epigenetic connection. Mutat. Res. 714,113-125.
95. Infante-Rivard, C., Mathonnet, G., and Sinnett, D. (2000). Risk of childhood leukemia associated with diagnostic irradiation and polymorphisms in DNA repair genes. Environ. Health Perspect. 108, 495-498.
96. Itoh, M., Terayama, H., Naito, M., Ogawa, Y., and Tainosho, S. (2005). Tissue microcircumstances for leuko-cytic infiltration into the testis and epididymis in mice. J. Reprod. Immunol. 67, 57-67.
97. Iyer, R., Lehnert, B. E., and Svensson, R. (2000). Factors underlying the cell growth-related bystander responses to alpha particles. Cancer Res. 60, 1290-1298.
98. Jaenisch, R., and Bird, A. (2003). Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat. Genet. 33(Suppl.), 245-254.
99. Jeggo, P. A., and Lobrich, M. (2006). Contribution of DNA repair and cell cycle checkpoint arrest to the maintenance of genomic stability. DNA Repair (Amst) 5, 1192-1198.
100. Jenuwein, T., and Allis, C. D. (2001). Translating the histone code. Science 293,1074-1080.
101. Jirtle, R. L., and Skinner, M. K. (2007). Environmental epigenomics and disease susceptibility. Nat. Rev. Genet. 8, 253-262.
102. Kaplan, M. I., Limoli, C. L., and Morgan, W. E (1997). Perpetuating radiation-induced chromosomal instability. Radiat. Oncol. Investig. 5, 124-128.
103. Kato, Y., Kaneda, M., Hata, K., Kumaki, K., Hisano, M., Kohara, Y., et al. (2007). Role of the Dnmt3 family in de novo methylation of imprinted and repetitive sequences during male germ cell development in the mouse. Hum.Mol. Genet. 16,2272-2280.
104. Kaup, S., Grandjean, V., Mukherjee, R., Kapoor, A., Keyes, E., Seymour, C. B., et al. (2006). Radiation-induced genomic instability is associated with DNA methylation changes in cultured human keratinocytes. Mutat. Res. 597, 87-97.
105. Kelly, R., Bulfield, G., Collick, A., Gibbs, M., and Jeffreys, A. J. (1989). Characterization of a highly unstable mouse minisatellite locus: evidence for somatic mutation during early development. Genomics 5, 844-856.
106. Khan, M. A., Hill, R. P., and Van Dyk, J. (1998). Partial volume rat lung irradiation: an evaluation of early DNA damage. Int. J. Radiat. Oncol. Biol. Phys. 40, 467-476.
107. Khan, M. A., Van Dyk, J., Yeung, I. W., and Hill, R. P. (2003). Partial volume rat lung irradiation; assessment of early DNA damage in different lung regions and effect of radical scavengers. Radiother. Oncol. 66, 95-102.
108. Klattenhoff, C., Bratu, D. P., McGinnis-Schultz, N., Koppetsch, B. S., Cook, H., A., and Theurkauf, W. E. (2007). Drosophila rasiRNA pathway mutations disrupt embryonic axis specification through activation of an ATR/Chk2 DNA damage response. Dev. Cell 12,45-55.
109. Kleinerman, R. A. (2006). Cancer risks following diagnostic and therapeutic radiation exposure in children. Pediatr. Radiol. 36(Suppl 2), 121-125.
110. Klose, R. J., and Bird, A. P. (2006). Genomic DNA methylation: the mark and its mediators. Trends Biochem. Sci. 31,89-97.
111. Kossenko, M. M. (1996). Cancer mortality in the exposed population of the Techa River area. World Health Stat. Q 49,17-21.
112. Koturbash, I., Baker, M., Loree, J., Kutanzi, K., Hudson, D., Pogribny, I., et al. (2006a). Epigenetic dysregulation underlies radiation-induced transgenerational genome instability in vivo. Int. J. Radiat. Oncol. Biol. Phys. 66, 327-330.
113. Koturbash, I., Rugo, R. E., Hendricks, C. A., Loree, J., Thibault, B., Kutanzi, K., et al. (2006b). Irradiation induces DNA damage and modulates epigenetic effectors in distant bystander tissue in vivo. Oncogene 25, 4267-4275.
114. Koturbash, I., Boyko, A., Rodriguez-Juarez, R., McDonald, R. J., Tryndyak, V P., Kovalchuk, I., et al. (2007). Role of epigenetic effectors in maintenance of the long-term persistent bystander effect in spleen in vivo. Carcinogenesis 28, 1831-1838.
115. Koturbash, I., Pogribny, I., and Kovalchuk, O. (2005). Stable loss of global DNA methylation in the radiation-target tissue - a possible mechanism contributing to radiation carcinogenesis? Biochem. Biophys. Res. Commun. 337, 526-533.
116. Kovalchuk, O., and Baulch, J. E. (2008). Epigenetic changes and nontargeted radiation effects - is there a link? Environ. Mol. Mutagen. 49, 16-25.
117. Kuramochi-Miyagawa, S., Kimura, T., Ijiri, T. W., Isobe, T., Asada, N., Fujita, Y., et al. (2004). Mili, a mammalian member of piwi family gene, is essential for spermatogenesis. Development 131, 839-849.
118. Kuramochi-Miyagawa, S., Watanabe, T., Gotoh, K., Totoki, Y., Toyoda, A., Ikawa, M., et al. (2008). DNA methylation of retrotransposon genes is regulated by Piwi family members MILI and MIWI2 in murine fetal testes. Genes Dev. 22, 908-917.
119. Lau, N. C., Seto, A. G., Kim, J., Kuramochi-Miyagawa, S., Nakano, T., Bartel, D. P., etal. (2006). Characterization of the piRNA complex from rat testes. Science 313, 363-367.
120. Lees-Murdock, D. J., De Felici, M., and Walsh, C. P. (2003). Methylation dynamics of repetitive DNA elements in the mouse germ cell lineage. Genomics 82,230-237.
121. Leone, G., Mele, L., Pulsoni, A., Equitani, F., and Pagano, L. (1999). The incidence of secondary leukemias. Haematologica 84, 937-945.
122. Limoli, C. L., Corcoran, J. J., Milligan, J. R., Ward, J. F., and Morgan, W E (1999). Critical target and dose and doserate responses for the induction of chromosomal instability by ionizing radiation. Radiat. Res. 151, 677-685.
123. Limoli, C. L., Ponnaiya, B., Corcoran, J. J., Giedzinski, E., Kaplan, M. I., Hartmann, A., et al. (2000). Genomic instability induced by high and low LET ionizing radiation. Adv. Space Res. 25,2107-2117.
124. Little, J. B. (1998). Radiation-induced genomic instability. Int. J. Radiat. Biol. 74, 663-671.
125. Little, J. B. (1999). Induction of genetic instability by ionizing radiation. C R Acad. Sci. III 322, 127-134.
126. Little, J. B. (2000). Radiation carcinogenesis. Carcinogenesis 21, 397-404.
127. Little, J. B. (2003). Genomic instability and radiation. J. Radiol. Prot. 23, 173-181.
128. Little, J. B. (2006). Cellular radiation effects and the bystander response. Mutat. Res. 597, 113-118.
129. Liu, D., Momoi, H., Li, L., Ishikawa, Y., and Fukumoto, M. (2002). Microsatellite instability in thorotrast-induced human intrahep-atic cholangiocarcinoma. Int. J. Cancer 102,366-371.
130. Liu, Z., Mothersill, C. E., McNeill, E E., Lyng, E M., Byun, S. H., Seymour, C. B., et al. (2006). A dose threshold for a medium transfer bystander effect for a human skin cell line. Radiat. Res. 166(Pt 1), 19-23.
131. Loeb, L. A., Loeb, K. R., and Anderson, J. P. (2003). Multiple mutations and cancer. Proc. Natl. Acad. Sci. U.S.A. 100,776-781.
132. Lord, B. I., Woolford, L. B., Wang, L., McDonald, D., Lorimore, S. A., Stones, V A., et al. (1998). Induction of lympho-haemopoietic malignancy: impact of preconception paternal irradiation. Int. J. Radiat. Biol. 74,721-728.
133. Loree, J., Koturbash, I., Kutanzi, K., Baker, M., Pogribny, I., and Kovalchuk, O. (2006). Radiation-induced molecular changes in rat mammary tissue. possible implications for radiation-induced carcinogenesis. Int. J. Radiat. Biol. 82, 805-815.
134. Lorimore, S. A., Coates, P. J., and Wright, E. G. (2003). Radiation-induced genomic instability and bystander effects: inter-related non-targeted effects of exposure to ionizing radiation. Oncogene 22, 7058-7069.
135. Luning, K. G., Frolen, H., and Nilsson, A. (1976). Genetic effects of 239Pu salt injections in male mice. Mutat. Res. 34, 539-542.
136. Lyng, F. M., Maguire, P., McClean, B., Seymour, C., and Mothersill, C. (2006). The involvement of calcium and MAP kinase signaling pathways in the production of radiation-induced bystander effects. Radiat. Res. 165,400-409.
137. Lyng, F. M., Seymour, C. B., and Mothersill, C. (2000). Production of a signal by irradiated cells which leads to a response in unirradiated cells characteristic of initiation of apoptosis. Br. J. Cancer 83, 1223-1230.
138. Lyng, F. M., Seymour, C. B., and Mothersill, C. (2002). Initiation of apoptosis in cells exposed to medium from the progeny of irradiated cells: a possible mechanism for bystander-induced genomic instability? Radiat. Res. 157,365-370.
139. Lyon, M. F. (1964). The overall rates of dominant and recessive lethal and visible mutation induced by sper-matogonial X-irradiation of mice. Genet. Res. 5, 448-467.
140. Maguire, P., Mothersill, C., McClean, B., Seymour, C., and Lyng, E M. (2007). Modulation of radiation responses by pre-exposure to irradiated cell conditioned medium. Radiat. Res. 167, 485-492.
141. McKinney, P. A., Fear, N. T., Stockton, D., and U. K. C. C. S. Investigators (2003). Parental occupation at peri-conception: findings from the United Kingdom Childhood Cancer Study. Occup. Environ. Med. 60, 901-909.
142. Morgan, W. E (2003a). 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.
143. Morgan, W F. (2003b). 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.
144. Morgan, W F. (2003c). Is there a common mechanism underlying genomic instability, bystander effects and other nontargeted effects of exposure to ionizing radiation? Oncogene 22, 7094-7099.
145. Morgan, W E, and Sowa, M. B. (2005). Effects of ionizing radiation in non-irradiated cells. Proc. Natl. Acad. Sci. U.SA. 102, 14127-14128.
146. Morimura, K., Romanenko, A., Min, W., Salim, E. I., Kinoshita, A., Wanibuchi, H., et al. (2004). Possible distinct molecular carcinogenic pathways for bladder cancer in Ukraine, before and after the Chernobyl disaster. Oncol. Rep. 11,881-886.
147. Mothersill, C., and Seymour, C. B. (2004). Radiation-induced bystander effects - implications for cancer. Nat. Rev. Cancer 4,158-164.
148. Mothersill, C., Smith, R. W., Agnihotri, N., and Seymour, C. B. (2007). Characterization of a radiation-induced stress response communicated in vivo between zebrafish. Environ. Sci. Tech-nol. 41, 3382-3387.
149. Mruk, D. D., and Cheng, C. Y (2004). Sertoli-Sertoli and Sertoli-germ cell interactions and their significance in germ cell movement in the seminiferous epithelium during spermatogen-esis. Endocr. Rev. 25, 747-806.
150. Murphy, J. B., and Morton, J. (1915). Action of serum from X-rayed animals on lymphoid cells in vitro. J. Exp.Med. XXii,800.
151. Murphy, J. B., Liu, J. H., and Sturm, E. (1922). Studies on x-ray effects: Ix. The action of serum from x-rayed animals on lymphoid cells in vitro. J. Exp. Med. 35, 373-384.
152. Nagar, S., Smith, L. E., and Morgan, W. F. (2003). Characterization of a novel epigenetic effect of ionizing radiation: the death-inducing effect. Cancer Res. 63, 324-328.
153. Nagasawa, H., and Little, J. B. (1992). Induction of sister chromatid exchanges by extremely low doses of alpha-particles. Cancer Res. 52, 6394-6396.
154. Nomura, T. (1982). Parental exposure to x rays and chemicals induces heritable tumours and anomalies in mice. Nature 296, 575-577.
155. Nomura, T. (1993). Leukemia in children whose parents have been exposed to radiation. BMJ 306,1412.
156. Nomura, T. (2003). Transgenera-tional carcinogenesis: induction and transmission of genetic alterations and mechanisms of carcinogenesis. Mu tat. Res. 544, 425-432.
157. Nomura, T. (2006). Transgenerational effects of radiation and chemicals in mice and humans. J. Radiat. Res. 47, B83-B97.
158. Nomura, T. (2008). Transgenerational effects from exposure to environmental toxic substances. Mutat. Res. 659, 185-193.
159. Pant, G. S., and Kamada, N. (1977). Chromosome aberrations in normal leukocytes induced by the plasma of exposed individuals. Hiroshima J. Med. Sci. 26, 149-154.
160. Paquette, B., and Little, J. B. (1994). In vivo enhancement of genomic instability in minisatellite sequences of mouse C3H/10T1/2 cells transformed in vitro by X-rays. Cancer Res. 54,3173-3178.
161. Parreira, G. G., Melo, R. C., and Russell, L. D. (2002). Relationship of sertoli-sertoli tight junctions to ectoplasmic specialization in conventional and en face views. Biol Reprod. 67, 1232-1241.
162. Parsons, W. B. Jr., Watkins, C. H., Pease, G. L., and Childs, D. S. Jr. (1954). Changes in sternal marrow following roentgen-ray therapy to the spleen in chronic granulocytic leukemia. Cancer7, 179-189.
163. Penttila, T. L., Yuan, L., Mali, P., Hoog, C., and Parvinen, M. (1995). Haploid gene expression: temporal onset and storage patterns of 13 novel transcripts during rat and mouse spermiogenesis. Biol. Reprod. 53, 499-510.
164. Persaud, R., Zhou, H., Baker, S. E., Hei, T. K., and Hall, E. J. (2005). Assessment of low linear energy transfer radiation-induced bystander mutagenesis in a three-dimensional culture model. Cancer Res. 65, 9876- 9882.
165. Petersen, C., and Soder, O. (2006). The sertoli cell - a hormonal target and 'super' nurse for germ cells that determines testicular size. Horm. Res. 66, 153-161.
166. Pilch, D. R., Sedelnikova, O. A., Redon, C., Celeste, A., Nussenzweig, A., and Bonner, W. M. (2003). Characteristics of gamma-H2AX foci at DNA double-strand breaks sites. Biochem. Cell Biol. 81, 123-129.
167. Pils, S., Muller, W. U., and Streffer, C. (1999). Lethal and teratogenic effects in two successive generations of the HLG mouse strain after radiation exposure of zygotes - association with genomic instability? Mutat. Res. 429,85-92.
168. Pogribny, I., Koturbash, I., Tryndyak, V., Hudson, D., Stevenson, S. M., Sedelnikova, O., et al. (2005). Fractionated low-dose radiation exposure leads to accumulation of DNA damage and profound alterations in DNA and histone methylation in the murine thymus. Mol. Cancer Res. 3, 553-561.
169. Pogribny, I., Raiche, J., Slovack, M., and Kovalchuk, O. (2004). Dose-dependence, sexand tissue-specificity, and persistence of radiation-induced genomic DNA methylation changes. Biochem. Bio-phys. Res. Commun. 320, 1253-1261.
170. Pollack, A., Zagars, G. K., Smith, L. G., Lee, J. J., von Eschenbach, A. C., Antolak, J. A., et al. (2000). Preliminary results of a randomized radiotherapy dose-escalation study comparing 70 Gy with 78 Gy for prostate cancer. J. Clin. Oncol. 18,3904-3911.
171. Powell, S. N., and Kachnic, L. A. (2003). Roles of BRCA1 and BRCA2 in homologous recombination, DNA replication fidelity and the cellular response to ionizing radiation. Oncogene 22, 5784-5791.
172. Preston-Martin, S., Thomas, D. C., Yu, M. C., and Henderson, B. E. (1989). Diagnostic radiography as a risk factor for chronic myeloid and monocytic leukaemia (CML). Br. J. Cancer 59, 639-644.
173. Prysyazhnyuk, A., Gristchenko, V., Fedorenko, Z., Gulak, L., Fuzik, M., Slipenyuk, K., et al. (2007). Twenty years after the Chernobyl accident: solid cancer incidence in various groups of the Ukrainian population. Radiat. Environ. Biophys. 46, 43-51.
174. Pukkala, E., Kesminiene, A., Poliakov, S., Ryzhov, A., Drozdovitch, V., Kovgan, L., et al. (2006). Breast cancer in Belarus and Ukraine after the Chernobyl accident. Int. J. Cancer, 119, 651-658.
175. Raiche, J., Rodriguez-Juarez, R., Pogribny, I., and Kovalchuk, O. (2004). Sexand tissue-specific expression of maintenance and de novo DNA methyltransferases upon low dose X-irradiation in mice. Biochem. Biophys. Res. Commun. 325, 39-47.
176. Randers-Pehrson, G., Geard, C. R., Johnson, G., Elliston, C. D., and Brenner, D. J. (2001). The Columbia University singleion microbeam. Radiat. Res. 156,210-214.
177. Robertson, K. D. (2001). DNA methylation, methyltransferases, and cancer. Oncogene 20, 3139-3155.
178. Robertson, K. D. (2002). DNA methylation and chromatin - unraveling the tangled web. Oncogene 21, 5361- 5379.
179. ;UTR-directed primary piRNAs. Curr. Biol. 19,2066-2076.
180. Robison, L. L., and Mertens, A. (1993). Second tumors after treatment of childhood malignancies. Hematol. Oncol. Clin North Am. 7, 401-415.
181. Rodemann, H. P., and Blaese, M. A. (2007). Responses of normal cells to ionizing radiation. Semin. Radiat. Oncol. 17,81-88.
182. Rodriguez, A., Griffiths-Jones, S., Ashurst, J. L., and Bradley, A. (2004). Identification of mammalian microRNA host genes and transcription units. Genome Res. 14, 1902-1910.
183. Rogakou, E. P., Pilch, D. R., Orr, A. H., Ivanova, V. S., and Bonner, W. M. (1998). DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J. Biol. Chem. 273, 5858-5868.
184. Roman, E., Doyle, P., Maconochie, N., Davies, G., Smith, P. G., and Beral, V. (1999). Cancer in children of nuclear industry employees: report on children aged under 25 years from nuclear industry family study. BMJ 318,1443-1450.
185. Romanenko, A., Morell-Quadreny, L., Nepomnyaschy, V., Vozianov, A., and Llombart-Bosch, A. (2000). Pathology and proliferative activity of renal-cell carcinomas (RCCS) and renal oncocytomas in patients with different radiation exposure after the Chernobyl accident in Ukraine. Int. J. Cancer. 87, 880-883.
186. Roof, K. S., Fidias, P., Lynch, T. J., Ancukiewicz, M., and Choi, N. C. (2003). Radiation dose escalation in limited-stage small-cell lung cancer. Int. J. Radiat. Oncol. Biol. Phys. 57, 701-708.
187. Rountree, M. R., Bachman, K. E., Herman, J. G., and Baylin, S. B. (2001). DNA methylation, chromatin inheritance, and cancer. Oncogene 20, 3156-3165.
188. Saha, A., Wittmeyer, J., and Cairns, B. R. (2006). Chromatin remodelling: the industrial revolution of DNA around histones. Nat. Rev. Mol. Cell Biol. 7, 437-447.
189. Salomaa, S., Lindholm, C., Tankimanova, M. K., Mamyrbaeva, Z., Koivistoinen, A., Hulten, M., et al. (2002). Stable chromosome aberrations in the lymphocytes of a population living in the vicinity of the Semi-palatinsk nuclear test site. Radiat. Res. 158,591-596.
190. Sanders, S. L., Portoso, M., Mata, J., Bahler, J., Allshire, R. C., and Kouzarides, T. (2004). Methylation of histone H4 lysine 20 controls recruitment of Crb2 to sites of DNA damage. Cell 119,603-614.
191. Sedelnikova, O. A., Nakamura, A., Kovalchuk, O., Koturbash, I., Mitchell, S. A., Marino, S. A., et al. (2007). DNA double-strand breaks form in bystander cells after microbeam irradiation of three-dimensional human tissue models. Cancer Res. 67, 4295-4302.
192. Sedelnikova, O. A., Pilch, D. R., Redon, C., and Bonner, W. M. (2003). Histone H2AX in DNA damage and repair. Cancer Biol. Ther. 2, 233-235.
193. Seto, A. G., Kingston, R. E., and Lau, N. C. (2007). The coming of age for Piwi proteins. Mol. Cell 26, 603-609.
194. Shao, C., Furusawa, Y., Aoki, M., and Ando, K. (2003). Role of gap junctional intercellular communication in radiation-induced bystander effects in human fibroblasts. Radiat. Res. 160,318-323.
195. Shelby, M. D. (1996). Selecting chemicals and assays for assessing mammalian germ cell mutagenicity. Mutat. Res. 352, 159-167.
196. Shilnikova, N. S., Preston, D. L., Ron, E., Gilbert, E. S., Vassilenko, E. K., Romanov, S. A., et al. (2003). Cancer mortality risk among workers at the Mayak nuclear complex. Radiat. Res. 159,787-798.
197. Shiono, P. H., Chung, C. S., and Myrianthopoulos, N. C. (1980). Preconception radiation, intrauterine diagnostic radiation, and childhood neoplasia. J. Natl. Cancer Inst. 65, 681-686.
198. Shivdasani, R. A. (2006). Micro RNAs regulators of gene expression and cell differentiation. Blood 108, 3646-3653.
199. Shu, X. O., Gao, Y. T., Brinton, L. A., Linet, M. S., Tu, J. T., Zheng, W., et al. (1988). A population-based case-control study of childhood leukemia in Shanghai. Cancer 62, 635-644.
200. Shu, X. O., Potter, J. D., Linet, M. S., Severson, R. K., Han, D., Kersey, J. H., et al. (2002). Diagnostic X-rays and ultrasound exposure and risk of childhood acute lymphoblastic leukemia by immunophenotype. Cancer Epidemiol. Biomarkers Prev. 11,177-185.
201. Sowa, M., Arthurs, B. J., Estes, B. J., and Morgan, W. E (2006). Effects of ionizing radiation on cellular structures, induced instability and carcinogenesis. EXS 96,293-301.
202. Sugimoto, K., Kage, H., Aki, N., Sano, A., Kitagawa, H., Nagase, T., et al. (2007). The induction of H3K9 methylation by PIWIL4 at the p16Ink4a locus. Biochem. Biophys. Res. Commun. 359,497-502.
203. Suzuki, M., and Tsuruoka, C. (2004). Heavy charged particles produce a bystander effect via cell-cell junctions. Biol. Sci. Space 18,241-246.
204. Suzuki, M., Zhou, H., Hei, T. K., Tsuruoka, C., and Fujitaka, K. (2003). Induction of a bystander chromosomal damage of Heion microbeams in mammalian cells. Biol. Sci. Space 17,251-252.
205. Tamminga, J., Kathiria, P., Koturbash, I., and Kovalchuk, O. (2008a). DNA damage-induced upregulation of miR-709 in the germline downregulates BORIS to counteract aberrant DNA hypomethylation. Cell Cycle 7, 3731-3736.
206. Tamminga, J., Koturbash, I., Baker, M., Kutanzi, K., Kathiria, P., Pogribny, I. P., et al. (2008b). Paternal cranial irradiation induces distant bystander DNA damage in the germline and leads to epigenetic alterations in the offspring. Cell Cycle 7,1238-1245.
207. Tanaka, K., Iida, S., Takeichi, N., Chaizhunusova, N. J., Gusev, B. I., Apsalikov, K. N., et al. (2006). Unstable-type chromosome aberrations in lymphocytes from individuals living near Semipalatinsk nuclear test site. J. Radiat. Res. 47(Suppl. A), A159-A164.
208. Thomson, T., and Lin, H. (2009). The biogenesis and function of PIWI proteins and piRNAs: progress and prospect. Annu. Rev. Cell Dev. Biol. 25, 355-376.
209. Tryndyak, V. P., Kovalchuk, O., and Pogribny, I. P. (2006). Loss of DNA methylation and histone H4 lysine 20 trimethylation in human breast cancer cells is associated with aberrant expression of DNA methyltransferase 1, Suv4-20h2 histone methyltransferase and methyl-binding proteins. Cancer Biol. Ther. 5, 65-70.
210. Unhavaithaya, Y., Hao, Y., Beyret, E., Yin, H., Kuramochi-Miyagawa, S., Nakano, T., et al. (2009). MILI, a PIWI-interacting RNA-binding protein, is required for germ line stem cell self-renewal and appears to positively regulate translation. J. Biol. Chem. 284,6507-6519.
211. Vagin, V. V., Sigova, A., Li, C., Seitz, H., Gvozdev, V., and Zamore, P. D. (2006). A distinct small RNA pathway silences selfish genetic elements in the germline. Science 313, 320-324.
212. Valerie, K., Yacoub, A., Hagan, M. P., Curiel, D. T., Fisher, P. B., Grant, S., et al. (2007). Radiation-induced cell signaling: inside-out and outside-in. Mol. Cancer Ther. 6, 789-801.
213. Volinia, S., Calin, G.A.,Liu, C. G.,Ambs, S., Cimmino, A., Petrocca, F., et al. (2006). A microRNA expression signature of human solid tumors defines cancer gene targets. Proc. Natl. Acad. Sci. U.S.A. 103,2257-2261.
214. Wakabayashi, T., Kato, H., Ikeda, T., and Schull, W. J. (1983). Studies of the mortality of A-bomb survivors, report 7. Part III. incidence of cancer in 1959-1978, based on the tumor registry, Nagasaki. Radiat. Res. 93, 112-146.
215. Ward, J. E (1995). Radiation mutagenesis: the initial DNA lesions responsible. Radiat. Res. 142, 362-368.
216. Watanabe, S., Shimosato, Y., Okita, T., Ezaki, H., and Shigemitsu, T. (1972). Leukemia and thyroid carcinoma found among A-bomb survivors in Hiroshima. Recent Results Cancer Res. 39, 57-83.
217. Watson, G. E., Lorimore, S. A., Clutton, S. M., Kadhim, M. A., and Wright, E. G. (1997). Genetic factors influencing alpha-particle-induced chromosomal instability. Int. J. Radiat. Biol. 71,497-503.
218. Weber, M., and Schubeler, D. (2007). Genomic patterns of DNA methylation: targets and function of an epigenetic mark. Curr. Opin. Cell Biol. 19,273-280.
219. Weidman, J. R., Dolinoy, D. C., Murphy, S. K., and Jirtle, R. L. (2007). Cancer susceptibility: epigenetic manifestation of environmental exposures. Cancer J. 13,9-16.
220. Wiemer, E. A. (2007). The role of microRNAs in cancer: no small matter. Eur. I Cancer 43, 1529-1544.
221. Wiley, L. M., Baulch, J. E., Raabe, O. G., and Straume, T. (1997). Impaired cell proliferation in mice that persists across at least two generations after paternal irradiation. Radiat. Res. 148, 145-151.
222. Witt, K. L., and Bishop, J. B. (1996). Mutagenicity of anticancer drugs in mammalian germ cells. Mutat. Res. 355,209-234.
223. Wright, E. G., and Coates, P. J. (2006). Untargeted effects of ionizing radiation: implications for radiation pathology. Mutat. Res. 597,119-132.
224. Wu, L. J., Randers-Pehrson, G., Xu, A., Waldren, C. A., Geard, C. R., Yu, Z., et al. (1999). Targeted cytoplasmic irradiation with alpha particles induces mutations in mammalian cells. Proc. Natl. Acad. Sci. U.S.A. 96, 4959-4964.
225. Xu, G. L., Bestor, T. H., Bourc'his, D., Hsieh, C. L., Tommerup, N., Bugge, M., et al. (1999). Chromosome instability and immunodeficiency syndrome caused by mutations in a DNA methyltransferase gene. Nature 402, 187-191.
226. Yang, H., Asaad, N., and Held, K. D. (2005a). Medium-mediated intercellular communication is involved in bystander responses of X-ray-irradiated normal human fibroblasts. Oncogene 24, 2096-2103.
227. Yang, J., Medvedev, S., Reddi, P. P., Schultz, R. M., and Hecht, N. B. (2005b). The DNA/RNA-binding protein MSY2 marks specific transcripts for cytoplasmic storage in mouse male germ cells. Proc. Natl. Acad. Sci. U.S.A. 102, 1513-1518.
228. Yauk, C., Polyzos, A., Rowan-Carroll, A., Somers, C. M., Godschalk, R. W., Van Schooten, F. J., et al. (2008). Germ-line mutations, DNA damage, and global hypermethylation in mice exposed to particulate air pollution in an urban/industrial location. Proc. Natl. Acad. Sci. U.S.A. 105, 605-610.
229. Yekta, S., Shih, I. H., and Bartel, D. P. (2004). MicroRNA-directed cleavage of HOXB8 mRNA. Science 304, 594-596.
230. Yu, F., Zingler, N., Schumann, G., and Stratling, W H. (2001). Methyl-CpG-binding protein 2 represses LINE-1 expression and retrotransposition but not Alu transcription. Nucleic Acids Res. 29,4493-4501.
231. Yu, Z., Guo, R., Ge, Y., Ma, J., Guan, J., Li, S., et al. (2003). Gene expression profiles in different stages of mouse spermatogenic cells during spermatogenesis. Biol. Reprod. 69, 37-47.
232. Zeng, Y. (2006). Principles of microRNA production and maturation. Oncogene 25, 6156-6162.
233. Zhou, H., Suzuki, M., Geard, C. R., and Hei, T. K. (2002). Effects of irradiated medium with or without cells on bystander cell responses. Mutat. Res. 499,135-141.