Vol. 5, No. 10, p. 577-588 - Aug. 31, 2018
Assessment of pesticide residue on cocoa beans in Ondo State, Nigeria
Joseph O. Akinneye




Abstract
Effects of radiation in biological systems are quite interesting. Interaction of radiation to epigenetic mechanisms has been also demonstrated earlier. The aim of this review is to sketch a current scenario on radiation exposure/insults on the epigenetic mechanisms in mammalian cells. Evidence from the databases, mainly from Pubmed and Science Direct were considered. Findings suggest that radiation has a dose and time-dependent effect in our body. Cells and tissues from different sources have differential responses towards radiation insults. Although radiation has impacts on epigenetic modulation, but it has beneficial combinatorial effects with a number of epigenetic modalities. Radiation has both bad and good impacts on epigenetic mechanisms.
Keywords
Radiation; Epigenetics; Combined therapy; Cancer.
DOI
10.21472/bjbs.051032
Full text
PDF
References
Abdelfatah, E.; Kerner, Z.; Nanda, N.; Ahuja, N. Epigenetic therapy in gastrointestinal cancer: The right
combination. Ther. Adv. Gastroenterol., v. 9, p. 560-579, 2016. https://doi.org/10.1177/1756283X16644247
Amendola, P. G.; Zaghet, N.; Ramalho, J. J.; Johansen, J. V.; Boxem, M.; Salcini, A. E. JMJD-5/KDM8
regulates H3K36me2 and is required for late steps of homologous recombination and genome integrity.
PLoS Genet., v. 13, e1006632, 2017. https://doi.org/10.1371/journal.pgen.1006632
An, Y. S.; Kim, M. R.; Lee, S. S.; Lee, Y. S.; Chung, E.; Song, J. Y.; Lee, J.; Yi, J. Y. TGF-β
signaling plays an important role in resisting γ-irradiation. Exp. Cell Res., v. 319,
p. 466-473, 2013.
Bar-Sela, G.; Jacobs, K. M.; Gius, D. Histone deacetylase inhibitor and demethylating agent chromatin
compaction and the radiation response by cancer cells. Cancer J., v. 13, p. 65-69, 2007.
Belinsky, S. A.; Klinge, D. M.; Liechty, K. C.; March, T. H.; Kang, T.; Gilliland, F. D.; Sotnic, N.;
Adamova, G.; Rusinova, G.; Telnov, V. Plutonium targets the p16 gene for inactivation by promoter
hypermethylation in human lung adenocarcinoma. Carcinogenesis, v. 25, p. 1063-1067, 2004.
Biade, S.; Stobbe, C. C.; Boyd, J. T.; Chapman, J. D. Chemical agents that promote chromatin compaction
radiosensitize tumour cells. Int. J. Rad. Biol., v. 77, p. 1033-1042, 2001.
Boerma, M.; Sridharan, V.; Mao, X. W.; Nelson, G. A.; Cheema, A. K.; Koturbash, I.; Singh, S. P.; Tackett,
A. J.; Hauer-Jensen, M. Effects of ionizing radiation on the heart. Mutat. Res.-Rev. Mutat., v. 770,
p. 319-327, 2016.
Burk, U.; Schubert, J.; Wellner, U.; Schmalhofer, O.; Vincan, E.; Spaderna, S.; Brabletz, T. A reciprocal
repression between ZEB1 and members of the miR-200 family promotes EMT and invasion in cancer cells.
EMBO Rep., v. 9, p. 582-589, 2008. https://doi.org/10.1038/embor.2008.74
Bussing, I.; Slack, F. J.; Grosshans, H. Let-7 microRNAs in development, stem cells and cancer. Trends
Mol. Med., v. 14, p. 400-409, 2008.
Chaudhry, M. A.; Omaruddin, R. A. Differential DNA methylation alterations in radiation-sensitive and
-resistant cells. DNA Cell Biol., v. 31, p. 908-916, 2012. https://doi.org/10.1089/dna.2011.1509
Dahle, J.; Kvam, E. Induction of delayed mutations and chromosomal instability in fibroblasts after
UVA-, UVB-, and X-radiation. Cancer Res., v. 63, p. 1464-1469, 2003.
Deng, S.; Calin, G. A.; Croce, C. M.; Coukos, G.; Zhang, L. Mechanisms of microRNA deregulation in human
cancer. Cell Cycle, v. 7, p. 2643-2646, 2008.
Dent, P.; Yacoub, A.; Fisher, P. B.; Hagan, M. P.; Grant, S. MAPK pathways in radiation responses.
Oncogene, v. 22, p. 5885-5896, 2003.
Dickey, J. S.; Zemp, F. J.; Martin, O. A.; Kovalchuk, O. The role of miRNA in the direct and indirect
effects of ionizing radiation. Radiat. Environ. Biophys., v. 50, p. 491-499, 2011.
Engels, B. M.; Hutvagner, G. Principles and effects of microRNA-mediated post-transcriptional gene
regulation. Oncogene, v. 25, p. 6163-6169, 2006.
Espada, J.; Esteller, M. Epigenetic control of nuclear architecture. Cell Mol. Life Sci., v. 64,
p. 449-457, 2007.
Fokas, E.; Yoshimura, M.; Prevo, R.; Higgins, G.; Hackl, W.; Maira, S. M.; Bernhard, E. J.; McKenna, W. G.;
Muschel, R. J. NVP-BEZ235 and NVP-BGT226, dual phosphatidylinositol 3-kinase/mammalian target of rapamycin
inhibitors, enhance tumor and endothelial cell radiosensitivity. Radiat. Oncol., 7:48, 2012.
Ghosh, S. P.; Singh, R.; Chakraborty, K.; Kulkarni, S.; Uppal, A.; Luo, Y.; Kaur, P.; Pathak, R.; Kumar,
K. S.; Hauer-Jensen, M.; Cheema, A. K. Metabolomic changes in gastrointestinal tissues after whole body
radiation in a murine model. Mol. Biosyst., v. 9, p. 723-731, 2013.
Gravina, G. L.; Festuccia, C.; Marampon, F.; Popov, V. M.; Pestell, R. G.; Zani, B. M.; Tombolini, V.
Biological rationale for the use of DNA methyltransferase inhibitors as new strategy for modulation of
tumor response to chemotherapy and radiation. Molec. Cancer, 9:305, 2010.
Grelier, G.; Voirin, N.; Ay, A. S.; Cox, D. G.; Chabaud, S.; Treilleux, I.; Léon-Goddard, S.;
Rimokh, R.; Mikaelian, I.; Venoux, C.; Puisieux, A.; Lasset, C.; Moyret-Lalle, C. Prognostic value of
Dicer expression in human breast cancers and association with the mesenchymal phenotype. Br. J.
Cancer, v. 101, no. 4, p. 673-683, 2009.
Guo, X.; Liao, Q.; Chen, P.; Li, X.; Xiong, W.; Ma, J.; Li, X.; Luo, Z.; Tang, H.; Deng, M.; Zheng, Y.;
Wang, R.; Zhang, W.; Li. G. The microRNA-processing enzymes: Drosha and Dicer can predict prognosis of
nasopharyngeal carcinoma. J. Cancer Res. Clin. Oncol., v. 138, p. 49-56, 2012. https://doi.org/10.1007/s00432-011-1058-1
Hall, E.; Giaccia, A. Radiobiology for the radiologist. 7. ed. Philadelphia: Lippincott Williams
and Wilkins, 2011.
Ilnytskyy, Y.; Zemp, F. J.; Koturbash, I.; Kovalchuk, O. Altered microRNA expression patterns in irradiated
hematopoietic tissues suggest a sex-specific protective mechanism. Biochem. Biophys. Res. Commun.,
v. 377, p. 41-45, 2008.
Jaklevic, B.; Uyetake, L.; Wichmann, A.; Bilak, A.; English, C. N.; Su, T. T. Modulation of ionizing
radiation-induced apoptosis by bantam microRNA in Drosophila. Develop. Biol., v. 320,
p. 122-130, 2008.
Johnson, S. M.; Grosshans, H.; Shingara, J.; Byrom, M.; Jarvis, R.; Cheng, A.; Labourier, E.; Reinert,
K. L.; Brown, D.; Slack, F. J. RAS is regulated by the let-7 microRNA family. Cell, v. 120,
p. 635-647, 2005.
Joiner, M. C.; Lambin, P.; Malaise, E. P.; Robson, T.; Arrand, J. E.; Skov, K. A.; Marples, B.
Hypersensitivity to very-low single radiation doses: Its relationship to the adaptive response and
induced radioresistance. Mutat. Res., v. 358, p. 171-183, 1996.
Jones, P. A. Functions of DNA methylation: Islands, start sites, gene bodies and beyond. Nat. Rev.
Genet., v. 13, p. 484-492, 2012.
Kalinich, J. F.; Catravas, G. N.; Snyder, S. L. The effect of γ-radiation on DNA methylation.
Radiat. Res., v. 117, p. 185-197, 1989.
Karube, Y.; Tanaka, H.; Osada, H.; Tomida, S.; Tatematsu, Y.; Yanagisawa, K.; Yatabe, Y.; Takamizawa,
J.; Miyoshi, S.; Mitsudomi, T.; Takahashi T. Reduced expression of Dicer associated with poor prognosis
in lung cancer patients. Cancer Sci., v. 96, p. 111-115, 2005.
Kim, G. J.; Fiskum, G. M.; Morgan, W. F. A role for mitochondrial dysfunction in perpetuating
radiation-induced genomic instability. Cancer Res., v. 66, p. 10377-10383, 2006.
Koturbash, I.; Boyko, A.; Rodriguez-Juarez, R.; McDonald, R. J.; Tryndyak, V. P.; Kovalchuk, I.;
Pogribny, I. P.; Kovalchuk, O. Role of epigenetic effectors in maintenance of the long-term
persistent bystander effect in spleen in vivo. Carcinogenesis, v. 28, p. 1831-1838,
2007.
Koturbash, I.; Miousse, I. R.; Sridharan, V.; Nzabarushimana, E.; Skinner, C. M.; Melnyk, S. B.;
Pavliv, O.; Hauer-Jensen, M.; Nelson, G. A.; Boerma, M. Radiation-induced changes in DNA methylation
of repetitive elements in the mouse heart. Mutat. Res.-Fund. Mol. M., v. 787, p. 43-53, 2016.
Koturbash, I.; Pogribny, I.; Kovalchuk, O. Stable loss of global DNA methylation in the radiation-target
tissue: A possible mechanism contributing to radiation carcinogenesis? Biochem. Bioph. Res. Co.,
v. 337, p. 526-533, 2005.
Koturbash, I.; Zemp, F.; Kolb, B.; Kovalchuk, O. Sex-specific radiation-induced microRNAome responses in
the hippocampus, cerebellum and frontal cortex in a mouse model. Mutat. Res., v. 722, p. 114-118,
2011.
Kovalchuk, O.; Burke, P.; Besplug, J.; Slovack, M.; Filkowski, J.; Pogribny, I. Methylation changes in
muscle and liver tissues of male and female mice exposed to acute and chronic low-dose X-ray-irradiation.
Mutat. Res., v. 548, p. 75-84, 2004.
Kraemer, A.; Anastasov, N.; Angermeier, M.; Winkler, K.; Atkinson, M. J.; Moertl, S. MicroRNA-mediated
processes are essential for the cellular radiation response. Radiat. Res., v. 176, p. 575-586,
2011.
Kumar, M. S.; Pester, R. E.; Chen, C. Y.; Lane, K.; Chin, C.; Lu, J.; Kirsch, D. G.; Golub, T. R.; Jacks,
T. Dicer1 functions as a haploinsufficient tumor suppressor. Genes Dev., v. 23, p. 2700-2704, 2009.
https://doi.org/10.1101/gad.1848209
Kutanzi, K. R.; Lumen, A.; Koturbash, I.; Miousse, I. R. Pediatric exposures to ionizing radiation:
Carcinogenic considerations. Int. J. Env. Res. Pub. Health, v. 13, no. 11, p. 1057, 2016.
https://doi.org/10.3390/ijerph13111057
Lee, K.-F.; Chen, Y.-C.; Hsu, P. W.-C.; Liu, I. Y.; Wu, L. S.-H. MicroRNA expression profiling altered
by variant dosage of radiation exposure. BioMed Res. Int., v. 2014, Article ID 456323, 10 p., 2014.
https://doi.org/10.1155/2014/456323
Lin, R. J.; Lin, Y. C.; Chen, J.; Kuo, H. H.; Chen, Y. Y.; Diccianni, M. B.; London, W. B.; Chang, C. H.;
Yu, A. L. MicroRNA signature and expression of Dicer and Drosha can predict prognosis and delineate risk
groups in neuroblastoma. Cancer Res., v. 70, p. 7841-7850, 2010. https://doi.org/10.1158/0008-5472.CAN-10-0970
Luzhna, L.; Kovalchuk, O. Modulation of DNA methylation levels sensitizes doxorubicin-resistant breast
adenocarcinoma cells to radiation-induced apoptosis. Biochem. Biophys. Res. Commun., v. 392,
p. 113-117, 2010. https://doi.org/10.1016/j.bbrc.2009.12.093
Ma, S.; Liu, X.; Jiao, B.; Yang, Y.; Liu, X. Low-dose radiation-induced responses: Focusing on epigenetic
regulation. Int. J. Radiat. Biol., v. 86, p. 517-528, 2010. https://doi.org/10.3109/09553001003734592
Mailand, N.; Bekker-Jensen, S.; Faustrup, H.; Melander, F.; Bartek, J.; Lukas, C.; Lukas, J. RNF8 ubiquitylates
histones at DNA double-strand breaks and promotes assembly of repair proteins. Cell, v. 131, p. 887-900,
2007.
Marta, G. N.; Garicochea, B.; Carvalho, A. L.; Real, J. M.; Kowalski, L. P. MicroRNAs, cancer and ionizing
radiation: Where are we? Rev. Assoc. Med. Bras., v. 61, p. 275-281, 2015. https://doi.org/10.1590/1806-9282.61.03.275
Martello, G.; Rosato, A.; Ferrari, F.; Manfrin, A.; Cordenonsi, M.; Dupont, S.; Enzo, E.; Guzzardo, V.;
Rondina, M.; Spruce, T.; Parenti, A. R.; Daidone, M. G.; Bicciato, S.; Piccolo, S. A MicroRNA targeting
dicer for metastasis control. Cell, v. 141, p. 1195-1207, 2010. https://doi.org/10.1016/j.cell.2010.05.017
Maxwell, C. A.; Fleisch, M. C.; Costes, S. V.; Erickson, A. C.; Boissiere, A.; Gupta, R.; Ravani, S. A.;
Parvin, B.; Barcellos-Hoff, M. H. Targeted and non-targeted effects of ionizing radiation that impact
genomic instability. Cancer Res., v. 68, p. 8304-8311, 2008.
Miousse, I. R.; Shao, L.; Chang, J.; Feng, W.; Wang, Y.; Allen, A. R.; Turner, J.; Stewart, B.; Raber,
J.; Zhou, D.; Koturbash, I. Exposure to low-dose Fe-56-ion radiation induces long-term epigenetic
alterations in mouse bone marrow hematopoietic progenitor and stem cells. Radiat. Res., v. 182,
p. 92-101, 2014.
Miousse, I. R.; Tobacyk, J.; Melnyk, S.; James, S. J.; Cheema, A. K.; Boerma, M.; Hauer-Jensen, M.;
Koturbash, I. One-carbon metabolism and ionizing radiation: A multifaceted interaction. Bio. Mol.
Concepts, v. 8, p. 83-92, 2017.
Mott, J. L.; Kurita, S.; Cazanave, S. C.; Bronk, S. F.; Werneburg, N. W.; Fernandez-Zapico, M. E.
Transcriptional suppression of mir-29b-1/mir-29a promoter by c-Myc, hedgehog, and NF-kappaB. J.
Cell Biochem., v. 110, p. 1155-1164, 2010
Pfeifer, G. P.; Rauch, T. A. DNA methylation patterns in lung carcinomas. Semin. Cancer Biol.,
v. 19, p. 181-187, 2009.
Piovan, C.; Palmieri, D.; Di Leva, G.; Braccioli, L.; Casalini, P.; Nuovo, G.; Tortoreto, M.; Sasso, M.;
Plantamura, I.; Triulzi, T.; Taccioli, C.; Tagliabue, E.; Iorio, M. V.; Croce, C. M. Oncosuppressive role
of p53-induced miR-205 in triple negative breast cancer. Mol. Oncol., v. 6, p. 458-472, 2012.
Pogrlbny, I.; Koturbash, I.; Tryndyak, V.; Hudson, D.; Stevenson, S. M. L.; Sedelnikova, O.; Bonner, W.;
Kovalchuk, O. 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., v. 3, p. 553-561,
2005.
Pollack, B. P.; Sapkota, B.; Boss, J. M. Ultraviolet radiationinduced transcription is associated with
gene-specific histone acetylation. Photochem. Photobiol., v. 85, p. 652-662, 2009.
Prior, S.; Miousse, I. R.; Nzabarushimana, E.; Pathak, R.; Skinner, C.; Kutanzi, K. R.; Allen, A. R.;
Raber, J.; Tackett, A. J.; Hauer-Jensen, M.; Nelson, G. A.; Koturbash, I. Densely ionizing radiation
affects DNA methylation of selective LINE-1 elements. Environ. Res., v. 150, p. 470-481, 2016.
Qiu, H.; Yashiro, M.; Shinto, O.; Matsuzaki, T.; Hirakawa, K. DNA methyltransferase inhibitor
5-aza-CdR enhances the radiosensitivity of gastric cancer cells. Cancer Sci., v. 1,
p. 181-188, 2009.
Ree, A.; Dueland, S.; Folkvord, S.; Hole, K.; Seierstad, T.; Johansen, M.; Abrahamsen, T. W.; Flatmark, K.
Vorinostat, a histone deacetylase inhibitor, combined with pelvic palliative radiotherapy for gastrointestinal
carcinoma: the pelvic radiation and vorinostat (PRAVO) phase I study. Lancet Oncol., v. v. 11, p. 459-464,
2010.
Rhodes, L. V.; Nitschke, A. M.; Segar, H. C.; Martin, E. C.; Driver, J. L.; Elliott, S.; Nam, S. Y.; Li, M.;
Nephew, K. P.; Burow, M. E.; Collins-Burow, B. M. The histone deacetylase inhibitor trichostatin A alters
microRNA expression profiles in apoptosis-resistant breast cancer cells. Oncol. Rep., v. 27, p. 10-16,
2012. https://doi.org/10.3892/or.2011.1488
Rivera, S.; Leteur, C.; Mégnin, F.; Law, F.; Martins, I.; Kloos, I.; Depil, S.; Modjtahedi, N.; Perfettini,
J. L.; Hennequin, C.; Deutsch, E. Time dependent modulation of tumor radiosensitivity by a pan HDAC inhibitor.
Abexinostat. Oncotarget, v. 8, p. 56210-56227, 2017.
Sak, A.; Kübler, D.; Bannik, K.; Groneberg, M.; Strunz, S.; Kriehuber, R.; Stuschke, M. Epigenetic silencing
and activation of transcription: Influence on the radiation sensitivity of glioma cell lines. Int. J. Radiat.
Biol., v. 93, no. 5, p. 494-506, 2017. https://doi.org/10.1080/09553002.2017.1270472
Shogren-Knaak, M.; Ishii, H.; Sun, J. M.; Pazin, M. J.; Davie, J. R.; Peterson, C. L. Histone H4-K16 acetylation
controls chromatin structure and protein interactions. Science, v. 311, no. 5762, p. 844-847, 2006. https://doi.org/10.1126/science.1124000
Simone, N. L.; Soule, B. P; Ly, D.; Saleh, A. D.; Savage, J. E.; Degraff, W.; Cook, J.; Harris, C. C.; Gius, D.;
Mitchell, J. B. Ionizing radiation-induced oxidative stress alters miRNA expression. PLoS One, 4:e6377,
2009. https://doi.org/10.1371/journal.pone.0006377
Strickland, F. M.; Richardson, B. C. Epigenetics in human autoimmunity (Epigenetics in autoimmunity-DNA methylation
in systemic lupus erythematosus and beyond). Autoimmunity, v. 41, no. 4, p. 278-286, 2008. https://doi.org/10.1080/08916930802024616
Surova O, Akbar NS, Zhivotovsky B. Knock-down of core proteins regulating microRNA biogenesis has no effect
on sensitivity of lung cancer cells to ionizing radiation. PLoS One, v. 7, no. 3, e33134, 2012. https://doi.org/10.1371/journal.pone.0033134
Tarasov, V.; Jung, P.; Verdoodt, B.; Lodygin, D.; Epanchintsev, A.; Menssen, A.; Meister, G.; Hermeking, H.
Differential regulation of microRNAs by p53 revealed by massively parallel sequencing: miR-34a is a p53
target that induces apoptosis and G1-arrest. Cell Cycle, v. 6, p. 1586-1593, 2007. https://doi.org/10.4161/cc.6.13.4436
Valinciute, G.; Weigel, C.; Veldwijk, M. R.; Oakes, C. C.; Herskind, C.; Wenz, F.; Plass, C.; Schmezer, P.;
Popanda, O. BET-bromodomain inhibitors modulate epigenetic patterns at the diacylglycerol kinase alpha
enhancer associated with radiation-induced fibrosis. Radiother. and Oncol., v. 125, no. 1,
p. 168-174, 2017. https://doi.org/10.1016/j.radonc.2017.08.028
Vaquero, A.; Loyola, A.; Reinberg, D. The constantly changing face of chromatin. Sci. Aging Knowl.
Environ., v. 2003, no. 14, 2003. https://doi.org/10.1126/sageke.2003.14.re4
Veuger, S. J.; Hunter, J. E.; Durkacz, B. W. Ionizing radiation-induced NF-kappaB activation requires
PARP-1 function to confer radioresistance. Oncogene, v. 28, p. 832-842, 2009.
Wang, Y.; Medvid, R.; Melton, C.; Jaenisch, R.; Blelloch, R. DGCR8 is essential for microRNA biogenesis
and silencing of embryonic stem cell self-renewal. Nat. Genet., v. 39, p. 380-385, 2007.
Yang, A. Y.; Lee, J. H.; Shu, L.; Zhang, C.; Su, Z.-Y.; Lu, Y.; Huang, M.-T.; Ramirez, C.; Pung, D.;
Huang, Y.; Verzi, M.; Hart, R. P.; Kong, A.-N. T. Genome-wide analysis of DNA methylation in UVB- and
DMBA/TPA-induced mouse skin cancer models. Life Sci., v. 113, p. 45-54, 2014. https://doi.org/10.1016/j.lfs.2014.07.031
Yu, Y.; Waters, R. Histone acetylation, chromatin remodelling and nucleotide excision repair: Hint
from the study on MFA2 in Saccharomyces cerevisiae. Cell Cycle, v. 4, p. 1043-1045, 2005.
Zhan, M.; Han, Z. C. Phosphatidylinositide 3-kinase/AKT in radiation responses. Histol.
Histopathol., v. 19, p. 915-923, 2004.
Zhao, L.; Lu, X.; Cao, Y. MicroRNA and signal transduction pathways in tumor radiation response.
Cell. Signal., v. 25, no. 7, p. 1625-1634, 2013. https://doi.org/10.1016/j.cellsig.2013.04.004