Radiation-induced senescence and thyroid cancer: a barrier or a driving force
DOI:
https://doi.org/10.15448/2357-9641.2015.1.21138Keywords:
Ionizing radiation, Thyroid cancer, Senescence, DNA damage, RET/PTC.Abstract
Aims: The main goal of this review-article was to shed light on the impact of senescence on thyroid carcinogenesis, a promising but still neglected field. Source of data: PubMed database and Google Scholar search was performed for English language articles with terms: ionizing radiation exposure, thyroid cancer, radiation signature, RET/PTC, senescence and radiation-induced senescence. We have no date restrictions.
Summary of findings: Ionizing radiation (IR) is undoubtedly the most well characterized risk factor for thyroid cancer of the papillary histotype and its pivotal role as senescence inducer has been proposed. A paradoxical role of senescence on carcinogenesis – a barrier to cancer cell proliferation in early steps and a driving force to cancer progression by secreting proinflamatory cytokines and matrix degrading enzymes – is the heart of the matter of age- related cancer and bring to life new insights to thyroid cancer research field. This review-article briefly points out the major findings that link ionizing radiation to thyroid carcinogenesis, highlighting the molecular alterations mediated by acute and chronic radiation exposure in thyroid cells.
Conclusions: Evidences provided by our group and other few reports suggest that, like other oncogenic stimuli in different cell types, IR induces a senescent phenotype in thyroid cells, what could represent an initial barrier to transformation. However, how senescence could contribute to tumor progression still remains elusive. The comprehension of these mechanisms could not only help elucidating thyroid cancer initiation and progression, but could also indicate new therapeutical targets.
Downloads
References
DeLellis RA, Lloyd RV, Heitz PU. World Health Organization Classification of Tumours. Pathology and Genetics of Tumours of Endocrine Organs. IARC Press: Lyon (France); 2004.
Instituto Nacional do Câncer (INCA). Estimativa 2014 de Incidência de Câncer no Brasil. Rio de Janeiro (Brazil): INCA; 2014.
Albores-Saavedra J, Henson DE, Glazer E, et al. Changing patterns in the incidence and survival of thyroid cancer with follicular phenotype papillary, follicular, and anaplastic: a morphological and epidemiological study. Endocr Pathol. 2007;18:1-7.
Kondo T, Ezzat S, Asa SL. Pathogenetic mechanisms in thyroid follicular cell neoplasia. Nat Rev Cancer 2006;6: 292-306.
American Cancer Society. Cancer Facts & Figures 2014. Atlanta (US): American Cancer Society; 2014.
Ron E, Lubin JH, Shore RE, et al. Thyroid Cancer after Exposure to External Radiation: A Pooled Analysis of Seven Studies. Radiat. Res. 1995;141:259-277.
Land CE, Bouville A, Apostoaei I, et al. Projected lifetime cancer risks from exposure to regional radioactive fallout in the Marshall Islands. Health Phys. 2010;99:201-15.
Pacini F, Vorontsova T, Demidchik EP, et al. Post-Chernobyl thyroid carcinoma in Belarus children and adolescents: comparison with naturally occurring thyroid carcinoma in Italy and France. J Clin Endocrinol Metab. 1997;82:3563-9.
Cardis E, Howe G, Ron E, et al. Cancer consequences of the Chernobyl accident: 20 years on. J Radiol Prot. 2006;26: 127-40.
United Nations Scientific Committee on the Effects of Atomic Radiation (UNSCEAR). Sources and effects of ionizing radiation. New York (US): 2008 Report; Sales No. E.10.XI.3.
Ward, J. DNA damage as the cause of ionizing radiationinduced gene activation. Radiat. Res. 1994;138:S85-S88.
Sarasin A, Bounacer A, Lepage F, et al. Mechanisms of mutagenesis in mammalian cells. Application to human thyroid tumours. C R Acad Sci III. 1999;322:143-9.
Little JB. Radiation carcinogenesis. Carcinogenesis. 2000; 21:397-404.
Caudill CM, Zhu Z, Ciampi R, et al. Dose-dependent generation of RET/PTC in human thyroid cells after in vitro exposure to γ-radiation: a model of carcinogenic chromosomal rearrangement induced by ionizing radiation. J Clin Endocrinol Metab 2005;90:2364-9.
Port M, Boltze C, Wang Y, et al. A radiation-induced gene signature distinguishes post-Chernobyl from sporadic papillary thyroid cancers. Radiat Res. 2007;168: 639-49.
Bounacer A, Wicker R, Caillou B, et al. High prevalence of activating ret proto-oncogene rearrangements, in thyroid tumors from patients who had received external radiation. Oncogene 1997;15:1263-73.
Tronko M, Bogdanova T, Voskoboynyk L, et al. Radiation induced thyroid cancer: fundamental and applied aspects. Exp Oncol. 2010;32:200-204.
Fusco A, Grieco M, Santoro M, et al. A new oncogene in human thyroid papillary carcinomas and their lymph-nodal metastases. Nature. 1987;328:170-2.
Lima J, Trovisco V, Soares P, et al. BRAF mutations are not a major event in post-Chernobyl childhood thyroid carcinomas. J Clin Endocrinol Metab. 2004;89:4267-71.
Ciampi R, Knauf JA, Kerler R, et al. Oncogenic AKAP9- BRAF fusion is a novel mechanism of MAPK pathway activation in thyroid cancer. J Clin Invest. 2005;115: 94-101.
Boltze C, Riecke A, Ruf CG, et al. Sporadic and radiationassociated papillary thyroid cancers can be distinguished using routine immunohistochemistry. Oncol Rep. 2009;22:459-67.
Abou-El-Ardat K, Monsieurs P, Anastasov N, et al. Low dose irradiation of thyroid cells reveals a unique transcriptomic and epigenetic signature in RET/PTC-positive cells. Mutat Res. 2012;731:27-40.
Rudqvist N, Schüler E, Parris TZ, et al. Dose-specific transcriptional responses in thyroid tissue in mice after (131) I administration. Nucl Med Biol. 2015;42:263-8.
Mizuno T, Kyoizumi S, Suzuki T, et al. Continued expression of a tissue specific activated oncogene in the early steps of radiation-induced human thyroid carcinogenesis. Oncogene. 1997;15:1455-60.
Gandhi M, Nikiforov YE. Suitability of animal models for studying radiation-induced thyroid cancer in humans: evidence from nuclear architecture. Thyroid. 2011;21: 1331-7.
Mizuno T, Iwamoto KS, Kyoizumi S, et al. Preferential induction of RET/PTC1 rearrangement by X-ray irradiation. Oncogene. 2000;19:438-43.
Trosko JE, Chang CC, Upham BL, et al. Low-dose ionizing radiation: induction of differential intracellular signalling possibly affecting intercellular communication. adiat Environ Biophys. 2005;44:3-9.
Suzuki K, Yamashita S. Low-dose radiation exposure and carcinogenesis. Jpn J Clin Oncol. 2012;42:563-8.
Seo D, Han S, Kim KH, et al. Evaluation based on Monte Carlo simulation of lifetime attributable risk of cancer after neck X-ray radiography. Radiol Med. 2015; Epub ahead of print.
Schonfeld SJ, Lee C, Berrington de González A. Medical exposure to radiation and thyroid cancer. Clin Oncol (R Coll Radiol) 2011;23:244-50.
Su YP, Niu HW, Chen JB, et al. Radiation dose in the thyroid and the thyroid cancer risk attributable to CT scans for pediatric patients in one general hospital of China. Int J Environ Res Public Health. 2014;11:2793-803.
Boice JD Jr. Radiation epidemiology and recent paediatric computed tomography studies. Ann ICRP. 2015;44:236-48.
Akulevich NM, Saenko VA, Rogounovitch TI, et al. Polymorphisms of DNA damage response genes in radiationrelated and sporadic papillary thyroid carcinoma. Endocr Relat Cancer. 2009;16:491-503.
Shkarupa VM, Henyk-Berezovska SO, Neumerzhytska LV, et al. Allelic polymorphism of DNA repair gene XRCC1 in patients with thyroid cancer who were exposed to ionizing radiation as a result of the Chernobyl accident. Probl Radiac Med Radiobiol. 2014;19:377-388.
Weismann, A. Collected Essays upon Heredity and Kindred Biological Problems (ed. Poulton, E. B.) (Clarendon, Oxford, 1889).
Hayflick L, Moorhead PS. The serial cultivation of human diploid cell strains. Exp. Cell Res. 1961;25:585-621.
Harley CB, Futcher AB, Greider CW. Telomeres shorten during ageing of human fibroblasts. Nature 1990;345: 458-460.
Hayflick, L. A brief overview of the discovery of cell mortality and immortality and of its influence on concepts about ageing and cancer. Pathol. Biol. 1999;47:1094-104.
Kuilman T, Michaloglou C, Mooi WJ, et al. The essence of senescence. Genes Dev. 2010;24:2463-79.
Coppé JP, Desprez PY, Krtolica A, et al. The senescenceassociated secretory phenotype: the dark side of tumor suppression. Annu Rev Pathol. 2010;5:99-118.
Klement K, Goodarzi AA. DNA double strand break responses and chromatin alterations within the aging cell. Exp Cell Res. 2014;329:42-52.
Serrano M, Lin AW, McCurrach ME, et al. Oncogenic ras provokes premature cell senescence associated with accumulation of p53 and p16INK4a. Cell. 1997;88:593-602.
Vizioli MG, Possik PA, Tarantino E, et al. Evidence of oncogene-induced senescence in thyroid carcinogenesis. Endocr Relat Cancer. 2011;18:743-57.
Cisowski J, Sayin VI, Liu M, et al. Oncogene-induced senescence underlies the mutual exclusive nature of oncogenic KRAS and BRAF. Oncogene. 2015; Epub ahead of print.
Suzuki K, Mori I, Nakayama Y, et al. Radiation-induced senescence-like growth arrest requires TP53 function but not telomere shortening. Radiat Res. 2001;155:248-253.
Meng A, Wang Y, Van Zant G, et al. Ionizing radiation and busulfan induce premature senescence in murine bone marrow hematopoietic cells. Cancer Res. 2003;63:5414-9.
Mirzayans R, Andrais B, Scott A, et al. Ionizing radiationinduced responses in human cells with differing TP53 status. Int J Mol Sci. 2013;14:22409-35.
Matsuse M, Saenko V, Sedliarou I, et al. A novel role for thyroid hormone receptor beta in cellular radiosensitivity. J Radiat Res. 2008;49:17-27.
Zambrano A, García-Carpizo V, Gallardo ME, et al. The thyroid hormone receptor β induces DNA damage and premature senescence. J Cell Biol. 2014;204:129-46.
Ewald JA, Desotelle JA, Wilding G, et al. Therapy-Induced Senescence in Cancer. Natl Cancer Inst. 2010;102:1536-46.
Downloads
Published
How to Cite
Issue
Section
License
Copyright
The submission of originals to PAJAR implies the transfer by the authors of the right for publication. Authors retain copyright and grant the journal right of first publication. If the authors wish to include the same data into another publication, they must cite PAJAR as the site of original publication.
Creative Commons License
Except where otherwise specified, material published in this journal is licensed under a Creative Commons Attribution 4.0 International license, which allows unrestricted use, distribution and reproduction in any medium, provided the original publication is correctly cited.
