Suitability of animal models for studying radiation-induced thyroid cancer in humans: Evidence from nuclear architecture

Thyroid

Volumn 21, Issue 12, 2011, Pages 1331-1337

  Gandhi, Manoj ^a   Nikiforov, Yuri E ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN RET;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CHROMOSOME 16P; CHROMOSOME 4Q; CHROMOSOME 6; CHROMOSOME 9Q; CONFOCAL MICROSCOPY; FLUORESCENCE IN SITU HYBRIDIZATION; GENE REARRANGEMENT; HUMAN; HUMAN CELL; HUMAN TISSUE; MOUSE; NONHUMAN; PRIORITY JOURNAL; RADIATION INDUCED NEOPLASM; RAT; THYROID CANCER;

ANIMALS; CELL NUCLEUS; CYTOSKELETAL PROTEINS; DISEASE MODELS, ANIMAL; GENE REARRANGEMENT; HUMANS; IN SITU HYBRIDIZATION, FLUORESCENCE; MICE; MICE, INBRED C57BL; MICROSCOPY, CONFOCAL; NEOPLASMS, RADIATION-INDUCED; NUCLEAR RECEPTOR COACTIVATORS; PROTO-ONCOGENE PROTEINS C-RET; RATS; RATS, SPRAGUE-DAWLEY; REPRODUCIBILITY OF RESULTS; SPECIES SPECIFICITY; THYROID GLAND; THYROID NEOPLASMS;

EID: 82955186926     PISSN: 10507256     EISSN: 15579077     Source Type: Journal    
DOI: 10.1089/thy.2011.0269     Document Type: Article

References (64)

1. Duffy BJ Jr., Fitzgerald PJ 1950 Cancer of the thyroid in children: a report of 28 cases. J Clin Endocrinol Metab 10: 1296-1308.
2. Ron E, Lubin JH, Shore RE, Mabuchi K, Modan B, Pottern LM, Schneider AB, Tucker MA, Boice JD Jr. 1995 Thyroid cancer after exposure to external radiation: a pooled analysis of seven studies. Radiat Res 141:259-277.
3. Winship T, Rosvoll RV 1970 Cancer of the thyroid in children. Proc Natl Cancer Conf 6:677-681.
4. Ezaki H, Takeichi N, Yoshimoto Y 1991 Thyroid cancer: epidemiological study of thyroid cancer in A-bomb survivors from extended life span study cohort in Hiroshima. J Radiat Res (Tokyo) 32 Suppl:193-200.
5. Morimoto I, Yoshimoto Y, Sato K, Hamilton HB, Kawamoto S, Izumi M, Nagataki S 1987 Serum TSH, thyroglobulin, and thyroidal disorders in atomic bomb survivors exposed in youth: 30-year follow-up study. J Nucl Med 28:1115-1122. (Pubitemid 17146830)
6. Parker LN, Belsky JL, Yamamoto T, Kawamoto S, Keehn RJ 1974 Thyroid carcinoma after exposure to atomic radiation. A continuing survey of a fixed population, Hiroshima and Nagasaki, 1958-1971. Ann Intern Med 80:600-604.
7. Prentice RL, Kato H, Yoshimoto K, Mason M 1982 Radiation exposure and thyroid cancer incidence among Hiroshima and Nagasaki residents. Natl Cancer Inst Monogr 62:207-212. (Pubitemid 13102246)
8. Takeichi N, Ezaki H, Dohi K 1991 A review of forty-five years study of Hiroshima and Nagasaki atomic bomb survivors. Thyroid cancer: reports up to date and a review. J Radiat Res (Tokyo) 32 Suppl:180-188.
9. Conrad R 1984 Late radiation effects in Marshall Islanders exposed to fallout 28 years ago. In: Boice JJ, Fraumeni JJ (eds) Radiation Carcinogenesis: Epidemiology and Biological Significance. Raven Press, New York, pp 57-65.
10. Hamilton TE, van Belle G, LoGerfo JP 1987 Thyroid neoplasia in Marshall Islanders exposed to nuclear fallout. JAMA 258:629-635.
11. Kazakov VS, Demidchik EP, Astakhova LN 1992 Thyroid cancer after Chernobyl. Nature 359:21.
12. Nikiforov Y, Gnepp DR 1994 Pediatric thyroid cancer after the Chernobyl disaster. Pathomorphologic study of 84 cases (1991-1992) from the Republic of Belarus. Cancer 74:748-766. (Pubitemid 24217643)
13. Cardis E, Howe G, Ron E, Bebeshko V, Bogdanova T, Bouville A, Carr Z, Chumak V, Davis S, Demidchik Y, Drozdovitch V, Gentner N, Gudzenko N, Hatch M, Ivanov V, Jacob P, Kapitonova E, Kenigsberg Y, Kesminiene A, Kopecky KJ, Kryuchkov V, Loos A, Pinchera A, Reiners C, Repacholi M, Shibata Y, Shore RE, Thomas G, Tirmarche M, Yamashita S, Zvonova I 2006 Cancer consequences of the Chernobyl accident: 20 years on. J Radiol Prot 26:127-140. (Pubitemid 43861071)
14. Fusco A, Grieco M, Santoro M, Berlingieri MT, Pilotti S, Pierotti MA, Della Porta G, Vecchio G 1987 A new oncogene in human thyroid papillary carcinomas and their lymphnodal metastases. Nature 328:170-172. (Pubitemid 17108219)
15. Grieco M, Santoro M, Berlingieri MT, Melillo RM, Donghi R, Bongarzone I, Pierotti MA, Della Porta G, Fusco A, Vecchio G 1990 PTC is a novel rearranged form of the ret protooncogene and is frequently detected in vivo in human thyroid papillary carcinomas. Cell 60:557-563.
16. Cohen Y, Xing M, Mambo E, Guo Z, Wu G, Trink B, Beller U, Westra WH, Ladenson PW, Sidransky D 2003 BRAF mutation in papillary thyroid carcinoma. J Natl Cancer Inst 95:625-627. (Pubitemid 36553510)
17. Fukushima T, Suzuki S, Mashiko M, Ohtake T, Endo Y, Takebayashi Y, Sekikawa K, Hagiwara K, Takenoshita S 2003 BRAF mutations in papillary carcinomas of the thyroid. Oncogene 22:6455-6457. (Pubitemid 37281692)
18. Kimura ET, Nikiforova MN, Zhu Z, Knauf JA, Nikiforov YE, Fagin JA 2003 High prevalence of BRAF mutations in thyroid cancer: genetic evidence for constitutive activation of the RET/PTC-RAS-BRAF signaling pathway in papillary thyroid carcinoma. Cancer Res 63:1454-1457. (Pubitemid 36373628)
19. Soares P, Trovisco V, Rocha AS, Lima J, Castro P, Preto A, Maximo V, Botelho T, Seruca R, Sobrinho-Simoes M 2003 BRAF mutations and RET/PTC rearrangements are alternative events in the etiopathogenesis of PTC. Oncogene 22:4578-4580. (Pubitemid 36920701)
20. Xu X, Quiros RM, Gattuso P, Ain KB, Prinz RA 2003 High prevalence of BRAF gene mutation in papillary thyroid carcinomas and thyroid tumor cell lines. Cancer Res 63:4561-4567. (Pubitemid 36951030)
21. Bounacer A, Wicker R, Caillou B, Cailleux AF, Sarasin A, Schlumberger M, Suarez HG 1997 High prevalence of activating Ret proto-oncogene rearrangements, in thyroid tumors from patients who had received external radiation. Oncogene 15:1263-1273. (Pubitemid 27429741)
22. Collins BJ, Chiappetta G, Schneider AB, Santoro M, Pentimalli F, Fogelfeld L, Gierlowski T, Shore-Freedman E, Jaffe G, Fusco A 2002 RET expression in papillary thyroid cancer from patients irradiated in childhood for benign conditions. J Clin Endocrinol Metab 87:3941-3946. (Pubitemid 34879552)
23. Rabes HM, Demidchik EP, Sidorow JD, Lengfelder E, Beimfohr C, Hoelzel D, Klugbauer S 2000 Pattern of radiation-induced RET and NTRK1 rearrangements in 191 postchernobyl papillary thyroid carcinomas: biological, phenotypic, and clinical implications. Clin Cancer Res 6:1093-1103. (Pubitemid 30159372)
24. Smida J, Salassidis K, Hieber L, Zitzelsberger H, Kellerer AM, Demidchik EP, Negele T, Spelsberg F, Lengfelder E, Werner M, Bauchinger M 1999 Distinct frequency of ret rearrangements in papillary thyroid carcinomas of children and adults from Belarus. Int J Cancer 80:32-38. (Pubitemid 28559772)
25. Butti MG, Bongarzone I, Ferraresi G, Mondellini P, Borrello MG, Pierotti MA 1995 A sequence analysis of the genomic regions involved in the rearrangements between TPM3 and NTRK1 genes producing TRK oncogenes in papillary thyroid carcinomas. Genomics 28:15-24.
26. Greco A, Mariani C, Miranda C, Pagliardini S, Pierotti MA 1993 Characterization of the NTRK1 genomic region involved in chromosomal rearrangements generating TRK oncogenes. Genomics 18:397-400. (Pubitemid 23339553)
27. Ciampi R, Knauf JA, Kerler R, Gandhi M, Zhu Z, Nikiforova MN, Rabes HM, Fagin JA, Nikiforov YE 2005 Oncogenic AKAP9-BRAF fusion is a novel mechanism of MAPK pathway activation in thyroid cancer. J Clin Invest 115:94-101. (Pubitemid 40385509)
28. Nikiforova MN, Ciampi R, Salvatore G, Santoro M, Gandhi M, Knauf JA, Thomas GA, Jeremiah S, Bogdanova TI, Tronko MD, Fagin JA, Nikiforov YE 2004 Low prevalence of BRAF mutations in radiation-induced thyroid tumors in contrast to sporadic papillary carcinomas. Cancer Lett 209:1-6. (Pubitemid 38656111)
29. Xing M 2005 BRAF mutation in thyroid cancer. Endocr Relat Cancer 12:245-262. (Pubitemid 40896444)
30. Ciampi R, Nikiforov YE 2005 Alterations of the BRAF gene in thyroid tumors. Endocr Pathol 16:163-172. (Pubitemid 41687187)
31. Hamatani K, Eguchi H, Ito R, Mukai M, Takahashi K, Taga M, Imai K, Cologne J, Soda M, Arihiro K, Fujihara M, Abe K, Hayashi T, Nakashima M, Sekine I, Yasui W, Hayashi Y, Nakachi K 2008 RET/PTC rearrangements preferentially occurred in papillary thyroid cancer among atomic bomb survivors exposed to high radiation dose. Cancer Res 68:7176-7182.
32. Takahashi K, Eguchi H, Arihiro K, Ito R, Koyama K, Soda M, Cologne J, Hayashi Y, Nakata Y, Nakachi K, Hamatani K 2007 The presence of BRAF point mutation in adult papillary thyroid carcinomas from atomic bomb survivors correlates with radiation dose. Mol Carcinog 46:242-248. (Pubitemid 46399523)
33. Caudill CM, Zhu Z, Ciampi R, Stringer JR, Nikiforov YE 2005 Dose-dependent generation of RET/PTC in human thyroid cells after in vitro exposure to gamma-radiation: a model of carcinogenic chromosomal rearrangement induced by ionizing radiation. J Clin Endocrinol Metab 90:2364-2369. (Pubitemid 40586286)
34. Ito T, Seyama T, Iwamoto KS, Hayashi T, Mizuno T, Tsuyama N, Dohi K, Nakamura N, Akiyama M 1993 In vitro irradiation is able to cause RET oncogene rearrangement. Cancer Res 53:2940-2943. (Pubitemid 23210290)
35. Mizuno T, Kyoizumi S, Suzuki T, Iwamoto KS, Seyama T 1997 Continued expression of a tissue specific activated oncogene in the early steps of radiation-induced human thyroid carcinogenesis. Oncogene 15:1455-1460. (Pubitemid 27437835)
36. Mizuno T, Iwamoto KS, Kyoizumi S, Nagamura H, Shinohara T, Koyama K, Seyama T, Hamatani K 2000 Preferential induction of RET/PTC1 rearrangement by X-ray irradiation. Oncogene 19:438-443. (Pubitemid 30077345)
37. Sacher GA 1950 The survival of mice under duration-of-life exposure to X-rays at various dose rates. In: University of Chicago Report CH-3900, University of Chicago, Chicago.
38. Pearl R, Doering CR 1923 A Comparison of the mortality of certain lower organismswith that ofman. Science 57:209-212.
39. Grahn D 1970 Biological effects of protracted low dose radiation exposure of man and animals. In: Fry RJM, Grahn D, Griem ML, Rust JH (eds) Late Effects of Radiation. Taylor and Francis, New York, pp 181-190.
40. Greenwood M 1928 Laws of mortality from the biological point of view. J Hyg 28:267-294.
41. Walinder G, Jonsson CJ, Sjoden AM 1972 Dose rate dependence in the goitrogen stimulated mouse thyroid. A comparative investigation of the effects of roentgen, 131 I and 132 I irradiation. Acta Radiol Ther Phys Biol 11:24-36.
42. Walinder G, Sjoden AM 1972 Late effects of irradiation on the thyroid gland in mice. II. Irradiation of mouse foetuses. Acta Radiol Ther Phys Biol 11:577-589.
43. Doniach I 1957 Comparison of the carcinogenic effect of xirradiation with radioactive iodine on the rat's thyroid. Br J Cancer 11:67-76.
44. Lindsay S, Potter GD, Chaikoff IL 1957 Thyroid neoplasms in the rat: a comparison of naturally occurring and I131-induced tumors. Cancer Res 17:183-189.
45. Lindsay S, Sheline GE, Potter GD, Chaikoff IL 1961 Induction of neoplasms in the thyroid gland of the rat by x-irradiation of the gland. Cancer Res 21:9-16.
46. Lee W, Chiacchierini RP, Shleien B, Telles NC 1982 Thyroid tumors following 131I or localized X irradiation to the thyroid and pituitary glands in rats. Radiat Res 92:307-319. (Pubitemid 13233254)
47. Jhiang SM, Cho JY, Furminger TL, Sagartz JE, Tong Q, Capen CC, Mazzaferri EL 1998 Thyroid carcinomas in RET/PTC transgenic mice. Recent Results Cancer Res 154:265-270.
48. Nikiforova MN, Stringer JR, Blough R, Medvedovic M, Fagin JA, Nikiforov YE 2000 Proximity of chromosomal loci that participate in radiation-induced rearrangements in human cells. Science 290:138-141.
49. Gandhi M, Medvedovic M, Stringer JR, Nikiforov YE 2006 Interphase chromosome folding determines spatial proximity of genes participating in carcinogenic RET/PTC rearrangements. Oncogene 25:2360-2366.
50. Roccato E, Bressan P, Sabatella G, Rumio C, Vizzotto L, Pierotti MA, Greco A 2005 Proximity of TPR and NTRK1 rearranging loci in human thyrocytes. Cancer Res 65:2572-2576. (Pubitemid 40490053)
51. Lin C, Yang L, Tanasa B, Hutt K, Ju BG, Ohgi K, Zhang J, Rose DW, Fu XD, Glass CK, Rosenfeld MG 2009 Nuclear receptor-induced chromosomal proximity and DNA breaks underlie specific translocations in cancer. Cell 139:1069-1083.
52. Mani RS, Tomlins SA, Callahan K, Ghosh A, Nyati MK, Varambally S, Palanisamy N, Chinnaiyan AM 2009 Induced chromosomal proximity and gene fusions in prostate cancer. Science 326:1230.
53. Kozubek S, Lukasova E, Ryznar L, Kozubek M, Liskova A, Govorun RD, Krasavin EA, Horneck G 1997 Distribution of ABL and BCR genes in cell nuclei of normal and irradiated lymphocytes. Blood 89:4537-4545. (Pubitemid 27260264)
54. Roix JJ, McQueen PG, Munson PJ, Parada LA, Misteli T 2003 Spatial proximity of translocation-prone gene loci in human lymphomas. Nat Genet 34:287-291. (Pubitemid 36792860)
55. Comfort A 1979 The Biology of Senescence, 3rd edition. Elsevier Science, New York.
56. Kirkwood TB 1992 Comparative life spans of species: why do species have the life spans they do? Am J Clin Nutr 55:1191S-1195S.
57. Solovei I, Cavallo A, Schermelleh L, Jaunin F, Scasselati C, Cmarko D, Cremer C, Fakan S, Cremer T 2002 Spatial preservation of nuclear chromatin architecture during threedimensional fluorescence in situ hybridization (3D-FISH). Exp Cell Res 276:10-23. (Pubitemid 34948347)
58. Solovei I, Walter J, Cremer F, Habermann L, Schermeller L, Cremer T 2002 FISH on three-dimensionally preserved nuclei. In: Beatty B, Sabine M, Squire J (eds) FISH: A Practical Approach. Oxford University Press, New York, pp 119-158.
59. Conover W 1971 Practical Nonparametric Statistics. Wiley, New York.
60. Clifton KH 1990 The clonogenic cells of the rat mammary and thyroid glands: their biology, frequency of initiation and promotion/progression to cancer. In: Moolgavkar SH (ed) Scientific Issues in Quantitative Risk Assessment. Birkhauser, Boston, pp 1-21.
61. Dumont JE, Malone JF, Van Herle AJ 1980 Irradiation and Thyroid Disease: Dosimetric, Clinical and Carcinogenic Aspects. Commission of the European Communities, Brussels.
62. Barrett JC, Wiseman RW 1992 Molecular carcinogenesis in humans and rodents. Prog Clin Biol Res 376:1-30.
63. Lemoine NR, Mayall ES, Williams ED, Thurston V, Wynford-Thomas D 1988 Agent-specific ras oncogene activation in rat thyroid tumours. Oncogene 3:541-544. (Pubitemid 19003659)
64. Shore RE 1992 Issues and epidemiological evidence regarding radiation-induced thyroid cancer. Radiat Res 131:98-111.