A radiation-induced gene signature distinguishes post-chernobyl from sporadic papillary thyroid cancers

Radiation Research

Volumn 168, Issue 6, 2007, Pages 639-649

  Port, M ^a,b   Boltze, C ^c   Wang, Y ^d   Roper B ^e   Meineke, V ^a   Abend, M ^a  

^a Bundeswehr Institute of Radiobiology   (Germany)

^b HANNOVER MEDICAL SCHOOL   (Germany)

^c UNIVERSITY OF ROSTOCK   (Germany)

^d INSTITUTE OF EPIDEMIOLOGY   (Germany)

^e TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ENDOTHELIAL CELL SPECIFIC MOLECULE 1; GROWTH FACTOR; GUANINE NUCLEOTIDE BINDING PROTEIN; IMMUNOGLOBULIN; INTERSTITIAL COLLAGENASE; KERATIN ASSOCIATED PROTEIN 2 1; KERATIN ASSOCIATED PROTEIN 2 4; OXIDOREDUCTASE; PROTEIN BAALC; PROTEIN COL13A1; PROTEIN PAGE1; REGULATOR PROTEIN; RNA; SECRETED FRIZZLED RELATED PROTEIN 1; UNCLASSIFIED DRUG;

ADOLESCENT; ADULT; ARTICLE; CHERNOBYL ACCIDENT; CLINICAL ARTICLE; CONTROLLED STUDY; DOWN REGULATION; FEMALE; GENE EXPRESSION; GENE MUTATION; GENE TARGETING; GENETIC CODE; GENETIC SCREENING; HUMAN; HUMAN GENOME; HUMAN TISSUE; HYBRIDIZATION; MALE; MICROARRAY ANALYSIS; PAPILLARY CARCINOMA; PATHOGENESIS; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; RADIATION DOSE; RADIATION EXPOSURE; REAL TIME POLYMERASE CHAIN REACTION; RNA ISOLATION; THYROID CANCER; UPREGULATION; AGED; ALGORITHM; CLASSIFICATION; DNA MICROARRAY; GENE EXPRESSION REGULATION; GENETICS; GENOME; MIDDLE AGED; RADIATION INJURY; SENSITIVITY AND SPECIFICITY; THYROID TUMOR;

ADOLESCENT; ADULT; AGED; AGED, 80 AND OVER; ALGORITHMS; CARCINOMA, PAPILLARY; CHERNOBYL NUCLEAR ACCIDENT; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GENOME, HUMAN; HUMANS; MALE; MIDDLE AGED; NEOPLASMS, RADIATION-INDUCED; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; SENSITIVITY AND SPECIFICITY; THYROID NEOPLASMS;

EID: 38849153640     PISSN: 00337587     EISSN: None     Source Type: Journal    
DOI: 10.1667/RR0968.1     Document Type: Article

References (63)

1. R. Feinmesser, E. Lubin, K. Segal and A. Noyek, Carcinoma of the thyroid in children - a review. J. Pediatr. Endocrinol. Metab. 10, 561-568 (1997).
2. B. J. Collins, A. B. Schneider, R. A. Prinz and X. Xu, Low frequency of BRAF mutations in adult patients with papillary thyroid cancers following childhood radiation exposure. Thyroid 16, 61-66 (2006).
3. D. J. Blackburn, L. A. Michel, A. Rosiere, J. P. Trigaux and J. E. Donckier, Occurrence of thyroid papillary carcinoma in young patients. A Chernobyl connection? J. Pediatr. Endocrinol. Metab. 14, 503-506 (2001).
4. M. Schlumberger, A. F. Cailleux, H. G. Suarez and F. de Vathaire, Irradiation and second cancers. The thyroid as a case in point. C. R. Acad. Sci. III 322, 205-213 (1999).
5. W. M. Wiersinga, Thyroid cancer in children and adolescents - consequences in later life. J. Pediatr. Endocrinol. Metab. 14 (Suppl. 5), 1289-1298 (2001).
6. F. Pacini, T. Vorontsova, E. Molinaro, E. Shavrova, L. Agate, E. Kuchinskaya, R. Elisei, E. P. Demidchik and A. Pinchera, Thyroid consequences of the Chernobyl nuclear accident. Acta Paediatr. Suppl. 88, 23-27 (1999).
7. E. D. Williams, A. Abrosimov, T. Bogdanova, E. P. Demidchik, M. Ito, V. LiVolsi, E. Lushnikov, J. Rosai, Y. Sidorov and G. A. Thomas, Thyroid carcinoma after Chernobyl latent period, morphology and aggressiveness. Br. J. Cancer 90, 2219-2224 (2004).
8. S. J. Rybakov, I. V. Komissarenko, N. D. Tronko, A. N. Kvachenyuk, T. I. Bogdanova, A. E. Kovalenko and M. Y. Bolgov, Thyroid cancer in children of Ukraine after the Chernobyl accident. World J. Surg. 24, 1446-1449 (2000).
9. M. Ito, S. Yamashita, K. Ashizawa, H. Namba, M. Hoshi, Y. Shibata, I. Sekine, S. Nagataki and I. Shigematsu, Childhood thyroid diseases around Chernobyl evaluated by ultrasound examination and fine needle aspiration cytology. Thyroid 5, 365-368 (1995).
10. Y. E. Nikiforov, C. S. Heffess, A. V. Korzenko, J. A. Fagin and D. R. Gnepp, Characteristics of follicular tumors and nonneoplastic thyroid lesions in children and adolescents exposed to radiation as a result of the Chernobyl disaster. Cancer 76, 900-909 (1995).
11. M. D. Tronko, T. I. Bogdanova, I. V. Komissarenko, O. V. Epstein, V. Oliynyk, A. Kovalenko, I. A. Likhtarev, I. Kairo, S. B. Peters and V. A. LiVolsi, Thyroid carcinoma in children and adolescents in Ukraine after the Chernobyl nuclear accident: statistical data and clinicomorphologic characteristics. Cancer 86, 149-156 (1999).
12. Y. Shirahige, M. Ito, K. Ashizawa, T. Motomura, N. Yokoyama, H. Namba, S. Fukata, T. Yokozawa, N. Ishikawa and S. Nagataki, Childhood thyroid cancer: comparison of Japan and Belarus. Endocr. J. 45, 203-209 (1998).
13. Y. Nikiforov and D. R. Gnepp, Pediatric thyroid cancer after the Chernobyl disaster. Pathomorphologic study of 84 cases (1991-1992) from the Republic of Belarus. Cancer 74, 748-766 (1994).
14. L. Leenhardt, R Grosclaude and L. Cherie-Challine, Increased incidence of thyroid carcinoma in France: a true epidemic or thyroid nodule management effects? Report from the French Thyroid Cancer Committee. Thyroid 14, 1056-1060 (2004).
15. S. J. Cotterill, M. S. Pearce and L. Parker, Thyroid cancer in children and young adults in the North of England. Is increasing incidence related to the Chernobyl accident? Eur. J. Cancer 37, 1020-1026 (2001).
16. T. Abelin, J. I. Averkin, M. Egger, B. Egloff, A. W. Furmanchuk, F. Gurtner, J. A. Korotkevich, A. Marx, I. I. Matveyenko and A. E. Okeanov, Thyroid cancer in Belarus post-Chernobyl: improved detection or increased incidence? Soz. Praventivmed. 39, 189-197 (1994).
17. Z. Jaworowski, Editorial: Chernobyl proportions. Environ. Int. 14, 69-73 (1988).
18. A. R. Shaha, TNM classification of thyroid carcinoma. World J. Surg. 31, 879-887 (2007).
19. Y. Wang, I. V. Tetko, M. A. Hall, E. Frank, A. Facius, K. F. Mayer and H. W. Mewes, Gene selection from microarray data for cancer classification - a machine learning approach. Comput. Biol. Chem. 29, 37-46 (2005).
20. 2 arrest and up-regulation of genes known to prevent apoptosis but induced necrosis and mitotic catastrophe. Mol. Cancer Ther. 6, 2346-2359 (2007).
21. C. Maenhaut, Gene expression profiling in human thyroid tumors. Bull. Mem. Acad. R. Med. Belg. 159, 533-539 (2004).
22. M. Takahashi, Oncogenic activation of the ret protooncogene in thyroid cancer. Crit. Rev. Oncog. 6, 35-46 (1995).
23. R. Ciampi, J. A. Knauf, R. Kerler, M. Gandhi, Z. Zhu, M. N. Nikiforova, H. M. Rabes, J. A. Fagin and Y. E. Nikiforov, Oncogenic AKAP9-BRAF fusion is a novel mechanism of MAPK pathway activation in thyroid cancer. J. Clin. Invest. 115, 94-101 (2005).
24. V. Detours, S. Wattel, D. Venet, N. Hutsebaut, T. Bogdanova, M. D. Tronko, J. E. Dumont, B. Franc, G. Thomas and C. Maenhaut, Absence of a specific radiation signature in post-Chernobyl thyroid cancers. Br. J. Cancer 92, 1545-1552 (2005).
25. K. Unger, H. Zitzelsberger, G. Salvatore, M. Santoro, T. Bogdanova, H. Braselmann, P. Kastner, L. Zurnadzhy, N. Tronko and G. Thomas, Heterogeneity in the distribution of RET/PTC rearrangements within individual post-Chernobyl papillary thyroid carcinomas. J. Clin. Endocrinol. Metab. 89, 4272-4279 (2004).
26. H. M. Rabes, Gene rearrangements in radiation-induced thyroid carcinogenesis. Med. Pediatr. Oncol. 36, 574-582 (2001).
27. H. Richter, H. Braselmann, L. Hieber, G. Thomas, T. Bogdanova, N. Tronko and H. Zitzelsberger, Chromosomal imbalances in post-Chernobyl thyroid tumors. Thyroid 14, 1061-1064 (2004).
28. R. R. Kimmel, L. P. Zhao, D. Nguyen, S. Lee, M. Aronszajn, C. Cheng, V. P. Troshin, A. Abrosimov, J. Delrow and P. E. Neiman, Microarray comparative genomic hybridization reveals genome-wide patterns of DNA gains and losses in post-Chernobyl thyroid cancer. Radiat. Res. 166, 519-531 (2006).
29. S. P. Finn, P. Smyth, E. O'Regan, S. Cahill, R. Flavin, J. O'Leary and O. Sheils, Array comparative genomic hybridisation analysis of gamma-irradiated human thyrocytes. Virchows Arch. 445, 396-404 (2004).
30. M. Ito, M. Nakashima, T. Nakayama, A. Ohtsuru, Y. Nagayama, N. Takamura, E. P. Demedchik, I. Sekine and S. Yamashita, Expression of receptor-type tyrosine kinase, Ax1, and its ligand, Gas6, in pediatric thyroid carcinomas around Chernobyl. Thyroid 12, 971-975 (2002).
31. Y. Mizukami, A. Nonomura, T. Hashimoto, S. Terahata, F. Matsubara, T. Michigishi and M. Noguchi, Immunohistochemical demonstration of ras p21 oncogene product in normal, benign, and malignant human thyroid tissues. Cancer 61, 873-880 (1988).
32. S. Szkanderova, M. Port, J. Stulik, L. Hernychova, I. Kasalova, D. Van Beuningen and M. Abend, Comparison of the abundance of 10 radiation-induced proteins with their differential gene expression in L929 cells. Int. J. Radiat. Biol. 79, 623-633 (2003).
33. V. Waldmann and H. M. Rabes, Absence of G(s)alpha gene mutations in childhood thyroid tumors after Chernobyl in contrast to sporadic adult thyroid neoplasia. Cancer Res. 57, 2358-2361 (1997).
34. T. Fukushima, S. Suzuki, M. Mashiko, T. Ohtake, Y. Endo, Y. Takebayashi, K. Sekikawa, K. Hagiwara and S. Takenoshita, BRAF mutations in papillary carcinomas of the thyroid. Oncogene. 22, 6455-6457 (2003).
35. Z. H. Lu, G. C. Luo, J. M. Lu and C. Y. Pan, The expression of G proteins alpha-subunit mRNA in different thyroid diseases. Zhonghua Nei Ke. Za Zhi. 42, 103-105 (2003).
36. S. Scarpino, F. C. D'Alena, A. Di Napoli, F. Ballarini, M. Prat and L. P. Ruco, Papillary carcinoma of the thyroid: evidence for a role for hepatocyte growth factor (HGF) in promoting tumour angiogenesis. J. Pathol. 199, 243-250 (2003).
37. B. Song, Immunohistochemical demonstration of epidermal growth factor receptor and ceruloplasmin in thyroid diseases. Acta Pathol. Jpn. 41, 336-343 (1991).
38. Y. Yano, N. Uematsu, T. Yashiro, H. Hara, E. Ueno, M. Miwa, G. Tsujimoto, Y. Aiyoshi and K. Uchida, Gene expression profiling identifies platelet-derived growth factor as a diagnostic molecular marker for papillary thyroid carcinoma. Clin. Cancer Res. 10, 2035-2043 (2004).
39. Z. Pasieka, H. Stepien, J. Komorowski, K. Kolomecki and K. Kuzdak, Evaluation of the levels of bFGF, VEGF, sICAM-1, and s-VCAM-1 in serum of patients with thyroid cancer. Recent Results Cancer Res. 162, 189-194 (2003).
40. X. M. Yu, C. Y. Lo, W. F. Chan, K. Y. Lam, P. Leung and J. M. Luk, Increased expression of vascular endothelial growth factor C in papillary thyroid carcinoma correlates with cervical lymph node metastases. Clin. Cancer Res. 11, 8063-8069 (2005).
41. P. Siironen, J. Louhimo, S. Nordling, A. Ristimaki, H. Maenpaa, R. Haapiainen and C. Haglund, Prognostic factors in papillary thyroid cancer: an evaluation of 601 consecutive patients. Tumour Biol. 26, 57-64 (2005).
42. D. Fuhrer, M. Eszlinger, S. Karger, K. Krause, C. Engelhardt, D. Hasenclever, H. Dralle and R. Paschke, Evaluation of insulin-like growth factor II, cyclooxygenase-2, ets-1 and thyroid-specific thyroglobulin mRNA expression in benign and malignant thyroid tumours. Eur. J. Endocrinol. 152, 785-790 (2005).
43. C. Y. Lo, K. Y. Lam, P. P. Leung and J. M. Luk, High prevalence of cyclooxygenase 2 expression in papillary thyroid carcinoma. Eur. J. Endocrinol. 152, 545-550 (2005).
44. K. B. Weber, K. R. Shroyer, D. E. Heinz, S. Nawaz, M. S. Said and B. R. Haugen, The use of a combination of galectin-3 and thyroid peroxidase for the diagnosis and prognosis of thyroid cancer. Am. J. Clin. Pathol. 122, 524-531 (2004).
45. K. Iwase, A. Nagasaka, K. Kato, S. Ohtani, T. Tsujimura, A. Inagaki, S. Jimbo, A. Nakai, R. Masunaga and M. Hamada, Localization of Cu/Zn and Mn superoxide dismutase in various thyroid disorders. Acta Endocrinol. (Copenh.) 129, 573-578 (1993).
46. P. Siironen, A. Ristimaki, S. Nordling, J. Louhimo, R. Haapiainen and C. Haglund, Expression of COX-2 is increased with age in papillary thyroid cancer. Histopathology 44, 490-497 (2004).
47. S. Mardente, L. Lenti, E. Lococo, F. Consorti, R. C. Della, S. Romeo, R. Misasi and A. Antonaci, Phenotypic and functional characterization of lymphocytes in autoimmune thyroiditis and in papillary carcinoma. Anticancer Res. 25, 2483-2488 (2005).
48. S. H. Van, Jr., S. M. Hughes, C. Bower and D. M. Parham, Lymphocytic infiltration in pediatric thyroid carcinomas. Pediatr. Dev. Pathol. 7, 487-492 (2004).
49. J. Modi, A. Patel, R. Terrell, R. M. Tuttle and G. L. Francis, Papillary thyroid carcinomas from young adults and children contain a mixture of lymphocytes. J. Clin. Endocrinol. Metab. 88, 4418-4425 (2003).
50. E. Lindhorst, P. M. Schumm-Draeger, J. Bojunga, K. H. Usadel and G. Herrmann, Differences in tumor cell proliferation, HLA DR expression and lymphocytic infiltration in various types of thyroid carcinoma. Exp. Clin. Endocrinol. Diabetes 110, 27-31 (2002).
51. S. Gupta, A. Patel, A. Folstad, C. Fenton, C. A. Dinauer, R. M. Tuttle, R. Conran and G. L. Francis, Infiltration of differentiated thyroid carcinoma by proliferating lymphocytes is associated with improved disease-free survival for children and young adults. J. Clin. Endocrinol. Metab. 86, 1346-1354 (2001).
52. S. Matsubayashi, K. Kawai, Y. Matsumoto, T. Mukuta, T. Morita, K. Hirai, F. Matsuzuka, K. Kakudoh, K. Kuma and H. Tamai, The correlation between papillary thyroid carcinoma and lymphocytic infiltration in the thyroid gland. J. Clin. Endocrinol. Metab. 80, 3421-3424 (1995).
53. B. Jarzab, M. Wiench, K. Fujarewicz, K. Simek, M. Jarzab, M. Oczko-Wojciechowska, J. Wloch, A. Czarniecka, E. Chmielik and A. Swierniak, Gene expression profile of papillary thyroid cancer: sources of variability and diagnostic implications. Cancer Res. 65, 1587-1597 (2005).
54. K. Kameyama, Expression of MMP-1 in the capsule of thyroid cancer - relationship with invasiveness. Pathol. Res. Pract. 192, 20-26 (1996).
55. S. Korem, M. B. Resnick and Z. Kraiem, Similar and divergent patterns in the regulation of matrix metalloproteinase-1 (MMP-1) and tissue inhibitor of MMP-1 gene expression in benign and malignant human thyroid cells. J. Clin. Endocrinol. Metab. 84, 3322-3327 (1999).
56. A. Patel, A. M. Straight, H. Mann, E. Duffy, C. Fenton, C. Dinauer, R. M. Tuttle and G. L. Francis, Matrix metalloproteinase (MMP) expression by differentiated thyroid carcinoma of children and adolescents. J. Endocrinol. Invest. 25, 403-408 (2002).
57. S. Y. Lin, Y. Y. Wang and W. H. Sheu, Preoperative plasma concentrations of vascular endothelial growth factor and matrix metalloproteinase 9 are associated with stage progression in papillary thyroid cancer. Clin. Endocrinol. (Oxf.) 58, 513-518 (2003).
58. P. Hall, Radiation-induced thyroid cancer. Med. Oncol. Tumor Pharmacother. 9, 183-189 (1992).
59. E. D. Williams, F. Pacini and A. Pinchera, Thyroid cancer following Chernobyl. J. Endocrinol. Invest. 18, 144-146 (1995).
60. C. Boltze, G. Brabant, H. Dralle, R. Gerlach, A. Roessner and C. Hoang-Vu, Radiation-induced thyroid carcinogenesis as a function of time and dietary iodine supply: an in vivo model of tumorigenesis in the rat. Endocrinology 143, 2584-2592 (2002).
61. T. Fukui, M. Kondo, G. Ito, O. Maeda, N. Sato, H. Yoshioka, K. Yokoi, Y. Ueda, K. Shimokata and Y. Sekido, Transcriptional silencing of secreted frizzled related protein 1 (SFRP 1) by promoter hypermethylation in non-small-cell lung cancer. Oncogene 24, 6323-6327 (2005).
62. J. Ko, K. S. Ryu, Y. H. Lee, D. S. Na, Y. S. Kim, Y. M. Oh, I. S. Kim and J. W. Kim, Human secreted frizzled-related protein is down-regulated and induces apoptosis in human cervical cancer. Exp. Cell Res. 280, 280-287 (2002).
63. T. H. Liu, A. Raval, S. S. Chen, J. J. Matkovic, J. C. Byrd and C. Plass, CpG island methylation and expression of the secreted frizzled-related protein gene family in chronic lymphocytic leukemia. Cancer Res. 66, 653-658 (2006).