RET/PTC rearrangement is prevalent in follicular Hürthle cell carcinomas

Histopathology

Volumn 61, Issue 5, 2012, Pages 833-843

  de Vries, Margriet M ^a,b   Celestino, Ricardo ^b,c   Castro, Patricia ^b,c   Eloy, Catarina ^b,c,d   Máximo, Valdemar ^b,c   van der Wal, Jacqueline E ^e   Plukker, John T M ^a   Links, Thera P ^a   Hofstra, Robert M W ^a,f   Sobrinho Simões, Manuel ^b,c,d   Soares, Paula ^b,c  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^b UNIVERSITY OF PORTO   (Portugal)

^c University of Porto   (Portugal)

^d HOSPITAL DE SÃO JOÃO   (Portugal)

^e MARTINI HOSPITAL   (Netherlands)

^f ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

Follicular carcinoma; Genetics; H rthle; RET PTC; Thyroid

Indexed keywords

B RAF KINASE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; TRANSCRIPTION FACTOR PAX8;

ADULT; AGED; ARTICLE; CANCER CELL; CANCER GROWTH; CHROMOSOME REARRANGEMENT; CLINICAL ARTICLE; FEMALE; FOLLICULAR HURTHLE CELL CARCINOMA; GENE MUTATION; HUMAN; MALE; ONCOCYTOMA; ONCOGENE H RAS; ONCOGENE N RAS; PRIORITY JOURNAL; THYROID CARCINOMA; TUMOR GROWTH;

ADENOMA, OXYPHILIC; ADULT; AGED; AGED, 80 AND OVER; FEMALE; GENE REARRANGEMENT; GENES, RAS; HUMANS; IN SITU HYBRIDIZATION, FLUORESCENCE; MALE; MIDDLE AGED; MUTATION; ONCOGENE PROTEINS, FUSION; PROTEIN-TYROSINE KINASES; PROTO-ONCOGENE PROTEINS B-RAF; PROTO-ONCOGENE PROTEINS C-RET; PROTO-ONCOGENE PROTEINS P21(RAS); THYROID NEOPLASMS;

EID: 84864414111     PISSN: 03090167     EISSN: 13652559     Source Type: Journal    
DOI: 10.1111/j.1365-2559.2012.04276.x     Document Type: Article

References (53)

1. Dean DS, Hay ID. Prognostic indicators in differentiated thyroid carcinoma. Cancer Control 2000; 7; 229-239.
2. DeLellis RA, Lloyd RV, Heitz PU, Eng C. Who classification of tumours. Pathology and genetics of tumours of endocrine organs. Lyon: IARC Press, 2004.
3. Hundahl SA, Fleming ID, Fremgen AM, Menck HR. A National Cancer Data Base report on 53, 856 cases of thyroid carcinoma treated in the U.S., 1985-1995 [see commetns]. Cancer 1998; 83; 2638-2648.
4. Maxwell EL, Palme CE, Freeman J. Hurthle cell tumors: applying molecular markers to define a new management algorithm. Arch. Otolaryngol. Head Neck Surg. 2006; 132; 54-58.
5. Sanders LE, Silverman M. Follicular and Hurthle cell carcinoma: predicting outcome and directing therapy. Surgery 1998; 124; 967-974.
6. Har-El G, Hadar T, Segal K, Levy R, Sidi J. Hurthle cell carcinoma of the thyroid gland. A tumor of moderate malignancy. Cancer 1986; 57; 1613-1617.
7. Rosai J, Carcangiu ML, DeLellis R. Tumors of the thyroid gland: atlas of tumor pathology. Washington, DC: Armed Forces Institute of Pathology, 1992.
8. Evans HL, Vassilopoulou-Sellin R. Follicular and Hurthle cell carcinomas of the thyroid: a comparative study. Am. J. Surg. Pathol. 1998; 22; 1512-1520.
9. Cheung CC, Ezzat S, Ramyar L, Freeman JL, Asa SL. Molecular basis off hurthle cell papillary thyroid carcinoma. J. Clin. Endocrinol. Metab. 2000; 85; 878-882.
10. Trovisco V, Soares P, Preto A et al. Type and prevalence of BRAF mutations are closely associated with papillary thyroid carcinoma histotype and patients' age but not with tumour aggressiveness. Virchows Arch. 2005; 446; 589-595.
11. Trovisco V, Vieira de Castro I, Soares P et al. BRAF mutations are associated with some histological types of papillary thyroid carcinoma. J. Pathol. 2004; 202; 247-251.
12. Maximo V, Sobrinho-Simoes M. Hurthle cell tumours of the thyroid. A review with emphasis on mitochondrial abnormalities with clinical relevance. Virchows Arch. 2000; 437; 107-115.
13. Maximo V, Lima J, Soares P, Sobrinho-Simoes M. Mitochondria and cancer. Virchows Arch. 2009; 454; 481-495.
14. Marques AR, Espadinha C, Frias MJ et al. Underexpression of peroxisome proliferator-activated receptor (PPAR)gamma in PAX8/PPARgamma-negative thyroid tumours. Br. J. Cancer 2004; 91; 732-738.
15. Unger K, Zitzelsberger H, Salvatore G et al. Heterogeneity in the distribution of RET/PTC rearrangements within individual post-Chernobyl papillary thyroid carcinomas. J. Clin. Endocrinol. Metab. 2004; 89; 4272-4279.
16. Castro P, Rebocho AP, Soares RJ et al. PAX8-PPARgamma rearrangement is frequently detected in the follicular variant of papillary thyroid carcinoma. J. Clin.Endocrinol. Metab. 2006; 91; 213-220.
17. Airaksinen MS, Titievsky A, Saarma M. GDNF family neurotrophic factor signaling: four masters, one servant? Mol. Cell. Neurosci. 1999; 13; 313-325.
18. Santoro M, Carlomagno F, Melillo RM, Fusco A. Dysfunction of the RET receptor in human cancer. Cell. Mol. Life Sci. 2004; 61; 2954-2964.
19. Di Cristofaro J, Marcy M, Vasko V et al. Molecular genetic study comparing follicular variant versus classic papillary thyroid carcinomas: association of N-ras mutation in codon 61 with follicular variant. Hum. Pathol. 2006; 37; 824-830.
20. Tallini G, Santoro M, Helie M et al. RET/PTC oncogene activation defines a subset of papillary thyroid carcinomas lacking evidence of progression to poorly differentiated or undifferentiated tumor phenotypes. Clin. Cancer Res. 1998; 4; 287-294.
21. Thomas GA, Bunnell H, Cook HA et al. High prevalence of RET/PTC rearrangements in Ukrainian and Belarussian post-Chernobyl thyroid papillary carcinomas: a strong correlation between RET/PTC3 and the solid-follicular variant. J. Clin. Endocrinol. Metab. 1999; 84; 4232-4238.
22. Zhu Z, Ciampi R, Nikiforova MN, Gandhi M, Nikiforov YE. Prevalence of RET/PTC rearrangements in thyroid papillary carcinomas: effects of the detection methods and genetic heterogeneity. J. Clin. Endocrinol. Metab. 2006; 91; 3603-3610.
23. Zhu Z, Gandhi M, Nikiforova MN, Fischer AH, Nikiforov YE. Molecular profile and clinical-pathologic features of the follicular variant of papillary thyroid carcinoma. An unusually high prevalence of ras mutations. Am. J. Clin. Pathol. 2003; 120; 71-77.
24. Chiappetta G, Toti P, Cetta F et al. The RET/PTC oncogene is frequently activated in oncocytic thyroid tumors (Hurthle cell adenomas and carcinomas), but not in oncocytic hyperplastic lesions. J. Clin. Endocrinol. Metab. 2002; 87; 364-369.
25. Musholt PB, Imkamp F, von Wasielewski R, Schmid KW, Musholt TJ. RET rearrangements in archival oxyphilic thyroid tumors: new insights in tumorigenesis and classification of Hurthle cell carcinomas? Surgery 2003; 134; 881-889. discussion 9.
26. Rhoden KJ, Unger K, Salvatore G et al. RET/papillary thyroid cancer rearrangement in nonneoplastic thyrocytes: follicular cells of Hashimoto's thyroiditis share low-level recombination events with a subset of papillary carcinoma. J. Clin. Endocrinol. Metab. 2006; 91; 2414-2423.
27. Nikiforov YE, Rowland JM, Bove KE, Monforte-Munoz H, Fagin JA. Distinct pattern of retoncogene rearrangements in morphological variants of radiation-induced and sporadic thyroid papillary carcinomas in children. Cancer Res. 1997; 57; 1690-1694.
28. Cheung L, Messina M, Gill A et al. Detection of the PAX8-PPAR gamma fusion oncogene in both follicular thyroid carcinomas and adenomas. J. Clin. Endocrinol. Metab. 2003; 88; 354-357.
29. Chia WK, Sharifah NA, Reena RM et al. Fluorescence in situ hybridization analysis using PAX8- and PPARG-specific probes reveals the presence of PAX8-PPARG translocation and 3p25 aneusomy in follicular thyroid neoplasms. Cancer Genet. Cytogenet. 2010; 196; 7-13.
30. Di Cristofaro J, Silvy M, Lanteaume A, Marcy M, Carayon P, De Micco C. Expression of tpo mRNA in thyroid tumors: quantitative PCR analysis and correlation with alterations of ret, Braf, ras and pax8 genes. Endocr. Relat. Cancer 2006; 13; 485-495.
31. French CA, Alexander EK, Cibas ES et al. Genetic and biological subgroups of low-stage follicular thyroid cancer. Am. J. Pathol. 2003; 162; 1053-1060.
32. Nikiforova MN, Biddinger PW, Caudill CM, Kroll TG, Nikiforov YE. PAX8-PPARgamma rearrangement in thyroid tumors: RT-PCR and immunohistochemical analyses. Am. J. Surg. Pathol. 2002; 26; 1016-1023.
33. Nikiforova MN, Lynch RA, Biddinger PW et al. RAS point mutations and PAX8-PPAR gamma rearrangement in thyroid tumors: evidence for distinct molecular pathways in thyroid follicular carcinoma. J. Clin.Endocrinol. Metab. 2003; 88; 2318-2326.
34. Sahin M, Allard BL, Yates M et al. PPARgamma staining as a surrogate for PAX8/PPARgamma fusion oncogene expression in follicular neoplasms: clinicopathological correlation and histopathological diagnostic value. J. Clin. Endocrinol. Metab. 2005; 90; 463-468.
35. Kroll TG, Sarraf P, Pecciarini L et al. PAX8-PPARgamma1 fusion oncogene in human thyroid carcinoma [corrected]. Science 2000; 289; 1357-1360.
36. Xing M. BRAF mutation in thyroid cancer. Endocr. Relat. Cancer 2005; 12; 245-262.
37. Davies H, Bignell GR, Cox C et al. Mutations of the BRAF gene in human cancer. Nature 2002; 417; 949-954.
38. Cohen Y, Xing M, Mambo E et al. BRAF mutation in papillary thyroid carcinoma. J. Natl Cancer Inst. 2003; 95; 625-627.
39. Kimura ET, Nikiforova MN, Zhu Z, Knauf JA, Nikiforov YE, Fagin JA. High prevalence of BRAF mutations in thyroid cancer: genetic evidence for constitutive activation of the RET/PTCRAS-BRAF signaling pathway in papillary thyroid carcinoma. Cancer Res. 2003; 63; 1454-1457.
40. Musholt PB, Musholt TJ, Morgenstern SC, Worm K, Sheu SY, Schmid KW. Follicular histotypes of oncocytic thyroid carcinomas do not carry mutations of the BRAF hot-spot. World J. Surg. 2008; 32; 722-728.
41. Nikiforova MN, Kimura ET, Gandhi M et al. BRAF mutations in thyroid tumors are restricted to papillary carcinomas and anaplastic or poorly differentiated carcinomas arising from papillary carcinomas. J. Clin. Endocrinol. Metab. 2003; 88; 5399-5404.
42. Woodford RL, Nikiforov YE, Hunt JL et al. Encapsulated papillary oncocytic neoplasms of the thyroid: morphologic, immunohistochemical, and molecular analysis of 18 cases. Am. J. Surg. Pathol. 2010; 34; 1582-1590.
43. Banito A, Pinto AE, Espadinha C, Marques AR, Leite V. Aneuploidy and RAS mutations are mutually exclusive events in the development of well-differentiated thyroid follicular tumours. Clin. Endocrinol. (Oxf) 2007; 67; 706-711.
44. Vasko V, Ferrand M, Di Cristofaro J, Carayon P, Henry JF, de Micco C. Specific pattern of RAS oncogene mutations in follicular thyroid tumors. J. Clin. Endocrinol. Metab. 2003; 88; 2745-2752.
45. Bouras M, Bertholon J, Dutrieux-Berger N, Parvaz P, Paulin C, Revol A. Variability of Haras (codon 12) proto-oncogene mutations in diverse thyroid cancers. Eur. J. Endocrinol. 1998; 139; 209-216.
46. Esapa CT, Johnson SJ, Kendall-Taylor P, Lennard TW, Harris PE. Prevalence of Ras mutations in thyroid neoplasia. Clin. Endocrinol. (Oxf) 1999; 50; 529-535.
47. Liu RT, Hou CY, You HL et al. Selective occurrence of ras mutations in benign and malignant thyroid follicular neoplasms in Taiwan. Thyroid 2004; 14; 616-621.
48. Schark C, Fulton N, Jacoby RF, Westbrook CA, Straus FH II, Kaplan EL. N-ras 61 oncogene mutations in Hurthle cell tumors. Surgery 1990; 108; 994-999. discussion 9-1000.
49. Tallini G, Hsueh A, Liu S, Garcia-Rostan G, Speicher MR, Ward DC. Frequent chromosomal DNA unbalance in thyroid oncocytic (Hurthle cell) neoplasms detected by comparative genomic hybridization. Lab. Invest. 1999; 79; 547-555.
50. Soares P, Trovisco V, Rocha AS et al. BRAF mutations and RET/PTC rearrangements are alternative events in the etiopathogenesis of PTC. Oncogene 2003; 22; 4578-4580.
51. Carcangiu ML, Bianchi S, Savino D, Voynick IM, Rosai J. Follicular Hurthle cell tumors of the thyroid gland. Cancer 1991; 68; 1944-1953.
52. Belchetz G, Cheung CC, Freeman J, Rosen IB, Witterick IJ, Asa SL. Hurthle cell tumors: using molecular techniques to define a novel classification system. Arch. Otolaryngol. Head Neck Surg. 2002; 128; 237-240.
53. Couto JP, Prazeres H, Castro P et al. How molecular pathology is changing and will change the therapeutics of patients with follicular cell-derived thyroid cancer. J. Clin. Pathol. 2009; 62; 414-421.