Gender differences in thyroid cancer: A critical review

Expert Review of Endocrinology and Metabolism

Volumn 6, Issue 2, 2011, Pages 215-243

  Yao, Reina ^a   Chiu, Connie G ^a   Strugnell, Scott S ^a   Gill, Sabrina ^a   Wiseman, Sam M ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

cancer; estrogen receptor; gender differences; sex steroid receptors; sex steroids; thyroid

Indexed keywords

2 METHOXYESTRADIOL; ANDROGEN RECEPTOR; ANDROSTENEDIONE; BETA CATENIN; CYCLIN D1; ESTROGEN; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; HORMONE RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; ORAL CONTRACEPTIVE AGENT; PROGESTERONE; PROGESTERONE RECEPTOR; SEX HORMONE; THYROGLOBULIN; THYROTROPIN;

BODY MASS; BODY WEIGHT; BREAST CANCER; CANCER CELL CULTURE; CANCER GROWTH; CANCER INCIDENCE; CANCER MORTALITY; CANCER RISK; CELL DIFFERENTIATION; CELL PROLIFERATION; CLINICAL FEATURE; DISEASE ASSOCIATION; DISTANT METASTASIS; DOWNSTREAM PROCESSING; GENE TARGETING; GENETIC ASSOCIATION; GONADECTOMY; HORMONE ACTION; HORMONE RELEASE; HORMONE SUBSTITUTION; HORMONE SYNTHESIS; HUMAN; IMMUNOCOMPETENT CELL; IMMUNOREACTIVITY; LYMPH NODE METASTASIS; MENARCHE; MENOPAUSE; NONHUMAN; OUTCOME ASSESSMENT; PRIORITY JOURNAL; PROGNOSIS; PROTEIN EXPRESSION; PROTEIN INDUCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; REVIEW; RISK FACTOR; SEX DIFFERENCE; SIGNAL TRANSDUCTION; THYROID CANCER; THYROID CELL; THYROID GLAND; TUMOR VOLUME;

EID: 79952717569     PISSN: 17446651     EISSN: None     Source Type: Journal    
DOI: 10.1586/eem.11.9     Document Type: Review

References (172)

1. Canadian Cancer Society and the National Cancer Institute of Canada. Canadian Cancer Statistics 2008. Toronto, ON, Canada, 1-14 (2008).
2. Ferlay J, Bray F, Pisani P, Parkin DM. GLOBOCAN 2002: Cancer Incidence, Mortality and Prevalence Worldwide. IARC CancerBase No. 5., version 2.0, IARC Press, Lyon, France (2004).
3. Curado MP, Edwards B, Shin HR et al. (Eds). Cancer Incidence in Five Continents, Vol. IX. IARC Scientific Publications No. 160. IARC Press, Lyon, France (2007).
4. Grubbs EG, Rich TA, Li G et al. Recent advances in thyroid cancer. Curr. Probl. Surg. 45(3), 156-250 (2008).
5. Iribarren C, Haselkorn T, Tekawa IS, Friedman GD. Cohort study of thyroid cancer in a San Francisco Bay area population. Int. J. Cancer 93, 745-750 (2001). • Only study to date that has analyzed female gender as a risk factor for thyroid cancer. Female gender was shown to have a relative risk of 1.56 for the development of thyroid cancer in this prospective cohort study.
6. Cady B, Rossi R. An expanded view of risk-group definition in differentiated thyroid carcinoma. Surgery 104(6), 947-953 (1988).
7. Brierly JD, Panzarella T, Tsang RW, Gospodarowicz MK, O'Sullivan B. A comparison of different staging systems predictability of patient outcome. Cancer 79(12), 2414-2423 (1997).
8. Farahati J, Bucsky P, Parlowsky T, Mader U, Reiners C. Characteristics of differentiated thyroid carcinoma in children and adolescents with respect to age, gender, and histology. Cancer 80(11), 2156-2162 (1997).
9. dos Santos Silva I, Swerdlow AJ. Sex differences in the risks of hormone-dependent cancers. Am. J. Epidemiol. 138(1), 10-28 (1993).
10. Henderson BE, Ross RK, Pike MC, Casagrande JT. Endogenous hormones as a major factor in human cancer. Cancer Res. 42, 3232-3239 (1982).
11. Morganti S, Ceda GP, Saccani M et al. Thyroid disease in the elderly: sex-related differences in clinical expression. J. Endocrinol. Invest. 28(11 Suppl. Proceedings), 101-104 (2005).
12. Libutti SK. Understanding the role of gender in the incidence of thyroid cancer. Cancer J. 11(2), 104-105 (2005).
13. Zheng T, Holford TR, Chen Y et al. Time trend and age-period-cohort effect on incidence of thyroid cancer in Connecticut, 1935-1992. Int. J. Cancer 67(4), 504-509 (1996).
14. Liu S, Semeciw R, Ugnat A-M, Mao Y. Increasing thyroid cancer incidence in Canada, 1970-1996: time trends and age-period-cohort effects. Br. J. Cancer 86(9), 1335-1339 (2001).
15. Wang C, Crapo LM. The epidemiology of thyroid disease and the implications for screening. Endocrinol. Metab. Clin. North Am. 26(1), 189-218 (1997).
16. [No authors listed]. Clinical guideline, part 1. Screening for thyroid disease. American College of Physicians. Ann. Intern. Med. 129(2), 141-143 (1998).
17. Helfand M, Redfern CC. Clinical guideline, part 2. Screening for thyroid disease: an update. American College of Physicians. Ann. Intern. Med. 129(2), 144-158 (1998).
18. Bertakis KD, Azari R, Helms J, Callahan EJ, Robbins JA. Gender differences in the utilization of health care services. J. Fam. Pract. 49(2), 147-152 (2000).
19. Verbrugge LM. Sex differences in health. Public Health Rep. 97(5), 417-437 (1982).
20. Bertakis KD. The influence of gender on the doctor-patient interaction. Patient Educ. Couns. 76(3), 356-360 (2009).
21. Kaplan SH, Gandek B, Greenfield S, Rogers W, Ware JE. Patient and visit characteristics related to physicians' participatory decision-making style. Med. Care 33(12), 1176-1187 (1995).
22. Rasmussen NG, Hornnes PJ, Hegedus L, Feldt-Rasmussen U. Serum thyroglobulin during the menstrual cycle, during pregnancy, and post-partum. Acta Endocrinol. (Copenh). 121(2), 168-173 (1989).
23. Pacchiarotti A, Martino E, Bartalena L et al. Serum thyrotropin by ultrasensitive immunoradiometric assay and serum free thyroid hormones in pregnancy. J. Endocrinol. Invest. 9(2), 185-189 (1986).
24. Knudsen N, Bulow I, Laurberg P, Perrild H, Ovesen L, Jorgensen T. Low goiter prevalence among users of oral contraceptives in a population sample of 3712 women. Clin. Endocrinol. (Oxf). 57, 71-76 (2002).
25. Banu SK, Govindarajulu P, Aruldhas MM. Testosterone and estradiol differentially regulate TSH-induced thyrocyte proliferation in immature and adult rats. Steroids 67, 573-579 (2002). • Only study to demonstrate genderspecific responses to sex steroid exposure in thyrocytes. Estradiol (E2) was shown to stimulate proliferation of thyrocytes from adult female rats while inhibiting that of thyrocytes from adult male rats, while testosterone had opposite effects.
26. Frazell EL, Schottenfeld D, Hutter RVP. The prognosis and insurability of thyroid cancer patients. CA Cancer J. Clin. 20, 270-275 (1970).
27. Mitchell I, Livingston EH, Chang AY et al. Trends in thyroid cancer demographics and surgical therapy in the United States. Surgery 142(6), 823-828 (2007).
28. Machens A, Hauptmann S, Dralle H. Disparities between male and female patients with thyroid cancers: sex difference or gender divide? Clin. Endocrinol. (Oxf). 65, 500-505 (2006). • Retrospective cohort analysis of surgical thyroid cancer patients looking at histopathological disparities between male and female patients. Significant differences were seen in sporadic but not hereditary medullary carcinoma patients, with the authors suggesting that gender-specific behavioral differences in seeking medical attention may be responsible for the observed differences in sporadic thyroid tumor characteristics.
29. Loh KC, Greenspan FS, Gee L, Miller TR, Yeo PRB. Pathological tumor-node-metastasis staging for papillary and follicular thyroid carcinomas: a retrospective analysis of 700 patients. J. Clin. Endocrinol. Metab. 82(11), 3553-3562 (1997).
30. Ron E, Curtis R, Hoffman DA, Flannery JT. Multiple primary breast and thyroid cancer. Br. J. Cancer 49(1), 87-92 (1984).
31. McTiernan A, Weiss NS, Daling JR. Incidence of thyroid cancer in women in relation to known or suspected risk factors for breast cancer. Cancer Res. 47, 292-295 (1987).
32. Teppo L, Pukkala E, Saxen E. Multiple cancer - an epidemiologic exercise in Finland. J. Natl Cancer Inst. 75, 207-217 (1985).
33. Schottenfeld D, Berg J. Incidence of multiple primary cancers: IV. Cancers of the female breast and genital organs. J. Natl Cancer Inst. 46, 161-170 (1971).
34. Chen AY, Levy L, Goepfert H, Brown BW, Spitz MR, Vassilopoulou-Sellin R. The development of breast carcinoma in women with thyroid carcinoma. Cancer 92(2), 225-231 (2001).
35. Navarro Silvera SA, Miller AB, Rohan TE. Risk factors for thyroid cancer: a prospective cohort study. Int. J. Cancer 116, 433-438 (2005).
36. Negri E, Dal Maso L, Ron E et al. A pooled analysis of case-control studies of thyroid cancer: II. Menstrual and reproductive factors. Cancer Causes Control 10, 143-155 (1999).
37. Levi F, Franceschi S, Gulie C, Negri E, La Vecchia C. Female thyroid cancer: the role of reproductive and hormonal factors in Switzerland. Oncology 50(4), 309-315 (1993).
38. Brindel P, Doyon F, Rachedi F et al. Menstrual and reproductive factors in the risk of differentiated thyroid carcinoma in native women in French Polynesia: a population-based case-control study. Am. J. Epidemiol. 167(2), 219-229 (2008).
39. Galanti MR, Hansson L, Lund E et al. Reproductive history and cigarette smoking as risk factors for thyroid cancer in women: a population-based case-control study. Cancer Epidemiol. Biomarkers Prev. 5, 425-431 (1996).
40. Memon A, Darif M, Al-Saleh K, Suresh A. Epidemiology of reproductive and hormonal factors in thyroid cancer: evidence from a case-control study in the Middle East. Int. J. Cancer 97(1), 82-89 (2002).
41. Sakoda LC, Horn-Ross PL. Reproductive and menstrual history and PTC risk: the San Francisco Bay area thyroid cancer study. Cancer Epidemiol. Biomarkers Prev. 11, 51-57 (2002).
42. Mack WJ, Preston-Martin S, Bernstein L, Qian D, Xiang M. Reproductive and hormonal risk factors for thyroid cancer in Los Angeles County females. Cancer Epidemiol. Biomarkers Prev. 8(11), 991-997 (1999).
43. Cady B, Sedgwick CE, Meissner WA, Wool MS, Salzman FA, Werber J. Risk factor analysis in differentiated thyroid cancer. Cancer 43(3), 810-820 (1979).
44. La Vecchia C, Ron E, Franceschi S et al. A pooled analysis of case-control studies of thyroid cancer: III. Oral contraceptives, menopausal replacement therapy and other female hormones. Cancer Causes Control 10, 157-166 (1999).
45. Zivaljevic V, Vlajinac H, Jankovic R et al. Case-control study of female thyroid cancer - menstrual, reproductive and hormonal factors. Eur. J. Cancer Prev. 12, 63-66 (2003).
46. Rossing MA, Voigt LF, Wicklund KG, Williams M, Daling JR. Use of exogenous hormones and risk of papillary thyroid cancer (Washington, United States). Cancer Causes Control 9, 341-349 (1998).
47. Ceresini G, Milli B, Morganti S et al. Effect of estrogen therapy for 1 year on thyroid volume and thyroid nodules in postmenopausal women. Menopause 15(2), 326-331 (2008).
48. Akslen LA, Nilssen S, Kvale G. Reproductive factors and risk of thyroid cancer. A prospective study of 63,090 women from Norway. Br. J. Cancer 65, 772-774 (1992).
49. Pham TM, Fujino Y, Mikami H et al. Reproductive and menstrual factors and thyroid cancer among Japanese women: the Japan Collaborative Cohort Study. J. Womens Health 18(3), 331-335 (2009).
50. Hallquist A, Hardell L, Degerman A, Boquist L. Thyroid cancer: reproductive factors, previous diseases, drug intake, family history and diet. A case-control study. Eur. J. Cancer Prev. 3, 481-488 (1994).
51. Dal Maso L, La Vecchia C, Franceschi S et al. A pooled analysis of thyroid cancer studies: V. Anthropometric factors. Cancer Causes Control 11, 137-144 (2000).
52. Renehan AG, Tyson M, Egger M, Heller RF, Zwahlen M. Body-mass index and incidence of cancer: a systematic review and metaanalysis of prospective observational studies. Lancet 371, 569-578 (2008).
53. Guignard R, Truong T, Rougier Y, Baron-Dubourdieu D, Guenel P. Alcohol drinking, tobacco smoking, and anthropometric characteristics as risk factors for thyroid cancer: a countrywide case-control study in New Caledonia. Am. J. Epidemiol. 166(10), 1140-1149 (2007).
54. Engeland A, Tretli S, Akslen LA, Bjorge T. Body size and thyroid cancer in two million Norwegian men and women. Br. J. Cancer 95, 366-370 (2006).
55. Goodman MT, Kolonel LN, Wilkens LR. The association of body size, reproductive factors and thyroid cancer. Br. J. Cancer 66(6), 1180-1184 (1992).
56. Endogenous Hormones Breast Cancer Collaborative Group. Body mass index, serum sex hormones, and breast cancer risk in postmenopausal women. J. Natl Cancer Inst. 95(16), 1218-1226 (2003).
57. Manole D, Schildknecht B, Gosnell B, Adams E, Derwahl M. Estrogen promotes growth of human thyroid tumor cells by different molecular mechanisms. J. Clin. Endocrinol. Metab. 86(3), 1072-1077 (2001).
58. Mazzaferri EL, Jhiang SM. Long-term impact of initial surgical and medical therapy on papillary and follicular thyroid cancer. Am. J. Med. 97, 418-428 (1994).
59. Salvesan H, Njolstad PR, Akslen LA, Albrektsen G, Soreide O, Varhaug JE. Papillary thyroid carcinoma: a multivariate analysis of prognostic factors including an evaluation of the p-TNM staging system. Eur. J. Surg. 158(11-12), 583-589 (1992).
60. Byar DP, Green SB, Dor P et al. A prognostic index for thyroid carcinoma: a study of the E.O.R.T.C. thyroid cancer cooperative group. Eur. J. Cancer 15, 1033-1041 (1979).
61. Cunningham MP, Duda RP, Recant W, Chmiel JS, Sylvester J, Fremgen A. Survival discriminants for differentiated thyroid cancer. Am. J. Surg. 160(4), 344-347 (1990).
62. Lundgren CI, Hall P, Ekbom A, Frisell J, Zedenius J, Dickman PW. Incidence and survival of Swedish patients with differentiated thyroid cancer. Int. J. Cancer. 106, 569-573 (2003).
63. Levi F, Randimbison L, Te VC, La Vecchia C. Thyroid cancer in Vaud, Switzerland: an update. Thyroid 12(2), 163-168 (2002).
64. Shaha AR, Shah JP, Loree TR. Risk group stratification and prognostic factors in papillary carcinoma of thyroid. Ann. Surg. Oncol. 3(6), 534-538 (1996).
65. Gilliland FD, Hunt WC, Morris DM, Key CR. Prognostic factors for thyroid cancer: a population-based study of 15,698 cases from the Surveillance, Epidemiology, and End Results (SEER) program 1973-1991. Cancer 79(3), 564-573 (1997).
66. Levi F, Franceschi S, Te VC, Negri E, La Vecchia C. Descriptive epidemiology of thyroid cancer in the Swiss Canton of Vaud. J. Cancer Res. Clin. Oncol. 116(6), 639-647 (1990).
67. Kjellman P, Zedenius J, Lundell G et al. Predictors of outcome in patients with papillary thyroid carcinoma. Eur.J. Surg. Oncol. 32(3), 345-352 (2005).
68. Jukkola A, Bloigu R, Ebeling T, Salmela P, Blanco G. Prognostic factors in differentiated thyroid carcinomas and their implications for current staging classifications. Endocr. Relat. Cancer 11(3), 571-579 (2004).
69. Kushchayeva Y, Duh QY, Kebebew E, D'Avanzo A, Clark O. Comparison of clinical characteristics at diagnosis and during follow-up in 118 patients with Hurthle cell or follicular thyroid cancer. Am. J. Surg. 195, 457-462 (2007).
70. Wada N, Hasegawa S, Masudo Y et al. Clinical outcome by AMES risk definition in Japanese differentiated thyroid carcinoma patients. Asian J. Surg. 30(2), 102-107 (2007).
71. Haigh P, Urbach D, Rotstein L. AMES prognostic index and extent of thyroidectomy for well-differentiated thyroid cancer in the United States. Surgery 136(3), 609-616 (2004).
72. Machens A, Holzhausen H, Lautenschlager C, Thanh PN, Dralle H. Enhancement of lymph node metastasis and distant metastasis of thyroid carcinoma: a multivariate analysis of clinical risk factors. Cancer 98(4), 712-719 (2003).
73. Yamamoto Y, Maeda T, Izumi K, Otsuka H. Occult papillary carcinoma of the thyroid: a study of 408 autopsy cases. Cancer 65(5), 1173-1179 (1990).
74. Mangelsdorf DJ, Thummel C, Beato M et al. The nuclear receptor superfamily: the second decade. Cell 83(6), 835-839 (1995).
75. Simoncini T, Genazzani AR. Non-genomic actions of sex steroid hormones. Eur. J. Endocrinol. 148, 281-292 (2003).
76. Levin ER. Rapid signaling by steroid receptors. Am. J. Physiol. Regul. Integr. Comp. Physiol. 295, R1425-R1430 (2008).
77. Pedram A, Razandi M, Sainson RCA, Kim JK, Hughes CC, Levin ER. A conserved mechanism for steroid receptor translocation to the plasma membrane. J. Biol. Chem. 282(31), 22278-22288 (2007).
78. Levin ER. Integration of the extranuclear and nuclear actions of estrogen. Mol. Endocrinol. 19(8), 1951-1959 (2005).
79. Hiroi H, Inoue S, Watanabe T et al. Differential immunolocalization of estrogen receptor α and β in rat ovary and uterus. J. Mol. Endocrinol. 22(1), 37-44 (1999).
80. Nilsson S, Makela S, Treuter E et al. Mechanisms of estrogen action. Physiol. Rev. 81, 1535-1565 (2001).
81. McDonnell DP, Norris JD. Connections and regulation of the human estrogen receptor. Science 296, 1642-1644 (2002).
82. Wierman ME. Sex steroid effects at target tissues - mechanism of action. Adev. Physiol. Educ. 31, 26-33 (2007).
83. Giangrande PH, McDonnell DP. The A and B isoforms of the human progesterone receptor: two functionally different transcriptional factors encoded by single gene. Recent Prog. Horm. Res. 54, 291-313 (1999).
84. Vegeto E, Shahbaz MM, Wen DX, Goldman ME, O'Malley BW, McDonnell DP. Human progesterone receptor A form is a cell- and promoter-specific repressor of human progesterone receptor B function. Mol. Endocrinol. 7(10), 1244-1255 (1993).
85. Kastner P, Krust A, Turcotte B et al. distinct estrogen-regulated promoters generate transcripts encoding the two functionally different human progesterone forms A and B. EMBO J. 9(5), 1603-1614 (1990).
86. Graham JD, Clarke CL. Physiological action of progesterone in target tissues. Endocr. Rev. 18(4), 502-519 (1997).
87. Tenbaum S, Baniahmad A. Nuclear receptors: structure, function and involvement in disease. Int. J. Biochem. Cell Biol. 29(12), 1325-1341 (1997).
88. Keller ET, Ershler WB, Chang C. The androgen receptor: a mediator of diverse responses. Front. Biosci. 1, D59-D71 (1996).
89. Platet N, Cathiard AM, Gleizes M, Garcia M. Estrogens and their receptors in breast cancer progression: a dual role in cancer proliferation and invasion. Crit. Rev. Oncol. Hematol. 51(1), 55-67 (2004).
90. Chambers JT. Sex steroids in endometrial cancer. Yale J. Biol. Med. 61(4), 339-350 (1988).
91. Stabile LP, Siegfried JM. Estrogen receptor pathways in lung cancer. Curr. Oncol. Rep. 6(4), 259-267 (2004).
92. Pignata S, Daniele B, Gallo C, De Vivo R, Monfardini S, Perrone F. Endocrine treatment of hepatocellular carcinoma: any evidence of benefit? Eur. J. Cancer 34(1), 25-32 (1998).
93. Di Maio M, Daniele B, Pignata S et al. Is human hepatocellular carcinoma a hormone-responsive tumor? World J. Gastroenterol. 14(11), 1682-1689 (2008).
94. Nagasue N, Kohno H. Hepatocellular carcinoma and sex hormones. HPB Surgery 6(1), 1-6 (1992).
95. Wong NA, Malcomson RD, Jodrell DI, Groome NP, Harrison DJ, Saunders PT. ERb isoform expression in colorectal carcinoma: an in vivo and in vitro study of clinicopathological and molecular correlates. J. Pathol. 207(1), 53-60 (2005).
96. Pravdenkova S, Al-Mefty O, Sawyer J, Husain M. Progesterone and estrogen receptors: opposing prognostic indicators in meningiomas. J. Neurosurg. 105(2), 163-173 (2006).
97. Roser F, Nakamura M, Bellinzona M, Rosahl SK, Ostertag H, Samii M. The prognostic value of progesterone receptor status in meningiomas. J. Clin. Pathol. 57(10), 1033-1037 (2004).
98. Avila DM, Zoppi S, McPhaul MJ. The androgen receptor (AR) in syndromes of androgen insensitivity and in prostate cancer. J. Steroid Biochem. Mol. Biol. 76(1-5), 135-142 (2001).
99. Pijnenborg JMA, Romano A, Dam-de Veen GC et al. Aberrations in the progesterone receptor gene and the risk of recurrent endometrial carcinoma. J. Pathol. 205(5), 597-605 (2005).
100. Simpson E, Rubin G, Clyne C et al. Local estrogen biosynthesis in males and females. Endocr. Relat. Cancer 6(2), 131-137 (1999).
101. Longcope C. Adrenal and gonadal secretion in normal females. Clin. Endocrinol. Metab. 15(2), 213-228 (1986).
102. Utian WH. Menopause-related definitions. Int. Congr. Series 1266, 133-138 (2004).
103. Chahal HS, Drake WM. The endocrine system and ageing. J. Pathol. 211, 173-180 (2007).
104. Santoro N, Adel T, Skurnick JH. Decreased inhibin tone and increased activin A secretion characterize reproductive aging in women. Fertil. Steril. 71(4), 658-662 (1999).
105. Welt CK, McNicholl DJ, Taylor AE, Hall JE. Female reproductive aging in marked by decreased secretion of dimeric inhibin. J. Clin. Endocrinol. Metab. 84, 105-111 (1999).
106. Santoro N, Brown JR, Adel T, Skurnick JH. Characterization of reproductive hormonal dynamics in the perimenopause. J. Clin. Endocrinol. Metab. 81, 1495-1501 (1996).
107. Burger HG, Hale GE, Robertson DM, Dennerstein L. A review of hormonal changes during the menopausal transition: focus on findings from the Melbourne Women's Midlife Health Project. Hum. Reprod. Update 13(6), 559-565 (2007).
108. Sherman BM, West JH, Korenman SG. The menopausal transition: analysis of LH, FSH, estradiol, and progesterone concentrations during menstrual cycles of older women. J. Clin. Endocrinol. Metab. 42(4), 629-636 (1976).
109. Burger H. The menopausal transition - endocrinology. J. Sex. Med. 5(10), 2266-2273 (2008).
110. Simon JA. Estrogen replacement therapy: effects on the endogenous androgen milieu. Fertil. Steril. 77(S4), 77-82 (2002).
111. Burger HG. Androgen production in women. Fertil. Steril. 77(Suppl. 4), 3-5 (2002).
112. Tahboub R, Arafah BM. Sex steroids and the thyroid. Best Pract. Res. Clin. Endocrinol. Metab. 23, 769-780 (2009).
113. del Senno L, degli Uberti E, Hanau S, Piva R, Rossi R, Trasforini G. In vitro effects of estrogen on tgb and c-myc gene expression in normal and neoplastic human thyroids. Mol. Cell Endocrinol. 63(1-2), 67-74 (1989).
114. Furlanetto TW, Nguyen LQ, Jameson JL. Estradiol increases proliferation and down-regulates the sodium/iodide symporter gene in FRTL-5 cells. Endocrinology 140(12), 5705-5711 (1999).
115. Christianson D, Roti E, Vagenakis AG, Braverman LE. The sex-related difference in serum thyrotropin concentration is androgen mediated. Endocrinology 108(2), 529-535 (1981).
116. Rajoria S, Suriano R, Shanmugam A et al. Metastatic phenotype is regulated by estrogen in thyroid cells. Thyroid 20(1), 33-41 (2010). • A recent study on the effect of E2 on modulation of metastatic phenotype in a normal thyroid cell line and a thyroid cancer cell line. E2 enhanced adhesion, migration and invasiveness of both cell lines, with β-catenin suggested as modulating these effects.
117. Dalla Valle LD, Ramina A, Vianello S, Fassina A, Belvedere P, Colombo L. Potential for estrogen synthesis and action in human normal and neoplastic thyroid tissues. J. Clin. Endocrinol. Metab. 83(10), 3702-3709 (1998).
118. Kawabata W, Suzuki T, Moriya T et al. Estrogen receptors (α and β) and 17 β-hydroxysteroid dehydrogenase type 1 and 2 in thyroid disorders: possible in situ estrogen synthesis and actions. Mod. Pathol. 16(5), 437-444 (2003).
119. Mori M, Naito M, Watanabe H, Takeichi N, Dohi K, Ito A. Effects of sex difference, gonadectomy, and estrogen on N-methyl-N-nitrosourea induced rat thyroid tumors. Cancer Res. 50, 7662-7667 (1990).
120. Thiruvengadam A, Govindarajulu P, Aruldhas MM. Modulatory effect of estradiol and testosterone on the development of N-nitrosodiisopropranolamine induced thyroid tumors in female rats. Endocr. Res. 29(1), 43-51 (2003).
121. Bosland MC, Prinsen MK, Rivenson A, Weisburger JH. Induction of skin and thyroid tumors in male rats by N-methyl-N-nitrosourea after sequential treatment with cyproterone acetate and testosterone proprionate: effects of castration, rat strain and time of carcinogen injection. Carcinogenesis 13(4), 669-674 (1992).
122. Hofmann C, Oslapas R, Nayyar R, Paloyan E. Androgen-mediated development of irradiation-induced thyroid tumors in rats: dependence on animal age during interval of androgen replacement in castrated males. J. Natl Cancer Inst. 77(1), 253-260 (1986).
123. Hofmann C, Oslapas R, Nayyar R, McCall A, Paloyan E. Testosterone enhancement of thyroid carcinoma in rats: the role of TSH. Surgery 100(6), 1078-1087 (1986).
124. Banu SK, Govindarajulu P, Aruldhas MM. Testosterone and estradiol have specific differential modulatory effect on the proliferation of human thyroid papillary and follicular carcinoma cell lines independent of TSH action. Endocr. Pathol. 12(3), 315-327 (2001).
125. Lee ML, Chen GG, Vlantis AC, Tse GM, Leung BC, van Hasselt CA. Induction of thyroid papillary carcinoma cell proliferation by estrogen is associated with an altered expression of Bcl-xL. Cancer J. 11(2), 113-121 (2005).
126. Zeng Q, Chen GG, Vlantis AC, van Hasselt CA. Oestrogen mediates the growth of human thyroid carcinoma via an oestrogen receptor-ERK pathway. Cell Prolif. 40, 921-935 (2007).
127. Inoue H, Oshimo K, Miki H, Kawano M, Monden Y. Immunohistochemical study of estrogen receptors and the responsiveness to estrogen in papillary thyroid carcinoma. Cancer 72(4), 1364-1368 (1993).
128. Kavanagh DO, McIlroy M, Myers E et al. The role of oestrogen receptor a in human thyroid cancer: contributions from coregulatory proteins and the tyrosine kinase receptor HER2. Endocr. Relat. Cancer 17(1), 255-264 (2010). • A recent study on the role of estrogen receptor (ER)a in a follicular thyroid carcinoma cell line and an anaplastic thyroid carcinoma cell line. E2 induced cell proliferation in the follicular thyroid carcinoma but not anaplastic thyroid carcinoma cells, and expression of ERa was significantly associated with well-differentiated tumors.
129. Farid NR, Shi Y, Zou M. Molecular basis of thyroid cancer. Endocr. Rev. 15(2), 202-232 (1994).
130. Vivacqua A, Bonofiglio D, Albanito L et al. 17-estradiol, genistein, and 4-hydroxytamoxifen induce the proliferation of thyroid cancer cells through the G protein-coupled receptor GPR30. Mol. Pharmacol. 70, 1414-1423 (2006).
131. Zeng Q, Chen GG, Vlantis AC, Tse GM, van Hasselt CA. The contributions of oestrogen receptor isoforms to the development of papillary and anaplastic thyroid carcinomas. J. Pathol. 214, 425-433 (2008).
132. Schweppe RE, Klopper JP, Korch C et al. Deoxyribonucleic acid profiling analysis of 40 human thyroid cancer cell lines reveals cross-contamination resulting in cell line redundancy and misidentification. J. Clin. Endocrinol. Metab. 93(11), 4331-4341 (2008).
133. Chen GG, Vlantis AC, Zeng Q, van Hasselt CA. Regulation of cell growth by estrogen signaliing and potential targets in thyroid cancer. Curr. Cancer Drug Targets 8, 367-377 (2008).
134. Kossmehl P, Shakibaei M, Cogoli A et al. Weightlessness induced apoptosis in normal thyroid cells and papillary thyroid carcinoma cells via extrinsic and intrinsic pathways. Endocrinology 144(9), 172-179 (2003).
135. Memon GR, Arain SA, Jamal Q, Ansari T. Immunohistochemical study of progesterone receptors in thyroid gland. J. Pak. Med. Assoc. 55, 321-324 (2005).
136. Roswell P, Bu S, Rubin K, Landstrom M, Heldin NE. 2-methoxyestradiol induces apoptosis in cultured human anaplastic thyroid carcinoma cells. Thyroid 12(2), 143-150 (2006).
137. Mueck AO, Seeger H. 2-methoxyestradiol - biology and mechanism of action. Steroids 75(10), 625-631 (2010).
138. Fujimoto N, Sakai Y, Ito A. Increase in estrogen receptor levels in MNU-induced thyroid tumors in LE rats. Carcinogenesis 13(8), 1315-1318 (1992).
139. Molteni A, Bahu RM, Battifora HA et al. Estradiol receptor assays in normal and neoplastic tissues. A possible diagnostic acid for tumor differentiation. Ann. Clin. Lab. Sci. 9(2), 103-108 (1979).
140. Molteni A, Warpeha RL, Brizio-Molteni L, Fors EM. Estradiol receptor-binding protein in head and neck neoplastic and normal tissue. Arch. Surg. 116, 207-210 (1981). • First study to demonstrate ER expression in thyroid cancer tissue. A measurable amount of E2 binding was found in two out of four papillary thyroid carcimona specimens.
141. Clark OH, Gerend PL, Davis M, Goretzki PE, Hoffman PG. Estrogen and thyroid-stimulating hormone receptors in neoplastic and non-neoplastic human thyroid tissue. J. Surg. Res. 38, 89-96 (1985).
142. Hampl R, Nemec J, Heresova J, Kimlova I, Starka L. Estrogen receptors in human goitrous and neoplastic thyroid. Endocrinol. Exp. 19, 227-230 (1985).
143. Hong GS, Sng IT, Soo KC. Oestrogen receptors in well-differentiated thyroid cancers. Ann. Acad. Med. Singapore 20(6), 767-769 (1991).
144. Jaklic BR, Rushin J, Ghosh BC. Estrogen and progesterone receptors in thyroid lesions. Ann. Surg. Oncol. 2(5), 429-434 (1995).
145. Karlsson MG, Hardell L, Hallquist A. No association between immunohistochemical expression of p53, c-erbb-2, Ki-67, estrogen and progesterone receptors in female papillary thyroid cancer and ionizing radiation. Cancer Lett. 120, 173-177 (1997).
146. Arain SA, Shah MH, Meo SA, Jamal Q. Estrogen receptors in human thyroid gland. An immunohistochemical study. Saudi Med. J. 24(2), 174-178 (2003).
147. Chauduri PK, Prinz R. Estrogen receptor in normal and neoplastic human thyroid tissue. Am. J. Otolaryngol. 10(5), 322-326 (1989).
148. Lewy-Trenda I. Estrogen and progesterone receptors in neoplastic and non-neoplastic thyroid lesions. Pol. J. Pathol. 53(2), 67-72 (2002).
149. Miki H, Oshimo K, Inoue H, Morimoto T, Monden Y. Sex hormone receptors in human thyroid tissues. Cancer 66, 1759-1762 (1990).
150. van Hoeven KH, Menendez-Botet CJ, Strong EW, Huvos AG. Estrogen and progesterone receptor content in human thyroid disease. Am. J. Clin. Pathol. 99, 175-181 (1993).
151. Bonacci R, Pinchera A, Fierabacci P, Giglotti A, Grasso L, Giani C. Relevance of estrogen and progesterone enzyme immunoassay in malignant, benign and surrounding normal thyroid tissue. J. Endocrinol. Invest. 19(3), 159-164 (1996).
152. Prinz RA, Sandberg L, Chaudhuri PK. Androgen receptors in human thyroid tissue. Surgery 96(9), 996-1000 (1984).
153. Tavangar SM, Monajemzadeh M, Larijani B, Haghpanah V. Immunohistochemical study of oestrogen receptors in 351 human thyroid glands. Singapore Med. J. 48(8), 744-747 (2007).
154. Hiasa Y, Nishioka H, Kitahori Y et al. Immunohistochemical analysis of estrogen receptors in 313 paraffin section cases of human thyroid tissue. Oncology 50, 132-136 (1993).
155. Diaz NM, Mazoujian G, Wick MR. Estrogen-receptor protein in thyroid neoplasms: an immunohistochemical analysis of papillary carcinoma, follicular carcinoma, and follicular adenoma. Arch. Pathol. Lab. Med. 115, 1203-1207 (1991).
156. Lee CH, Kao HL, Lin HS, Peng FK, Chi CW. Estrogen receptors and glucocorticoid receptors in human well-differentiated thyroid cancer. Int. J. Mol. Med. 2, 229-233 (1998).
157. Kansakar E, Chang YJ, Mehrabi M, Mittal V. Expression of estrogen receptor, progesterone receptor, and vascular endothelial growth factor-A in thyroid cancer. Am. Surg. 75, 785-789 (2009).
158. Egawa C, Miyoshi Y, Iwao K, Shiba E, Noguchi S. Quantitative analysis of estrogen receptor-α and -β messenger RNA expression in normal and malignant thyroid tissues by real-time polymerase chain reaction. Oncology 62, 293-298 (2001).
159. Takeichi N, Ito H, Haruta R, Matsuyama T, Dohi K, Tahara E. Relation between estrogen receptor and malignancy of thyroid cancer. Jpn. J. Cancer Res. 82, 19-22 (1991).
160. Inoue H, Oshimo K, Miki H et al. Immunohistochemical study of estrogen receptor and estradiol on papillary thyroid carcinoma in young patients. J. Surg. Oncol. 53, 226-230 (1993).
161. Wiseman SM, Masoudi H, Niblock P et al. Anaplastic thyroid carcinoma: expression profile of targets for therapy offers new insights for disease treatment. Ann. Surg. Oncol. 14(2), 719-729 (2007).
162. Wiseman SM, Griffith OL, Deen S et al. Identification of molecular markers altered during transformation of differentiated into anaplastic thyroid carcinoma. Arch. Surg. 142(8), 717-729 (2007).
163. Mizukami Y, Michigishi T, Nonomura A, Hashimoto T, Noguchi M, Matsubara F. Estrogen and estrogen receptors in thyroid carcinomas. J. Surg. Oncol. 47, 165-169 (1991).
164. Imai Y, Yamakawa M, Matsuda M, Kasajima T. Endogenous sex hormone and estrogen binding activity in thyroid cancer. Histol. Histopathol. 4(1), 39-45 (1989).
165. Yane K, Kitahori Y, Konishi N et al. Expression of the estrogen receptor in human thyroid neoplasms. Cancer Lett. 84(1), 59-66 (1994).
166. Metaye T, Millet C, Kraimps JL, Aubouin B, Barbier J, Begon F. Estrogen receptors and cathepsin D in human thyroid tissue. Cancer 52(6), 1991-1996 (1993).
167. Poulsen HS, Bukh A, Rytter L et al. Oestrogen receptor assay: false positive analysis? Acta Radiol. Oncol. 23(2-3), 109-117 (1984).
168. Anderson KM, Bonomi P, Marogil M, Hendrickson C, Economou S. Comparison of dextran-coated charcoal and sucrose density gradient analyses of estrogen and progesterone receptors in human breast cancer. Cancer Res. 40, 4127-4132 (1980).
169. Pavao M, Traish AM. Estrogen receptor antibodies: specificity and utility in detection, localization and analyses of estrogen receptor α and β. Steroids 66(1), 1-16 (2001).
170. Colomer A, Martinez-Mas JV, Matias-Guiu X et al. Sex-steroid hormone receptora in human medullary thyroid carcinoma. Mod. Pathol. 9(1), 68-72 (1996).
171. Blechet C, Lecomte P, De Calan L et al. Expression of sex steroid hormone receptors in C cell hyperplasia and medullary thyroid carcinoma. Virchows Arch. 450(4), 433-439 (2007).
172. Surveillance Epidemiology and End Results (SEER) Program, 2008 www.seer.cancer.gov (Accessed February 2011)