Cancer Letters
Volume 227, Issue 1 , Pages 59-73 , 8 September 2005

Expression profile of malignant and non-malignant diseases of the thyroid gland reveals altered expression of a common set of genes in goiter and papillary carcinomas

  • Beatriz S. Stolf

      Affiliations

    • Ludwig Institute for Cancer Research, São Paulo, Brazil
    • Instituto de Química, USP, São Paulo, Brazil
    • Current address: Laboratory of Immunology, Heart Institute of Sao Paulo, HC-FMUSP Av Dr Eneas de Carvalho Aguiar, 44 building 2, 9th floor 05403-900, Brazil.
  • ,
  • Cintia M. Abreu

      Affiliations

    • Hospital do Câncer A.C. Camargo, São Paulo, Brazil
  • ,
  • Maria B. Mahler-Araújo

      Affiliations

    • Hospital do Câncer A.C. Camargo, São Paulo, Brazil
  • ,
  • Márcia Dellamano

      Affiliations

    • Ludwig Institute for Cancer Research, São Paulo, Brazil
    • Hospital do Câncer A.C. Camargo, São Paulo, Brazil
  • ,
  • Waleska K. Martins

      Affiliations

    • Ludwig Institute for Cancer Research, São Paulo, Brazil
    • Hospital do Câncer A.C. Camargo, São Paulo, Brazil
  • ,
  • Marcos Brasilino de Carvalho

      Affiliations

    • Hospital Heliópolis, São Paulo, Brazil
  • ,
  • Maria P. Curado

      Affiliations

    • Hospital Araújo Jorge, Goiânia, GO, Brazil
  • ,
  • Juan P. Díaz

      Affiliations

    • Instituto Nacional de Enfermedades Neoplásicas, Lima, Peru
  • ,
  • Artur Fabri

      Affiliations

    • Hospital do Câncer A.C. Camargo, São Paulo, Brazil
  • ,
  • Helena Brentani

      Affiliations

    • Hospital do Câncer A.C. Camargo, São Paulo, Brazil
  • ,
  • Alex F. Carvalho

      Affiliations

    • Ludwig Institute for Cancer Research, São Paulo, Brazil
    • Hospital do Câncer A.C. Camargo, São Paulo, Brazil
  • ,
  • Fernando A. Soares

      Affiliations

    • Hospital do Câncer A.C. Camargo, São Paulo, Brazil
  • ,
  • Luiz P. Kowalski

      Affiliations

    • Hospital do Câncer A.C. Camargo, São Paulo, Brazil
  • ,
  • Roberto Hirata Jr

      Affiliations

    • Instituto de Matemática e Estatística, USP, São Paulo, Brazil
  • ,
  • Luiz F.L. Reis

      Affiliations

    • Ludwig Institute for Cancer Research, São Paulo, Brazil
    • Hospital do Câncer A.C. Camargo, São Paulo, Brazil
    • Corresponding Author InformationCorresponding author. Address: Rua Professor Antonio Prudente 109, 4th floor, São Paulo, SP 01509-010, São Paulo, Brazil. Tel.: +55 11 33883228; fax: +55 11 32077001.

Received 26 October 2004 ,Revised 25 November 2004 ,Accepted 28 November 2004.

References 

  1. Shaha AR. Controversies in the management of thyroid nodule. Laryngoscope. 2000;110:183–193
  2. Harach HR, Williams ED. Pathology of thyroid cancer. In:  Wheeler MH,  Lazarus JH editor. Diseases of the Thyroid. London: Chapman & Hall; 1994;p. 341–363
  3. Sugenoya A, Masuda H, Komatsu M, Yokoyama S, Shimizu T, Fujimori M, et al. Adenomatous goitre: therapeutic strategy, postoperative outcome, and study of epidermal growth factor receptor. Br. J. Surg. 1992;79:404–406
  4. Pelizzo MR, Piotto A, Rubello D, Casara D, Fassina A, Busnardo B. High prevalence of occult papillary thyroid carcinoma in a surgical series for benign thyroid disease. Tumori. 1990;76:255–257
  5. Koh KB, Chang KW. Carcinoma in multinodular goitre. Br. J. Surg. 1992;79:266–267
  6. Wahner HW, Cuello C, Correa P, Uribe LF, Gaitan E. Thyroid carcinoma in an endemic goiter area, Cali, Colombia. Am. J. Med. 1966;40:58–66
  7. Bakiri F, Djemli FK, Mokrane LA, Djidel FK. The relative roles of endemic goiter and socioeconomic development status in the prognosis of thyroid carcinoma. Cancer. 1998;82:1146–1153
  8. Belfiore A, La Rosa GL, La Porta GA, Giuffrida D, Milazzo G, Lupo L, et al. Cancer risk in patients with cold thyroid nodules: relevance of iodine intake, sex, age, and multinodularity. Am. J. Med. 1992;93:363–369
  9. Wahner HW, Gaitan E, Correa P. Studies of iodine metabolism in endemic nodular goiter. J. Clin. Endocrinol. Metab. 1966;26:279–286
  10. Stolf BS, Carvalho AF, Martins WK, Runza FB, Brun M, Hirata R, et al. Differential expression of IGFBP-5 and two human ESTs in thyroid glands with goiter, adenoma and papillary or follicular carcinomas. Cancer Lett. 2003;191:193–202
  11. Takano T, Miyauchi A, Matsuzuka F, Liu G, Higashiyama T, Yokozawa T, et al. Preoperative diagnosis of medullary thyroid carcinoma by RT-PCR using RNA extracted from leftover cells within a needle used for fine needle aspiration biopsy. J. Clin. Endocrinol. Metab. 1999;84:951–955
  12. Huang Y, Prasad M, Lemon WJ, Hampel H, Wright FA, Kornacker K, et al. Gene expression in papillary thyroid carcinoma reveals highly consistent profiles. Proc. Natl Acad. Sci. USA. 2001;98:15044–15049
  13. Yano Y, Uematsu N, Yashiro T, Hara H, Ueno E, Miwa M, et al. Gene expression profiling identifies platelet-derived growth factor as a diagnostic molecular marker for papillary thyroid carcinoma. Clin. Cancer Res. 2004;10:2035–2043
  14. Wasenius VM, Hemmer S, Kettunen E, Knuutila S, Franssila K, Joensuu H. Hepatocyte growth factor receptor, matrix metalloproteinase-11, tissue inhibitor of metalloproteinase-1, and fibronectin are up-regulated in papillary thyroid carcinoma: a cDNA and tissue microarray study. Clin. Cancer Res. 2003;9:68–75
  15. Prasad ML, Pellegata NS, Kloos RT, Barbacioru C, Huang Y, de la CA. CITED1 protein expression suggests Papillary Thyroid Carcinoma in high throughput tissue microarray-based study. Thyroid. 2004;14:169–175
  16. Gomes LI, Silva RL, Stolf BS, Cristo EB, Hirata R, Soares FA, et al. Comparative analysis of amplified and nonamplified RNA for hybridization in cDNA microarray. Anal. Biochem. 2003;321:244–251
  17. Bitomsky N, Bohm M, Klempnauer KH. Transformation suppressor protein Pdcd4 interferes with JNK-mediated phosphorylation of c-Jun and recruitment of the coactivator p300 by c-Jun. Oncogene. 2004;
  18. Shibahara K, Asano M, Ishida Y, Aoki T, Koike T. T.Honjo. Isolation of a novel mouse gene MA-3 that is induced upon programmed cell death, Gene. 1995;166:297–301
  19. Yoshinaga H, Matsuhashi S, Fujiyama C, Masaki Z. Novel human PDCD4 (H731) gene expressed in proliferative cells is expressed in the small duct epithelial cells of the breast as revealed by an anti-H731 antibody. Pathol. Int. 1999;49:1067–1077
  20. Tsai MS, Bogart DF, Castaneda JM, Li P, Lupu R. Cyr61 promotes breast tumorigenesis and cancer progression. Oncogene. 2002;21:8178–8185
  21. Kunz M, Moeller S, Koczan D, Lorenz P, Wenger RH, Glocker MO, et al. Mechanisms of hypoxic gene regulation of angiogenesis factor Cyr61 in melanoma cells. J. Biol. Chem. 2003;278:45651–45660
  22. Menendez JA, Mehmi I, Griggs DW, Lupu R. The angiogenic factor CYR61 in breast cancer: molecular pathology and therapeutic perspectives. Endocr. Relat. Cancer. 2003;10:141–152
  23. Xie D, Yin D, Tong X, O'Kelly J, Mori A, Miller C, et al. Cyr61 is overexpressed in gliomas and involved in integrin-linked kinase-mediated Akt and beta-catenin-TCF/Lef signaling pathways. Cancer Res. 2004;64:1987–1996
  24. Tong X, O'Kelly J, Xie D, Mori A, Lemp N, McKenna R, et al. Cyr61 suppresses the growth of non-small-cell lung cancer cells via the beta-catenin-c-myc-p53 pathway. Oncogene. 2004;23:4847–4855
  25. Tanaka M, Adzuma K, Iwami M, Yoshimoto K, Monden Y, Itakura M. Human calgizzarin; one colorectal cancer-related gene selected by a large scale random cDNA sequencing and northern blot analysis. Cancer Lett. 1995;89:195–200
  26. Shuja S, Murnane MJ. Marked increases in cathepsin B and L activities distinguish papillary carcinoma of the thyroid from normal thyroid or thyroid with non-neoplastic disease. Int. J. Cancer. 1996;66:420–426
  27. Meireles SI, Cristo EB, Carvalho AF, Hirata R, Pelosof A, Gomes LI, et al. Molecular classifiers for gastric cancer and nonmalignant diseases of the gastric mucosa. Cancer Res. 2004;64:1255–1265
  28. Eijan AM, Sandes EO, Riveros MD, Thompson S, Pasik L, Mallagrino H, et al. High expression of cathepsin B in transitional bladder carcinoma correlates with tumor invasion. Cancer. 2003;98:262–268
  29. Lee PD, Sladek R, Greenwood CM, Hudson TJ. Control genes and variability: absence of ubiquitous reference transcripts in diverse mammalian expression studies. Genome Res. 2002;12:292–297
  30. Trachte AL, Suthers SE, Lerner MR, Hanas JS, Jupe ER, Sienko AE, et al. Increased expression of alpha-1-antitrypsin, glutathione S-transferase pi and vascular endothelial growth factor in human pancreatic adenocarcinoma. Am. J. Surg. 2002;184:642–647
  31. Poblete MT, Nualart F, del Pozo M, Perez JA, Figueroa CD. Alpha 1-antitrypsin expression in human thyroid papillary carcinoma. Am. J. Surg. Pathol. 1996;20:956–963
  32. Hojilla CV, Mohammed FF, Khokha R. Matrix metalloproteinases and their tissue inhibitors direct cell fate during cancer development. Br. J. Cancer. 2003;89:1817–1821
  33. Hawthorn L, Stein L, Varma R, Wiseman S, Loree T, Tan D. TIMP1 and SERPIN-A overexpression and TFF3 and CRABP1 underexpression as biomarkers for papillary thyroid carcinoma. Head Neck. 2004;
  34. Buchwald PC, Akerstrom G, Westin G. Reduced p18INK4c, p21CIP1/WAF1 and p27KIP1 mRNA levels in tumours of primary and secondary hyperparathyroidism. Clin. Endocrinol. (Oxf). 2004;60:389–393
  35. Viglietto G, Motti ML, Bruni P, Melillo RM, D'Alessio A, Califano D, et al. Cytoplasmic relocalization and inhibition of the cyclin-dependent kinase inhibitor p27(Kip1) by PKB/Akt-mediated phosphorylation in breast cancer. Nat. Med. 2002;8:1136–1144
  36. Liang J, Zubovitz J, Petrocelli T, Kotchetkov R, Connor MK, Han K, et al. PKB/Akt phosphorylates p27, impairs nuclear import of p27 and opposes p27-mediated G1 arrest. Nat. Med. 2002;8:1153–1160
  37. Shin I, Yakes FM, Rojo F, Shin NY, Bakin AV, Baselga J, et al. PKB/Akt mediates cell-cycle progression by phosphorylation of p27(Kip1) at threonine 157 and modulation of its cellular localization. Nat. Med. 2002;8:1145–1152
  38. Wang S, Wuu J, Savas L, Patwardhan N, Khan A. The role of cell cycle regulatory proteins, cyclin D1, cyclin E, and p27 in thyroid carcinogenesis. Hum. Pathol. 1998;29:1304–1309
  39. Resnick MB, Schacter P, Finkelstein Y, Kellner Y, Cohen O. Immunohistochemical analysis of p27/kip1 expression in thyroid carcinoma. Mod. Pathol. 1998;11:735–739
  40. Galanti MR, Sparen P, Karlsson A, Grimelius L, Ekbom A. Is residence in areas of endemic goiter a risk factor for thyroid cancer?. Int. J. Cancer. 1995;61:615–621
  41. Harach HR, Williams ED. Thyroid cancer and thyroiditis in the goitrous region of Salta, Argentina, before and after iodine prophylaxis. Clin. Endocrinol. (Oxf). 1995;43:701–706
  42. Prades JM, Dumollard JM, Timoshenko A, Chelikh L, Michel F, Estour B, et al. Multinodular goiter: surgical management and histopathological findings. Eur. Arch. Otorhinolaryngol. 2002;259:217–221
  43. Tollin SR, Mery GM, Jelveh N, Fallon EF, Mikhail M, Blumenfeld W, et al. The use of fine-needle aspiration biopsy under ultrasound guidance to assess the risk of malignancy in patients with a multinodular goiter. Thyroid. 2000;10:235–241
  44. Rios A, Rodriguez JM, Canteras M, Galindo PJ, Balsalobre MD, Parrilla P. Risk factors for malignancy in multinodular goitres. Eur. J. Surg. Oncol. 2004;30:58–62
  45. Gandolfi PP, Frisina A, Raffa M, Renda F, Rocchetti O, Ruggeri C, et al. The incidence of thyroid carcinoma in multinodular goiter: retrospective analysis. Acta Biomed. Ateneo. Parmense. 2004;75:114–117
  46. Yamashita H, Noguchi S, Watanabe S, Uchino S, Kawamoto H, Toda M, et al. Thyroid cancer associated with adenomatous goiter: an analysis of the incidence and clinical factors. Surg. Today. 1997;27:495–499
  47. Alvarez CV, Zalvide JB, Cancio E, Dieguez C, Regueiro BJ, Vega FV, et al. Prothymosin alpha mRNA is expressed in competent and proliferating rat thyroid cells (FRTL-5) but is not sufficient to elicit cell progression through the cell cycle. J. Mol. Endocrinol. 1993;11:249–256
  48. Martini PG, Delage-Mourroux R, Kraichely DM, Katzenellenbogen BS. Prothymosin alpha selectively enhances estrogen receptor transcriptional activity by interacting with a repressor of estrogen receptor activity. Mol. Cell Biol. 2000;20:6224–6232
  49. Kawabata W, Suzuki T, Moriya T, Fujimori K, Naganuma H, Inoue S, et al. Estrogen receptors (alpha and beta) and 17beta-hydroxysteroid dehydrogenase type 1 and 2 in thyroid disorders: possible in situ estrogen synthesis and actions. Mod. Pathol. 2003;16:437–444
  50. Nogueira CR, Brentani MM. Triiodothyronine mimics the effects of estrogen in breast cancer cell lines. J. Steroid Biochem. Mol. Biol. 1996;59:271–279

PII: S0304-3835(04)00932-2

doi: 10.1016/j.canlet.2004.11.050

Cancer Letters
Volume 227, Issue 1 , Pages 59-73 , 8 September 2005