Molecular markers of aggressiveness of thyroid cancer

Current Opinion in Endocrinology, Diabetes and Obesity

Volumn 16, Issue 5, 2009, Pages 361-366

  Ringel, Matthew D ^a,b  

^a THE OHIO STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

^b 445D McCampbell Hall ^*  (United States)

Author keywords

BRAF; Methylation; microRNA; PI3 kinase; Tyrosine kinase inhibitors

Indexed keywords

B RAF KINASE; CYCLIN D1; ENZYME INHIBITOR; FIBROBLAST GROWTH FACTOR RECEPTOR; FLUORODEOXYGLUCOSE F 18; MAMMALIAN TARGET OF RAPAMYCIN INHIBITOR; MELANOMA ANTIGEN 3; MICRORNA; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; MITOGEN ACTIVATED PROTEIN KINASE KINASE; MUCIN 1; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3 KINASE INHIBITOR; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; POLO LIKE KINASE 1; PROTEIN KINASE B; PROTEIN P27; PROTEIN PATCHED; PROTEIN RET; PROTEIN TYROSINE KINASE INHIBITOR; RAF PROTEIN; RAS ASSOCIATION DOMAIN FAMILY PROTEIN 1A; RAS PROTEIN; RHOB GUANINE NUCLEOTIDE BINDING PROTEIN; SCATTER FACTOR RECEPTOR; STEM CELL FACTOR; TUMOR MARKER; VASCULOTROPIN RECEPTOR; WNT PROTEIN;

CANCER CELL; CANCER DIAGNOSIS; CANCER GENETICS; CANCER GROWTH; CANCER INVASION; CANCER MORTALITY; CANCER RECURRENCE; CANCER SIZE; CANCER STAGING; CANCER SURVIVAL; CARCINOGENESIS; COWDEN SYNDROME; DISTANT METASTASIS; DRUG TARGETING; EPIGENETICS; FOLLICULAR CARCINOMA; GENE MUTATION; HUMAN; LYMPH NODE METASTASIS; MALIGNANT TRANSFORMATION; MARKER GENE; METASTASIS; MICROENVIRONMENT; ONCOGENE; PAPILLARY CARCINOMA; POSITRON EMISSION TOMOGRAPHY; PROGNOSIS; REVIEW; THYROID CANCER; TREATMENT RESPONSE; TUMOR DIFFERENTIATION;

CARCINOMA; GENE EXPRESSION PROFILING; GENETIC MARKERS; HUMANS; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PROGNOSIS; SIGNAL TRANSDUCTION; THYROID NEOPLASMS;

EID: 69349084322     PISSN: 1752296X     EISSN: None     Source Type: Journal    
DOI: 10.1097/MED.0b013e32832ff2cb     Document Type: Review

References (60)

1. Davies L, Welch HG. Increasing incidence of thyroid cancer in the United States, 1973-2002. J Am Med Assoc 2006; 295:2164-2167.
2. Enewold L, Zhu K, Ron E, et al. Rising thyroid cancer incidence in the United States by demographic and tumor characteristics, 1980-2005. Cancer Epidemiol Biomarkers Prev 2009; 18:784-791. An analysis of the SEER data demonstrates an increase in both small and largersize PTCs.
3. Cooper DS, Doherty GM, Haugen BR, et al. Management guidelines for patients with thyroid nodules and differentiated thyroid cancer. Thyroid 2006; 16:109-142.
4. Sampson E, Brierly JD, Le LW, et al. Clinical management and outcome of papillary and follicular (differentiated) thyroid cancer presenting with distant metastasis at diagnosis. Cancer 2007; 110:1451-1456. (Pubitemid 47463058)
5. Durante C, Haddy N, Baudin E, et al. Long-term outcome of 444 patients with distant metastases from papillary and follicular thyroid carcinoma: benefits and limits of radioiodine therapy. J Clin Endocrinol Metab 2006; 91:2892-2899. (Pubitemid 44271732)
6. Robbins RJ, Wan Q, Grewal RK, et al. Real-time prognosis for metastatic thyroid carcinoma based on 2-[18F]fluoro-2-deoxy-D-glucose-positron emission tomography scanning. J Clin Endocrinol Metab 2006; 91:498-505. (Pubitemid 43236915)
7. Giordano TJ, Kuick R, Thomas DG, et al. Molecular classification of papillary thyroid carcinoma: distinct BRAF, RAS, and RET/PTC mutation-specific gene expression profiles discovered by DNA microarray analysis. Oncogene 2005; 24:6646-6656.
8. Ciampi R, Nikiforov YE. RET/PTC rearrangements and BRAF mutations in thyroid tumorigenesis. Endocrinology 2007; 148:936-941. (Pubitemid 46272777)
9. Espinosa AV, Porchia L, Ringel MD. Targeting BRAF in thyroid cancer. Br J Cancer 2007; 96:16-20.
10. Ouyang B, Knauf JA, Smith EP, et al. Inhibitors of Raf kinase activity block growth of thyroid cancer cells with RET/PTC or BRAF mutations in vitro and in vivo. Clin Cancer Res 2006; 12:1785-1793.
11. Romei C, Ciampi R, Faviana P, et al. BRAFV600E mutation, but not RET/PTC rearrangements, is correlated with a lower expression of both thyroperoxidase and sodium iodide symporter genes in papillary thyroid cancer. Endocr Relat Cancer 2008; 15:511-520. An evaluation of markers of thyroid dedifferentiation as a function of oncogene expression in PTCs. (Pubitemid 351880839)
12. Mitsutake N, Miyagishi M, Mitsutake S, et al. BRAF mediates RET/PTC-induced mitogen-activated protein kinase activation in thyroid cells: functional support for requirement of the RET/PTC-RAS-BRAF pathway in papillary thyroid carcinogenesis. Endocrinology 2006; 147:1014-1019. (Pubitemid 43113021)
13. Nikiforov YE. Thyroid carcinoma: molecular pathways and therapeutic targets. Mod Pathol 2008; 21 (Suppl 2):S37-S43. Comprehensive review of the topic.
14. Xing M. BRAF mutation in papillary thyroid cancer: pathogenic role, molecular bases, and clinical implications. Endocr Rev 2007; 28:742-762. (Pubitemid 350294294)
15. Elisei R, Ugolini C, Viola D, et al. BRAF(V600E) mutation and outcome of patients with papillary thyroid carcinoma: a 15-year median follow-up study. J Clin Endocrinol Metab 2008; 93:3943-3949. Patient population with a long follow-up confirms the association between BRAF mutation and poor outcome as an independent variable.
16. Oler G, Cerutti JM. High prevalence of BRAF mutation in a Brazilian cohort of patients with sporadic papillary thyroid carcinomas: correlation with more aggressive phenotype and decreased expression of iodide-metabolizing genes. Cancer 2009; 115:972-980. Confirms the association between BRAF mutation and a more aggressive phenotype in another cohort of patients.
17. Wang Y, Ji M, Wang W, et al. Association of the T1799A BRAF mutation with tumor extrathyroidal invasion, higher peripheral platelet counts, and overexpression of platelet-derived growth factor-B in papillary thyroid cancer. Endocr Relat Cancer 2008; 15:183-190. Demonstrates an association between BRAF and PDGF in PTC.
18. Kloos RT, Ringel MD, Knopp MV, et al. Phase II trial of sorafenib in metastatic thyroid cancer. J Clin Oncol 2009; 27:1675-1684. Phase 2 clinical study of sorafenib in progressive thyroid cancer. Very high incidence of BRAF mutations in this cohort.
19. Xing M. BRAF mutation in papillary thyroid microcarcinoma: the promise of better risk management. Ann Surg Oncol 2009; 16:801-803.
20. Xing M, Clark D, Guan H, et al. BRAF mutation testing of thyroid fine-needle aspiration biopsy specimens for preoperative risk stratification in papillary thyroid cancer. J Clin Oncol 2009 [Epub ahead of print]. Study demonstrating that detection of a BRAF mutation on DNA derived from an FNA sample predicted more aggressive disease.
21. Nikiforov YE, Steward DL, Robinson-Smith TM, et al. Molecular testing for mutations in improving the fine needle aspiration diagnosis of thyroid nodules. J Clin Endocrinol Metab 2009 [Epub ahead of print]. Prospective evaluation of the utility of analysis for gene mutations in thyroid FNAs.
22. Ball DW, Jin N, Rosen DM, et al. Selective growth inhibition in BRAF mutant thyroid cancer by the mitogen-activated protein kinase kinase 1/2 inhibitor AZD6244. J Clin Endocrinol Metab 2007; 92:4712-4718. (Pubitemid 350223448)
23. Leboeuf R, Baumgartner JE, Benezra M, et al. BRAFV600E mutation is associated with preferential sensitivity to mitogen-activated protein kinase kinase inhibition in thyroid cancer cell lines. J Clin Endocrinol Metab 2008; 93:2194-2201. Demonstrates that thyroid cancer cell lines with a BRAF mutation are more sensitive to MEK inhibition in vitro. (Pubitemid 351831535)
24. Xing M, Cohen Y, Mambo E, et al. Early occurrence of RASSF1A hypermethylation and its mutual exclusion with BRAF mutation in thyroid tumorigenesis. Cancer Res 2004; 64:1664-1668. (Pubitemid 38428687)
25. Nakamura N, Carney JA, Jin L, et al. RASSF1A and NORE1A methylation and BRAFV600E mutations in thyroid tumors. Lab Invest 2005; 85:1065-1075. (Pubitemid 43073981)
26. Guan H, Ji M, Hou P, et al. Hypermethylation of the DNA mismatch repair gene hMLH1 and its association with lymph node metastasis and T1799A BRAF mutation in patients with papillary thyroid cancer. Cancer 2008; 113:247-255. Demonstrates that loss of hMLH1 occurs in thyroid cancer in association with BRAF mutations.
27. Liaw D, Marsh DJ, Li J, et al. Germline mutations of the PTEN gene in Cowden disease, an inherited breast and thyroid cancer syndrome. Nat Genet 1997; 16:64-67. (Pubitemid 27198157)
28. Ringel MD, Hayre N, Saito J, et al. Overexpression and overactivation of Akt in thyroid carcinoma. Cancer Res 2001; 61:6105-6111. (Pubitemid 32762546)
29. Vasko V, Saji M, Hardy E, et al. Akt activation and localisation correlate with tumour invasion and oncogene expression in thyroid cancer. J Med Genet 2004; 41:161-170. (Pubitemid 38333792)
30. Paes JE, Ringel MD. Dysregulation of the phosphatidylinositol 3-kinase pathway in thyroid neoplasia. Endocrinol Metab Clin North Am 2008; 37:375-387; viii-ix.
31. Garcia-Rostan G, Costa AM, Pereira-Castro I, et al. Mutation of the PIK3CA gene in anaplastic thyroid cancer. Cancer Res 2005; 65:10199-10207. (Pubitemid 41743711)
32. Wu G, Mambo E, Guo Z, et al. Uncommon mutation, but common amplifications, of the PIK3CA gene in thyroid tumors. J Clin Endocrinol Metab 2005; 90:4688-4693. (Pubitemid 41159359)
33. Abubaker J, Jehan Z, Bavi P, et al. Clinicopathological analysis of papillary thyroid cancer with PIK3CA alterations in a Middle Eastern population. J Clin Endocrinol Metab 2008; 93:611-618. PIK3CA amplifications, when associated with BRAF mutations, are associated with more aggressive tumor behavior in this population. (Pubitemid 351240838)
34. Liu Z, Hou P, Ji M, et al. Highly prevalent genetic alterations in receptor tyrosine kinases and phosphatidylinositol 3-kinase/akt and mitogen-activated protein kinase pathways in anaplastic and follicular thyroid cancers. J Clin Endocrinol Metab 2008; 93:3106-3116. More aggressive thyroid cancers are associated with genetic abnormalities in both the PI3K and ERK signaling cascades.
35. Santarpia L, El-Naggar AK, Cote GJ, et al. Phosphatidylinositol 3-kinase/akt and ras/raf-mitogen-activated protein kinase pathway mutations in anaplastic thyroid cancer. J Clin Endocrinol Metab 2008; 93:278-284. Anaplastic thyroid cancers are commonly characterized by activation of both ERK and AKT.
36. Wiseman SM, Masoudi H, Niblock P, et al. Derangement of the E-cadherin/catenin complex is involved in transformation of differentiated to anaplastic thyroid carcinoma. Am J Surg 2006; 191:581-587.
37. Kondo T, Zheng L, Liu W, et al. Epigenetically controlled fibroblast growth factor receptor 2 signaling imposes on the RAS/BRAF/mitogen-activated protein kinase pathway to modulate thyroid cancer progression. Cancer Res 2007; 67:5461-5470. (Pubitemid 46997287)
38. Cheng S, Liu W, Mercado M, et al. Expression of the melanoma associated (MAGE) antigen is associated with progression of human thyroid cancer. Endocr Relat Cancer 2009 [Epub ahead of print]. MAGE represents a potential functionally important modulator of thyroid cancer behavior.
39. Min HS, Choe G, Kim SW, et al. S100A4 expression is associated with lymph node metastasis in papillary microcarcinoma of the thyroid. Mod Pathol 2008; 21:748-755. S1004A represents a potentially functionally important modulator of thyroid cancer behavior. (Pubitemid 351744841)
40. Marlow LA, Reynolds LA, Cleland AS, et al. Reactivation of suppressed RhoB is a critical step for the inhibition of anaplastic thyroid cancer growth. Cancer Res 2009; 69:1536-1544.
41. Siraj AK, Bavi P, Abubaker J, et al.Genome-wide expression analysis of Middle Eastern papillary thyroid cancer reveals c-MET as a novel target for cancer therapy. J Pathol 2007; 213:190-199. Microarray analysis and confirmatory studies demonstrate overexpression of CMET in association with AKT signaling in progressive thyroid cancers. (Pubitemid 47612241)
42. Nappi TC, Salerno P, Zitzelsberger H, et al. Identification of Polo-like kinase 1 as a potential therapeutic target in anaplastic thyroid carcinoma. Cancer Res 2009; 69:1916-1923. Polo-like kinase 1 is identified using unbiased approaches as a potentially important signaling node in anaplastic thyroid cancer.
43. Pfister DG, Fagin JA. Refractory thyroid cancer: a paradigm shift in treatment is not far off. J Clin Oncol 2008; 26:4701-4704. Commentary in an issue of J Clin Oncol addressing new data in the use of tyrosine kinase inhibitors for progressive thyroid cancer.
44. Polyak K, Haviv I, Campbell IG. Co-evolution of tumor cells and their microenvironment. Trends Genet 2009; 25:30-38.
45. Ryder M, Ghossein RA, Ricarte-Filho JC, et al. Increased density of tumor-associated macrophages is associated with decreased survival in advanced thyroid cancer. Endocr Relat Cancer 2008; 15:1069-1074. Study describes the new finding of a high frequency of tumor-associated macrophages in anaplastic thyroid cancers.
46. Vasko V, Espinosa AV, Scouten W, et al. Gene expression and functional evidence of epithelial-to-mesenchymal transition in papillary thyroid carcinoma invasion. Proc Natl Acad Sci U S A 2007; 104:2803-2808. (Pubitemid 46327960)
47. Smallridge RC, Marlow LA, Copland JA. Anaplastic thyroid cancer: molecular pathogenesis and emerging therapies. Endocr Relat Cancer 2009; 16:17-44. Comprehensive review of the current state of knowledge regarding anaplastic thyroid cancer.
48. Wreesmann VB, Sieczka EM, Socci ND, et al. Genome-wide profiling of papillary thyroid cancer identifies MUC1 as an independent prognostic marker. Cancer Res 2004; 64:3780-3789.
49. Abrosimov A, Saenko V, Meirmanov S, et al. The cytoplasmic expression of MUC1 in papillary thyroid carcinoma of different histological variants and its correlation with cyclin D1 overexpression. Endocr Pathol 2007; 18:68-75. (Pubitemid 47574989)
50. Siragusa M, Zerilli M, Iovino F, et al. MUC1 oncoprotein promotes refractoriness to chemotherapy in thyroid cancer cells. Cancer Res 2007; 67:5522-5530. (Pubitemid 46997294)
51. Cerutti JM, Oler G, Michaluart P Jr, et al. Molecular profiling of matched samples identifies biomarkers of papillary thyroid carcinoma lymph node metastasis. Cancer Res 2007; 67:7885-7892. SAGE analysis of paired normal, primary tumor, and nodal metastases identifies several unique markers in the nodal tissue. (Pubitemid 47281384)
52. Lee JJ, Au AY, Foukakis T, et al. Array-CGH identifies cyclin D1 and UBCH10 amplicons in anaplastic thyroid carcinoma. Endocr Relat Cancer 2008; 15:801-815. Detailed analysis using array-CGH identifies several genes in anaplastic thyroid cancer with potential functional relevance.
53. Rodrigues R, Roque L, Espadinha C, et al. Comparative genomic hybridization, BRAF, RAS, RET, and oligo-array analysis in aneuploid papillary thyroid carcinomas. Oncol Rep 2007; 18:917-926. Study focuses on aneuploid PTCs and identifies several genes uniquely associated with thyroid cancer distant metastases and death from disease.
54. Jazdzewski K, Murray EL, Franssila K, et al. Common SNP in premiR-146a decreases mature miR expression and predisposes to papillary thyroid carcinoma. Proc Natl Acad Sci U S A 2008; 105:7269-7274. Identifies a polymorphism in pre-miR-146a as a predisposing gene for PTC. (Pubitemid 351754467)
55. He H, Jazdzewski K, Li W, et al. The role of microRNA genes in papillary thyroid carcinoma. Proc Natl Acad Sci U S A 2005; 102:19075-19080. (Pubitemid 43049568)
56. Pallante P, Visone R, Ferracin M, et al. MicroRNA deregulation in human thyroid papillary carcinomas. Endocr Relat Cancer 2006; 13:497-508. (Pubitemid 43886672)
57. Weber F, Teresi RE, Broelsch CE, et al. A limited set of human microRNA is deregulated in follicular thyroid carcinoma. J Clin Endocrinol Metab 2006; 91:3584-3591. (Pubitemid 44402141)
58. Chen YT, Kitabayashi N, Zhou XK, et al. MicroRNA analysis as a potential diagnostic tool for papillary thyroid carcinoma. Mod Pathol 2008; 21:1139-1146. Analyzes the relationship between particular miR profiles obtained on FNA at the time of surgery with histological diagnosis.
59. Nikiforova MN, Chiosea SI, Nikiforov YE. MicroRNA expression profiles in thyroid tumors. Endocr Pathol 2009 [Epub ahead of print].
60. Nikiforova MN, Tseng GC, Steward D, et al. MicroRNA expression profiling of thyroid tumors: biological significance and diagnostic utility. J Clin Endocrinol Metab 2008; 93:1600-1608. Identifies panels of miRs that may have diagnostic potential in thyroid cancer. (Pubitemid 351656494)