Advances in thyroid cancer treatment: Latest evidence and clinical potential

Therapeutic Advances in Medical Oncology

Volumn 7, Issue 1, 2015, Pages 22-38

  Alonso Gordoa, T ^a   Diez J J ^a   Duran M ^b   Grande, Enrique ^a  

^a HOSPITAL RAMÓN Y CAJAL   (Spain)

^b HOSPITAL UNIVERSITARIO REY JUAN CARLOS   (Spain)

Author keywords

angiogenesis; phosphatidylinositide 3 kinase Akt mammalian target of rapamycin; RAS RAF mitogen activated protein kinase; targeted agents; thyroid carcinoma

Indexed keywords

CABOZANTINIB; EPIDERMAL GROWTH FACTOR RECEPTOR KINASE INHIBITOR; HYPOXIA INDUCIBLE FACTOR 1ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MAMMALIAN TARGET OF RAPAMYCIN; MAMMALIAN TARGET OF RAPAMYCIN INHIBITOR; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B INHIBITOR; PROTEIN RET; RAF PROTEIN; RAS PROTEIN; SORAFENIB; VANDETANIB; VEMURAFENIB;

CANCER THERAPY; CARCINOGENESIS; DIFFERENTIATED THYROID CANCER; EPIGENETICS; GENE MUTATION; HUMAN; MOLECULAR THERAPY; POINT MUTATION; REVIEW; SIGNAL TRANSDUCTION; THYROID CANCER; THYROID CARCINOMA; THYROID MEDULLARY CARCINOMA; WNT SIGNALING PATHWAY;

EID: 84918554601     PISSN: 17588340     EISSN: 17588359     Source Type: Journal    
DOI: 10.1177/1758834014551936     Document Type: Review

References (80)

1. Adjei A. Cohen R. Franklin W. Morris C. Wilson D. Molina J. et al. (2008) Phase I pharmacokinetic and pharmacodynamic study of the oral, small-molecule mitogen-activated protein kinase 1 / 2 inhibitor AZD 6244 (ARRY-142886) in patients with advanced cancers. J Clin Oncol 26: 2139–2146.
2. Agrawal N. Jiao Y. Sausen M. Leary R. Bettegowda C. Roberts N.J. et al. (2013) Exomic sequencing of medullary thyroid cancer reveals dominant and mutually exclusive oncogenic mutations in RET and RAS. J Clin Endocrinol Metab 98: E364–E369.
3. Ahmed M. Barbachano Y. Riddell A. Hickey J. Newbold K. Viros A. et al. (2011) Analysis of the efficacy and toxicity of sorafenib in thyroid cancer: a phase II study in a UK based population. Eur J Endocrinol 165: 315–322.
4. Akeno-Stuart N. Croyle M. Knauf J.A. Malaguarnera R. Vitagliano D. Santoro M. et al. (2007) The RET kinase inhibitor NVP-AST487 blocks growth and calcitonin gene expression through distinct mechanisms in medullary thyroid cancer cells. Cancer Res 67: 6956–6964.
5. Antonelli A. Fallahi P. Ferrari S. Mancusi C. Colaci M. Santarpia L. et al. (2012) RET TKI: potential role in thyroid cancers. Curr Oncol Rep 14: 97–104.
6. Bible K. Suman V.J. Molina J.R. Smallridge R.C. Maples W.J. Menefee M.E. et al. (2010) Efficacy of pazopanib in progressive, radioiodine-refractory, metastatic differentiated thyroid cancers: results of a phase 2 consortium study. Lancet Oncol 11: 962–972.
7. Brewer C. Yeager N. Di Cristofano A. (2007) Thyroid-stimulating hormone initiated proliferative signals converge in vivo on the mTOR kinase without activating AKT. Cancer Res 67: 8002–8006.
8. Brose M. Nutting C. Jarzab B. Elisei R. Siena S. Bastholt L. et al. (2014) Sorafenib in radioactive iodine-refractory, locally advanced or metastatic differentiated thyroid cancer: a randomised, double-blind, phase 3 trial. The Lancet 384: 319-328.
9. Cabanillas M. Waguespack S. Bronstein Y. Williams M. Feng L. Hernandez M. et al. (2010) Treatment with tyrosine kinase inhibitors for patients with differentiated thyroid cancer: the M.D. Anderson experience. J Clin Epidemiol Metab 95: 2588–2595.
10. Capdevila J. Iglesias L. Halperin I. Segura A. Martinez-Trufero J. Vaz M. et al. (2012) Sorafenib in metastatic thyroid cancer. Endocr Relat Cancer 19: 209–216.
11. Carlomagno F. Vitagliano D. Guida T. (2002) ZD6474, an orally available inhibitor of KDR tyrosine kinase activity, efficiently blocks oncogenic RET kinases. Cancer Res 62: 7284–7290.
12. Caronia L. Phay J. Shah M. (2011) Role of BRAF in thyroid oncogenesis. Clin Cancer Res 17: 7511–7517.
13. Carr L. Mankoff D. Goulart B. (2010) Phase II study of daily sunitinib in FDG-PET-positive, iodine-refractory differentiated thyroid cancer and metastatic medullary carcinoma of the thyroid with functional imaging correlation. Clin Cancer Res 16: 5260–5268.
14. Ciampi R. Mian C. Fugazzola L. Cosci B. Romei C. Barollo S. et al. (2013) Evidence of a low prevalence of RAS mutations in a large medullary thyroid cancer series. Thyroid 23: 50–57.
15. Cohen E. Rosen L.S. Vokes E. Kies M. Forastiere A. Worden F.P. et al. (2008) Axitinib is an active treatment for all histologic subtypes of advanced thyroid cancer: results from a phase II study. J Clin Oncol 26: 4708–4713.
16. de Groot J. Links T. Plukker J.T.M. Lips C.J.M. Hofstra R.M.W. et al. (2006) RET as a diagnostic and therapeutic target in sporadic and hereditary endocrine tumors. Endocr Rev 27: 535–560.
17. de Souza E. Ferreira A. de Carvalho D. (2011) The mTOR protein as a target in thyroid cancer. Exp Opin Ther Targets 15: 1099–1112.
18. de Souza J.A. Busaidy N.L. Zimrin A. Seiwert T.Y. Villaflor V.M. Poluru K.B. et al. (2010) Phase II trial of sunitinib in medullary thyroid cancer (MTC). J Clin Oncol 28(15 Suppl.): abstract 5504.
19. Deshpande H. Roman S. Jaykumar T. Ann Sosa J. et al. (2011) Vandetanib (ZD6474) in the treatment of medullary thyroid cancer. Clin Med Insights Oncol 5: 213–221.
20. Elisei R. Ugolini C. Viola D. Lupi C. Biagini A. Giannini R. et al. (2008) BRAF V600E mutation and outcome of patients with papillary thyroid carcinoma: a 15-year median follow-up study. J Clin Endocrinol Metab 93: 3943–3949.
21. Elisei R. et al. (2012) The BRAFV600E mutation is an independent, poor prognostic factor for the outcome of patients with low-risk intrathyroid papillary thyroid carcinoma: single-institution results from a large cohort study. J Clin Endocrinol Metab 97: 4390–4398.
22. Elisei R. Schlumberger M. Muller S.P. Schoffski P. Brose M.S. Shah M. et al. (2013) Cabozantinib in progressive medullary thyroid cancer. J Clin Oncol 31: 3639–3646.
23. EMA (2014) Cabozantinib. Summary of Product Characteristics. London: European Medicines Agency.
24. Frank-Raue K. Rondot S. Raue F. (2010) Molecular and cellular endocrinology. Mol Cell Endocrinol 322: 2–7.
25. Fukahori M. Yoshida A. Hayashi H. Yoshihara M. Matsukuma S. Sakuma Y. et al. (2012) The associations between RAS mutations and clinical characteristics in follicular thyroid tumors: new insights from a single center and a large patient cohort. Thyroid 22: 683–689.
26. Garcia-Echeverria C. Sellers W. (2008) Drug discovery approaches targeting the PI3K/Akt pathway in cancer. Oncogene 27: 5511–5526.
27. Garcia-Rostan G. Tallini G. Herrero A D Aquila T. Carcangiu M. Rimm D. et al. (1999) Frequent mutation and nuclear localization of beta-catenin in anaplastic thyroid carcinoma. Cancer Res 59: 1811–1815.
28. Garcia-Rostan G. Camp R.L. Herrero A. Carcangiu M.L. Rimm D.L. Tallini G. et al. (2001) Beta-catenin dysregulation in thyroid neoplasms. Down-regulation, aberrant nuclear expression, and CTNNB 1 exon 3 mutations are markers for aggressive tumor phenotypes and poor prognosis. Am J Pathol 158: 987–996.
29. Garcia-Rostan G. Zhao H. Camp R.L. Pollan M. Herrero A. Pardo J. et al. (2003) ras mutations are associated with aggressive tumor phenotypes and poor prognosis in thyroid cancer. J Clin Oncol 21: 3226–3235.
30. Guerra A. Zeppa P. Bifulco M. Vitale M. (2014) Concomitant BRAF V600E mutation and RET / PTCRe arrangement is a frequent occurrence in papillary thyroid carcinoma. Thyroid 24: 254–259.
31. Gupta-Abramson V. Troxel A. Nellore A. Puttaswamy K. Redlinger M. Ransone K V. et al. (2008) Phase II trial of sorafenib in advanced thyroid cancer. J Clin Oncol 26: 4714–4719.
32. Hamatani K. Eguchi H. Ito R. Mukai M. Takahashi K. Taga M. et al. (2008) RET / PTC rearrangements preferentially occurred in papillary thyroid cancer among atomic bomb survivors exposed to high radiation dose. Cancer Res 68: 7176–7182.
33. Harris P. Bible K. (2011) Emerging therapeutics for advanced thyroid malignancies: rationale and targeted approaches. Exp Opin Investig Drugs 20: 1357–1375.
34. Hayes D. Lucas A. Tanvetyanon T. Krzyzanowska M.K. Chung C.H. Murphy B.A. et al. (2012) Phase II efficacy and pharmacogenomic study of selumetinib (AZD6244; ARRY-142886) in iodine-131 refractory papillary thyroid carcinoma with or without follicular elements. Clin Cancer Res 18: 2056–2065.
35. Ho A.L. Grewal R. Leboeuf R. Sherman E. Pfister D.G. Deandreis D. et al. (2013) Selumetinib-enhanced radioiodine uptake in advanced thyroid cancer. N Engl J Med 368: 623–632.
36. Holden S.N. Eckhardt S.G. Basser R. de Boer R. Rischin D. Green M. et al. (2005) Clinical evaluation of ZD6474, an orally active inhibitor of VEGF and EGF receptor signaling, in patients with solid, malignant tumors. Ann Oncol 16: 1391–1397.
37. Hu S. Liu D. Tufano R. Carson K. Rosenbaum E. Cohen Y. et al. (2006) Association of aberrant methylation of tumor suppressor genes with tumor aggressiveness and BRAF mutation in papillary thyroid cancer. Int J Cancer 119: 2322–2329.
38. Jin N. Jiang T. Rosen D.M. Nelkin B.D. Ball D.W. et al. (2011) Synergistic action of a RAF inhibitor and a dual PI3K/mTOR inhibitor in thyroid cancer. Clin Cancer Res 17: 6482–6489.
39. Kebebew E. Lindsay S.H.C.O. Woeber K. Hawkins R.E. Greenspan F. et al. (2009) Results of rosiglitazone therapy in patients with thyroglobulin-positive and radioiodine-negative advanced differentiated thyroid cancer. Thyroid 19: 953–956.
40. Kim K.B. Cabanillas M.E. Lazar A.J. Williams M.D. Sanders D.L. Ilagan J.L. et al. (2013) Clinical responses to vemurafenib in patients with metastatic papillary thyroid cancer harboring BRAF V600E mutation. Thyroid 23: 1277–1283.
41. Kloos R.T. Ringel M.D. Knopp M.V. Hall N.C. King M. Stevens R. et al. (2009) Phase II trial of sorafenib in metastatic thyroid cancer. J Clin Oncol 27: 1675–1684.
42. Kondo T. Zheng L. Liu W. Kurebayashi J. Asa S.L. Ezzat S. et al. (2007) 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 67: 5461–5470.
43. Kurzrock R. Sherman S.I. Ball D.W. Forastiere A.A. Cohen R.B. Mehra R. et al. (2011) Activity of XL 184 (cabozantinib), an oral tyrosine kinase inhibitor, in patients with medullary thyroid cancer. J Clin Oncol 29: 2660–2666.
44. Lam E.T. Ringel M.D. Kloos R.T. Prior T.W. Knopp M.V. Liang J. et al. (2010) Phase II clinical trial of sorafenib in metastatic medullary thyroid cancer. J Clin Oncol 28: 2323–2330.
45. Leboeuf R. Baumgartner J.E. Benezra M. Malaguarnera R. Solit D. Pratilas C.A. et al. (2008) BRAF V600E mutation is associated with preferential sensitivity to mitogen-activated protein kinase kinase inhibition in thyroid cancer cell lines. J Clin Endocrinol Metab 93: 2194–2201.
46. Leboulleux S. Bastholt L. Krause T. de la Fouchardiere C. Tennvall J. Awada A. et al. (2012) Vandetanib in locally advanced or metastatic differentiated thyroid cancer: a randomised, double-blind, phase 2 trial. Lancet Oncol 13: 897–905.
47. Li C. Lee K.C. Schneider E.B. Zeiger M.A. et al. (2012) BRAFV600E mutation and its association with clinicopathological features of papillary thyroid cancer: a meta-analysis. J Clin Endocrinol Metab 97: 4559–4570.
48. Lim S.M. Chang H. Yoon M.J. Hong Y.K. Kim H. Chung W.Y. et al. (2013) A multicenter, phase II trial of everolimus in locally advanced or metastatic thyroid cancer of all histologic subtypes. Ann Oncol 24: 3089–3094.
49. Liu Z. Hou P. Ji M. Guan H. Studeman K. Jensen K. et al. (2008) 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 93: 3106–3116.
50. Moura M.M. Cavaco B.M. Pinto A.E. Leite V. et al. (2011) High prevalence of RAS mutations in RET-negative sporadic medullary thyroid carcinomas. J Clin Endocrinol Metab 96: E863–E868.
51. Mulligan L. (2014) RET revisited: expanding theoncogenic portfolio. Nat Rev Cancer 14: 173–186.
52. Nikiforov Y. (2002) RET / PTC rearrangement in thyroid tumors. Endocr Pathol 13: 1–14.
53. Nikiforova M. Nikiforov Y. (2008) Molecular genetics of thyroid cancer: implications for diagnosis, treatment and prognosis. Exp Rev Mol Diagn 8: 83–95.
54. Nikiforov Y. Nikiforova M. (2011) Molecular genetics and diagnosis of thyroid cancer. Nat Rev Endocrinol 7: 569–580.
55. Nucera C. Nehs M.A. Nagarkatti S.S. Sadow P.M. Mekel M. Fischer A.H. et al. (2011) Targeting BRAFV600E with PLX 4720 displays potent antimigratory and anti-invasive activity in preclinical models of human thyroid cancer. The Oncologist 16: 296–309.
56. Omur O. Baran Y. (2014) An update on molecular biology of thyroid cancers. Crit Rev Oncol Hematol 90: 233-252.
57. Pallante P. (2006) MicroRNA deregulation in human thyroid papillary carcinomas. Endocr Relat Cancer 13: 497–508.
58. Peters S. Adjei A. (2012) MET: a promising anticancer therapeutic target. Nat Rev Clin Oncol 9: 314–326.
59. Pusztaszeri M. Bongiovanni M. Faquin W. (2014) Update on the cytologic and molecular features of medullary thyroid carcinoma. Adv Anat Pathol 21: 26–35.
60. Ravaud A. La Fouchardiere de C. Courbon F. Asselineau J. Klein M. Nicoli-Sire P. et al. (2008) Sunitinib in patients with refractory advanced thyroid cancer: the THYSU phase II trial. J Clin Oncol 26(15 Suppl.): abstract 6058.
61. Rezk S. Brynes R.K. Nelson V. Thein M. Patwardhan N. Fischer A. et al. (2004) Beta-catenin expression in thyroid follicular lesions: potential role in nuclear envelope changes in papillary carcinomas. Endocr Pathol 15: 329–338.
62. Ricarte-Filho J.C. Ryder M. Chitale D.A. Rivera M. Heguy A. Ladanyi M. et al. (2009) Mutational profile of advanced primary and metastatic radioactive iodine-refractory thyroid cancers reveals distinct pathogenetic roles for BRAF, PIK3CA, and AKT1. Cancer Res 69: 4885–4893.
63. Savvides P. Nagaiah G. Lavertu P. Fu P. Wright J.J. Chapman R. et al. (2013) Phase II trial of sorafenib in patients with advanced anaplastic carcinoma of the thyroid. Thyroid 23: 600–604.
64. Schlumberger M.J. Elisei R. Bastholt L. Wirth L.J. Martins R.G. Locati L.D. et al. (2009) Phase II study of safety and efficacy of motesanib in patients with progressive or symptomatic, advanced or metastatic medullary thyroid cancer. J Clin Oncol 27: 3794–3801.
65. Schlumberger M. Jarzab B. Cabanillas M.E. Robinson B.G. Pacini F. Ball D.W. et al. (2012) A phase II trial of the multitargeted kinase inhibitor lenvatinib (E7080) in advanced medullary thyroid cancer (MTC). J Clin Oncol 30(Suppl.): abstract 5591.
66. Schlumberger M. Tahara M. Wirth L.J. Robinson B. Brose M.S. Elisei R. et al. (2014) A phase 3, multicenter, randomized, double-blind, placebo-controlled trial of lenvatinib (E7080) in patients with 131I-refractory differentiated thyroid cancer (SELECT). J Clin Oncol 32(5 Suppl.): abstract 6008.
67. Schneider T.C. Abdulrahman R.M. Corssmit E.P. Morreau H. Smit J.W.A. Kapiteijn E. et al. (2012) Long-term analysis of the efficacy and tolerability of sorafenib in advanced radio-iodine refractory differentiated thyroid carcinoma: final results of a phase II trial. Eur J Endocrinol 167: 643–650.
68. Shen C. Qiu Z. Luo Q. (2014) Sorafenib in the treatment of radioiodine-refractory differentiated thyroid cancer: a meta-analysis. Endocr Relat Cancer 21: 253–261.
69. Sherman S.I. Wirth L.J. Droz J.P. Hofmann M. Bastholt L. Martins R.G. et al. (2008) Motesanib diphosphate in progressive differentiated thyroid cancer. N Engl J Med 359: 31–42.
70. Sherman S.I. Cohen E.E.W. Schoffski P. Elisei R. Schlumberger M. Wirth L.J. et al. (2013) Efficacy of cabozantinib (Cabo) in medullary thyroid cancer (MTC) patients with RAS or RET mutations: results from a phase 3 study. J Clin Oncol 31(15 Suppl.): abstract 6000.
71. Tamura T. Minami H. Yamada Y. Yamamoto N. Shimoyama T. Murakami H. et al. (2006) A phase I dose-escalation study of ZD 6474 in Japanese patients with solid, malignant tumors. J Thorac Oncol 1: 1002-1009.
72. Tuttle R. Ball D. Byrd D. (2013) Thyroid carcinoma. NCCN Clinical Practice Guidelines in Oncology (NCCN Guidelines) Version 2.2013. Fort Washington, PA: National Comprehensive Cancer Network.
73. Viola D. Cappagli V. Elisei R. (2013) Cabozantinib (XL184) for the treatment of locally advanced or metastatic progressive medullary thyroid cancer. Fut Oncol 9: 1083–1092.
74. Volante M. Rapa I. Gandhi M. Bussolati G. Giachino D. Papotti M. et al. (2009) RAS mutations are the predominant molecular alteration in poorly differentiated thyroid carcinomas and bear prognostic impact. J Clin Endocrinol Metab 94: 4735–4741.
75. Wells S.A. Gosnell J.E. Gagel R.F. Moley J. Pfister D. Sosa J.A. et al. (2010) Vandetanib for the treatment of patients with locally advanced or metastatic hereditary medullary thyroid cancer. J Clin Oncol 28: 767–772.
76. Wells S.A. Robinson B.G. Gagel R.F. Dralle H. Fagin J.A. Santoro M. et al. (2012) Vandetanib in patients with locally advanced or metastatic medullary thyroid cancer: a randomized, double-blind phase III trial. J Clin Oncol 30: 134–141.
77. Xing M. (2007) Gene methylation in thyroid tumorigenesis. Endocrinology 148: 948–953.
78. Xing M. (2013) Molecular pathogenesis and mechanisms of thyroid cancer. Nat Rev Cancer 13: 184–199.
79. Xing M. Haugen B. Schlumberger M. (2013) Progress in molecular-based management of differentiated thyroid cancer. The Lancet 381: 1058–1069.
80. Yakes F.M. Chen J. Tan J. Yamaguchi K. Shi Y. Yu P. et al. (2011) Cabozantinib (XL184), a novel MET and VEGFR 2 inhibitor, simultaneously suppresses metastasis, angiogenesis, and tumor growth. Mol Cancer Ther 10: 2298–2308.