Metastasis-associated MCL1 and P16 copy number alterations dictate resistance to vemurafenib in a BRAFV600E patient-derived papillary thyroid carcinoma preclinical model

Oncotarget

Volumn 6, Issue 40, 2015, Pages 42445-42467

  Duquette, Mark ^a   Sadow, Peter M ^b   Husain, Amjad ^a   Sims, Jennifer N ^a   Antonello, Zeus A ^a   Fischer, Andrew H ^c   Song, Chen ^a   Castellanos Rizaldos, Elena ^a   Mike Makrigiorgos, G ^a   Kurebayashi, Junichi ^d   Nose, Vania ^b   Van Hummelen, Paul ^a   Bronson, Roderick T ^a   Vinco, Michelle ^e   Giordano, Thomas J ^e   Dias Santagata, Dora ^b   Pandolfi, Pier Paolo ^a   Nucera, Carmelo ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^d KAWASAKI MEDICAL SCHOOL   (Japan)

^e UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

BRAFV600E papillary thyroid cancer pre clinical model; MCL1 and P16 CDKN2A somatic copy number; Microenvironment; Vemurafenib resisatnce

Indexed keywords

B RAF KINASE; OBATOCLAX; PROTEIN MCL 1; PROTEIN P16; VEMURAFENIB; ANTINEOPLASTIC AGENT; BRAF PROTEIN, HUMAN; INDOLE DERIVATIVE; MCL1 PROTEIN, HUMAN; SULFONAMIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAF GENE; CANCER COMBINATION CHEMOTHERAPY; CANCER RESISTANCE; CAPILLARY ENDOTHELIAL CELL; CELL DEATH; CELL INVASION; CHROMOSOME 1Q; CHROMOSOME 9P; CONTROLLED STUDY; COPY NUMBER VARIATION; DOWN REGULATION; DRUG POTENTIATION; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; MCL1 GENE; METASTASIS; MIGRATION; MOUSE; NONHUMAN; P16 GENE; PAPILLARY THYROID CARCINOMA CELL; PARACRINE SIGNALING; THYROID PAPILLARY CARCINOMA; TUMOR MICROENVIRONMENT; ANIMAL; APOPTOSIS; CARCINOMA; CELL SURVIVAL; DISEASE MODEL; DNA MICROARRAY; DRUG EFFECTS; DRUG RESISTANCE; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE DOSAGE; GENETIC TRANSFECTION; GENETICS; IMMUNOHISTOCHEMISTRY; MUTATION; NEOVASCULARIZATION (PATHOLOGY); NONOBESE DIABETIC MOUSE; PATHOLOGY; SCID MOUSE; THYROID TUMOR; TUMOR SUPPRESSOR GENE; TUNEL ASSAY; WESTERN BLOTTING; XENOGRAFT;

ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; BLOTTING, WESTERN; CARCINOMA; CELL SURVIVAL; DISEASE MODELS, ANIMAL; DRUG RESISTANCE, NEOPLASM; ENZYME-LINKED IMMUNOSORBENT ASSAY; GENE DOSAGE; GENES, P16; HETEROGRAFTS; HUMANS; IMMUNOHISTOCHEMISTRY; IN SITU NICK-END LABELING; INDOLES; MICE; MICE, INBRED NOD; MICE, SCID; MUTATION; MYELOID CELL LEUKEMIA SEQUENCE 1 PROTEIN; NEOPLASM METASTASIS; NEOVASCULARIZATION, PATHOLOGIC; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PROTO-ONCOGENE PROTEINS B-RAF; SULFONAMIDES; THYROID NEOPLASMS; TRANSFECTION;

EID: 84952333894     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.6442     Document Type: Article

References (51)

1. Nucera, C., et al., B-Raf(V600E) and thrombospondin-1 promote thyroid cancer progression. Proc Natl Acad Sci U S A, 2010. 107: p. 10649-54.
2. Franco, A.T., et al., Thyrotrophin receptor signaling dependence of Braf-induced thyroid tumor initiation in mice. Proc Natl Acad Sci U S A, 2011. 108: p. 1615-20.
3. Smallridge, R.C., et al., American Thyroid Association guidelines for management of patients with anaplastic thyroid cancer. Thyroid, 2012. 22: p. 1104-39.
4. Ricarte-Filho, J.C., et al., Mutational profile of advanced primary and metastatic radioactive iodine-refractory thyroid cancers reveals distinct pathogenetic roles for BRAF, PIK3CA, and AKT1. Cancer Res, 2009. 69: p. 4885-93.
5. Network, C.G.A.R., Integrated genomic characterization of papillary thyroid carcinoma. Cell, 2014. 159: p. 676-90.
6. Xing, M., BRAF mutation in papillary thyroid cancer: pathogenic role, molecular bases, and clinical implications. Endocr Rev, 2007. 28: p. 742-62.
7. Chakravarty, D., et al., Small-molecule MAPK inhibitors restore radioiodine incorporation in mouse thyroid cancers with conditional BRAF activation. J Clin Invest, 2011. 121: p. 4700-11.
8. Xing, M., et al., Association between BRAF V600E mutation and mortality in patients with papillary thyroid cancer. JAMA, 2013. 309: p. 1493-501.
9. Elisei, R., 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: p. 3943-9.
10. Xing, M., et al., BRAF mutation testing of thyroid fine-needle aspiration biopsy specimens for preoperative risk stratification in papillary thyroid cancer. J Clin Oncol, 2009. 27: p. 2977-82.
11. Alzahrani, A.S. and M. Xing, Impact of lymph node metastases identified on central neck dissection (CND) on the recurrence of papillary thyroid cancer: potential role of BRAFV600E mutation in defining CND. Endocr Relat Cancer, 2012.
12. Xing, M., et al., BRAF V600E and TERT Promoter Mutations Cooperatively Identify the Most Aggressive Papillary Thyroid Cancer With Highest Recurrence. J Clin Oncol, 2014. 32: p. 2718-26.
13. Haugen, B.R. and M.A. Kane, Approach to the thyroid cancer patient with extracervical metastases. J Clin Endocrinol Metab, 2010. 95: p. 987-93.
14. Xing, M., Molecular pathogenesis and mechanisms of thyroid cancer. Nat Rev Cancer, 2013. 13: p. 184-99.
15. Bollag, G., et al., Clinical efficacy of a RAF inhibitor needs broad target blockade in BRAF-mutant melanoma. Nature, 2010. 467: p. 596-9.
16. Bollag, G., et al., Vemurafenib: the first drug approved for BRAF-mutant cancer. Nat Rev Drug Discov, 2012. 11: p. 873-86.
17. Kim, K.B., et al., Clinical Responses to Vemurafenib in Patients with Metastatic Papillary Thyroid Cancer Harboring BRAF(V600E) Mutation. Thyroid, 2013. 23: p. 1277-83.
18. Montero-Conde, C., et al., Relief of feedback inhibition of HER3 transcription by RAF and MEK inhibitors attenuates their antitumor effects in BRAF-mutant thyroid carcinomas. Cancer Discov, 2013. 3: p. 520-33.
19. Sullivan, R.J. and K.T. Flaherty, Resistance to BRAF-targeted therapy in melanoma. Eur J Cancer, 2013. 49: p. 1297-304.
20. Sondergaard, J.N., et al., Differential sensitivity of melanoma cell lines with BRAFV600E mutation to the specific Raf inhibitor PLX4032. J Transl Med, 2010. 8: p. 39.
21. Beroukhim, R., et al., The landscape of somatic copy-number alteration across human cancers. Nature, 2010. 463: p. 899-905.
22. Nehs, M.A., et al., Thyroidectomy with neoadjuvant PLX4720 extends survival and decreases tumor burden in an orthotopic mouse model of anaplastic thyroid cancer. Surgery, 2010. 148: p. 1154-62; discussion 1162.
23. Nucera, C., et al., Targeting BRAFV600E with PLX4720 displays potent antimigratory and anti-invasive activity in preclinical models of human thyroid cancer. Oncologist, 2011. 16: p. 296-309.
24. Nehs, M.A., et al., Late intervention with anti-BRAF(V600E) therapy induces tumor regression in an orthotopic mouse model of human anaplastic thyroid cancer. Endocrinology, 2012. 153: p. 985-94.
25. Zhang, Z., et al., Histone deacetylation of NIS promoter underlies BRAF V600E-promoted NIS silencing in thyroid cancer. Endocr Relat Cancer, 2014. 21: p. 161-73.
26. Chan, C.M., et al., Targeted inhibition of Src kinase with dasatinib blocks thyroid cancer growth and metastasis. Clin Cancer Res, 2012. 18: p. 3580-91.
27. Antonello, Z.A. and C. Nucera, Orthotopic mouse models for the preclinical and translational study of targeted therapies against metastatic human thyroid carcinoma with BRAF or wild-type BRAF. Oncogene, 2013.
28. Haq, R., et al., BCL2A1 is a lineage-specific antiapoptotic melanoma oncogene that confers resistance to BRAF inhibition. Proc Natl Acad Sci U S A, 2013. 110: p. 4321-6.
29. Champa, D., et al., Obatoclax overcomes resistance to cell death in aggressive thyroid carcinomas by countering Bcl2a1 and Mcl1 overexpression. Endocr Relat Cancer, 2014. 21: p. 755-67.
30. Faber, A.C., et al., Differential induction of apoptosis in HER2 and EGFR addicted cancers following PI3K inhibition. Proc Natl Acad Sci U S A, 2009. 106: p. 19503-8.
31. Faber, A.C., et al., mTOR inhibition specifically sensitizes colorectal cancers with KRAS or BRAF mutations to BCL-2/BCL-XL inhibition by suppressing MCL-1. Cancer Discov, 2014. 4: p. 42-52.
32. Nucera, C., et al., Human galectin-3 immunoexpression in thyroid follicular adenomas with cell atypia. J Endocrinol Invest, 2005. 28: p. 106-12.
33. Nucera, C., et al., Maternal thyroid hormones are transcriptionally active during embryo-foetal development: results from a novel transgenic mouse model. J Cell Mol Med, 2010. 14: p. 2417-35.
34. Matulonis, U.A., et al., High throughput interrogation of somatic mutations in high grade serous cancer of the ovary. PLoS One, 2011. 6: p. e24433.
35. Namba, H., et al., Clinical implication of hot spot BRAF mutation, V599E, in papillary thyroid cancers. J Clin Endocrinol Metab, 2003. 88: p. 4393-7.
36. Frasca, F., et al., BRAF(V600E) mutation and the biology of papillary thyroid cancer. Endocr Relat Cancer, 2008. 15: p. 191-205.
37. Dias-Santagata, D., et al., Rapid targeted mutational analysis of human tumours: a clinical platform to guide personalized cancer medicine. EMBO Mol Med, 2010. 2: p. 146-58.
38. Hettmer, S., et al., Mutations in Hedgehog pathway genes in fetal rhabdomyomas. J Pathol, 2013. 231: p. 44-52.
39. Li, J., et al., Antiprimer quenching-based real-time PCR and its application to the analysis of clinical cancer samples. Clin Chem, 2006. 52: p. 624-33.
40. Takei, H., et al., Low-level copy gain versus amplification of myc oncogenes in medulloblastoma: utility in predicting prognosis and survival. Laboratory investigation. J Neurosurg Pediatr, 2009. 3: p. 61-5.
41. Zack, T.I., et al., Pan-cancer patterns of somatic copy number alteration. Nat Genet, 2013. 45: p. 1134-1140.
42. Fischer, A.H., P. Taysavang, and S.M. Jhiang, Nuclear envelope irregularity is induced by RET/PTC during interphase. Am J Pathol, 2003. 163: p. 1091-100.
43. Bond, J.A., et al., In vitro reconstruction of tumour initiation in a human epithelium. Oncogene, 1994. 9: p. 281-90.
44. Fabien, N., et al., Description of a human papillary thyroid carcinoma cell line. Morphologic study and expression of tumoral markers. Cancer, 1994. 73: p. 2206-12.
45. Kurebayashi, J., et al., All-trans-retinoic acid modulates expression levels of thyroglobulin and cytokines in a new human poorly differentiated papillary thyroid carcinoma cell line, KTC-1. J Clin Endocrinol Metab, 2000. 85: p. 2889-96.
46. Shaik, S., et al., SCF(beta-TRCP) suppresses angiogenesis and thyroid cancer cell migration by promoting ubiquitination and destruction of VEGF receptor 2. J Exp Med, 2012. 209: p. 1289-307.
47. Debnath, J., S.K. Muthuswamy, and J.S. Brugge, Morphogenesis and oncogenesis of MCF-10A mammary epithelial acini grown in three-dimensional basement membrane cultures. Methods, 2003. 30: p. 256-68.
48. Ponce, M.L., In vitro matrigel angiogenesis assays. Methods Mol Med, 2001. 46: p. 205-9.
49. Shih, S.C. and L.E. Smith, Quantitative multi-gene transcriptional profiling using real-time PCR with a master template. Exp Mol Pathol, 2005. 79: p. 14-22.
50. Nucera, C., et al., A novel orthotopic mouse model of human anaplastic thyroid carcinoma. Thyroid, 2009. 19: p. 1077-84.
51. Bellelli, R., et al., FOXM1 is a molecular determinant of the mitogenic and invasive phenotype of anaplastic thyroid carcinoma. Endocr Relat Cancer, 2012. 19: p. 695-710.