BRAFV600E-Associated Gene Expression Profile: Early Changes in the Transcriptome, Based on a Transgenic Mouse Model of Papillary Thyroid Carcinoma

PLoS ONE

Volumn 10, Issue 12, 2015, Pages

  Rusinek, Dagmara ^a   Swierniak, Michal ^a,b   Chmielik, Ewa ^a   Kowal, Monika ^a   Kowalska, Malgorzata ^a   Cyplinska, Renata ^a   Czarniecka, Agnieszka ^a   Piglowski, Wojciech ^a   Korfanty, Joanna ^a   Chekan, Mykola ^a   Krajewska, Jolanta ^a   Szpak Ulczok, Sylwia ^a   Jarzab, Michal ^a   Widlak, Wieslawa ^a   Jarzab, Barbara ^a  

^a INSTITUTE OF ONCOLOGY   (Poland)

^b MEDICAL UNIVERSITY OF WARSAW   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

B RAF KINASE; PROTEIN RET; TRANSCRIPTOME;

AACS GENE; ALDH3B1 GENE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAF GENE; CARCINOGENESIS; CLINICAL ARTICLE; CLINICAL FEATURE; COHORT ANALYSIS; CONTROLLED STUDY; GENE; GENE EXPRESSION; GENE IDENTIFICATION; GENE MUTATION; GENE SEQUENCE; HISTOPATHOLOGY; HUMAN; HUMAN TISSUE; ITPR3 GENE; LAD1 GENE; MMD GENE; MOUSE; NONHUMAN; ONCOGENE RAS; PROTEIN EXPRESSION; PVRL3 GENE; RASA1 GENE; RET GENE; THYROID CARCINOMA; ANIMAL; CARCINOMA; FEMALE; GENE EXPRESSION REGULATION; GENETICS; MALE; METABOLISM; MICROARRAY ANALYSIS; MISSENSE MUTATION; THYROID TUMOR; TRANSGENIC MOUSE;

ANIMALS; CARCINOMA; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MALE; MICE; MICE, TRANSGENIC; MICROARRAY ANALYSIS; MUTATION, MISSENSE; PROTO-ONCOGENE PROTEINS B-RAF; THYROID NEOPLASMS; TRANSCRIPTOME;

EID: 84961322379     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0143688     Document Type: Article

References (55)

1. Davies H, Bignell GR, Cox C, Stephens P, Edkins S, Clegg S, et al. Mutations of the BRAF gene in human cancer. Nature. 2002; 417(6892):949-54. Epub 2002/06/18. doi: 10.1038/nature00766 nature00766 [pii]. PMID: 12068308.
2. Cohen Y, Xing M, Mambo E, Guo Z, Wu G, Trink B, et al. BRAF mutation in papillary thyroid carcinoma. J Natl Cancer Inst. 2003; 95(8):625-7. Epub 2003/04/17. PMID: 12697856.
3. Xing M, Tufano RP, Tufaro AP, Basaria S, Ewertz M, Rosenbaum E, et al. Detection of BRAF mutation on fine needle aspiration biopsy specimens: a new diagnostic tool for papillary thyroid cancer. J Clin Endocrinol Metab. 2004; 89(6):2867-72. Epub 2004/06/08. doi: 10.1210/jc.2003-032050 89/6/2867 [pii]. PMID: 15181070.
4. Soares P, Trovisco V, Rocha AS, Lima J, Castro P, Preto A, et al. BRAF mutations and RET/PTC rearrangements are alternative events in the etiopathogenesis of PTC. Oncogene. 2003; 22(29):4578-80. Epub 2003/07/26. doi: 10.1038/sj.onc.1206706 1206706 [pii]. PMID: 12881714.
5. Brzezianska E, Pastuszak-Lewandoska D, Wojciechowska K, Migdalska-Sek M, Cyniak-Magierska A, Nawrot E, et al. Investigation of V600E BRAF mutation in papillary thyroid carcinoma in the Polish population. Neuro Endocrinol Lett. 2007; 28(4):351-9. Epub 2007/08/19. doi: NEL280407A08 [pii]. PMID: 17693984.
6. Wan PT, Garnett MJ, Roe SM, Lee S, Niculescu-Duvaz D, Good VM, et al. Mechanism of activation of the RAF-ERK signaling pathway by oncogenic mutations of B-RAF. Cell. 2004; 116(6):855-67. Epub 2004/03/24. doi: S0092867404002156 [pii]. PMID: 15035987.
7. Faustino A, Couto JP, Populo H, Rocha AS, Pardal F, Cameselle-Teijeiro JM, et al. mTOR pathway overactivation in BRAF mutated papillary thyroid carcinoma. J Clin Endocrinol Metab. 2012; 97(7): E1139-49. Epub 2012/05/03. doi: 10.1210/jc.2011-2748 jc.2011-2748 [pii]. PMID: 22549934.
8. Fagin JA. Challenging dogma in thyroid cancer molecular genetics-role of RET/PTC and BRAF in tumor initiation. J Clin Endocrinol Metab. 2004; 89(9):4264-6. Epub 2004/09/10. doi: 10.1210/jc.2004-1426 89/9/4264 [pii]. PMID: 15356019.
9. Knauf JA, Ma X, Smith EP, Zhang L, Mitsutake N, Liao XH, et al. Targeted expression of BRAFV600E in thyroid cells of transgenic mice results in papillary thyroid cancers that undergo dedifferentiation. Cancer Res. 2005; 65(10):4238-45. Epub 2005/05/19. doi: 65/10/4238 [pii] doi: 10.1158/0008-5472. CAN-05-0047 PMID: 15899815.
10. Mitsutake N, Knauf JA, Mitsutake S, Mesa C Jr., Zhang L, Fagin JA. Conditional BRAFV600E expression induces DNA synthesis, apoptosis, dedifferentiation, and chromosomal instability in thyroid PCCL3 cells. Cancer Res. 2005; 65(6):2465-73. Epub 2005/03/23. doi: 65/6/2465 [pii] doi: 10.1158/0008-5472.CAN-04-3314 PMID: 15781663.
11. Mitsutake N, Miyagishi M, Mitsutake S, Akeno N, Mesa C Jr., Knauf JA, 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(2):1014-9. Epub 2005/10/29. doi: en.2005-0280 [pii] doi: 10.1210/en.2005-0280 PMID: 16254036.
12. Xu X, Quiros RM, Gattuso P, Ain KB, Prinz RA. High prevalence of BRAF gene mutation in papillary thyroid carcinomas and thyroid tumor cell lines. Cancer Res. 2003; 63(15):4561-7. Epub 2003/08/09. PMID: 12907632.
13. Vasko V, Hu S, Wu G, Xing JC, Larin A, Savchenko V, et al. High prevalence and possible de novo formation of BRAF mutation in metastasized papillary thyroid cancer in lymph nodes. J Clin Endocrinol Metab. 2005; 90(9):5265-9. Epub 2005/07/07. doi: jc.2004-2353 [pii] doi: 10.1210/jc.2004-2353 PMID: 15998781.
14. Nikiforova MN, Kimura ET, Gandhi M, Biddinger PW, Knauf JA, Basolo F, et al. BRAF mutations in thyroid tumors are restricted to papillary carcinomas and anaplastic or poorly differentiated carcinomas arising from papillary carcinomas. J Clin Endocrinol Metab. 2003; 88(11):5399-404. Epub 2003/11/07. doi: 10.1210/jc.2003-030838 PMID: 14602780.
15. Lupi C, Giannini R, Ugolini C, Proietti A, Berti P, Minuto M, et al. Association of BRAF V600E mutation with poor clinicopathological outcomes in 500 consecutive cases of papillary thyroid carcinoma. J Clin Endocrinol Metab. 2007; 92(11):4085-90. Epub 2007/09/06. doi: jc.2007-1179 [pii] doi: 10.1210/jc. 2007-1179 PMID: 17785355.
16. Wang Y, Ji M, Wang W, Miao Z, Hou P, Chen X, et al. Association of the T1799A BRAF mutation with tumor extrathyroidal invasion, higher peripheral platelet counts, and over-expression of platelet-derived growth factor-B in papillary thyroid cancer. Endocr Relat Cancer. 2008; 15(1):183-90. Epub 2008/03/04. doi: 10.1677/ERC-07-0182 15/1/183 [pii]. PMID: 18310286.
17. Xing M, Alzahrani AS, Carson KA, Viola D, Elisei R, Bendlova B, et al. Association between BRAF V600E mutation and mortality in patients with papillary thyroid cancer. JAMA. 2013; 309(14):1493-501. Epub 2013/04/11. doi: 10.1001/jama.2013.3190 1677371 [pii]. PMID: 23571588; PubMed Central PMCID: PMC3791140.
18. Guerra A, Fugazzola L, Marotta V, Cirillo M, Rossi S, Cirello V, et al. A high percentage of BRAFV600E alleles in papillary thyroid carcinoma predicts a poorer outcome. J Clin Endocrinol Metab. 2012; 97 (7):2333-40. Epub 2012/04/18. doi: 10.1210/jc.2011-3106 jc.2011-3106 [pii]. PMID: 22508706.
19. Kaplan FM, Shao Y, Mayberry MM, Aplin AE. Hyperactivation of MEK-ERK1/2 signaling and resistance to apoptosis induced by the oncogenic B-RAF inhibitor, PLX4720, in mutant N-RAS melanoma cells. Oncogene. 2011; 30(3):366-71. Epub 2010/09/08. doi: 10.1038/onc.2010.408 onc2010408 [pii]. PMID: 20818433.
20. Tuma RS. Getting around PLX4032: studies turn up unusual mechanisms of resistance to melanoma drug. J Natl Cancer Inst. 2011; 103(3):170-1, 7. Epub 2011/01/19. doi: 10.1093/jnci/djr016 djr016 [pii]. PMID: 21242335.
21. Frattini M, Ferrario C, Bressan P, Balestra D, De Cecco L, Mondellini P, et al. Alternative mutations of BRAF, RET and NTRK1 are associated with similar but distinct gene expression patterns in papillary thyroid cancer. Oncogene. 2004; 23(44):7436-40. Epub 2004/07/27. doi: 10.1038/sj.onc.1207980 1207980 [pii]. PMID: 15273715.
22. Giordano TJ, Kuick R, Thomas DG, Misek DE, Vinco M, Sanders D, 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(44):6646-56. Epub 2005/07/12. doi: 1208822 [pii] doi: 10.1038/sj.onc.1208822 PMID: 16007166.
23. Oler G, Camacho CP, Hojaij FC, Michaluart P Jr., Riggins GJ, Cerutti JM. Gene expression profiling of papillary thyroid carcinoma identifies transcripts correlated with BRAF mutational status and lymph node metastasis. Clin Cancer Res. 2008; 14(15):4735-42. Epub 2008/08/05. doi: 10.1158/1078-0432. CCR-07-4372 14/15/4735 [pii]. PMID: 18676742; PubMed Central PMCID: PMC2742302.
24. Rusinek D, Szpak-Ulczok S, Jarzab B. Gene expression profile of human thyroid cancer in relation to its mutational status. J Mol Endocrinol. 2011; 47(3):R91-103. Epub 2011/07/30. doi: 10.1530/JME-11-0023 JME-11-0023 [pii]. PMID: 21798995.
25. Integrated genomic characterization of papillary thyroid carcinoma. Cell. 2014; 159(3):676-90. Epub 2014/11/25. doi: 10.1016/j.cell.2014.09.050 S0092-8674(14)01238-0 [pii]. PMID: 25417114; PubMed Central PMCID: PMC4243044.
26. Sims AH, Smethurst GJ, Hey Y, Okoniewski MJ, Pepper SD, Howell A, et al. The removal of multiplicative, systematic bias allows integration of breast cancer gene expression datasets-improving metaanalysis and prediction of prognosis. BMC Med Genomics. 2008; 1:42. Epub 2008/09/23. doi: 10.1186/1755-8794-1-42 1755-8794-1-42 [pii]. PMID: 18803878; PubMed Central PMCID: PMC2563019.
27. Edgar R, Domrachev M, Lash AE. Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res. 2002; 30(1):207-10. Epub 2001/12/26. PMID: 11752295; PubMed Central PMCID: PMC99122.
28. Fagin JA. How thyroid tumors start and why it matters: kinase mutants as targets for solid cancer pharmacotherapy. J Endocrinol. 2004; 183(2):249-56. Epub 2004/11/09. doi: 183/2/249 [pii] doi: 10.1677/joe.1.05895 PMID: 15531713.
29. Fugazzola L, Puxeddu E, Avenia N, Romei C, Cirello V, Cavaliere A, et al. Correlation between BRAFV600E mutation and clinico-pathologic parameters in papillary thyroid carcinoma: data from a multicentric Italian study and review of the literature. Endocr Relat Cancer. 2006; 13(2):455-64. Epub 2006/05/27. doi: 13/2/455 [pii] doi: 10.1677/erc.1.01086 PMID: 16728573.
30. Truta B, Allen BA, Conrad PG, Kim YS, Berk T, Gallinger S, et al. Genotype and phenotype of patients with both familial adenomatous polyposis and thyroid carcinoma. Fam Cancer. 2003; 2(2):95-9. Epub 2003/10/24. doi: 5145666 [pii]. PMID: 14574158.
31. Nakazawa T, Celestino R, Machado JC, Cameselle-Teijeiro JM, Vinagre J, Eloy C, et al. Cribriformmorular variant of papillary thyroid carcinoma displaying poorly differentiated features. Int J Surg Pathol. 2013; 21(4):379-89. Epub 2013/01/26. doi: 10.1177/1066896912473355 1066896912473355 [pii]. PMID: 23349472.
32. Jung CK, Choi YJ, Lee KY, Bae JS, Kim HJ, Yoon SK, et al. The cytological, clinical, and pathological features of the cribriform-morular variant of papillary thyroid carcinoma and mutation analysis of CTNNB1 and BRAF genes. Thyroid. 2009; 19(8):905-13. Epub 2009/06/19. doi: 10.1089/thy.2008. 0332 PMID: 19534622.
33. Schuetze D, Hoschar AP, Seethala RR, Assaad A, Zhang X, Hunt JL. The T1799A BRAF mutation is absent in cribriform-morular variant of papillary carcinoma. Arch Pathol Lab Med. 2009; 133(5):803-5. Epub 2009/05/07. doi: 10.1043/1543-2165-133.5.803 2008-0304-OA [pii]. PMID: 19415957.
34. Yachida S, Mudali S, Martin SA, Montgomery EA, Iacobuzio-Donahue CA. Beta-catenin nuclear labeling is a common feature of sessile serrated adenomas and correlates with early neoplastic progression after BRAF activation. Am J Surg Pathol. 2009; 33(12):1823-32. Epub 2009/09/12. doi: 10.1097/PAS. 0b013e3181b6da19 PMID: 19745699; PubMed Central PMCID: PMC2788075.
35. Delmas V, Beermann F, Martinozzi S, Carreira S, Ackermann J, Kumasaka M, et al. Beta-catenin induces immortalization of melanocytes by suppressing p16INK4a expression and cooperates with NRas in melanoma development. Genes Dev. 2007; 21(22):2923-35. Epub 2007/11/17. doi: 21/22/2923 [pii] doi: 10.1101/gad.450107 PMID: 18006687; PubMed Central PMCID: PMC2049194.
36. Knauf JA, Sartor MA, Medvedovic M, Lundsmith E, Ryder M, Salzano M, et al. Progression of BRAFinduced thyroid cancer is associated with epithelial-mesenchymal transition requiring concomitant MAP kinase and TGFbeta signaling. Oncogene. 2011; 30(28):3153-62. Epub 2011/03/09. doi: 10. 1038/onc.2011.44 onc201144 [pii]. PMID: 21383698; PubMed Central PMCID: PMC3136543.
37. Nucera C, Porrello A, Antonello ZA, Mekel M, Nehs MA, Giordano TJ, et al. B-Raf(V600E) and thrombospondin-1 promote thyroid cancer progression. Proc Natl Acad Sci U S A. 2010; 107(23):10649-54. Epub 2010/05/26. doi: 10.1073/pnas.1004934107 1004934107 [pii]. PMID: 20498063; PubMed Central PMCID: PMC2890809.
38. Franco AT, Malaguarnera R, Refetoff S, Liao XH, Lundsmith E, Kimura S, et al. Thyrotrophin receptor signaling dependence of Braf-induced thyroid tumor initiation in mice. Proc Natl Acad Sci U S A. 2011; 108(4):1615-20. Epub 2011/01/12. doi: 10.1073/pnas.1015557108 1015557108 [pii]. PMID: 21220306; PubMed Central PMCID: PMC3029699.
39. Orim F, Bychkov A, Shimamura M, Nakashima M, Ito M, Matsuse M, et al. Thyrotropin signaling confers more aggressive features with higher genomic instability on BRAF(V600E)-induced thyroid tumors in a mouse model. Thyroid. 2014; 24(3):502-10. Epub 2013/08/09. doi: 10.1089/thy.2013.0038 PMID: 23924149; PubMed Central PMCID: PMC3949501.
40. Charles RP, Iezza G, Amendola E, Dankort D, McMahon M. Mutationally activated BRAF(V600E) elicits papillary thyroid cancer in the adult mouse. Cancer Res. 2011; 71(11):3863-71. Epub 2011/04/23. doi: 10.1158/0008-5472.CAN-10-4463 0008-5472.CAN-10-4463 [pii]. PMID: 21512141; PubMed Central PMCID: PMC3107361.
41. Hebrant A, van Staveren WC, Delys L, Solis DW, Bogdanova T, Andry G, et al. Long-term EGF/serumtreated human thyrocytes mimic papillary thyroid carcinomas with regard to gene expression. Exp Cell Res. 2007; 313(15):3276-84. Epub 2007/08/11. doi: S0014-4827(07)00282-0 [pii] doi: 10.1016/j.yexcr. 2007.06.019 PMID: 17689531.
42. Vasko V, Ferrand M, Di Cristofaro J, Carayon P, Henry JF, de Micco C. Specific pattern of RAS oncogene mutations in follicular thyroid tumors. J Clin Endocrinol Metab. 2003; 88(6):2745-52. Epub 2003/06/06. doi: 10.1210/jc.2002-021186 PMID: 12788883.
43. Hou P, Liu D, Shan Y, Hu S, Studeman K, Condouris S, et al. Genetic alterations and their relationship in the phosphatidylinositol 3-kinase/Akt pathway in thyroid cancer. Clin Cancer Res. 2007; 13(4):116170. Epub 2007/02/24. doi: 13/4/1161 [pii] doi: 10.1158/1078-0432.CCR-06-1125 PMID: 17317825.
44. Pita JM, Figueiredo IF, Moura MM, Leite V, Cavaco BM. Cell cycle deregulation and TP53 and RAS mutations are major events in poorly differentiated and undifferentiated thyroid carcinomas. J Clin Endocrinol Metab. 2014:jc20131512. Epub 2014/01/16. doi: 10.1210/jc.2013-1512 PMID: 24423316.
45. Durand S, Ferraro-Peyret C, Joufre M, Chave A, Borson-Chazot F, Selmi-Ruby S, et al. Molecular characteristics of papillary thyroid carcinomas without BRAF mutation or RET/PTC rearrangement: relationship with clinico-pathological features. Endocr Relat Cancer. 2009; 16(2):467-81. Epub 2009/02/12. doi: 10.1677/ERC-08-0081 ERC-08-0081 [pii]. PMID: 19208736.
46. Cheng SP, Yin PH, Chang YC, Lee CH, Huang SY, Chi CW. Differential roles of leptin in regulating cell migration in thyroid cancer cells. Oncol Rep. 2010; 23(6):1721-7. Epub 2010/04/30. PMID: 20428831.
47. Durante C, Puxeddu E, Ferretti E, Morisi R, Moretti S, Bruno R, et al. BRAF mutations in papillary thyroid carcinomas inhibit genes involved in iodine metabolism. J Clin Endocrinol Metab. 2007; 92 (7):2840-3. Epub 2007/05/10. doi: jc.2006-2707 [pii] doi: 10.1210/jc.2006-2707 PMID: 17488796.
48. Eder JP, Vande Woude GF, Boerner SA, LoRusso PM. Novel therapeutic inhibitors of the c-Met signaling pathway in cancer. Clin Cancer Res. 2009; 15(7):2207-14. Epub 2009/03/26. doi: 10.1158/1078-0432.CCR-08-1306 1078-0432.CCR-08-1306 [pii]. PMID: 19318488.
49. Mujoo K, Choi BK, Huang Z, Zhang N, An Z. Regulation of ERBB3/HER3 signaling in cancer. Oncotarget. 2014; 5(21):10222-36. Epub 2014/11/18. doi: 2655 [pii]. PMID: 25400118; PubMed Central PMCID: PMC4279368.
50. Li W, He F. Monocyte to macrophage differentiation-Associated (MMD) targeted by miR-140-5p regulates tumor growth in non-small cell lung cancer. Biochem Biophys Res Commun. 2014; 450(1):84450. Epub 2014/06/28. doi: 10.1016/j.bbrc.2014.06.075 S0006-291X(14)01149-8 [pii]. PMID: 24971538.
51. Shibao K, Fiedler MJ, Nagata J, Minagawa N, Hirata K, Nakayama Y, et al. The type III inositol 1,4,5-trisphosphate receptor is associated with aggressiveness of colorectal carcinoma. Cell Calcium. 2010; 48(6):315-23. Epub 2010/11/16. doi: 10.1016/j.ceca.2010.09.005 S0143-4160(10)00139-9 [pii]. PMID: 21075448; PubMed Central PMCID: PMC3572849.
52. Chen DR, Chien SY, Kuo SJ, Teng YH, Tsai HT, Kuo JH, et al. SLC34A2 as a novel marker for diagnosis and targeted therapy of breast cancer. Anticancer Res. 2010; 30(10):4135-40. Epub 2010/11/03. doi: 30/10/4135 [pii]. PMID: 21036732.
53. Boumber YA, Kondo Y, Chen X, Shen L, Gharibyan V, Konishi K, et al. RIL, a LIM gene on 5q31, is silenced by methylation in cancer and sensitizes cancer cells to apoptosis. Cancer Res. 2007; 67 (5):1997-2005. Epub 2007/03/03. doi: 67/5/1997 [pii] doi: 10.1158/0008-5472.CAN-06-3093 PMID: 17332327.
54. Jin SH, Akiyama Y, Fukamachi H, Yanagihara K, Akashi T, Yuasa Y. IQGAP2 inactivation through aberrant promoter methylation and promotion of invasion in gastric cancer cells. Int J Cancer. 2008; 122(5):1040-6. Epub 2007/10/25. doi: 10.1002/ijc.23181 PMID: 17957782.
55. Marchitti SA, Orlicky DJ, Brocker C, Vasiliou V. Aldehyde dehydrogenase 3B1 (ALDH3B1): immunohistochemical tissue distribution and cellular-specific localization in normal and cancerous human tissues. J Histochem Cytochem. 2010; 58(9):765-83. Epub 2010/08/24. doi: 10.1369/jhc.2009.955773 58/9/765 [pii]. PMID: 20729348; PubMed Central PMCID: PMC2924794.