B-Raf inhibitors induce epithelial differentiation in BRAF-mutant colorectal cancer cells

Cancer Research

Volumn 75, Issue 1, 2015, Pages 216-229

  Herr, Ricarda ^a   Köhler, Martin ^a   Andrlová, Hana ^b   Weinberg, Florian ^a   Möller, Yvonne ^c   Halbach, Sebastian ^a   Lutz, Lisa ^b   Mastroianni, Justin ^a,b   Klose, Martin ^a   Bittermann, Nicola ^b   Kowar, Silke ^a   Zeiser, Robert ^a,b   Olayioye, Monilola A ^c   Lassmann, Silke ^a,b,d   Busch, Hauke ^a,d   Boerries, Melanie ^a,d   Brummer, Tilman ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

^b UNIVERSITY OF FREIBURG   (Germany)

^c UNIVERSITY OF STUTTGART   (Germany)

^d GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

B RAF KINASE; BETA1 INTEGRIN; BETA4 INTEGRIN; DABRAFENIB; DOXYCYCLINE; EPIDERMAL GROWTH FACTOR RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE; N [3 (5 CHLORO 1H PYRROLO[2,3 B]PYRIDINE 3 CARBONYL) 2,4 DIFLUOROPHENYL]PROPANESULFONAMIDE; RAC1 PROTEIN; TRAMETINIB; TRANSCRIPTION FACTOR CDX2; UVOMORULIN; VEMURAFENIB; BRAF PROTEIN, HUMAN; PROTEIN KINASE INHIBITOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER PROGNOSIS; CELL ADHESION; CELL DIFFERENTIATION; CELL FUNCTION; CELL MIGRATION; CELL MOTILITY; CLDN1 GENE; CLDN15 GENE; CLDN18 GENE; COLO 205 CELL LINE; COLORECTAL CANCER CELL LINE; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; EPITHELIUM CELL; GENE; GENE FUNCTION; GENE REPRESSION; GENE SILENCING; HT 29 CELL LINE; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; ONCOGENE; PRIMARY TUMOR; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; TUMOR INVASION; TUMOR XENOGRAFT; UPREGULATION; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL PROLIFERATION; COLORECTAL NEOPLASMS; DRUG EFFECTS; DRUG SCREENING; ENZYMOLOGY; GENETICS; PHOSPHORYLATION; RANDOMIZATION; SCID MOUSE; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE;

ANIMALS; CELL DIFFERENTIATION; CELL PROLIFERATION; COLORECTAL NEOPLASMS; GENE KNOCKDOWN TECHNIQUES; HT29 CELLS; HUMANS; MICE; MICE, SCID; MICE, TRANSGENIC; PHOSPHORYLATION; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS B-RAF; RANDOM ALLOCATION; SIGNAL TRANSDUCTION; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84920661910     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-13-3686     Document Type: Article

References (55)

1. Sadanandam A, Lyssiotis CA, Homicsko K, Collisson EA, Gibb WJ, Wullschleger S, et al. A colorectal cancer classification system that associates cellular phenotype and responses to therapy. Nat Med 2013;19:619-25.
2. De Sousa EMF, Wang X, Jansen M, Fessler E, Trinh A, de Rooij LP, et al. Poor-prognosis colon cancer is defined by a molecularly distinct subtype and develops from serrated precursor lesions. Nat Med 2013;19:614-8.
3. Clancy C, Burke JP, Kalady MF, Coffey JC. BRAF mutation is associated with distinct clinicopathological characteristics in colorectal cancer: a systematic review and meta-analysis. Colorectal Dis 2013;15:e711-8.
4. Rad R, Cadinanos J, Rad L, Varela I, Strong A, Kriegl L, et al. A genetic progression model of braf-induced intestinal tumorigenesis reveals targets for therapeutic intervention. Cancer Cell 2013;24:15-29.
5. Sinicrope FA, Shi Q, Thibodeau SN, Goldberg RM, Sargent DJ, Alberts SR. Molecular subtyping of colon cancers and distinct prognostic groups [NCCTG N0147 (Alliance)]. J Clin Oncol 32:5s, 2014 (suppl; abstr 3512).
6. Roth AD, Delorenzi M, Tejpar S, Yan P, Klingbiel D, Fiocca R, et al. Integrated analysis of molecular and clinical prognostic factors in stage II/III colon cancer. J Natl Cancer Inst 2012;104:1635-46.
7. Landau MS, Kuan SF, Chiosea S, Pai RK. BRAF-mutated microsatellite stable colorectal carcinoma: an aggressive adenocarcinoma with reduced CDX2 and increased cytokeratin 7 immunohistochemical expression. Hum Pathol 2014;45:1704-12.
8. Pai RK, Jayachandran P, Koong AC, Chang DT, Kwok S, Ma L, et al. BRAF-mutated, microsatellite-stable adenocarcinoma of the proximal colon: an aggressive adenocarcinoma with poor survival, mucinous differentiation, and adverse morphologic features. Am J Surg Pathol 2012;36:744-52.
9. Popovici V, Budinska E, Tejpar S, Weinrich S, Estrella H, Hodgson G, et al. Identification of a poor-prognosis BRAF-mutant-like population of patients with colon cancer. J Clin Oncol 2012;30:1288-95.
10. Tie J, Gibbs P, Lipton L, Christie M, Jorissen RN, Burgess AW, et al. Optimizing targeted therapeutic development: analysis of a colorectal cancer patient population with the BRAF(V600E) mutation. Int J Cancer 2011;128:2075-84.
11. Yaeger R, Cercek A, Chou JF, Sylvester BE, Kemeny NE, Hechtman JF, et al. BRAF mutation predicts for poor outcomes after metastasectomy in patients with metastatic colorectal cancer. Cancer 2014;120:2316-24.
12. Tran B, Kopetz S, Tie J, Gibbs P, Jiang ZQ, Lieu CH, et al. Impact of BRAF mutation and microsatellite instability on the pattern of metastatic spread and prognosis in metastatic colorectal cancer. Cancer 2011;117:4623-32.
13. Bollag G, Hirth P, Tsai J, Zhang J, Ibrahim PN, Cho H, et al. Clinical efficacy of a RAF inhibitor needs broad target blockade in BRAF-mutant melanoma. Nature 2010;467:596-9.
14. Falchook GS, Long GV, Kurzrock R, Kim KB, Arkenau TH, Brown MP, et al. Dabrafenib in patients with melanoma, untreated brain metastases, and other solid tumours: a phase 1 dose-escalation trial. Lancet 2012;379:1893-901.
15. Morris V, Kopetz S. BRAF inhibitors in clinical oncology. F1000prime Rep 2013;5:11.
16. Yamaguchi T, Kakefuda R, Tajima N, Sowa Y, Sakai T. Antitumor activities of JTP-74057 (GSK1120212), a novel MEK1/2 inhibitor, on colorectal cancer cell lines in vitro and in vivo. Int J Oncol 2011;39:23-31.
17. Yang H, Higgins B, Kolinsky K, Packman K, Bradley WD, Lee RJ, et al. Antitumor activity of BRAF inhibitor vemurafenib in preclinical models of BRAF-mutant colorectal cancer. Cancer Res 2012;72:779-89.
18. Coffee EM, Faber AC, Roper J, Sinnamon MJ, Goel G, Keung L, et al. Concomitant BRAF and PI3K/mTOR blockade is required for effective treatment of BRAF(V600E) colorectal cancer. Clin Cancer Res 2013;19:2688-98.
19. Prahallad A, Sun C, Huang S, Di Nicolantonio F, Salazar R, Zecchin D, et al. Unresponsiveness of colon cancer to BRAF(V600E) inhibition through feedback activation of EGFR. Nature 2012;483:100-3.
20. Corcoran RB, Ebi H, Turke AB, Coffee EM, Nishino M, Cogdill AP, et al. EGFR-mediated re-activation of MAPK signaling contributes to insensitivity of BRAF mutant colorectal cancers to RAF inhibition with vemurafenib. Cancer Discov 2012;2:227-35.
21. Misale S, Arena S, Lamba S, Siravegna G, Lallo A, Hobor S, et al. Blockade of EGFR and MEK intercepts heterogeneous mechanisms of acquired resistance to anti-EGFR therapies in colorectal cancer. Sci Translational Med 2014;6:224ra26.
22. Connolly K, Brungs D, Szeto E, Epstein RJ. Anticancer activity of combination targeted therapy using cetuximab plus vemurafenib for refractory BRAF (V600E)-mutant metastatic colorectal carcinoma. Curr Oncol 2014;21:e151-4.
23. Röring M, Herr R, Fiala GJ, Heilmann K, Braun S, Eisenhardt AE, et al. Distinct requirement for an intact dimer interface in wild-type, V600E and kinase-dead B-Raf signalling. EMBO J 2012;31:2629-47.
24. Herr R, Wohrle FU, Danke C, Berens C, Brummer T. A novel MCF-10A line allowing conditional oncogene expression in 3D culture. Cell Commun Signal 2011;9:17.
25. Timpson P, McGhee EJ, Erami Z, Nobis M, Quinn JA, Edward M, et al. Organotypic collagen I assay: amalleable platformto assess cell behaviour in a 3-dimensional context. J Vis Exp 2011;56:e3089.
26. Hoffmann C, Pop M, Leemhuis J, Schirmer J, Aktories K, Schmidt G. The Yersinia pseudotuberculosis cytotoxic necrotizing factor (CNFY) selectively activates RhoA. J Biol Chem 2004;279:16026-32.
27. Gout S, Marie C, Laine M, Tavernier G, Block MR, Jacquier-Sarlin M. Early enterocytic differentiation of HT-29 cells: biochemical changes and strength increases of adherens junctions. Exp Cell Res 2004;299:498-510.
28. Esufali S, Charames GS, Pethe VV, Buongiorno P, Bapat B. Activation of tumor-specific splice variant Rac1b by dishevelled promotes canonical Wnt signaling and decreased adhesion of colorectal cancer cells. Cancer Res 2007;67:2469-79.
29. Jaffe AB, Kaji N, Durgan J, Hall A. Cdc42 controls spindle orientation to position the apical surface during epithelial morphogenesis. J Cell Biol 2008;183:625-33.
30. Pratilas CA, Taylor BS, Ye Q, Viale A, Sander C, Solit DB, et al. (V600E)BRAF is associated with disabled feedback inhibition of RAF-MEK signaling and elevated transcriptional output of the pathway. Proc Natl Acad Sci U S A 2009;106:4519-24.
31. Pieters T, van Roy F, van Hengel J. Functions of p120ctn isoforms in cell-cell adhesion and intracellular signaling. Front Biosci 2012;17:1669-94.
32. Ferby I, Reschke M, Kudlacek O, Knyazev P, Pante G, Amann K, et al. Mig6 is a negative regulator of EGF receptor-mediated skin morphogenesis and tumor formation. Nat Med 2006;12:568-73.
33. Hinoi T, Gesina G, Akyol A, Kuick R, Hanash S, Giordano TJ, et al. CDX2-regulated expression of iron transport protein hephaestin in intestinal and colonic epithelium. Gastroenterology 2005;128:946-61.
34. Ni H, Dydensborg AB, Herring FE, Basora N, Gagne D, Vachon PH, et al. Upregulation of a functional form of the beta4 integrin subunit in colorectal cancers correlates with c-Myc expression. Oncogene 2005;24:6820-9.
35. Vignjevic D, Schoumacher M, Gavert N, Janssen KP, Jih G, Lae M, et al. Fascin, a novel target of beta-catenin-TCF signaling, is expressed at the invasive front of human colon cancer. Cancer Res 2007;67:6844-53.
36. Turtoi A, Blomme A, Bellahcene A, Gilles C, Hennequiere V, Peixoto P, et al. Myoferlin is a key regulator of EGFR activity in breast cancer. Cancer Res 2013;73:5438-48.
37. Wang WS, Liu XH, Liu LX, Lou WH, Jin DY, Yang PY, et al. iTRAQ-based quantitative proteomics reveals myoferlin as a novel prognostic predictor in pancreatic adenocarcinoma. J Proteomics 2013;91C:453-65.
38. Koskensalo S, Hagstrom J, Louhimo J, Stenman UH, Haglund C. Tumour-associated trypsin inhibitor TATI is a prognostic marker in colorectal cancer. Oncology 2012;82:234-41.
39. Sabates-Bellver J, Van der Flier LG, de Palo M, Cattaneo E, Maake C, Rehrauer H, et al. Transcriptome profile of human colorectal adenomas. Mol Cancer Res 2007;5:1263-75.
40. Birkenkamp-Demtroder K, Maghnouj A, Mansilla F, Thorsen K, Andersen CL, Oster B, et al. Repression of KIAA1199 attenuates Wnt-signalling and decreases the proliferation of colon cancer cells. Br J Cancer 2011;105:552-61.
41. Siddiqi S, Matushansky I. Piwis and piwi-interacting RNAs in the epigenetics of cancer. J Cell Biochem 2012;113:373-80.
42. Ziskin JL, Dunlap D, Yaylaoglu M, Fodor IK, Forrest WF, Patel R, et al. In situ validation of an intestinal stem cell signature in colorectal cancer. Gut 2013;62:1012-23.
43. Brabletz T, Spaderna S, Kolb J, Hlubek F, Faller G, Bruns CJ, et al. Down-regulation of the homeodomain factor Cdx2 in colorectal cancer by collagen type I: an active role for the tumor environment in malignant tumor progression. Cancer Res 2004;64:6973-7.
44. Baba Y, Nosho K, Shima K, Freed E, Irahara N, Philips J, et al. Relationship of CDX2 loss with molecular features and prognosis in colorectal cancer. Clin Cancer Res 2009;15:4665-73.
45. Magudia K, Lahoz A, Hall A. K-Ras and B-Raf oncogenes inhibit colon epithelial polarity establishment through up-regulation of c-myc. J Cell Biol 2012;198:185-94.
46. Gunzel D, Yu AS. Claudins and the modulation of tight junction permeability. Physiol Rev 2013;93:525-69.
47. Bhat AA, Sharma A, Pope J, Krishnan M, Washington MK, Singh AB, et al. Caudal homeobox protein Cdx-2 cooperates with Wnt pathway to regulate claudin-1 expression in colon cancer cells. PloS ONE 2012;7:e37174.
48. Krueger F, Madeja Z, Hemberger M, McMahon M, Cook SJ, Gaunt SJ. Down-regulation of Cdx2 in colorectal carcinoma cells by the Raf-MEKERK 1/2 pathway. Cell Signal 2009;21:1846-56.
49. Gross I, Duluc I, Benameur T, Calon A, Martin E, Brabletz T, et al. The intestine-specific homeobox gene Cdx2 decreases mobility and antagonizes dissemination of colon cancer cells. Oncogene 2008;27:107-15.
50. Gao N, Kaestner KH. Cdx2 regulates endo-lysosomal function and epithelial cell polarity. Genes Dev 2010;24:1295-305.
51. Funakoshi S, Kong J, Crissey MA, Dang L, Dang D, Lynch JP. Intestine-specific transcription factor Cdx2 induces E-cadherin function by enhancing the trafficking of E-cadherin to the cell membrane. Am J Physiol Gastrointest Liver Physiol 2010;299:G1054-67.
52. Zlobec I, Bihl MP, Schwarb H, Terracciano L, Lugli A. Clinicopathological and protein characterization of BRAF- and K-RAS-mutated colorectal cancer and implications for prognosis. Int J Cancer 2010;127:367-80.
53. Dawson H, Galvan JA, Helbling M, Muller DE, Karamitopoulou E, Koelzer VH, et al. Possible role of Cdx2 in the serrated pathway of colorectal cancer characterized by BRAF mutation, high-level CpG Island methylator phenotype and mismatch repair-deficiency. Int J Cancer 2014;134:2342-51.
54. Resnick MB, Konkin T, Routhier J, Sabo E, Pricolo VE. Claudin-1 is a strong prognostic indicator in stage II colonic cancer: a tissue microarray study. Mod Pathol 2005;18:511-8.
55. Evensen NA, Kuscu C, Nguyen HL, Zarrabi K, Dufour A, Kadam P, et al. Unraveling the role of KIAA1199, a novel endoplasmic reticulum protein, in cancer cell migration. J Natl Cancer Inst 2013;105:1402-16.