Dsh homolog DVL3 mediates resistance to IGFIR inhibition by regulating IGF-RAS signaling

Cancer Research

Volumn 74, Issue 20, 2014, Pages 5866-5877

  Gao, Shan ^a   Bajrami, Ilirjana ^b   Verrill, Clare ^c   Kigozi, Asha ^b   Ouaret, Djamila ^a   Aleksic, Tamara ^a   Asher, Ruth ^c   Han, Cheng ^a   Allen, Paul ^c   Bailey, Deborah ^c   Feller, Stephan ^a   Kashima, Takeshi ^d   Athanasou, Nicholas ^d   Blay, Jean Yves ^e   Schmitz, Sandra ^f   Machiels, Jean Pascal ^f   Upile, Nav ^g   Jones, Terry M ^g   Thalmann, George ^h   Ashraf, Shazad Q ^a   Wilding, Jennifer L ^a   Bodmer, Walter F ^a   Middleton, Mark R ⁱ   Ashworth, Alan ^b   Lord, Christopher J ^b   Macaulay, Valentine M ^a,i   more..

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b INSTITUTE OF CANCER RESEARCH   (United Kingdom)

^c JOHN RADCLIFFE HOSPITAL   (United Kingdom)

^d NUFFIELD ORTHOPAEDIC CENTRE   (United Kingdom)

^e UNIVERSITÉ LYON 1   (France)

^f CLINIQUES UNIVERSITAIRES SAINT LUC   (Belgium)

^g ROYAL LIVERPOOL UNIVERSITY HOSPITAL   (United Kingdom)

^h UNIVERSITY OF BERN   (Switzerland)

ⁱ CHURCHILL HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

7,8 DIHYDRO 2 [4 (TRIFLUOROMETHYL)PHENYL] 5H THIOPYRANO[4,3 D]PYRIMIDIN 4 OL; AVE 1642; AXIN; AZ 12253801; DISHEVELLED HOMOLOG 3 PROTEIN; DISHEVELLED PROTEIN; DUAL SPECIFICITY PHOSPHATASE 5; FIGITUMUMAB; GROWTH FACTOR RECEPTOR BOUND PROTEIN 2; HORMONALLY UPREGULATED NEU ASSOCIATED KINASE; LEMUR TYROSINE KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE KINASE; PHOSPHATASE; PHOSPHOTRANSFERASE; PROTEIN S6; PROTEIN SHC; PROTEIN TYROSINE KINASE; PROTEIN TYROSINE KINASE INHIBITOR; RAS PROTEIN; SOMATOMEDIN C RECEPTOR; SOS PROTEIN; TUMOR SUPPRESSOR DAB2 PROTEIN; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; DISHEVELLED PROTEINS; IGF1 PROTEIN, HUMAN; ISOXAZOLE DERIVATIVE; PHOSPHOPROTEIN; PYRIMIDINE DERIVATIVE; SIGNAL TRANSDUCING ADAPTOR PROTEIN; SOMATOMEDIN C; WNT PROTEIN;

3' UNTRANSLATED REGION; ANIMAL EXPERIMENT; ARTICLE; BREAST CANCER; CANCER CELL; CELL VIABILITY; CONTROLLED STUDY; DRUG RESISTANCE; DRUG SENSITIZATION; ENZYME ACTIVATION; ENZYME ACTIVITY; GENETIC SCREENING; HUMAN; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; PROGRESSION FREE SURVIVAL; PROSTATE CANCER; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY; SIGNAL TRANSDUCTION; UPREGULATION; ANIMAL; ANTAGONISTS AND INHIBITORS; DRUG SCREENING; GENE EXPRESSION; HEAD AND NECK TUMOR; IC50; METABOLISM; PHYSIOLOGY; SQUAMOUS CELL CARCINOMA; TUMOR CELL LINE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; ANTINEOPLASTIC AGENTS; CARCINOMA, SQUAMOUS CELL; CELL LINE, TUMOR; DRUG RESISTANCE, NEOPLASM; GENE EXPRESSION; HEAD AND NECK NEOPLASMS; HUMANS; INHIBITORY CONCENTRATION 50; INSULIN-LIKE GROWTH FACTOR I; ISOXAZOLES; MALE; MAP KINASE SIGNALING SYSTEM; MICE; PHOSPHOPROTEINS; PYRIMIDINES; RAS PROTEINS; RECEPTOR, IGF TYPE 1; WNT PROTEINS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84908120492     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-14-0806     Document Type: Article

References (50)

1. Chitnis MM, Yuen JS, Protheroe AS, Pollak M, Macaulay VM. The type 1 insulin-like growth factor receptor pathway. Clin Cancer Res 2008;14:6364-70.
2. Pollak M. The insulin and insulin-like growth factor receptor family in neoplasia: an update. Nat Rev Cancer 2012;12:159-69.
3. Guevara-Aguirre J, Balasubramanian P, Guevara-Aguirre M, Wei M, Madia F, Cheng CW, et al. Growth hormone receptor deficiency is associated with a major reduction in pro-aging signaling, cancer, and diabetes in humans. Sci Transl Med 2011;3:70ra13.
4. Olmos D, Postel-Vinay S, Molife LR, Okuno SH, Schuetze SM, Paccagnella ML, et al. Safety, pharmacokinetics, and preliminary activity of the anti-IGF-1R antibody figitumumab (CP-751,871) in patients with sarcoma and Ewing's sarcoma: a phase 1 expansion cohort study. Lancet Oncol 2010;11:129-35.
5. Tolcher AW, Sarantopoulos J, Patnaik A, Papadopoulos K, Lin CC, Rodon J, et al. Phase I, pharmacokinetic, and pharmacodynamic study of AMG 479, a fully human monoclonal antibody to insulin-like growth factor receptor 1. J Clin Oncol 2009;27:5800-7.
6. Javle MM, Varadhachary GR, Fogelman DR, Shroff RT, Overman MJ, Ukegbu L, et al. Randomized phase II study of gemcitabine (G) plus anti-IGF-1R antibody MK-0646, G plus erlotinib (E) plus MK-0646 and G plus E for advanced pancreatic cancer. J Clin Oncol 2011;29 (suppl: abstr 4026).
7. Molife LR, Fong PC, Paccagnella L, Reid AH, Shaw HM, Vidal L, et al. The insulin-like growth factor-I receptor inhibitor figitumumab (CP-751,871) in combination with docetaxel in patients with advanced solid tumours: results of a phase Ib dose-escalation, open-label study. Br J Cancer 2010;103:332-9.
8. Macaulay VM, Middleton MR, Eckhardt SG, Juergens RA, Rudin CA, Manukyants A, et al. Phase I study of OSI-906, dual tyrosine kinase inhibitor of insulin-like growth factor-1 receptor (IGF-1R) and insulin receptor (IR) in combination with erlotinib (E) in patients with advanced solid tumors. J Clin Oncol 2011;29 (suppl; abstr 3098).
9. Macaulay VM, Middleton MR, Protheroe AS, Tolcher A, Dieras V, Sessa C, et al. Phase I study of humanized monoclonal antibody AVE1642 directed against the type 1 insulin-like growth factor receptor (IGF-1R), administered in combination with anticancer therapies to patients with advanced solid tumors. Ann Oncol 2013;24:784-91.
10. Yee D. Insulin-like growth factor receptor inhibitors: baby or the bathwater? J Natl Cancer Inst 2012;104:975-81.
11. Demaison C, Parsley K, Brouns G, Scherr M, Battmer K, Kinnon C, et al. High-level transduction and gene expression in hematopoietic repopulating cells using a human immunodeficiency [correction of imunodeficiency] virus type 1-based lentiviral vector containing an internal spleen focus forming virus promoter. Hum Gene Ther 2002;13:803-13.
12. Chitnis MM, Lodhia KA, Aleksic T, Gao S, Protheroe AS, Macaulay VM. IGF-1R inhibition enhances radiosensitivity and delays double-strand break repair by both non-homologous end-joining and homologous recombination. Oncogene 2013 Nov 4. [Epub ahead of print].
13. Iorns E, Turner NC, Elliott R, Syed N, Garrone O, Gasco M, et al. Identification of CDK10 as an important determinant of resistance to endocrine therapy for breast cancer. Cancer Cell 2008;13:91-104.
14. Lord CJ, McDonald S, Swift S, Turner NC, Ashworth A. A high-throughput RNA interference screen for DNA repair determinants of PARP inhibitor sensitivity. DNA Repair (Amst) 2008;7:2010-9.
15. Boutros M, Ahringer J. The art and design of genetic screens: RNA interference. Nat Rev Genet 2008;9:554-66.
16. Martin SA, Hewish M, Sims D, Lord CJ, Ashworth A. Parallel high-throughput RNA interference screens identify PINK1 as a potential therapeutic target for the treatment of DNA mismatch repair-deficient cancers. Cancer Res 2011;71:1836-48.
17. Aleksic T, Chitnis MM, Perestenko OV, Gao S, Thomas PH, Turner GD, et al. Type 1 insulin-like growth factor receptor translocates to the nucleus of human tumor cells. Cancer Res 2010;70:6412-9.
18. Turney BW, Kerr M, Chitnis MM, Lodhia K, Wang Y, Riedemann J, et al. Depletion of the type 1 IGF receptor delays repair of radiation-induced DNA double strand breaks. Radiother Oncol 2012;103:402-9.
19. Playford MP, Bicknell D, Bodmer WF, Macaulay VM. Insulin-like growth factor 1 regulates the location, stability, and transcriptional activity of beta-catenin. Proc Natl Acad Sci U S A 2000;97:12103-8.
20. Chen J, Wu A, Sun H, Drakas R, Garofalo C, Cascio S, et al. Functional significance of type 1 insulin-like growth factor-mediated nuclear translocation of the insulin receptor substrate-1 and beta-catenin. J Biol Chem 2005;280:29912-20.
21. McManus EJ, Sakamoto K, Armit LJ, Ronaldson L, Shpiro N, Marquez R, et al. Role that phosphorylation of GSK3 plays in insulin and Wnt signalling defined by knockin analysis. EMBO J 2005;24:1571-83.
22. Gao C, Chen YG. Dishevelled: the hub of Wnt signaling. Cell Signal 2010;22:717-27.
23. Liu Y, Bodmer WF. Analysis of P53 mutations and their expression in 56 colorectal cancer cell lines. Proc Natl Acad Sci USA 2006;103:976-81.
24. Ashraf SQ, Nicholls AM, Wilding JL, Ntouroupi TG, Mortensen NJ, Bodmer WF. Direct and immune mediated antibody targeting of ERBB receptors in a colorectal cancer cell-line panel. Proc Natl Acad Sci U S A 2012;109:21046-51.
25. Chan DW, Chan CY, Yam JW, Ching YP, Ng IO. Prickle-1 negatively regulates Wnt/beta-catenin pathway by promoting dishevelled ubiquitination/degradation in liver cancer. Gastroenterology 2006;131:1218-27.
26. Inoki K, Ouyang H, Zhu T, Lindvall C, Wang Y, Zhang X, et al. TSC2 integrates Wnt and energy signals via a coordinated phosphorylation by AMPK and GSK3 to regulate cell growth. Cell 2006;126:955-68.
27. Boros J, O'Donnell A, Donaldson IJ, Kasza A, Zeef L, Sharrocks AD. Overlapping promoter targeting by Elk-1 and other divergent ETSdomain transcription factor family members. Nucleic Acids Res 2009;37:7368-80.
28. Stambolic V, Suzuki A, de la Pompa JL, Brothers GM, Mirtsos C, Sasaki T, et al. Negative regulation of PKB/Akt-dependent cell survival by the tumor suppressor PTEN. Cell 1998;95:29-39.
29. Caunt CJ, Keyse SM. Dual-specificity MAP kinase phosphatases (MKPs): shaping the outcome of MAP kinase signalling. FEBS J 2013;280:489-504.
30. Therrien M, Wong AM, Rubin GM. CNK, a RAF-binding multidomain protein required for RAS signaling. Cell 1998;95:343-53.
31. Giamas G, Filipovic A, Jacob J, Messier W, Zhang H, Yang D, et al. Kinome screening for regulators of the estrogen receptor identifies LMTK3 as a new therapeutic target in breast cancer. Nat Med 2011;17:715-9.
32. Komurov K, Padron D, Cheng T, Roth M, Rosenblatt KP, White MA. Comprehensive mapping of the human kinome to epidermal growth factor receptor signaling. J Biol Chem 2010;285:21134-42.
33. Huang SM, Mishina YM, Liu S, Cheung A, Stegmeier F, Michaud GA, et al. Tankyrase inhibition stabilizes axin and antagonizes Wnt signalling. Nature 2009;461:614-20.
34. Grandy D, Shan J, Zhang X, Rao S, Akunuru S, Li H, et al. Discovery and characterization of a small molecule inhibitor of the PDZ domain of dishevelled. J Biol Chem 2009;284:16256-63.
35. Haluska P, Dhar A, Hou X, Huang F, Nuyten DSA, Park J, et al. Phase II trial of the dual IGF-1R/IR inhibitor BMS-754807 with or without letrozole in aromatase inhibitor-resistant breast cancer. J Clin Oncol 2011;29 (suppl; abstr TPS111).
36. Liu BY, Soloviev I, Huang X, Chang P, Ernst JA, Polakis P, et al. Mammary tumor regression elicited by Wnt signaling inhibitor requires IGFBP5. Cancer Res 2012;72:1568-78.
37. Lito P, Pratilas CA, Joseph EW, Tadi M, Halilovic E, Zubrowski M, et al. Relief of profound feedback inhibition of mitogenic signaling by RAF inhibitors attenuates their activity in BRAFV600E melanomas. Cancer Cell 2012;22:668-82.
38. Bikkavilli RK, Malbon CC. Mitogen-activated protein kinases and Wnt/beta-catenin signaling: molecular conversations among signaling pathways. Commun Integr Biol 2009;2:46-9.
39. Buck E, Eyzaguirre A, Rosenfeld-Franklin M, Thomson S, Mulvihill M, Barr S, et al. Feedback mechanisms promote cooperativity for small molecule inhibitors of epidermal and insulin-like growth factor receptors. Cancer Res 2008;68:8322-32.
40. Bisson N, James DA, Ivosev G, Tate SA, Bonner R, Taylor L, et al. Selected reaction monitoring mass spectrometry reveals the dynamics of signaling through the GRB2 adaptor. Nat Biotechnol 2011;29:653-8.
41. Crampton SP, Wu B, Park EJ, Kim JH, Solomon C, Waterman ML, et al. Integration of the beta-catenin-dependent Wnt pathway with integrin signaling through the adaptor molecule Grb2. PLoS ONE 2009;4:e7841.
42. Xu XX, Yi T, Tang B, Lambeth JD. Disabled-2 (Dab2) is an SH3 domain-binding partner of Grb2. Oncogene 1998;16:1561-9.
43. Zhou J, Hsieh JT. The inhibitory role of DOC-2/DAB2 in growth factor receptor-mediated signal cascade. DOC-2/DAB2-mediated inhibition of ERK phosphorylation via binding to Grb2. J Biol Chem 2001;276:27793-8.
44. Hocevar BA, Mou F, Rennolds JL, Morris SM, Cooper JA, Howe PH. Regulation of the Wnt signaling pathway by disabled-2 (Dab2). EMBOJ 2003;22:3084-94.
45. Egan SE, Giddings BW, Brooks MW, Buday L, Sizeland AM, Weinberg RA. Association of Sos Ras exchange protein with Grb2 is implicated in tyrosine kinase signal transduction and transformation. Nature 1993;363:45-51.
46. Tap WD, Demetri G, Barnette P, Desai J, Kavan P, Tozer R, et al. Phase II study of ganitumab, a fully human anti-type-1 insulin-like growth factor receptor antibody, in patients with metastatic Ewing family tumors or desmoplastic small round cell tumors. J Clin Oncol 2012;30:1849-56.
47. Malempati S, Weigel B, Ingle AM, Ahern CH, Carroll JM, Roberts CT, et al. Phase I/II trial and pharmacokinetic study of cixutumumab in pediatric patients with refractory solid tumors and Ewing sarcoma: a report from the Children's Oncology Group. J Clin Oncol 2012;30:256-62.
48. Schmitz S, Kaminsky-Forrett MC, Henry S, Zanetta S, Geoffrois L, Bompas E, et al. Phase II study of figitumumab in patients with recurrent and/or metastatic squamous cell carcinoma of the head and neck: clinical activity and molecular response (GORTEC 2008-02). Ann Oncol 2012;23:2153-61.
49. Molina-Arcas M, Hancock DC, Sheridan C, Kumar MS, Downward J. Coordinate direct input of both KRAS and IGF1 receptor to activation of PI3 kinase in KRAS-mutant lung cancer. Cancer Discov 2013;3:548-63.
50. Pao W, Chmielecki J. Rational, biologically based treatment of EGFR-mutant non-small-cell lung cancer. Nat Rev Cancer 2010;10:760-74.