CRIPTO1 expression in EGFR-mutant NSCLC elicits intrinsic EGFR-inhibitor resistance

Journal of Clinical Investigation

Volumn 124, Issue 7, 2014, Pages 3003-3015

  Park, Kang Seo ^a,b   Raffeld, Mark ^a   Moon, Yong Wha ^a   Xi, Liqiang ^a   Bianco, Caterina ^c   Pham, Trung ^a   Lee, Liam C ^a   Mitsudomi, Tetsuya ^d   Yatabe, Yasushi ^d   Okamoto, Isamu ^e   Subramaniam, Deepa ^b   Mok, Tony ^f   Rosell, Rafael ^g   Luo, Ji ^a   Salomon, David S ^c   Wang, Yisong ^a,b   Giaccone, Giuseppe ^a,b  

^a NATIONAL CANCER INSTITUTE   (United States)

^b GEORGETOWN UNIVERSITY   (United States)

^c NATIONAL CANCER INSTITUTE   (United States)

^d KINKI UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^e AICHI CANCER CENTER HOSPITAL   (Japan)

^f CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

^g HOSPITAL UNIVERSITARI GERMANS TRIAS I PUJOL   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CISPLATIN; CRIPTO1 PROTEIN; DACOMITINIB; EPIDERMAL GROWTH FACTOR; EPIDERMAL GROWTH FACTOR RECEPTOR; ERLOTINIB; MICRORNA 205; NERVE CELL ADHESION MOLECULE; PACLITAXEL; UNCLASSIFIED DRUG; UVOMORULIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER RESISTANCE; CONTROLLED STUDY; DOWN REGULATION; DRUG SENSITIVITY; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; IC 50; LUNG NON SMALL CELL CANCER; MOUSE; NONHUMAN; PRIMARY CELL; PRIMARY TUMOR; PRIORITY JOURNAL; TUMOR XENOGRAFT; UPREGULATION;

ANIMALS; ANTINEOPLASTIC AGENTS; CARCINOMA, NON-SMALL-CELL LUNG; CELL LINE, TUMOR; DRUG RESISTANCE, NEOPLASM; EPITHELIAL-MESENCHYMAL TRANSITION; GENES, ERBB-1; GPI-LINKED PROTEINS; HOMEODOMAIN PROTEINS; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; LUNG NEOPLASMS; MICE; MICE, NUDE; MICRORNAS; MUTATION; NEOPLASM PROTEINS; PROTEIN KINASE INHIBITORS; QUINAZOLINES; RECEPTOR, EPIDERMAL GROWTH FACTOR; SRC-FAMILY KINASES; TRANSCRIPTION FACTORS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84903767202     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI73048     Document Type: Article

References (64)

1. Pao W, et al. EGF receptor gene mutations are common in lung cancers from "never smokers" and are associated with sensitivity of tumors to gefitinib and erlotinib. Proc Natl Acad Sci U S A. 2004; 101(36):13306-13311.
2. Lynch TJ, et al. Activating mutations in the epidermal growth factor receptor underlying responsiveness of non-small-cell lung cancer to gefitinib. N Engl J Med. 2004;350(21):2129-2139.
3. Paez JG, et al. EGFR mutations in lung cancer: correlation with clinical response to gefitinib therapy. Science. 2004;304(5676):1497-1500.
4. Kosaka T, Yatabe Y, Endoh H, Kuwano H, Takahashi T, Mitsudomi T. Mutations of the epidermal growth factor receptor gene in lung cancer: biological and clinical implications. Cancer Res. 2004;64(24):8919-8923.
5. Riely GJ, Politi KA, Miller VA, Pao W. Update on epidermal growth factor receptor mutations in non-small cell lung cancer. Clin Cancer Res. 2006; 12(24):7232-7241.
6. Inoue A, et al. Prospective phase II study of gefitinib for chemotherapy-naive patients with advanced non-small-cell lung cancer with epidermal growth factor receptor gene mutations. J Clin Oncol. 2006;24(21):3340-3346.
7. Mitsudomi T, et al. Mutations of the epidermal growth factor receptor gene predict prolonged survival after gefitinib treatment in patients with non-small-cell lung cancer with postoperative recurrence. J Clin Oncol. 2005;23(11):2513-2520.
8. Takeda M, et al. De novo resistance to epidermal growth factor receptor-tyrosine kinase inhibitors in EGFR mutation-positive patients with non-small cell lung cancer. J Thorac Oncol. 2010;5(3):399-400.
9. Maemondo M, et al. Gefitinib or chemotherapy for non-small-cell lung cancer with mutated EGFR. N Engl J Med. 2010;362(25):2380-2388.
10. Kwak EL, et al. Irreversible inhibitors of the EGF receptor may circumvent acquired resistance to gefitinib. Proc Natl Acad Sci U S A. 2005; 102(21):7665-7670.
11. Kobayashi S, et al. EGFR mutation and resistance of non-small-cell lung cancer to gefitinib. N Engl J Med. 2005;352(8):786-792.
12. Pao W, et al. Acquired resistance of lung adenocarcinomas to gefitinib or erlotinib is associated with a second mutation in the EGFR kinase domain. PLoS Med. 2005;2(3):e73.
13. Engelman JA, et al. MET amplification leads to gefitinib resistance in lung cancer by activating ERBB3 signaling. Science. 2007;316(5827):1039-1043.
14. Engelman JA, et al. Allelic dilution obscures detection of a biologically significant resistance mutation in EGFR-amplified lung cancer. J Clin Invest. 2006;116(10):2695-2706.
15. Sequist LV, et al. Genotypic and histological evolution of lung cancers acquiring resistance to EGFR inhibitors. Sci Transl Med. 2011;3(75):75ra26.
16. Zhang Z, et al. Activation of the AXL kinase causes resistance to EGFR-targeted therapy in lung cancer. Nat Genet. 2012;44(8):852-860.
17. Cheung HW, et al. Amplification of CRKL induces transformation and epidermal growth factor receptor inhibitor resistance in human non-small cell lung cancers. Cancer Discov. 2011;1(7):608-625.
18. Pao W, et al. KRAS mutations and primary resistance of lung adenocarcinomas to gefitinib or erlotinib. PLoS Med. 2005;2(1):e17.
19. Sequist LV, Bell DW, Lynch TJ, Haber DA. Molecular predictors of response to epidermal growth factor receptor antagonists in non-small-cell lung cancer. J Clin Oncol. 2007;25(5):587-595.
20. Ng KP, et al. A common BIM deletion polymorphism mediates intrinsic resistance and inferior responses to tyrosine kinase inhibitors in cancer. Nat Med. 2012;18(4):521-528.
21. Nakagawa T, et al. EGFR-TKI resistance due to BIM polymorphism can be circumvented in combination with HDAC inhibition. Cancer Res. 2013; 73(8):2428-2434.
22. Lee JK, et al. Primary resistance to epidermal growth factor receptor (EGFR) tyrosine kinase inhibitors (TKIs) in patients with non-small-cell lung cancer harboring TKI-sensitive EGFR mutations: an exploratory study. Ann Oncol. 2013;24(8):2080-2087.
23. Faber AC, et al. BIM expression in treatment-naïve cancers predicts responsiveness to kinase inhibitors. Cancer Discov. 2011;1(4):352-365.
24. Costa C, et al. The impact of EGFR T790M mutations and BIM mRNA expression on outcome in patients with EGFR-mutant NSCLC treated with erlotinib or chemotherapy in the randomized phase III EURTAC trial. Clin Cancer Res. 2014;20(7):2001-2010.
25. Bianco C, Strizzi L, Normanno N, Khan N, Salomon DS. Cripto-1: an oncofetal gene with many faces. Curr Top Dev Biol. 2005;67:85-133.
26. Strizzi L, Bianco C, Normanno N, Salomon D. Cripto-1: a multifunctional modulator during embryogenesis and oncogenesis. Oncogene. 2005; 24(37):5731-5741.
27. Saeki T, et al. Differential immunohistochemical detection of amphiregulin and cripto in human normal colon and colorectal tumors. Cancer Res. 1992;52(12):3467-3473.
28. Panico L, et al. Differential immunohistochemical detection of transforming growth factor alpha, amphiregulin and CRIPTO in human normal and malignant breast tissues. Int J Cancer. 1996; 65(1):51-56.
29. Bianco C, Salomon DS. Targeting the embryonic gene Cripto-1 in cancer and beyond. Expert Opin Ther Pat. 2010;20(12):1739-1749.
30. Zhong XY, et al. Positive association of up-regulated Cripto-1 and down-regulated E-cadherin with tumour progression and poor prognosis in gastric cancer. Histopathology. 2008;52(5):560-568.
31. Miyoshi N, Ishii H, Mimori K, Sekimoto M, Doki Y, Mori M. TDGF1 is a novel predictive marker for metachronous metastasis of colorectal cancer. Int J Oncol. 2010;36(3):563-568.
32. Gong YP, et al. Overexpression of Cripto and its prognostic significance in breast cancer: a study with longterm survival. Eur J Surg Oncol. 2007;33(4):438-443.
33. Strizzi L, et al. Epithelial mesenchymal transition is a characteristic of hyperplasias and tumors in mammary gland from MMTV-Cripto-1 transgenic mice. J Cell Physiol. 2004;201(2):266-276.
34. Bianco C, et al. Cripto-1 activates nodal-and ALK4-dependent and-independent signaling pathways in mammary epithelial Cells. Mol Cell Biol. 2002; 22(8):2586-2597.
35. Yeo C, Whitman M. Nodal signals to Smads through Cripto-dependent and Cripto-independent mechanisms. Mol Cell. 2001;7(5):949-957.
36. Bianco C, et al. A Nodal-and ALK4-independent signaling pathway activated by Cripto-1 through Glypican-1 and c-Src. Cancer Res. 2003;63(6):1192-1197.
37. Witta SE, et al. Restoring E-cadherin expression increases sensitivity to epidermal growth factor receptor inhibitors in lung cancer cell lines. Cancer Res. 2006;66(2):944-950.
38. Hiscox S, Morgan L, Green TP, Barrow D, Gee J, Nicholson RI. Elevated Src activity promotes cellular invasion and motility in tamoxifen resistant breast cancer cells. Breast Cancer Res Treat. 2006;97(3):263-274.
39. Leung EL, et al. SRC promotes survival and invasion of lung cancers with epidermal growth factor receptor abnormalities and is a potential candidate for molecular-targeted therapy. Mol Cancer Res. 2009; 7(6):923-932.
40. Thomson S, et al. Epithelial to mesenchymal transition is a determinant of sensitivity of non-smallcell lung carcinoma cell lines and xenografts to epidermal growth factor receptor inhibition. Cancer Res. 2005;65(20):9455-9462.
41. Xing PX, Hu XF, Pietersz GA, Hosick HL, McKenzie IF. Cripto: a novel target for antibody-based cancer immunotherapy. Cancer Res. 2004;64(11):4018- 4023.
42. Hu XF, Li J, Yang E, Vandervalk S, Xing PX. Anti-Cripto Mab inhibit tumour growth and overcome MDR in a human leukaemia MDR cell line by inhibition of Akt and activation of JNK/SAPK and bad death pathways. Br J Cancer. 2007;96(6):918-927.
43. Soifer HS, Rossi JJ, Saetrom P. MicroRNAs in disease and potential therapeutic applications. Mol Ther. 2007;15(12):2070-2079.
44. Gregory PA, et al. The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat Cell Biol. 2008; 10(5):593-601.
45. Majid S, et al. MicroRNA-205 inhibits Src-mediated oncogenic pathways in renal cancer. Cancer Res. 2011;71(7):2611-2621.
46. Sun C, et al. CRIPTO3, a presumed pseudogene, is expressed in cancer. Biochem Biophys Res Commun. 2008;377(1):215-220.
47. Stabile LP, et al. c-Src activation mediates erlotinib resistance in head and neck cancer by stimulating c-Met. Clin Cancer Res. 2013;19(2):380-392.
48. Frederick BA, et al. Epithelial to mesenchymal transition predicts gefitinib resistance in cell lines of head and neck squamous cell carcinoma and nonsmall cell lung carcinoma. Mol Cancer Ther. 2007; 6(6):1683-1691.
49. Rho JK, et al. Epithelial to mesenchymal transition derived from repeated exposure to gefitinib determines the sensitivity to EGFR inhibitors in A549, a non-small cell lung cancer cell line. Lung Cancer. 2009;63(2):219-226.
50. Boerner JL. Role of Src family kinases in acquired resistance to EGFR therapies in cancer. Cancer Biol Ther. 2009;8(8):704-706.
51. Ettinger DS. Taxol in the treatment of lung cancer. J Natl Cancer Inst Monogr. 1993;(15):177-179.
52. Naito Y, et al. Concurrent chemoradiotherapy with cisplatin and vinorelbine for stage III non-small cell lung cancer. J Thorac Oncol. 2008;3(6):617-622.
53. Normanno N, et al. Cripto-1 overexpression leads to enhanced invasiveness and resistance to anoikis in human MCF-7 breast cancer cells. J Cell Physiol. 2004;198(1):31-39.
54. De Luca A, et al. Expression and functional role of Cripto-1 in cutaneous melanoma. Br J Cancer. 2011; 105(7):1030-1038.
55. Christiansen JJ, Rajasekaran AK. Reassessing epithelial to mesenchymal transition as a prerequisite for carcinoma invasion and metastasis. Cancer Res. 2006;66(17):8319-8326.
56. Burk U, et al. A reciprocal repression between ZEB1 and members of the miR-200 family promotes EMT and invasion in cancer cells. EMBO Rep. 2008;9(6):582-589.
57. Tellez CS, et al. EMT and stem cell-like properties associated with miR-205 and miR-200 epigenetic silencing are early manifestations during carcinogen-induced transformation of human lung epithelial cells. Cancer Res. 2011;71(8):3087-3097.
58. Lebanony D, et al. Diagnostic assay based on hsamiR-205 expression distinguishes squamous from nonsquamous non-small-cell lung carcinoma. J Clin Oncol. 2009;27(12):2030-2037.
59. Avizienyte E, et al. Src-induced de-regulation of E-cadherin in colon cancer cells requires integrin signalling. Nat Cell Biol. 2002;4(8):632-638.
60. Serrels A, Canel M, Brunton VG, Frame MC. Src/FAK-mediated regulation of E-cadherin as a mechanism for controlling collective cell movement: insights from in vivo imaging. Cell Adh Migr. 2011; 5(4):360-365.
61. Raje N, et al. Combination of the mTOR inhibitor rapamycin and CC-5013 has synergistic activity in multiple myeloma. Blood. 2004;104(13):4188-4193.
62. Quail DF, Siegers GM, Jewer M, Postovit LM. Nodal signalling in embryogenesis and tumourigenesis. Int J Biochem Cell Biol. 2013;45(4):885-898.
63. Quail DF, Zhang G, Findlay SD, Hess DA, Postovit LM. Nodal promotes invasive phenotypes via a mitogen-activated protein kinase-dependent pathway. Oncogene. 2014;33(4):461-473.
64. Liu X, et al. ROCK inhibitor and feeder cells induce the conditional reprogramming of epithelial cells. Am J Pathol. 2012;180(2):599-607.