Crizotinib inhibits metabolic inactivation of gemcitabine in c-Met-driven pancreatic carcinoma

Cancer Research

Volumn 73, Issue 22, 2013, Pages 6745-6756

  Avan, Amir ^a   Caretti, Viola ^a,d   Funel, Niccola ^e   Galvani, Elena ^a   Maftouh, Mina ^a   Honeywell, Richard J ^a   Lagerweij, Tonny ^a   Van Tellingen, Olaf ^b   Campani, Daniela ^e   Fuchs, Dieter ^c   Verheul, Henk M ^a   Schuurhuis, Gerrit Jan ^a   Boggi, Ugo ^e   Peters, Godefridus J ^a   Würdinger, Thomas ^a,f   Giovannetti, Elisa ^a  

^a VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^b NETHERLANDS CANCER INSTITUTE   (Netherlands)

^c BV   (Netherlands)

^d STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY OF PISA   (Italy)

^f MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CRIZOTINIB; DN 30; GEMCITABINE; MONOCLONAL ANTIBODY; SCATTER FACTOR RECEPTOR; TIVANTINIB; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER COMBINATION CHEMOTHERAPY; CANCER INHIBITION; CLINICAL ARTICLE; CONTROLLED STUDY; DRUG BLOOD LEVEL; DRUG EFFICACY; DRUG INACTIVATION; DRUG INHIBITION; DRUG METABOLISM; DRUG POTENTIATION; DRUG TARGETING; DRUG TUMOR LEVEL; FEMALE; GENE DOSAGE; GENE OVEREXPRESSION; HISTOPATHOLOGY; HUMAN; HUMAN CELL; IC 50; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; LIVER METASTASIS; LUNG METASTASIS; LYMPH NODE METASTASIS; MALE; MONOTHERAPY; MOUSE; NONHUMAN; PANCREAS ADENOCARCINOMA; PRIORITY JOURNAL; TUMOR GROWTH; TUMOR XENOGRAFT;

ANIMALS; ANTINEOPLASTIC AGENTS; CARCINOMA, PANCREATIC DUCTAL; CELL TRANSFORMATION, NEOPLASTIC; DEOXYCYTIDINE; FEMALE; HUMANS; METABOLIC DETOXICATION, DRUG; MICE; MICE, NUDE; PANCREATIC NEOPLASMS; PROTO-ONCOGENE PROTEINS C-MET; PYRAZOLES; PYRIDINES; TUMOR CELLS, CULTURED; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84888347646     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-13-0837     Document Type: Article

References (49)

1. Simard EP, Ward EM, Siegel R, Jemal A. Cancers with increasing incidence trends in the United States: 1999 through 2008. CA Cancer J Clin. 2012 Jan 4. [Epub ahead of print].
2. Vincent A, Herman J, Schulick R, Hruban RH, Goggins M. Pancreatic cancer. Lancet 2011;378:607-20.
3. Hidalgo M. Pancreatic cancer. N Engl J Med 2010;362:1605-17.
4. Frese KK, Neesse A, Cook N, Bapiro TE, Lolkema MP, Jodrell DI, et al. nab-Paclitaxel potentiates gemcitabine activity by reducing cytidine deaminase levels in a mouse model of pancreatic cancer. Cancer Discov 2012;2:260-9.
5. Jones S, Zhang X, Parsons DW, Lin JC, Leary RJ, Angenendt P, et al. Core signaling pathways in human pancreatic cancers revealed by global genomic analyses. Science 2008;321:1801-6.
6. Li C, Heidt DG, Dalerba P, Burant CF, Zhang L, Adsay V, et al. Identification of pancreatic cancer stem cells. Cancer Res 2007;67:1030-7.
7. Hermann PC, Huber SL, Herrler T, Aicher A, Ellwart JW, Guba M, et al. Distinct populations of cancer stem cells determine tumor growth and metastatic activity in human pancreatic cancer. Cell Stem Cell 2007;1:313-23.
8. Haeno H, Gonen M, Davis MB, Herman JM, Iacobuzio-Donahue CA, Michor F. Computational modeling of pancreatic cancer reveals kinetics of metastasis suggesting optimum treatment strategies. Cell 2012;148:362-75.
9. Frese KK, Tuveson DA. Maximizing mouse cancer models. Nat Rev Cancer 2007;7:645-58.
10. Neesse A, Michl P, Frese KK, Feig C, Cook N, Jacobetz MA, et al. Stromal biology and therapy in pancreatic cancer. Gut 2011;60:861-8.
11. Zhang Y, Chen L, Yang J, Fleming JB, Chiao PJ, Logsdon CD, et al. Study human pancreatic cancer in mice: how close are they? Biochim Biophys Acta 2013;1835:110-8.
12. Voskoglou-Nomikos T, Pater JL, Seymour L. Clinical predictive value of the in vitro cell line, human xenograft, and mouse allograft preclinical cancer models. Clin Cancer Res 2003;9:4227-39.
13. Hidalgo M, Bruckheimer E, Rajeshkumar NV, Garrido-Laguna I, De Oliveira E, Rubio-Viqueira B, et al. A pilot clinical study of treatment guided by personalized tumorgrafts in patients with advanced cancer. Mol Cancer Ther 2011;10:1311-6.
14. Garrido-Laguna I, Uson M, Rajeshkumar NV, Tan AC, de Oliveira E, Karikari C, et al. Tumor engraftment in nude mice and enrichment in stroma- related gene pathways predict poor survival and resistance to gemcitabine in patients with pancreatic cancer. Clin Cancer Res 2011;17:5793-800.
15. Kerbel RS. Human xenografts as predictive models for anticancer drug activity in humans: better than commonly perceived-but they can be improved. Cancer Biol Ther 2003;2:134-9.
16. Park JK, Kim MA, Ryu JK, Yoon YB, Kim SW, Han HS, et al. Postoperative prognostic predictors of pancreatic ductal adenocarcinoma: clinical analysis and immunoprofile on tissue microarrays. Ann Surg Oncol 2012;19:2664-72.
17. Wurdinger T, Badr C, Pike L, de Kleine R, Weissleder R, Breakefield XO, et al. A secreted luciferase for ex vivo monitoring of in vivo processes. Nat Methods 2008;5:171-3.
18. Caretti V, Zondervan I, Meijer DH, Idema S, Vos W, Hamans B, et al. Monitoring of tumor growth and post-irradiation recurrence in a diffuse intrinsic pontine glioma mouse model. Brain Pathol 2011;21:441-51.
19. Lee JH, Giovannetti E, Hwang JH, Petrini I, Wang Q, Voortman J, et al. Loss of 18q22.3 involving the carboxypeptidase of glutamate-like gene is associated with poor prognosis in resected pancreatic cancer. Clin Cancer Res 2012;18:524-33.
20. Funel N, Giovannetti E, Del Chiaro M, Mey V, Pollina LE, Nannizzi S, et al. Laser microdissection and primary cell cultures improve pharmacogenetic analysis in pancreatic adenocarcinoma. Lab Invest 2008;88:773-84.
21. Verheul HM, Hammers H, van Erp K, Wei Y, Sanni T, Salumbides B, et al. Vascular endothelial growth factor trap blocks tumor growth, metastasis formation, and vascular leakage in an orthotopic murine renal cell cancer model. Clin Cancer Res 2007;13:4201-8.
22. Ino Y, Yamazaki-Itoh R, Oguro S, Shimada K, Kosuge T, Zavada J, et al. Arginase II expressed in cancer-associated fibroblasts indicates tissue hypoxia and predicts poor outcome in patients with pancreatic cancer. PLoS ONE 2013;8:e55146.
23. Avan A, Quint K, Nicolini F, Funel N, Frampton AE, Maftouh M, et al. Enhancement of the antiproliferative activity of gemcitabine by modulation of c-Met pathway in pancreatic cancer. Curr Pharm Des 2013;19:940-50.
24. Zucali PA, Ruiz MG, Giovannetti E, Destro A, Varella-Garcia M, Floor K, et al. Role of cMET expression in non-small-cell lung cancer patients treated with EGFR tyrosine kinase inhibitors. Ann Oncol 2008;19:1605-12.
25. Bergman AM, Eijk PP, Ruiz van Haperen VW, Smid K, Veerman G, Hubeek I, et al. In vivo induction of resistance to gemcitabine results in increased expression of ribonucleotide reductase subunit M1 as the major determinant. Cancer Res 2005;65:9510-6.
26. Zhou WJ, Zhang X, Cheng C, Wang F, Wang XK, Liang YJ, et al. Crizotinib (PF-02341066) reverses multidrug resistance in cancer cells by inhibiting the function of P-glycoprotein. Br J Pharmacol 2012;166:1669-83.
27. Honeywell R, Yarzadah K, Giovannetti E, Losekoot N, Smit EF, Walraven M, et al. Simple and selective method for the determination of various tyrosine kinase inhibitors used in the clinical setting by liquid chromatography tandem mass spectrometry. J Chromatogr B Analyt Technol Biomed Life Sci 2010;878:1059-68.
28. Komar G, Kauhanen S, Liukko K, Seppanen M, Kajander S, Ovaska J, et al. Decreased blood flow with increased metabolic activity: a novel sign of pancreatic tumor aggressiveness. Clin Cancer Res 2009;15:5511-7.
29. Shoemaker RH. The NCI60 human tumour cell line anticancer drug screen. Nat Rev Cancer 2006;6:813-23.
30. Hughes P, Marshall D, Reid Y, Parkes H, Gelber C. The costs of using unauthenticated, over-passaged cell lines: how much more data do we need? Biotechniques 2007;43:577-8.
31. Pérez-Torras S, Vidal-Pla A, Miquel R, Almendro V, Fernández-Cruz L, Navarro S, et al. Characterization of human pancreatic orthotopic tumor xenografts suitable for drug screening. Cell Oncol 2011;34:511-21.
32. Klerk CP, Overmeer RM, Niers TM, Versteeg HH, Richel DJ, Buckle T, et al. Validity of bioluminescence measurements for noninvasive in vivo imaging of tumor load in small animals. Biotechniques 2007;43:7-13.
33. Dimayuga VM, Rodriguez-Porcel M. Molecular imaging of cell therapy for gastroenterologic applications. Pancreatology 2011;11:414-27.
34. Tuli R, Surmak A, Reyes J, Hacker-Prietz A, Armour M, Leubner A, et al. Development of a novel preclinical pancreatic cancer research model: bioluminescence image-guided focal irradiation and tumor monitoring of orthotopic xenografts. Transl Oncol 2012;5:77-84.
35. Cooper CS, Park M, Blair DG, Tainsky MA, Huebner K, Croce CM, et al. Molecular cloning of a new transforming gene from a chemically transformed human cell line. Nature 1984;311:29-33.
36. Di Renzo MF, Narsimhan RP, Olivero M, Bretti S, Giordano S, Medico E, et al. Expression of the Met/HGF receptor in normal and neoplastic human tissues. Oncogene 1991;6:1997-2003.
37. Organ SL, Tsao MS. An overview of the c-MET signaling pathway. Ther Adv Med Oncol 2011;3:7-19.
38. Boccaccio C, Comoglio PM. Invasive growth: a MET-driven genetic programme for cancer and stem cells. Nat Rev Cancer 2006;6:637-45.
39. Ebert M, Yokoyama M, Friess H, Büchler MW, Korc M. Coexpression of the c-met proto-oncogene and hepatocyte growth factor in human pancreatic cancer. Cancer Res 1994;54:5775-8.
40. Di Renzo MF, Poulsom R, Olivero M, Comoglio PM, Lemoine NR. Expression of the Met/hepatocyte growth factor receptor in human pancreatic cancer. Cancer Res 1995;55:1129-38.
41. Zhu GH, Huang C, Qiu ZJ, Liu J, Zhang ZH, Zhao N, et al. Expression and prognostic significance of CD151, c-Met, and integrin alpha3/alpha6 in pancreatic ductal adenocarcinoma. Dig Dis Sci 2011;56:1090-8.
42. Li C, Wu JJ, Hynes M, Dosch J, Sarkar B, Welling TH, et al. c-Met is a marker of pancreatic cancer stem cells and therapeutic target. Gastroenterology 2011;141:2218-27.
43. Gandhi L, Janne PA. Crizotinib for ALK-rearranged non-small cell lung cancer: a new targeted therapy for a new target. Clin Cancer Res 2012;18:3737-42.
44. Ou SH, Kwak EL, Siwak-Tapp C, Dy J, Bergethon K, Clark JW, et al. Activity of crizotinib (PF02341066), a dual mesenchymal-epithelial transition (MET) and anaplastic lymphoma kinase (ALK) inhibitor, in a non-small cell lung cancer patient with de novo MET amplification. J Thorac Oncol 2011;6:942-6.
45. Fukuyoshi Y, Inoue H, Kita Y, Utsunomiya T, Ishida T, Mori M. EML4-ALK fusion transcript is not found in gastrointestinal and breast cancers. Br J Cancer 2008;98:1536-9.
46. Sennino B, Ishiguro-Oonuma T, Wei Y, Naylor RM, Williamson CW, Bhagwandin V, et al. Suppression of tumor invasion and metastasis by concurrent inhibition of c-Met and VEGF signaling in pancreatic neuroendocrine tumors. Cancer Discov 2012;2:270-87.
47. Gómez-Quiroz LE, Factor VM, Kaposi-Novak P, Coulouarn C, Conner EA, Thorgeirsson SS. Hepatocyte-specific c-Met deletion disrupts redox homeostasis and sensitizes to Fas-mediated apoptosis. J Biol Chem 2008;283:14581-9.
48. Uddin S, Hussain AR, Ahmed M, Al-Sanea N, Abduljabbar A, Ashari LH, et al. Coexpression of activated c-Met and death receptor 5 predicts better survival in colorectal carcinoma. Am J Pathol 2011;179:3032-44.
49. Bijnsdorp IV, Giovannetti E, Peters GJ. Analysis of drug interactions. Methods Mol Biol 2011;731:421-34.