Synergistic proapoptotic effects of the two tyrosine kinase inhibitors pazopanib and lapatinib on multiple carcinoma cell lines

Oncogene

Volumn 28, Issue 48, 2009, Pages 4249-4260

  Olaussen, K A ^a,b,c   Commo, F ^b   Tailler, M ^a,b,c   Lacroix, L ^b   Vitale, I ^a,b,c   Raza, S Q ^a,b,c   Richon, C ^b   Dessen, P ^b   Lazar, V ^b   Soria, J C ^b,c   Kroemer, G ^a,b,c  

^a INSERM   (France)

^b INSTITUT GUSTAVE ROUSSY   (France)

^c UNIVERSITÉ PARIS SACLAY   (France)

Author keywords

Apoptosis; Kinome; Lapatinib; Pazopanib; TKIs; Transcriptome

Indexed keywords

ABELSON KINASE; CISPLATIN; EPIDERMAL GROWTH FACTOR RECEPTOR; FIBROBLAST GROWTH FACTOR RECEPTOR 1; FIBROBLAST GROWTH FACTOR RECEPTOR 3; FOCAL ADHESION KINASE; LAPATINIB; PAZOPANIB; PEMETREXED; PROTEIN KINASE FYN; PROTEIN KINASE ZAP 70; PROTEIN TYROSINE KINASE INHIBITOR; SCATTER FACTOR RECEPTOR; TRANSCRIPTOME; VASCULOTROPIN RECEPTOR 1;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CARCINOMA CELL; CELL SURVIVAL; COLON CANCER; CONTROLLED STUDY; DOWN REGULATION; DRUG CYTOTOXICITY; DRUG POTENTIATION; ENZYME INHIBITION; GENE CONTROL; HELA CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; LUNG NON SMALL CELL CANCER; PHARMACOGENETICS; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; STOMACH CANCER; UPREGULATION;

ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; APOPTOSIS; CELL LINE, TUMOR; DRUG SYNERGISM; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HUMANS; MALE; PROTEIN KINASE INHIBITORS; PROTEIN-TYROSINE KINASES; PROTO-ONCOGENE PROTEINS C-BCL-2; PYRIMIDINES; QUINAZOLINES; SIGNAL TRANSDUCTION; SULFONAMIDES; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 71249164372     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2009.277     Document Type: Article

References (64)

1. Barnes CJ, Kumar R. (2003). Epidermal growth factor receptor family tyrosine kinases as signal integrators and therapeutic targets. Cancer Metastasis Rev 22: 301-307.
2. Bianco R, Rosa R, Damiano V, Daniele G, Gelardi T, Garofalo S et al. (2008). Vascular endothelial growth factor receptor-1 contributes to resistance to anti-epidermal growth factor receptor drugs in human cancer cells. Clin Cancer Res 14: 5069-5080.
3. Bliss CI. (1939). The toxicity of poisons applied jointly. Ann Appl Biol 26: 585-615.
4. Bozec A, Formento P, Lassalle S, Lippens C, Hofman P, Milano G. (2007). Dual inhibition of EGFR and VEGFR pathways in combination with irradiation: antitumour supra-additive effects on human head and neck cancer xenografts. Br J Cancer 97: 65-72.
5. Calandrella N, Risuleo G, Scarsella G, Mustazza C, Castelli M, Galati F et al. (2007). Reduction of cell proliferation induced by PD166866: an inhibitor of the basic fibroblast growth factor. J Exp Clin Cancer Res 26: 405-409.
6. Cameron DA, Stein S. (2008). Drug Insight: intracellular inhibitors of HER2-clinical development of lapatinib in breast cancer. Nat Clin Pract Oncol 5: 512-520.
7. Castedo M, Coquelle A, Vivet S, Vitale I, Kauffmann A, Dessen P et al. (2006). Apoptosis regulation in tetraploid cancer cells. EMBO J 25: 2584-2595.
8. Castedo M, Ferri K, Roumier T, Metivier D, Zamzami N, Kroemer G. (2002). Quantitation of mitochondrial alterations associated with apoptosis. J Immunol Methods 265: 39-47.
9. Chien AJ, Illi JA, Ko AH, Dubey S, Jahan TM, Hylton NM et al. (2008). A phase I dose escalation study of a 2 day lapatinib chemosensitization pulse preceding weekly intravenous nanoparticle albumin-bound paclitaxel (nab-paclitaxel) in patients with advanced cancer. J Clin Oncol 26: Abstract number 3595.
10. Ciardiello F, Tortora G. (2008). EGFR antagonists in cancer treatment. N Engl J Med 358: 1160-1174.
11. Comoglio PM, Giordano S, Trusolino L. (2008). Drug development of MET inhibitors: targeting oncogene addiction and expedience. Nat Rev Drug Discov 7: 504-516.
12. Danilov AV, Klein AK, Lee HJ, Baez DV, Huber BT. (2005). Differential control of G0 programme in chronic lympho-cytic leukaemia: a novel prognostic factor. Br J Haematol 128: 472-481.
13. de La Motte Rouge T, Galluzzi L, Olaussen KA, Zermati Y, Tasdemir E, Robert T et al. (2007). A novel epidermal growth factor receptor inhibitor promotes apoptosis in non-small cell lung cancer cells resistant to erlotinib. Cancer Res 67: 6253-6262.
14. Donnem T, Al-Saad S, Al-Shibli K, Delghandi MP, Persson M, Nilsen MN et al. (2007). Inverse prognostic impact of angiogenic marker expression in tumor cells versus stromal cells in non small cell lung cancer. Clin Cancer Res 13: 6649-6657.
15. Druker BJ, Talpaz M, Resta DJ, Peng B, Buchdunger E, Ford JM et al. (2001). Efficacy and safety of a specific inhibitor of the BCR-ABL tyrosine kinase in chronic myeloid leukemia. N Engl J Med 344: 1031-1037.
16. Edinger AL. (2007). Controlling cell growth and survival through regulated nutrient transporter expression. Biochem J 406: 1-12.
17. Fan F, Wey JS, McCarty MF, Belcheva A, Liu W, Bauer TW et al. (2005). Expression and function of vascular endothelial growth factor receptor-1 on human colorectal cancer cells. Oncogene 24: 2647-2653.
18. Flier JS, Mueckler MM, Usher P, Lodish HF. (1987). Elevated levels of glucose transport and transporter messenger RNA are induced by ras or src oncogenes. Science 235: 1492-1495.
19. Fransson A, Ruusala A, Aspenstrom P. (2003). Atypical Rho GTPases have roles in mitochondrial homeostasis and apoptosis. J Biol Chem 278: 6495-6502.
20. Geyer CE, Forster J, Lindquist D, Chan S, Romieu CG, Pienkowski T et al. (2006). Lapatinib plus capecitabine for HER2-positive advanced breast cancer. N Engl J Med 355: 2733-2743.
21. Golubovskaya V, Beviglia L, Xu LH, Earp 3rd HS, Craven R, Cance W. (2002). Dual inhibition of focal adhesion kinase and epidermal growth factor receptor pathways cooperatively induces death receptor-mediated apoptosis in human breast cancer cells. J Biol Chem 277: 38978-38987.
22. Harris PA, Boloor A, Cheung M, Kumar R, Crosby RM, Davis-Ward RG et al. (2008). Discovery of 5-[[4-[(2,3-dimethyl-2H-indazol-6-yl)methylamino]-2- pyrimidinyl]amino]-2-m ethyl-benzenesulfona-mide (Pazopanib), a novel and potent vascular endothelial growth factor receptor inhibitor. J Med Chem 51: 4632-4640.
23. Hayashida N, Inouye S, Fujimoto M, Tanaka Y, Izu H, Takaki E et al. (2006). A novel HSF1-mediated death pathway that is suppressed by heat shock proteins. EMBO J 25: 4773-4783.
24. Hegde PS, Rusnak D, Bertiaux M, Alligood K, Strum J, Gagnon R et al. (2007). Delineation of molecular mechanisms of sensitivity to lapatinib in breast cancer cell lines using global gene expression profiles. Mol Cancer Ther 6: 1629-1640.
25. Helfrich BA, Raben D, Varella-Garcia M, Gustafson D, Chan DC, Bemis L et al. (2006). Antitumor activity of the epidermal growth factor receptor (EGFR) tyrosine kinase inhibitor gefitinib (ZD1839, Iressa) in non-small cell lung cancer cell lines correlates with gene copy number and EGFR mutations but not EGFR protein levels. Clin Cancer Res 12: 7117-7125.
26. Houge G, Robaye B, Eikhom TS, Golstein J, Mellgren G, Gjertsen BT et al. (1995). Fine mapping of 28S rRNA sites specifically cleaved in cells undergoing apoptosis. Mol Cell Biol 15: 2051-2062.
27. Hulit J, Lee RJ, Russell RG, Pestell RG. (2002). ErbB-2-induced mammary tumor growth: the role of cyclin D1 and p27Kip1. Biochem Pharmacol 64: 827-836.
28. Hurwitz HI, Dowlati A, Saini S, Savage S, Suttle AB, Gibson DM et al. (2009). Phase I trial of pazopanib in patients with advanced cancer. Clin Cancer Res 15: 4220-4227.
29. Johnson SA, Hunter T. (2005). Kinomics: methods for deciphering the kinome. Nat Methods 2: 17-25.
30. Joo JH, Liao G, Collins JB, Grissom SF, Jetten AM. (2007). Farnesol-induced apoptosis in human lung carcinoma cells is coupled to the endoplasmic reticulum stress response. Cancer Res 67: 7929-7936.
31. Karaman MW, Herrgard S, Treiber DK, Gallant P, Atteridge CE, Campbell BT et al. (2008). A quantitative analysis of kinase inhibitor selectivity. Nat Biotechnol 26: 127-132.
32. Kerbel RS. (2008). Tumor angiogenesis. N Engl J Med 358: 2039-2049.
33. Klawitter J, Zhang YL, Anderson N, Serkova NJ, Christians U. (2009). Development and validation of a sensitive assay for the quantification of imatinib using LC/LC-MS/MS in human whole blood and cell culture. Biomed Chromatogr (e-pub ahead of print 10 June 2009.
34. Konecny GE, Pegram MD, Venkatesan N, Finn R, Yang G, Rahmeh M et al. (2006). Activity of the dual kinase inhibitor lapatinib (GW572016) against HER-2-overexpressing and trastuzumab-treated breast cancer cells. Cancer Res 66: 1630-1639.
35. Kroemer G, Galluzzi L, Vandenabeele P, Abrams J, Alnemri ES, Baehrecke EH et al. (2009). Classification of cell death: recommendations of the Nomenclature Committee on Cell Death 2009. Cell Death Differ 16: 3-11.
36. Kumar R, Knick VB, Rudolph SK, Johnson JH, Crosby RM, Crouthamel MC et al. (2007). Pharmacokinetic-pharmacodynamic correlation from mouse to human with pazopanib, a multikinase angiogenesis inhibitor with potent antitumor and antiangiogenic activity. Mol Cancer Ther 6: 2012-2021.
37. Lee TH, Seng S, Sekine M, Hinton C, Fu Y, Avraham HK et al. (2007). Vascular endothelial growth factor mediates intracrine survival in human breast carcinoma cells through internally expressed VEGFR1/FLT1. PLoS Med 4: e186.
38. Manning G, Whyte DB, Martinez R, Hunter T, Sudarsanam S. (2002). The protein kinase complement of the human genome. Science 298: 1912-1934.
39. Monks A, Scudiero D, Skehan P, Shoemaker R, Paull K, Vistica D et al. (1991). Feasibility of a high-flux anticancer drug screen using a diverse panel of cultured human tumor cell lines. J Natl Cancer Inst 83: 757-766.
40. Mourali J, Benard A, Lourenco FC, Monnet C, Greenland C, Moog-Lutz C et al. (2006). Anaplastic lymphoma kinase is a dependence receptor whose proapoptotic functions are activated by caspase cleavage. Mol Cell Biol 26: 6209-6222.
41. Nadano D, Sato TA. (2000). Caspase-3-dependent and-independent degradation of 28 S ribosomal RNA may be involved in the inhibition of protein synthesis during apoptosis initiated by death receptor engagement. J Biol Chem 275: 13967-13973.
42. Noble ME, Endicott JA, Johnson LN. (2004). Protein kinase inhibitors: insights into drug design from structure. Science 303: 1800-1805.
43. Oberst MD, Beberman SJ, Zhao L, Yin JJ, Ward Y, Kelly K. (2008). TDAG51 is an ERK signaling target that opposes ERK-mediated HME16C mammary epithelial cell transformation. BMC Cancer 8: 189.
44. Peruzzi B, Bottaro DP. (2006). Targeting the c-Met signaling pathway in cancer. Clin Cancer Res 12: 3657-3660.
45. Petit AM, Rak J, Hung MC, Rockwell P, Goldstein N, Fendly B et al. (1997). Neutralizing antibodies against epidermal growth factor and ErbB-2/neu receptor tyrosine kinases down-regulate vascular endothelial growth factor production by tumor cells in vitro and in vivo: angiogenic implications for signal transduction therapy of solid tumors. Am J Pathol 151: 1523-1530.
46. Pietsch EC, Sykes SM, McMahon SB, Murphy ME. (2008). The p53 family and programmed cell death. Oncogene 27: 6507-6521.
47. Podar K, Tonon G, Sattler M, Tai YT, Legouill S, Yasui H et al. (2006). The small-molecule VEGF receptor inhibitor pazopanib (GW786034B) targets both tumor and endothelial cells in multiple myeloma. Proc Natl Acad Sci USA 103: 19478-19483.
48. Press MF, Finn RS, Cameron D, Di Leo A, Geyer CE, Villalobos IE et al. (2008). HER-2 gene amplification, HER-2 and epidermal growth factor receptor mRNA and protein expression, and lapatinib efficacy in women with metastatic breast cancer. Clin Cancer Res 14: 7861-7870.
49. Puri N, Khramtsov A, Ahmed S, Nallasura V, Hetzel JT, Jagadees-waran R et al. (2007). A selective small molecule inhibitor of c-Met, PHA665752, inhibits tumorigenicity and angiogenesis in mouse lung cancer xenografts. Cancer Res 67: 3529-3534.
50. Puri N, Salgia R. (2008). Synergism of EGFR and c-Met pathways, cross-talk and inhibition, in non-small cell lung cancer. J Carcinog 7: 9.
51. Riely GJ, Rizvi NA, Kris MG, Milton DT, Solit DB, Rosen N et al. (2009). Randomized phase II study of pulse erlotinib before or after carboplatin and paclitaxel in current or former smokers with advanced non-small-cell lung cancer. J Clin Oncol 27: 264-270.
52. Simiantonaki N, Jayasinghe C, Michel-Schmidt R, Peters K, Hermanns MI, Kirkpatrick CJ. (2008). Hypoxia-induced epithelial VEGF-C/VEGFR-3 upregulation in carcinoma cell lines. Int J Oncol 32: 585-592.
53. Sini P, Samarzija I, Baffert F, Littlewood-Evans A, Schnell C, Theuer A et al. (2008). Inhibition of multiple vascular endothelial growth factor receptors (VEGFR) blocks lymph node metastases but inhibition of VEGFR-2 is sufficient to sensitize tumor cells to platinum-based chemotherapeutics. Cancer Res 68: 1581-1592.
54. Sleijfer S, Wiemer E, Verweij J. (2008). Drug insight: gastrointestinal stromal tumors (GIST)-the solid tumor model for cancer-specific treatment. Nat Clin Pract Oncol 5: 102-111.
55. Sloan B, Scheinfeld NS. (2008). Pazopanib, a VEGF receptor tyrosine kinase inhibitor for cancer therapy. Curr Opin Investig Drugs 9: 1324-1335.
56. Sonpavde G, Hutson TE, Sternberg CN. (2008). Pazopanib, a potent orally administered small-molecule multitargeted tyrosine kinase inhibitor for renal cell carcinoma. Expert Opin Investig Drugs 17: 253-261.
57. Storey JD, Tibshirani R. (2003). Statistical methods for identifying differentially expressed genes in DNA microarrays. Methods Mol Biol 224: 149-157.
58. Storniolo AM, Pegram MD, Overmoyer B, Silverman P, Peacock NW, Jones SF et al. (2008). Phase I dose escalation and pharmacokinetic study of lapatinib in combination with trastuzumab in patients with advanced ErbB2-positive breast cancer. J Clin Oncol 26: 3317-3323.
59. Thompson HJ, Zhu Z, Jiang W. (2004). Identification of the apoptosis activation cascade induced in mammary carcinomas by energy restriction. Cancer Res 64: 1541-1545.
60. Vitale I, Galluzzi L, Vivet S, Nanty L, Dessen P, Senovilla L et al. (2007). Inhibition of Chk1 kills tetraploid tumor cells through a p53-dependent pathway. PLoS ONE 2: e1337.
61. Wettenhall JM, Smyth GK. (2004). limmaGUI: a graphical user interface for linear modeling of microarray data. Bioinformatics 20: 3705-3706.
62. Wood ER, Truesdale AT, McDonald OB, Yuan D, Hassell A, Dickerson SH et al. (2004). A unique structure for epidermal growth factor receptor bound to GW572016 (Lapatinib): relationships among protein conformation, inhibitor off-rate, and receptor activity in tumor cells. Cancer Res 64: 6652-6659.
63. Wu B. (2006). Differential gene expression detection and sample classification using penalized linear regression models. Bioinfor-matics 22: 472-476.
64. Zamzami N, Kroemer G. (2004). Methods to measure membrane potential and permeability transition in the mitochondria during apoptosis. Methods Mol Biol 282: 103-115