Lysosomal sequestration of sunitinib: A novel mechanism of drug resistance

Clinical Cancer Research

Volumn 17, Issue 23, 2011, Pages 7337-7346

  Gotink, Kristy J ^a   Broxterman, Henk J ^a   Labots, Mariette ^a   De Haas, Richard R ^a   Dekker, Henk ^a   Honeywell, Richard J ^a   Rudek, Michelle A ^c   Beerepoot, Laurens V ^b   Musters, René J ^a   Jansen, Gerrit ^a   Griffioen, Arjan W ^a   Assaraf, Yehuda G ^a,d   Pili, Roberto ^e   Peters, Godefridus J ^a   Verheul, Henk M W ^a  

^a VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^b CPRLab   (Netherlands)

^c JOHNS HOPKINS UNIVERSITY   (United States)

^d TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

^e ROSWELL PARK CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LYSOSOME ENZYME; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PROTEIN KINASE B; SUNITINIB;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER RESISTANCE; CELL PROLIFERATION; CLINICAL TRIAL; COLON CANCER; COLORECTAL CANCER; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG ACCUMULATION; DRUG BLOOD LEVEL; DRUG DISTRIBUTION; DRUG EFFICACY; DRUG MECHANISM; DRUG TUMOR LEVEL; ENZYME INHIBITION; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; IC 50; IN VITRO STUDY; KIDNEY CANCER; LEIOMYOSARCOMA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; TREATMENT RESPONSE; TUMOR CELL; TUMOR GROWTH;

ANGIOGENESIS INHIBITORS; ANIMALS; CARCINOMA, RENAL CELL; CELL LINE, TUMOR; CELL PROLIFERATION; DRUG RESISTANCE, NEOPLASM; FEMALE; HCT116 CELLS; HT29 CELLS; HUMANS; INDOLES; KIDNEY NEOPLASMS; LYSOSOMES; MICE; NEOPLASMS; PROTEIN-TYROSINE KINASES; PYRROLES;

EID: 82555189379     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-11-1667     Document Type: Article

References (34)

1. Bergers G, Hanahan D. Modes of resistance to anti-angiogenic therapy. Nat Rev Cancer 2008;8:592-603.
2. Motzer RJ, Michaelson MD, Rosenberg J, Bukowski RM, Curti BD, George DJ, et al. Sunitinib efficacy against advanced renal cell carcinoma. J Urol 2007;178:1883-7. (Pubitemid 47538608)
3. Motzer RJ, Hutson TE, Tomczak P, Michaelson MD, Bukowski RM, Oudard S, et al. Overall survival and updated results for sunitinib compared with interferon alfa in patients with metastatic renal cell carcinoma. J Clin Oncol 2009;27:3584-90.
4. Goodman VL, Rock EP, Dagher R, Ramchandani RP, Abraham S, Gobburu JV, et al. Approval summary: sunitinib for the treatment of imatinib refractory or intolerant gastrointestinal stromal tumors and advanced renal cell carcinoma. Clin Cancer Res 2007;13:1367-73. (Pubitemid 46450424)
5. Raymond E, Dahan L, Raoul JL, Bang YJ, Borbath I, Lombard-Bohas C, et al. Sunitinib malate for the treatment of pancreatic neuroendocrine tumors. N Engl J Med 2011;364:501-13.
6. Shojaei F, Lee JH, Simmons BH, Wong A, Esparza CO, Plumlee PA, et al. HGF/c-Met acts as an alternative angiogenic pathway in sunitinib-resistant tumors. Cancer Res 2010;70:10090-100.
7. Huang D, Ding Y, Zhou M, Rini BI, Petillo D, Qian CN, et al. Interleukin-8 mediates resistance to antiangiogenic agent sunitinib in renal cell carcinoma. Cancer Res 2010;70:1063-71.
8. Doberstein K, Wieland A, Lee SB, Blaheta RA, Wedel S, Moch H, et al. L1-CAM expression in ccRCC correlates with shorter patients survival times and confers chemoresistance in renal cell carcinoma cells. Carcinogenesis 2011;32:262-70.
9. Hammers HJ, Verheul HM, Salumbides B, Sharma R, Rudek M, Jaspers J, et al. Reversible epithelial to mesenchymal transition and acquired resistance to sunitinib in patients with renal cell carcinoma: evidence from a xenograft study. Mol Cancer Ther 2010;9:1525-35.
10. Broxterman HJ, Gotink KJ, Verheul HM. Understanding the causes of multidrug resistance in cancer: a comparison of doxorubicin and sunitinib. Drug Resist Updat 2009;12:114-26.
11. Fabian MA, Biggs WH III, Treiber DK, Atteridge CE, Azimioara MD, Benedetti MG, et al. A small molecule-kinase interaction map for clinical kinase inhibitors. Nat Biotechnol 2005;23:329-36. (Pubitemid 41094421)
12. Karaman MW, Herrgard S, Treiber DK, Gallant P, Atteridge CE, Campbell BT, et al. A quantitative analysis of kinase inhibitor selectivity. Nat Biotechnol 2008;26:127-32.
13. 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.
14. Holdhoff M, Supko JG, Gallia GL, Hann CL, Bonekamp D, Ye X, et al. Intratumoral concentrations of imatinib after oral administration in patients with glioblastoma multiforme. J Neurooncol 2010;97:241-5.
15. Franken NA, Rodermond HM, Stap J, Haveman J, van Bree C. Clonogenic assay of cells in vitro. Nat Protoc 2006;1:2315-9.
16. Mathews ST, Plaisance EP, Kim T. Imaging systems for westerns: chemiluminescence vs. infrared detection. Methods Mol Biol 2009;536:499-513.
17. Gotink KJ, Verheul HM. Anti-angiogenic tyrosine kinase inhibitors: what is their mechanism of action? Angiogenesis 2010;13:1-14.
18. Lemmon MA, Schlessinger J. Cell signaling by receptor tyrosine kinases. Cell 2010;141:1117-34.
19. Myers MP, Pass I, Batty IH, Van der Kaay J, Stolarov JP, Hemmings BA, et al. The lipid phosphatase activity of PTEN is critical for its tumor supressor function. Proc Natl Acad Sci U S A 1998;95:13513-8. (Pubitemid 28523003)
20. Bowman EJ, Siebers A, Altendorf K. Bafilomycins: a class of inhibitors of membrane ATPases from microorganisms, animal cells, and plant cells. Proc Natl Acad Sci U S A 1988;85:7972-6.
21. Ohkuma S, Poole B. Fluorescence probe measurement of the intralysosomal pH in living cells and the perturbation of pH by various agents. Proc Natl Acad Sci U S A 1978;75:3327-31. (Pubitemid 8389720)
22. Saftig P, Klumperman J. Lysosome biogenesis and lysosomal membrane proteins: trafficking meets function. Nat Rev Mol Cell Biol 2009;10:623-35.
23. Motzer RJ, Michaelson MD, Redman BG, Hudes GR, Wilding G, Figlin RA, et al. Activity of SU11248, a multitargeted inhibitor of vascular endothelial growth factor receptor and platelet-derived growth factor receptor, in patients with metastatic renal cell carcinoma. J Clin Oncol 2006;24:16-24. (Pubitemid 46630489)
24. Huang D, Ding Y, Li Y, Luo WM, Zhang ZF, Snider J, et al. Sunitinib acts primarily on tumor endothelium rather than tumor cells to inhibit the growth of renal cell carcinoma. Cancer Res 2010;70:1053-62.
25. Verheul HM, Lolkema MP, Qian DZ, Hilkes YH, Liapi E, Akkerman JW, et al. Platelets take up the monoclonal antibody bevacizumab. Clin Cancer Res 2007;13:5341-7. (Pubitemid 47510358)
26. Battinelli EM, Markens BA, Italiano JE Jr. Release of angiogenesis regulatory proteins from platelet alpha granules: modulation of physiological and pathological angiogenesis. Blood 2011;118:1359-69.
27. Chouaib S, Kieda C, Benlalam H, Noman MZ, Mami-Chouaib F, Ruegg C. Endothelial cells as key determinants of the tumor microenvironment: interaction with tumor cells, extracellular matrix and immune killer cells. Crit Rev Immunol 2010;30:529-45.
28. Yang F, Jove V, Xin H, Hedvat M, Van Meter TE, Yu H. Sunitinib induces apoptosis and growth arrest of medulloblastoma tumor cells by inhibiting STAT3 and AKT signaling pathways. Mol Cancer Res 2010;8:35-45.
29. Ellis LM, Hicklin DJ. Pathways mediating resistance to vascular endothelial growth factor-targeted therapy. Clin Cancer Res 2008;14:6371-5.
30. Ebos JM, Lee CR, Christensen JG, Mutsaers AJ, Kerbel RS. Multiple circulating proangiogenic factors induced by sunitinib malate are tumor-independent and correlate with antitumor efficacy. Proc Natl Acad Sci U S A 2007;104:17069-74. (Pubitemid 350210993)
31. Vroling L, van der Veldt AA, de Haas RR, Haanen JB, Schuurhuis GJ, Kuik DJ, et al. Increased numbers of small circulating endothelial cells in renal cell cancer patients treated with sunitinib. Angiogenesis 2009;12:69-79.
32. Ellis LM, Hicklin DJ. Resistance to targeted therapies: refining anticancer therapy in the era of molecular oncology. Clin Cancer Res 2009;15:7471-8.
33. Zama IN, Hutson TE, Elson P, Cleary JM, Choueiri TK, Heng DY, et al. Sunitinib rechallenge in metastatic renal cell carcinoma patients. Cancer 2010;116:5400-6.
34. Fehrenbacher N, Jaattela M. Lysosomes as targets for cancer therapy. Cancer Res 2005;65:2993-5. (Pubitemid 40524572)