Sunitinib and SU11652 inhibit acid sphingomyelinase, destabilize lysosomes, and inhibit multidrug resistance

Molecular Cancer Therapeutics

Volumn 12, Issue 10, 2013, Pages 2018-2030

  Ellegaard, Anne Marie ^a   Groth Pedersen, Line ^a,d   Oorschot, Viola ^c   Klumperman, Judith ^c   Kirkegaard, Thomas ^a,b   Nylandsted, Jesper ^a   Jäättelä, Marja ^a  

^a DANISH CANCER SOCIETY RESEARCH CENTER   (Denmark)

^b ORPHAZYME A S   (Denmark)

^c UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^d International Center for Research and Research Training in Endocrine Disruption of Male Reproduction and Child Health   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

HEAT SHOCK PROTEIN 70; PROTEIN BCL 2; PROTEIN TYROSINE KINASE INHIBITOR; PROTEINASE; SPHINGOMYELIN PHOSPHODIESTERASE; SU 11652; SUNITINIB; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CELL KILLING; CELL PH; CELL STRAIN MCF 7; CELL SURVIVAL; CELL ULTRASTRUCTURE; CELL VIABILITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOSOL; DRUG CYTOTOXICITY; DRUG POTENCY; DRUG TARGETING; ENZYME INHIBITION; HUMAN; HUMAN CELL; LYSOSOME; LYSOSOME MEMBRANE; MEMBRANE STABILIZATION; MULTIDRUG RESISTANCE; PHENOTYPE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

APOPTOSIS; CELL SURVIVAL; DRUG RESISTANCE, NEOPLASM; HELA CELLS; HUMANS; INDOLES; LYSOSOMES; MCF-7 CELLS; NEOPLASMS; PYRROLES; SPHINGOMYELIN PHOSPHODIESTERASE;

EID: 84883606763     PISSN: 15357163     EISSN: 15388514     Source Type: Journal    
DOI: 10.1158/1535-7163.MCT-13-0084     Document Type: Article

References (50)

1. Kaufmann SH, Hengartner MO. Programmed cell death: alive and well in the new millennium. Trends Cell Biol 2001;11: 526-34.
2. Taylor RC, Cullen SP, Martin SJ. Apoptosis: controlled demolition at the cellular level. Nat Rev Mol Cell Biol 2008;9: 231-41.
3. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011;144: 646-74.
4. Vandenabeele P, Galluzzi L, Vanden Berghe T, Kroemer G. Molecular mechanisms of necroptosis: an ordered cellular explosion. Nat Rev Mol Cell Biol 2010;11: 700-14.
5. Kirkegaard T, Jäättelä M. Lysosomal involvement in cell death and cancer. Biochim Biophys Acta 2009;1793: 746-54.
6. Fehrenbacher N, Bastholm L, Kirkegaard-Sørensen T, Rafn B, Bottzauw T, Nielsen C, et al. Sensitization to the lysosomal cell death pathway by oncogene-induced down-regulation of lysosome-associated membrane proteins 1 and 2. Cancer Res 2008;68: 6623-33.
7. Rafn B, Nielsen CF, Andersen SH, Szyniarowski P, Corcelle-Termeau E, Valo E, et al. ErbB2-driven breast cancer cell invasion depends on a complex signaling network activating myeloid zinc finger-1-dependent cathepsin B expression. Mol Cell 2012;45: 764-76.
8. Fehrenbacher N, Gyrd-Hansen M, Poulsen B, Felbor U, Kallunki T, Boes M, et al. Sensitization to the lysosomal cell death pathway upon immortalization and transformation. Cancer Res 2004;64: 5301-10.
9. Mohamed MM, Sloane BF. Cysteine cathepsins: multifunctional enzymes in cancer. Nat Rev Cancer 2006;6: 764-75.
10. Gocheva V, Joyce JA. Cysteine cathepsins and the cutting edge of cancer invasion. Cell Cycle 2007;6: 60-4.
11. Kallunki T, Olsen OD, Jaattela M. Cancer-associated lysosomal changes: friends or foes? Oncogene 2013;32: 1995-2004.
12. Ono K, Kim SO, Han J. Susceptibility of lysosomes to rupture is a determinant for plasma membrane disruption in tumor necrosis factor alpha-induced cell death. Mol Cell Biol 2003;23: 665-76.
13. Kagedal K, Zhao M, Svensson I, Brunk UT. Sphingosine-induced apoptosis is dependent on lysosomal proteases. Biochem J 2001; 359: 335-43.
14. Ostenfeld MS, Fehrenbacher N, Høyer-Hansen M, Thomsen C, Farkas T, Jäättelä M. Effective tumor cell death by sigma-2 receptor ligand siramesine involves lysosomal leakage and oxidative stress. Cancer Res 2005;65: 8975-83.
15. Rammer P, Groth-Pedersen L, Kirkegaard T, Daugaard M, Rytter A, Szyniarowski P, et al. BAMLET activates a lysosomal cell death program in cancer cells. Mol Cancer Ther 2010;9: 24-32.
16. Ivanov A, Beers SA, Walshe CA, Honeychurch J, Alduaij W, Cox KL, et al. Monoclonal antibodies directed to CD20 and HLA-DR can elicit homotypic adhesion followed by lysosome-mediated cell death in human lymphoma and leukemia cells. J Clin Invest 2009; 119: 2143-59.
17. Gonzalez P, Mader I, Tchoghandjian A, Enzenmuller S, Cristofanon S, Basit F, et al. Impairment of lysosomal integrity by B10, a glycosylated derivative of betulinic acid, leads to lysosomal cell death and converts autophagy into a detrimental process. Cell Death Differ 2012;19: 1337-46.
18. Gottesman MM, Fojo T, Bates SE. Multidrug resistance in cancer: role of ATP-dependent transporters. Nat Rev Cancer 2002;2: 48-58.
19. Groth-Pedersen L, Jäättelä M. Combating apoptosis and multidrug resistant cancers by targeting lysosomes. Cancer Lett 2013;332: 265-74.
20. Larsen AK, Escargueil AE, Skladanowski A. Resistance mechanisms associated with altered intracellular distribution of anticancer agents. Pharmacol Ther 2000;85: 217-29.
21. Sehested M, Skovsgaard T, van Deurs B, Winther-Nielsen H. Increased plasmamembrane traffic in daunorubicin resistantP388 leukaemic cells. Effect of daunorubicin and verapamil. Br J Cancer 1987;56: 747-51.
22. Raghunand N, Martinez-Zaguilan R, Wright SH, Gillies RJ. pH and drug resistance. II. Turnover of acidic vesicles and resistance to weakly basic chemotherapeutic drugs. Biochem Pharmacol 1999;57: 1047-58.
23. Jäättelä M, Benedict M, Tewari M, Shayman JA, Dixit VM. Bcl-x and Bcl-2 inhibit TNF and Fas-induced apoptosis and activation of phospholipase A2 in breast carcinoma cells. Oncogene 1995;10: 2297-305.
24. Høyer-Hansen M, Bastholm L, Szyniarowski P, Campanella M, Szabadkai G, Farkas T, et al. Control of macroautophagy by calcium, calmodulin-dependent kinase kinase-ß and Bcl-2. Mol Cell 2007;25: 193-205.
25. Bampton ET, Goemans CG, Niranjan D, Mizushima N, Tolkovsky AM. The dynamics of autophagy visualized in live cells: from autophagosome formation to fusion with endo/lysosomes. Autophagy 2005; 1: 23-36.
26. Jäättelä M, Wissing D, Bauer PA, Li GC. Major heat shock protein hsp70 protects tumor cells from tumor necrosis factor cytotoxicity. EMBO J 1992;11: 3507-12.
27. Foghsgaard L, Wissing D, Mauch D, Lademann U, Bastholm L, Boes M, et al. Cathepsin B acts as a dominant execution protease in tumor cell apoptosis induced by tumor necrosis factor. J Cell Biol 2001;153: 999-1010.
28. Slot JW, Geuze HJ. Cryosectioning and immunolabeling. Nat Protoc 2007;2: 2480-91.
29. Liou W, Geuze HJ, Slot JW. Improving structural integrity of cryosections for immunogold labeling. Histochem Cell Biol 1996;106: 41-58.
30. van Diggelen OP, Voznyi YV, Keulemans JL, Schoonderwoerd K, Ledvinova J, Mengel E, et al. A new fluorimetric enzyme assay for the diagnosis of Niemann-Pick A/B, with specificity of natural sphingomyelinase substrate. J Inherit Metab Dis 2005;28: 733-41.
31. Farkas T, Høyer-Hansen M, Jäättelä M. Identification of novel autophagy regulators by a luciferase-based assay for the kinetics of autophagic flux. Autophagy 2009;5: 1018-25.
32. Sun L, Liang C, Shirazian S, Zhou Y, Miller T, Cui J, et al. Discovery of 5- [5-fluoro-2-oxo-1,2- dihydroindol-(3Z)-ylidenemethyl]-2,4- dimethyl- 1H-pyrrole-3-carboxylic acid (2-diethylaminoethyl)amide, a novel tyrosine kinase inhibitor targeting vascular endothelial and plateletderived growth factor receptor tyrosine kinase. J Med Chem 2003; 46: 1116-9.
33. Zhao Y, Xue T, Yang X, Zhu H, Ding X, Lou L, et al. Autophagy plays an important role in sunitinib-mediated cell death in H9c2 cardiac muscle cells. Toxicol Appl Pharmacol 2010;248: 20-7.
34. Gotink KJ, Broxterman HJ, Labots M, de Haas RR, Dekker H, Honeywell RJ, et al. Lysosomal sequestration of sunitinib: a novel mechanism of drug resistance. Clin Cancer Res 2011;17: 7337-46.
35. Nadanaciva S, Lu S, Gebhard DF, Jessen BA, Pennie WD, Will Y. Ahigh content screening assay for identifying lysosomotropic compounds. Toxicol In Vitro 2011;25: 715-23.
36. Kirkegaard T, Roth AG, Petersen NH, Mahalka AK, Olsen OD, Moilanen I, et al. Hsp70 stabilizes lysosomes and reverts Niemann-Pick disease-associated lysosomal pathology. Nature 2010; 463: 549-53.
37. Kornhuber J, Tripal P, Reichel M, Muhle C, Rhein C, Muehlbacher M, et al. Functional Inhibitors of Acid Sphingomyelinase (FIASMAs): a novel pharmacologic group of drugs with broad clinical applications. Cell Physiol Biochem 2010;26: 9-20.
38. Nylandsted J, Gyrd-Hansen M, Danielewicz A, Fehrenbacher N, Lademann U, Høyer-Hansen M, et al. Heat shock protein 70 promotes cell survival by inhibiting lysosomal membrane permeabilization. J Exp Med 2004;200: 425-35.
39. Jaffrezou JP, Chen G, Duran GE, Muller C, Bordier C, Laurent G, et al. Inhibition of lysosomal acid sphingomyelinase by agents which reverse multidrug resistance. Biochim Biophys Acta 1995;1266: 1-8.
40. De Milito A, Fais S. Proton pump inhibitors may reduce tumour resistance. Expert Opin Pharmacother 2005;6: 1049-54.
41. Shiraishi N, Akiyama S, Kobayashi M, Kuwano M. Lysosomotropic agents reverse multiple drug resistance in human cancer cells. Cancer Lett 1986;30: 251-9.
42. Xin H, Zhang C, Herrmann A, Du Y, Figlin R, Yu H. Sunitinib inhibition of Stat3 induces renal cell carcinoma tumor cell apoptosis and reduces immunosuppressive cells. Cancer Res 2009;69: 2506-13.
43. Ding W, Cai T, Zhu H, Wu R, Tu C, Yang L, et al. Synergistic antitumor effect of TRAIL in combination with sunitinib in vitro and in vivo. Cancer Lett 2010;293: 158-66.
44. 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.
45. Repnik U, Turk B. Lysosomal-mitochondrial cross-talk during cell death. Mitochondrion 2010;10: 662-9.
46. Alakoskela JM, Vitovic P, Kinnunen PK. Screening for the drug-phospholipid interaction: correlation to phospholipidosis. ChemMedChem 2009;4: 1224-51.
47. Kolter T, Sandhoff K. Lysosomal degradation of membrane lipids. FEBS Lett 2010;584: 1700-12.
48. Mendez-Vidal MJ, Martinez Ortega E, Montesa Pino A, Perez Valderrama B, Viciana R. Management of adverse events of targeted therapies in normal and special patients with metastatic renal cell carcinoma. Cancer Metastasis Rev 2012;31 Suppl 1:S19-27.
49. Aparicio-Gallego G, Blanco M, Figueroa A, Garcia-Campelo R, Valladares-Ayerbes M, Grande-Pulido E, et al. New insights into molecular mechanisms of sunitinib-associated side effects. Mol Cancer Ther 2011;10: 2215-23.
50. Ikeda T, Ishii KA, Saito Y, Miura M, Otagiri A, Kawakami Y, et al. Inhibition of autophagy enhances sunitinib-induced cytotoxicity in rat pheochromocytoma PC12 cells. J Pharmacol Sci 2013;121: 67-73.