Vacuolar-ATPase-mediated intracellular sequestration of ellipticine contributes to drug resistance in neuroblastoma cells

International Journal of Oncology

Volumn 47, Issue 3, 2015, Pages 971-980

  Hrabeta, Jan ^a   Groh, Tomas ^a,b   Khalil, Mohamed Ashraf ^a   Poljakova, Jitka ^b   Adam, Vojtech ^c,d   Kizek, Rene ^c,d   Uhlik, Jiri ^b   Doktorova, Helena ^a   Cerna, Tereza ^b   Frei, Eva ^e   Stiborova, Marie ^b   Eckschlager, Tomas ^a  

^a UNIVERSITY HOSPITAL MOTOL   (Czech Republic)

^b CHARLES UNIVERSITY   (Czech Republic)

^c MENDEL UNIVERSITY IN BRNO   (Czech Republic)

^d BRNO UNIVERSITY OF TECHNOLOGY   (Czech Republic)

^e GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

Drug sequestration; Neuroblastoma; Resistance to ellipticine; Vacuolar ATPase; Vacuolation

Indexed keywords

ADENOSINE TRIPHOSPHATASE; BAFILOMYCIN; BAFILOMYCIN A; CHLOROQUINE; ELLIPTICINE; UNCLASSIFIED DRUG; WORTMANNIN; ANTINEOPLASTIC AGENT; DNA ADDUCT; ELLIPTICINE DERIVATIVE; MACROLIDE; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; AUTOPHAGY; CELL VACUOLE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DNA ADDUCT; DRUG RESISTANCE; HUMAN; HUMAN CELL; LYSOSOME; NEUROBLASTOMA; NEUROBLASTOMA CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; TRANSMISSION ELECTRON MICROSCOPY; UPREGULATION; DRUG EFFECTS; GENETICS; METABOLISM; TUMOR CELL LINE;

ANTINEOPLASTIC AGENTS; APOPTOSIS; CELL LINE, TUMOR; CHLOROQUINE; DNA ADDUCTS; DRUG RESISTANCE, NEOPLASM; ELLIPTICINES; HUMANS; MACROLIDES; NEUROBLASTOMA; VACUOLAR PROTON-TRANSLOCATING ATPASES; VACUOLES;

EID: 84938080027     PISSN: 10196439     EISSN: 17912423     Source Type: Journal    
DOI: 10.3892/ijo.2015.3066     Document Type: Article

References (48)

1. Brodeur GM: Neuroblastoma: Biological insights into a clinical enigma. Nat Rev Cancer 3: 203-216, 2003.
2. Schwab M, Westermann F, Hero B and Berthold F: Neuroblastoma: Biology and molecular and chromosomal pathology. Lancet Oncol 4: 472-480, 2003.
3. Morgenstern BZ, Krivoshik AP, Rodriguez V and Anderson PM: Wilms' tumor and neuroblastoma. Acta Paediatr (Suppl) 93: 78-85, 2004.
4. Kotchetkov R, Driever PH, Cinatl J, Michaelis M, Karaskova J, Blaheta R, Squire JA, Von Deimling A, Moog J and Cinatl J Jr: Increased malignant behavior in neuroblastoma cells with acquired multi-drug resistance does not depend on P-gp expression. Int J Oncol 27: 1029-1037, 2005.
5. Michaelis M, Klassert D, Barth S, Suhan T, Breitling R, Mayer B, Hinsch N, Doerr HW, Cinatl J and Cinatl J Jr: Chemoresistance acquisition induces a global shift of expression of aniogenesisassociated genes and increased pro-angogenic activity in neuroblastoma cells. Mol Cancer 8: 80, 2009.
6. Stiborová M, Rupertová M and Frei E: Cytochrome P450- and peroxidase-mediated oxidation of anticancer alkaloid ellipticine dictates its anti-tumor efficiency. Biochim Biophys Acta 1814: 175-185, 2011.
7. Stiborová M and Frei E: Ellipticines as DNA-targeted chemotherapeutics. Curr Med Chem 21: 575-591, 2014.
8. Poljaková J, Eckschlager T, Hrabeta J, Hrebacková J, Smutn? S, Frei E, Martínek V, Kizek R and Stiborová M: The mechanism of cytotoxicity and DNA adduct formation by the anticancer drug ellipticine in human neuroblastoma cells. Biochem Pharmacol 77: 1466-1479, 2009.
9. Poljakova J, Hrebackova J, Dvorakova M, Moserova M, Eckschlager T, Hrabeta J, Göttlicherova M, Kopejtkova B, Frei E, Kizek R, et al: Anticancer agent ellipticine combined with histone deacetylase inhibitors, valproic acid and trichostatin A, is an effective DNA damage strategy in human neuroblastoma. Neuro Endocrinol Lett 32 (Suppl 1): 101-116, 2011.
10. Stiborová M, Eckschlager T, Poljaková J, Hraběta J, Adam V, Kizek R and Frei E: The synergistic effects of DNA-targeted chemotherapeutics and histone deacetylase inhibitors as therapeutic strategies for cancer treatment. Curr Med Chem 19: 4218-4238, 2012.
11. Stiborova M, Poljakova J, Mrizova I, et al: Expression levels of enzymes metabolizing an anticancer drug ellipticine determined by electromigration assays influence its cytotoxicity to cancer cells - a comparative study. Int J Electrochem Sci 9: 5675-5689, 2014.
12. Stiborová M, Bieler CA, Wiessler M and Frei E: The anticancer agent ellipticine on activation by cytochrome P450 forms covalent DNA adducts. Biochem Pharmacol 62: 1675-1684, 2001.
13. Stiborová M, Sejbal J, Borek-Dohalská L, Aimová D, Poljaková J, Forsterová K, Rupertová M, Wiesner J, Hudecek J, Wiessler M, et al: The anticancer drug ellipticine forms covalent DNA adducts, mediated by human cytochromes P450, through metabolism to 13-hydroxyellipticine and ellipticine N2-oxide. Cancer Res 64: 8374-8380, 2004.
14. Stiborova M, Rupertova M, Schmeiser HH and Frei E: Molecular mechanisms of antineoplastic action of an anticancer drug ellipticine. Biomed Pap Med Fac Univ Palacky Olomouc Czech Repub 150: 13-23, 2006.
15. Stiborová M, Poljaková J, Ryslavá H, Dracínsk? M, Eckschlager T and Frei E: Mammalian peroxidases activate anticancer drug ellipticine to intermediates forming deoxyguanosine adducts in DNA identical to those found in vivo and generated from 12-hydroxyellipticine and 13-hydroxyellipticine. Int J Cancer 120: 243-251, 2007.
16. Kizek R, Adam V, Hrabeta J, Eckschlager T, Smutny S, Burda JV, Frei E and Stiborova M: Anthracyclines and ellipticines as DNA-damaging anticancer drugs: Recent advances. Pharmacol Ther 133: 26-39, 2012.
17. Procházka P, Libra A, Zemanová Z, Hřebačková J, Poljaková J, Hraběta J, Bunček M, Stiborová M and Eckschlager T: Mechanisms of ellipticine-mediated resistance in UKF-NB-4 neuroblastoma cells. Cancer Sci 103: 334-341, 2012.
18. Marshansky V, Rubinstein JL and Grüber G: Eukaryotic V-ATPase: Novel structural findings and functional insights. Biochim Biophys Acta 1837: 857-879, 2014.
19. Maxfield FR and McGraw TE: Endocytic recycling. Nat Rev Mol Cell Biol 5: 121-132, 2004.
20. Goldman SDB, Funk RS, Rajewski RA and Krise JP: Mechanisms of amine accumulation in, and egress from, lysosomes. Bioanalysis 1: 1445-1459, 2009.
21. Coutinho MF, Prata MJ and Alves S: Mannose-6-phosphate pathway: A review on its role in lysosomal function and dysfunction. Mol Genet Metab 105: 542-550, 2012.
22. Simon S, Roy D and Schindler M: Intracellular pH and the control of multidrug resistance. Proc Natl Acad Sci USA 91: 1128-1132, 1994.
23. Mahoney BP, Raghunand N, Baggett B and Gillies RJ: Tumor acidity, ion trapping and chemotherapeutics. I. Acid pH affects the distribution of chemotherapeutic agents in vitro. Biochem Pharmacol 66: 1207-1218, 2003.
24. Chapuy B, Koch R, Radunski U, Corsham S, Cheong N, Inagaki N, Ban N, Wenzel D, Reinhardt D, Zapf A, et al: Intracellular ABC transporter A3 confers multidrug resistance in leukemia cells by lysosomal drug sequestration. Leukemia 22: 1576-1586, 2008.
25. Spugnini EP, Citro G and Fais S: Proton pump inhibitors as anti vacuolar-ATPases drugs: A novel anticancer strategy. J Exp Clin Cancer Res 29: 44, 2010.
26. Yamagishi T, Sahni S, Sharp DM, Arvind A, Jansson PJ and Richardson DR: P-glycoprotein mediates drug resistance via a novel mechanism involving lysosomal sequestration. J Biol Chem 288: 31761-31771, 2013.
27. Frei E, Bieler CA, Arlt VM, Wiessler M and Stiborová M: Covalent binding of the anticancer drug ellipticine to DNA in V79 cells transfected with human cytochrome P450 enzymes. Biochem Pharmacol 64: 289-295, 2002.
28. Poljaková J, Frei E, Gomez JE, Aimová D, Eckschlager T, Hrabeta J and Stiborová M: DNA adduct formation by the anticancer drug ellipticine in human leukemia HL-60 and CCRF-CEM cells. Cancer Lett 252: 270-279, 2007.
29. Martinkova E, Dontenwill M, Frei E and Stiborova M: Cytotoxicity of and DNA adduct formation by ellipticine in human U87MG glioblastoma cancer cells. Neuro Endocrinol Lett 30 (Suppl 1): 60-66, 2009.
30. Martinkova E, Maglott A, Leger DY, Bonnet D, Stiborova M, Takeda K, Martin S and Dontenwill M: alpha5beta1 integrin antagonists reduce chemotherapy-induced premature senescence and facilitate apoptosis in human glioblastoma cells. Int J Cancer 127: 1240-1248, 2010.
31. Stiborová M, Breuer A, Aimová D, Stiborová-Rupertová M, Wiessler M and Frei E: DNA adduct formation by the anticancer drug ellipticine in rats determined by 32P postlabeling. Int J Cancer 107: 885-890, 2003.
32. Stiborová M, Rupertová M, Aimová D, Ryslavá H and Frei E: Formation and persistence of DNA adducts of anticancer drug ellipticine in rats. Toxicology 236: 50-60, 2007.
33. Stiborová M, Arlt VM, Henderson CJ, Wolf CR, Kotrbová V, Moserová M, Hudecek J, Phillips DH and Frei E: Role of hepatic cytochromes P450 in bioactivation of the anticancer drug ellipticine: studies with the hepatic NADPH:cytochrome P450 reductase null mouse. Toxicol Appl Pharmacol 226: 318-327, 2008.
34. Hunziker W and Geuze HJ: Intracellular trafficking of lysosomal membrane proteins. Bioessays 18: 379-389, 1996.
35. Oeste CL, Seco E, Patton WF, Boya P and Pérez-Sala D: Interactions between autophagic and endo-lysosomal markers in endothelial cells. Histochem Cell Biol 139: 659-670, 2013.
36. Garbett NC and Graves DE: Extending nature's leads: The anticancer agent ellipticine. Curr Med Chem Anticancer Agents 4: 149-172, 2004.
37. Wu Y, Sadatmousavi P, Wang R, Lu S, Yuan YF and Chen P: Selfassembling peptide-based nanoparticles enhance anticancer effect of ellipticine in vitro and in vivo. Int J Nanomed 7: 3221-3233, 2012.
38. Bowman EJ, Siebers A and Altendorf K: Bafilomycins: A class of inhibitors of membrane ATPases from microorganisms, animal cells, and plant cells. Proc Natl Acad Sci USA 85: 7972-7976, 1988.
39. Huss M and Wieczorek H: Inhibitors of V-ATPases: Old and new players. J Exp Biol 212: 341-346, 2009.
40. Shacka JJ, Klocke BJ, Shibata M, Uchiyama Y, Datta G, Schmidt RE and Roth KA: Bafilomycin A1 inhibits chloroquineinduced death of cerebellar granule neurons. Mol Pharmacol 69: 1125-1136, 2006.
41. Martínez-Zaguilán R, Raghunand N, Lynch RM, Bellamy W, Martinez GM, Rojas B, Smith D, Dalton WS and Gillies RJ: pH and drug resistance. I. Functional expression of plasmalemmal V-type H+-ATPase in drug-resistant human breast carcinoma cell lines. Biochem Pharmacol 57: 1037-1046, 1999.
42. Murakami T, Shibuya I, Ise T, Chen ZS , Akiyama S, Nakagawa M, Izumi H, Nakamura T, Matsuo K, Yamada Y, et al: Elevated expression of vacuolar proton pump genes and cellular PH in cisplatin resistance. Int J Cancer 93: 869-874, 2001.
43. Huang L, Lu Q, Han Y, Li Z, Zhang Z and Li X: ABCG2/ V-ATPase was associated with the drug resistance and tumor metastasis of esophageal squamous cancer cells. Diagn Pathol 7: 180, 2012.
44. Wymann MP, Bulgarelli-Leva G, Zvelebil MJ, Pirola L, Vanhaesebroeck B, Waterfield MD and Panayotou G: Wortmannin inactivates phosphoinositide 3-kinase by covalent modification of Lys-802, a residue involved in the phosphate transfer reaction. Mol Cell Biol 16: 1722-1733, 1996.
45. Arcaro A and Wymann MP: Wortmannin is a potent phosphatidylinositol 3-kinase inhibitor: The role of phosphatidylinositol 3,4,5-trisphosphate in neutrophil responses. Biochem J 296: 297-301, 1993.
46. Blommaart EF, Krause U, Schellens JP, Vreeling-Sindelárová H and Meijer AJ: The phosphatidylinositol 3-kinase inhibitors wortmannin and LY294002 inhibit autophagy in isolated rat hepatocytes. Eur J Biochem 243: 240-246, 1997.
47. Tanida I, Ueno T and Kominami E: LC3 and sutophagy. Methods Mol Biol 445: 77-88, 2008.
48. Solomon VR and Lee H: Chloroquine and its analogs: A new promise of an old drug for effective and safe cancer therapies. Eur J Pharmacol 625: 220-233, 2009.