Chloroquine synergizes sunitinib cytotoxicity via modulating autophagic, apoptotic and angiogenic machineries

Chemico-Biological Interactions

Volumn 217, Issue , 2014, Pages 28-40

  Abdel Aziz, Amal Kamal ^a,b   Shouman, Samia ^c   El Demerdash, Ebtehal ^a   Elgendy, Mohamed ^b   Abdel Naim, Ashraf B ^a  

^a Ain Shams University   (Egypt)

^b EUROPEAN INSTITUTE OF ONCOLOGY   (Italy)

^c CAIRO UNIVERSITY   (Egypt)

Author keywords

Angiogenesis; Apoptosis; Autophagy; Chloroquine; Oxidative stress; Sunitinib

Indexed keywords

BECLIN 1; CASPASE 3; CATALASE; CD34 ANTIGEN; CHLOROQUINE; GLUTATHIONE; GLUTATHIONE PEROXIDASE; INDUCIBLE NITRIC OXIDE SYNTHASE; LIPID PEROXIDE; NITRIC OXIDE; PCNA PROTEIN; PROTEIN P62; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE; SQTSM1 PROTEIN; SUNITINIB; UNCLASSIFIED DRUG;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIANGIOGENIC ACTIVITY; APOPTOSIS; ARTICLE; AUTOPHAGY; BREAST CANCER; CANCER CELL; CANCER SIZE; COLORECTAL CANCER; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG CYTOTOXICITY; DRUG POTENTIATION; EHRLICH ASCITES TUMOR; ENZYME ACTIVITY; FEMALE; HELA CELL LINE; HISTOPATHOLOGY; HUMAN; HUMAN CELL; LARYNX CANCER; LIVER CELL CARCINOMA; MALE; MOUSE; NONHUMAN; PERITONEUM; PROSTATE CANCER; PROTEIN EXPRESSION; SKIN; UPREGULATION;

ANGIOGENESIS; APOPTOSIS; AUTOPHAGY; CHLOROQUINE; OXIDATIVE STRESS; SUNITINIB;

ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; BLOTTING, WESTERN; CACO-2 CELLS; CARCINOMA, EHRLICH TUMOR; CELL LINE, TUMOR; CELL SURVIVAL; CHLOROQUINE; DRUG SYNERGISM; FEMALE; HCT116 CELLS; HELA CELLS; HEP G2 CELLS; HUMANS; IMMUNOHISTOCHEMISTRY; INDOLES; MCF-7 CELLS; MICE; NEOVASCULARIZATION, PATHOLOGIC; PYRROLES;

EID: 84899793680     PISSN: 00092797     EISSN: 18727786     Source Type: Journal    
DOI: 10.1016/j.cbi.2014.04.007     Document Type: Article

References (57)

1. R.J. Motzer, S. Hoosen, C.L. Bello, and J.G. Christensen Sunitinib malate for the treatment of solid tumours: a review of current clinical data Expert Opin Investig Drugs. 15 2006 553 561
2. H.J. Broxterman, K.J. Gotink, and H.M.W. Verheul Understanding the causes of multidrug resistance in cancer: a comparison of doxorubicin and sunitinib Drug Resist. Updat. 12 2009 114 126
3. T. Fuereder, A. Jaeger-Lansky, D. Hoeflmayer, M. Preusser, S. Strommer, and D. Cejka et al. MTOR inhibition by everolimus counteracts VEGF induction by sunitinib and improves anti-tumor activity against gastric cancer in vivo Cancer Lett. 296 2010 249 256
4. K.J. Gotink, H.J. Broxterman, M. Labots, R.R. de Haas, H. Dekker, and R.J. Honeywell et al. Lysosomal sequestration of sunitinib: a novel mechanism of drug resistance Clin. Cancer Res. 17 2011 7337 7346
5. R. Rahim, and J.S. Strobl Hydroxychloroquine, chloroquine, and all-trans retinoic acid regulate growth, survival, and histone acetylation in breast cancer cells Anticancer Drugs 20 2009 736 745
6. Z.-B. Ding, B. Hui, Y.-H. Shi, J. Zhou, Y.-F. Peng, and C.-Y. Gu et al. Autophagy activation in hepatocellular carcinoma contributes to the tolerance of oxaliplatin via reactive oxygen species modulation Clin. Cancer Res. 17 2011 6229 6238
7. K. Sasaki, N.H. Tsuno, E. Sunami, G. Tsurita, K. Kawai, and Y. Okaji et al. Chloroquine potentiates the anti-cancer effect of 5-fluorouracil on colon cancer cells BMC Cancer 10 2010 370
8. V.R. Solomon, and H. Lee Chloroquine and its analogs: a new promise of an old drug for effective and safe cancer therapies Eur. J. Pharmacol. 625 2009 220 233
9. Y. Xu, H. Yu, H. Qin, J. Kang, C. Yu, and J. Zhong et al. Inhibition of autophagy enhances cisplatin cytotoxicity through endoplasmic reticulum stress in human cervical cancer cells Cancer Lett. 314 2012 232 243
10. V. Deretic, Autophagosome and phagosome, in: Methods in Molecular Biology, vol. 445, Humana Press, Totowa, NJ, 2008.
11. C.Y. Yoon, J.S. Lee, B.S. Kim, S.J. Jeong, S.K. Hong, and S.S. Byun et al. Sunitinib malate synergistically potentiates antitumor effect of gemcitabine in human bladder cancer cells Korean J. Urol. 52 2011 55 63
12. T. Chou Theoretical basis, experimental design, and computerized simulation of synergism and antagonism in drug combination studies Pharmacol. Rev. 58 2006 621 681
13. C.-X. Xu, L. Zhao, P. Yue, G. Fang, H. Tao, and T.K. Owonikoko et al. Augmentation of NVP-BEZ235's anticancer activity against human lung cancer cells by blockage of autophagy Cancer Biol. Ther. 12 2011 549 555
14. R.P. Dings, Y. Yokoyama, S. Ramakrishnan, A.W. Griffioen, and K.H. Mayo The designed angiostatic peptide anginex synergistically improves chemotherapy and antiangiogenesis therapy with angiostatin Cancer Res. 63 2003 382 385
15. T. Mezei, M. Szakács, L. Dénes, J. Jung, and I. Egyed-Zsigmond Semiautomated image analysis of high contrast tissue areas using hue/saturation/ brightness based color filtering Acta Medica 57 2011 679 684
16. F. Rotondo, A. Rotondo, M. Jentoft, B.W. Scheithauer, L.V. Syro, J.H. Donado, J.E. Tarara, and K. Kovacs Microvessel density and VEGF expression in pituitaries of pregnant women Hormones 12 2013 292 297
17. H. Chandru, A.C. Sharada, B.K. Bettadaiah, C.S. Ananda Kumar, K.S. Rangappa, Sunilac, and K. Jayashreec In vivo growth inhibitory and anti-angiogenic effects of synthetic novel dienone cyclopropoxy curcumin analogs on mouse Ehrlich ascites tumor Bioorg. Med. Chem. 15 2007 7696 7703
18. K. Anand, A. Sarkar, A. Kumar, and R.K. Ambasta Combinatorial antitumor effect of naringenin and curcumin elicit angioinhibitory activities in vivo Nutr. Cancer 64 2012 1 11
19. B. Salimath, A. Tabassum, E.G. Anupama, Bindumalini, and G.B. Preeti Molecular mechanism of action of butyric acid in Ehrlich ascites tumor cells Nutr. Res. 19 1999 589 600
20. K.M. Miranda, M.G. Espey, and D.a. Wink A rapid, simple spectrophotometric method for simultaneous detection of nitrate and nitrite Nitric Oxide 5 2001 62 71
21. G.L. Ellman Tissue sulfhydryl groups Arch. Biochem. Biophys. 82 1959 70 77
22. M. Mihara, and M. Uchiyama Determination of malonaldehyde precursor in tissues by thiobarbituric acid test Anal. Biochem. 86 1978 271 278
23. D. Paglia, and W. Valentine Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase J. Lab. Clin. Med. 70 1967 158 169
24. H. Aebi Catalase in vitro Methods Enzymol. 105 1984 121 126
25. M.C. Maiuri, E. Zalckvar, A. Kimchi, and G. Kroemer Self-eating and self-killing: crosstalk between autophagy and apoptosis Nat. Rev. Mol. Cell Biol. 8 2007 741 752
26. T. Ikeda, K. Ishii, Y. Saito, M. Miura, A. Otagiri, and Y. Kawakami et al. Inhibition of autophagy enhances sunitinib-induced cytotoxicity in rat pheochromocytoma PC12 cells J. Pharmacol. Sci. 121 2013 67 73
27. C.I. Lin, E.E. Whang, J.H. Lorch, and D.T. Ruan Autophagic activation potentiates the antiproliferative effects of tyrosine kinase inhibitors in medullary thyroid cancer Surgery 152 2012 1142 1149
28. Y. Zhao, T. Xue, X. Yang, H. Zhu, X. Ding, and L. Lou et al. Autophagy plays an important role in sunitinib-mediated cell death in H9c2 cardiac muscle cells Toxicol. Appl. Pharmacol. 248 2010 20 27
29. A. Lopergolo, V. Nicolini, E. Favini, L.D. Bo, M. Tortoreto, and D. Cominetti et al. Synergistic cooperation between sunitinib and cisplatin promotes apoptotic cell death in human medullary thyroid cancer J. Clin. Endocrinol. Metab. 99 2014 498 509
30. M. Santoni, C. Amantini, M.B. Morelli, S. Liberati, V. Farfariello, and M. Nabissi et al. Pazopanib and sunitinib trigger autophagic and non-autophagic death of bladder tumour cells Br. J. Cancer 109 2013 1040 1050
31. P. Maycotte, S. Aryal, C.T. Cummings, J. Thorburn, M.J. Morgan, and A. Thorburn Chloroquine sensitizes breast cancer cells to chemotherapy independent of autophagy Autophagy 8 2012 200 212
32. Y.-L. Hu, M. DeLay, A. Jahangiri, A.M. Molinaro, S.D. Rose, and W.S. Carbonell et al. Hypoxia-induced autophagy promotes tumor cell survival and adaptation to antiangiogenic treatment in glioblastoma Cancer Res. 72 2012 1773 1783
33. S.P. Tu, X.H. Jiang, M.C.M. Lin, J.T. Cui, Y. Yang, and C.T. Lum et al. Suppression of survivin expression inhibits in vivo tumorigenicity and angiogenesis in gastric cancer suppression of survivin expression inhibits in vivo tumorigenicity and angiogenesis Gastric Cancer 63 2003 7724 7732
34. H.-W. Chiu, Y.-S. Ho, and Y.-J. Wang Arsenic trioxide induces autophagy and apoptosis in human glioma cells in vitro and in vivo through downregulation of survivin J. Mol. Med. (Berl) 89 2011 927 941
35. T.-K. Niu, Y. Cheng, X. Ren, and J.-M. Yang Interaction of Beclin 1 with survivin regulates sensitivity of human glioma cells to TRAIL-induced apoptosis FEBS Lett. 584 2010 3519 3524
36. R.L. Thomas, D.J. Roberts, D.A. Kubli, Y. Lee, M.N. Quinsay, and J.B. Owens et al. Loss of MCL-1 leads to impaired autophagy and rapid development of heart failure Genes Dev. 15 2013 1365 1377
37. Y. Zhu, L. Zhao, L. Liu, P. Gao, W. Tian, and X. Wang et al. Beclin 1 cleavage by caspase-3 inactivates autophagy and promotes apoptosis Protein Cell 1 2010 468 477
38. S. Shin, B.J. Sung, Y.S. Cho, H.J. Kim, N.C. Ha, and J.I. Hwang et al. An anti-apoptotic protein human survivin is a direct inhibitor of caspase-3 and -7 Biochemistry 40 2001 1117 1123
39. Y. Tong, Y. Liu, L. You, and W. Qian Perifosine induces protective autophagy and upregulation of ATG5 in human chronic myelogenous leukemia cells in vitro Acta Pharmacol. Sin. 33 2012 542 550
40. E.L. Kim, R. Wüstenberg, A. Rübsam, C. Schmitz-Salue, G. Warnecke, and E. Bücker et al. Chloroquine activates the p53 pathway and induces apoptosis in human glioma cells Neuro. Oncol. 12 2010 389 400
41. L. Hlatky, P. Hahnfeldt, and J. Folkman Clinical application of antiangiogenic therapy: microvessel density, what it does and doesn't tell us J. Natl Cancer Inst. 94 2002 883 893
42. S.P. Tu, X.H. Jiang, M.C.M. Lin, J.T. Cui, Y. Yang, and C.T. Lum et al. Suppression of survivin expression inhibits in vivo tumorigenicity and angiogenesis in gastric cancer suppression of survivin expression inhibits in vivo tumorigenicity and angiogenesis in gastric cancer Cancer Res. 2003 7724 7732
43. A. Grimaldi, M.L. Balestrieri, N. D'Onofrio, G. Di Domenico, C. Nocera, and M. Lamberti et al. The synergistic effect of everolimus and chloroquine on endothelial cell number reduction is paralleled by increased apoptosis and reduced autophagy occurrence PLoS ONE 11 2013
44. B. Brüne Nitric oxide: NO apoptosis or turning it ON? Cell Death Differ. 10 2003 864 869
45. B. Bonavida, S. Khineche, S. Huerta-Yepez, and H. Garbán Therapeutic potential of nitric oxide in cancer Drug Resist. Updat. 9 2006 157 173
46. N. Matthews, M. Adams, L. Maxwell, T. Gofton, and C. Graham Nitric oxide-mediated regulation of chemosensitivity in cancer cells J. Natl Cancer Inst. 93 2001 1879 1885
47. A. Sanchez, D. Tripathy, X. Yin, J. Luo, J.M. Martinez, and P. Grammas Sunitinib enhances neuronal survival in vitro via NF-κB-mediated signaling and expression of cyclooxygenase-2 and inducible nitric oxide synthase J. Neuroinflammation 10 2013
48. C.B. Evig, E.E. Kelley, C.J. Weydert, Y. Chu, G.R. Buettner, and C.P. Burns Endogenous production and exogenous exposure to nitric oxide augment doxorubicin cytotoxicity for breast cancer cells but not cardiac myoblasts Nitric Oxide 10 2004 119 129
49. T.H. Chen, P.C. Chang, M.C. Chang, Y.F. Lin, and H.M. Lee Chloroquine induces the expression of inducible nitric oxide synthase in C6 glioma cells Pharmacol. Res. 51 2005 329 336
50. D. Ghigo, E. Aldieri, R. Todde, C. Costamagna, G. Garbarino, G. Pescarmona, and A. Bosia Chloroquine stimulates nitric oxide synthesis in murine, porcine, and human endothelial cells J. Clin. Invest. 102 1998 595 605
51. W.R. Bruce, A. Giacca, and A. Medline Possible mechanisms relating diet and risk of colon cancer possible mechanisms relating diet and risk of colon cancer 1 Cancer Epidemiol. Biomarkers Prev. 9 2000 1271 1279
52. M.H. Kappers, V.J. de Beer, Z. Zhou, A.H. Danser, S. Sleijfer, and D.J. Duncker et al. Sunitinib-induced systemic vasoconstriction in swine is endothelin mediated and does not involve nitric oxide or oxidative stress Hypertension 59 2012 151 157
53. G.M. Suddek Sunitinib improves chemotherapeutic efficacy and ameliorates cisplatin-induced nephrotoxicity in experimental animals Cancer Chemother. Pharmacol. 67 2011 1035 1044
54. W.L. Wang, M.E. Healy, M. Sattler, S. Verma, J. Lin, and G. Maulik et al. Growth inhibition and modulation of kinase pathways of small cell lung cancer cell lines by the novel tyrosine kinase inhibitor STI 571 Oncogene 19 2000 3521 3528
55. A.C. Achudume The influence of chloroquine administration on antioxidant levels, oxidant marker and total cholesterol in Wistar rats Biol. Med. 1 2009 39 43
56. Y. Hirata, H. Yamamoto, M.S. Atta, S. Mahmoud, K. Oh-hashi, and K. Kiuchi Chloroquine inhibits glutamate-induced death of a neuronal cell line by reducing reactive oxygen species through sigma-1 receptor J. Neurochem. 119 2011 839 847
57. J.K. Kwee, D.G. Luque, A.C.D.S. Ferreira, F.D.C. Vasconcelos, K.L. Silva, and C.E. Klumb et al. Modulation of reactive oxygen species by antioxidants in chronic myeloid leukemia cells enhances imatinib sensitivity through survivin downregulation Anticancer Drugs 19 2008 975 981