Synergistic combination therapy with nanoliposomal C6-ceramide and vinblastine is associated with autophagy dysfunction in hepatocarcinoma and colorectal cancer models

Cancer Letters

Volumn 337, Issue 2, 2013, Pages 254-265

  Adiseshaiah, Pavan P ^a   Clogston, Jeffrey D ^a   McLeland, Christopher B ^a   Rodriguez, Jamie ^a   Potter, Timothy M ^a   Neun, Barry W ^a   Skoczen, Sarah L ^a   Shanmugavelandy, Sriram S ^b   Kester, Mark ^b   Stern, Stephan T ^a   McNeil, Scott E ^a  

^a SAIC FREDERICK INC   (United States)

^b PENN STATE COLLEGE OF MEDICINE   (United States)

Author keywords

Autophagy; Ceramide; Combination therapy

Indexed keywords

BECLIN 1; CASPASE 3; CASPASE 7; CERAMIDE; LIPOSOME; NANOCARRIER; VINBLASTINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; CANCER CELL CULTURE; CANCER CELL DESTRUCTION; CANCER COMBINATION CHEMOTHERAPY; CANCER INHIBITION; CELL MATURATION; COLORECTAL CANCER; CONTROLLED STUDY; DRUG CYTOTOXICITY; DRUG EFFICACY; DRUG MECHANISM; DRUG POTENTIATION; ENZYME ACTIVITY; FEMALE; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LIPOSOMAL DELIVERY; LIVER CELL CARCINOMA; MOUSE; NONHUMAN; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; WEIGHT REDUCTION;

AUTOPHAGY; CERAMIDE; COMBINATION THERAPY;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; AUTOPHAGY; CARCINOMA, HEPATOCELLULAR; CASPASE 3; CASPASE 7; CELL SURVIVAL; CERAMIDES; COLORECTAL NEOPLASMS; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG SYNERGISM; HEP G2 CELLS; HUMANS; INJECTIONS, INTRAVENOUS; LIPOSOMES; LIVER NEOPLASMS; MEMBRANE PROTEINS; MICE; MICE, NUDE; NANOPARTICLES; RNA INTERFERENCE; TRANSFECTION; TUMOR BURDEN; VINBLASTINE; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84880509983     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2013.04.034     Document Type: Article

References (50)

1. Amaravadi R.K., Lippincott-Schwartz J., Yin X.M., Weiss W.A., Takebe N., Timmer W., DiPaola R.S., Lotze M.T., White E. Principles and current strategies for targeting autophagy for cancer treatment. Clin. Cancer Res. 2011, 17:654-666.
2. Berkenstam A., Ahlberg J., Glaumann H. Isolation and characterization of autophagic vacuoles from rat kidney cortex. Virchows Arch. B Cell. Pathol. Incl. Mol. Pathol. 1983, 44:275-286.
3. Boland B., Kumar A., Lee S., Platt F.M., Wegiel J., Yu W.H., Nixon R.A. Autophagy induction and autophagosome clearance in neurons: relationship to autophagic pathology in Alzheimer's disease. J. Neurosci. 2008, 28:6926-6937.
4. Bourbon N.A., Yun J., Kester M. Ceramide directly activates protein kinase C zeta to regulate a stress-activated protein kinase signaling complex. J. Biol. Chem. 2000, 275:35617-35623.
5. Chou T.C., Talalay P. Quantitative analysis of dose-effect relationships: the combined effects of multiple drugs or enzyme inhibitors. Adv. Enzyme Regul. 1984, 22:27-55.
6. Coppola D., Khalil F., Eschrich S.A., Boulware D., Yeatman T., Wang H.G. Down-regulation of Bax-interacting factor-1 in colorectal adenocarcinoma. Cancer 2008, 113:2665-2670.
7. Daido S., Kanzawa T., Yamamoto A., Takeuchi H., Kondo Y., Kondo S. Pivotal role of the cell death factor BNIP3 in ceramide-induced autophagic cell death in malignant glioma cells. Cancer Res. 2004, 64:4286-4293.
8. Degenhardt K., Mathew R., Beaudoin B., Bray K., Anderson D., Chen G., Mukherjee C., Shi Y., Gelinas C., Fan Y., Nelson D.A., Jin S., White E. Autophagy promotes tumor cell survival and restricts necrosis, inflammation, and tumorigenesis. Cancer Cell 2006, 10:51-64.
9. Degtyarev M., De Maziere A., Orr C., Lin J., Lee B.B., Tien J.Y., Prior W.W., van Dijk S., Wu H., Gray D.C., Davis D.P., Stern H.M., Murray L.J., Hoeflich K.P., Klumperman J., Friedman L.S., Lin K. Akt inhibition promotes autophagy and sensitizes PTEN-null tumors to lysosomotropic agents. J. Cell Biol. 2008, 183:101-116.
10. Fan M., Goodwin M., Vu T., Brantley-Finley C., Gaarde W.A., Chambers T.C. Vinblastine-induced phosphorylation of Bcl-2 and Bcl-XL is mediated by JNK and occurs in parallel with inactivation of the Raf-1/MEK/ERK cascade. J. Biol. Chem. 2000, 275:29980-29985.
11. Garcia-Ma S., Alcaide A., Dominguez C. Pharmacological control of autophagy: therapeutic perspectives in inflammatory bowel disease and colorectal cancer. Curr. Pharm. Des. 2012.
12. Guenther G.G., Peralta E.R., Rosales K.R., Wong S.Y., Siskind L.J., Edinger A.L. Ceramide starves cells to death by downregulating nutrient transporter proteins. Proc Natl Acad Sci USA 2008, 105:17402-17407.
13. Iqbal J., Kucuk C., Deleeuw R.J., Srivastava G., Tam W., Geng H., Klinkebiel D., Christman J.K., Patel K., Cao K., Shen L., Dybkaer K., Tsui I.F., Ali H., Shimizu N., Au W.Y., Lam W.L., Chan W.C. Genomic analyses reveal global functional alterations that promote tumor growth and novel tumor suppressor genes in natural killer-cell malignancies. Leukemia 2009, 23:1139-1151.
14. Ji C., Yang B., Yang Y.L., He S.H., Miao D.S., He L., Bi Z.G. Exogenous cell-permeable C6 ceramide sensitizes multiple cancer cell lines to doxorubicin-induced apoptosis by promoting AMPK activation and mTORC1 inhibition. Oncogene 2010, 29:6557-6568.
15. Johnson-Lyles D.N., Peifley K., Lockett S., Neun B.W., Hansen M., Clogston J., Stern S.T., McNeil S.E. Fullerenol cytotoxicity in kidney cells is associated with cytoskeleton disruption, autophagic vacuole accumulation, and mitochondrial dysfunction. Toxicol. Appl. Pharmacol. 2010, 248:249-258.
16. Kanzawa T., Germano I.M., Komata T., Ito H., Kondo Y., Kondo S. Role of autophagy in temozolomide-induced cytotoxicity for malignant glioma cells. Cell Death Differ. 2004, 11:448-457.
17. Karmakar S., Choudhury S.R., Banik N.L., Ray S.K. Induction of mitochondrial pathways and endoplasmic reticulum stress for increasing apoptosis in ectopic and orthotopic neuroblastoma xenografts. J. Cancer Ther. 2011, 2:77-90.
18. Kim H.P., Wang X., Chen Z.H., Lee S.J., Huang M.H., Wang Y., Ryter S.W., Choi A.M. Autophagic proteins regulate cigarette smoke-induced apoptosis: protective role of heme oxygenase-1. Autophagy 2008, 4:887-895.
19. Klionsky D.J. Autophagy: from phenomenology to molecular understanding in less than a decade. Nat. Rev. Mol. Cell Biol. 2007, 8:931-937.
20. Kochl R., Hu X.W., Chan E.Y., Tooze S.A. Microtubules facilitate autophagosome formation and fusion of autophagosomes with endosomes. Traffic 2006, 7:129-145.
21. Komatsu M., Waguri S., Chiba T., Murata S., Iwata J., Tanida I., Ueno T., Koike M., Uchiyama Y., Kominami E., Tanaka K. Loss of autophagy in the central nervous system causes neurodegeneration in mice. Nature 2006, 441:880-884.
22. Kondo Y., Kanzawa T., Sawaya R., Kondo S. The role of autophagy in cancer development and response to therapy. Nat. Rev. Cancer 2005, 5:726-734.
23. Liang C., Feng P., Ku B., Dotan I., Canaani D., Oh B.H., Jung J.U. Autophagic and tumour suppressor activity of a novel Beclin 1-binding protein UVRAG. Nat. Cell Biol. 2006, 8:688-699.
24. Liang X.H., Jackson S., Seaman M., Brown K., Kempkes B., Hibshoosh H., Levine B. Induction of autophagy and inhibition of tumorigenesis by beclin 1. Nature 1999, 402:672-676.
25. Lieberman A.P., Puertollano R., Raben N., Slaugenhaupt S., Walkley S.U., Ballabio A. Autophagy in lysosomal storage disorders. Autophagy 2012, 8:719-730.
26. Liu X., Ryland L., Yang J., Liao A., Aliaga C., Watts R., Tan S.F., Kaiser J., Shanmugavelandy S.S., Rogers A., Loughran K., Petersen B., Yuen J., Meng F., Baab K.T., Jarbadan N.R., Broeg K., Zhang R., Liao J., Sayers T.J., Kester M., Loughran T.P. Targeting of survivin by nanoliposomal ceramide induces complete remission in a rat model of NK-LGL leukemia. Blood 2010, 116:4192-4201.
27. Marimpietri D., Brignole C., Nico B., Pastorino F., Pezzolo A., Piccardi F., Cilli M., Di Paolo D., Pagnan G., Longo L., Perri P., Ribatti D., Ponzoni M. Combined therapeutic effects of vinblastine and rapamycin on human neuroblastoma growth, apoptosis, and angiogenesis. Clin. Cancer Res. 2007, 13:3977-3988.
28. Marino G., Fernandez A.F., Lopez-Otin C. Autophagy and aging: lessons from progeria models. Adv. Exp. Med. Biol. 2010, 694:61-68.
29. Marino G., Salvador-Montoliu N., Fueyo A., Knecht E., Mizushima N., Lopez-Otin C. Tissue-specific autophagy alterations and increased tumorigenesis in mice deficient in Atg4C/autophagin-3. J. Biol. Chem. 2007, 282:18573-18583.
30. Pattingre S., Bauvy C., Carpentier S., Levade T., Levine B., Codogno P. Role of JNK1-dependent Bcl-2 phosphorylation in ceramide-induced macroautophagy. J. Biol. Chem. 2009, 284:2719-2728.
31. Ponnusamy S., Meyers-Needham M., Senkal C.E., Saddoughi S.A., Sentelle D., Selvam S.P., Salas A., Ogretmen B. Sphingolipids and cancer: ceramide and sphingosine-1-phosphate in the regulation of cell death and drug resistance. Future Oncol. 2010, 6:1603-1624.
32. Potter T.M., Stern S.T. Evaluation of cytotoxicity of nanoparticulate materials in porcine kidney cells and human hepatocarcinoma cells. Methods Mol. Biol. 2011, 697:157-165.
33. Potter T.M., Stern S.T. Monitoring nanoparticle-treated hepatocarcinoma cells for apoptosis. Methods Mol. Biol. 2011, 697:167-172.
34. Qu X., Yu J., Bhagat G., Furuya N., Hibshoosh H., Troxel A., Rosen J., Eskelinen E.L., Mizushima N., Ohsumi Y., Cattoretti G., Levine B. Promotion of tumorigenesis by heterozygous disruption of the beclin 1 autophagy gene. J. Clin. Invest. 2003, 112:1809-1820.
35. Sasaki K., Tsuno N.H., Sunami E., Tsurita G., Kawai K., Okaji Y., Nishikawa T., Shuno Y., Hongo K., Hiyoshi M., Kaneko M., Kitayama J., Takahashi K., Nagawa H. Chloroquine potentiates the anti-cancer effect of 5-fluorouracil on colon cancer cells. BMC Cancer 2010, 10:370.
36. Seglen P.O., Brinchmann M.F. Purification of autophagosomes from rat hepatocytes. Autophagy 2010, 6:542-547.
37. Shi Y.H., Ding Z.B., Zhou J., Hui B., Shi G.M., Ke A.W., Wang X.Y., Dai Z., Peng Y.F., Gu C.Y., Qiu S.J., Fan J. Targeting autophagy enhances sorafenib lethality for hepatocellular carcinoma via ER stress-related apoptosis. Autophagy 2011, 7:1159-1172.
38. Solomon V.R., Lee H. Chloroquine and its analogs: a new promise of an old drug for effective and safe cancer therapies. Eur. J. Pharmacol. 2009, 625:220-233.
39. Stern S.T., Zolnik B.S., McLeland C.B., Clogston J., Zheng J., McNeil S.E. Induction of autophagy in porcine kidney cells by quantum dots: a common cellular response to nanomaterials?. Toxicol. Sci. 2008, 106:140-152.
40. Stover T., Kester M. Liposomal delivery enhances short-chain ceramide-induced apoptosis of breast cancer cells. J. Pharmacol. Exp. Ther. 2003, 307:468-475.
41. Stover T.C., Sharma A., Robertson G.P., Kester M. Systemic delivery of liposomal short-chain ceramide limits solid tumor growth in murine models of breast adenocarcinoma. Clin. Cancer Res. 2005, 11:3465-3474.
42. Tagaram H.R., Divittore N.A., Barth B.M., Kaiser J.M., Avella D., Kimchi E.T., Jiang Y., Isom H.C., Kester M., Staveley-O'Carroll K.F. Nanoliposomal ceramide prevents in vivo growth of hepatocellular carcinoma. Gut 2011, 60:695-701.
43. van Vlerken L.E., Duan Z., Little S.R., Seiden M.V., Amiji M.M. Augmentation of therapeutic efficacy in drug-resistant tumor models using ceramide coadministration in temporal-controlled polymer-blend nanoparticle delivery systems. AAPS J. 2010, 12:171-180.
44. Wei Y., Sinha S., Levine B. Dual role of JNK1-mediated phosphorylation of Bcl-2 in autophagy and apoptosis regulation. Autophagy 2008, 4:949-951.
45. White E.J., Martin V., Liu J.L., Klein S.R., Piya S., Gomez-Manzano C., Fueyo J., Jiang H. Autophagy regulation in cancer development and therapy. Am. J. Cancer Res. 2011, 1:362-372.
46. Xie R., Nguyen S., McKeehan W.L., Liu L. Acetylated microtubules are required for fusion of autophagosomes with lysosomes. BMC Cell Biol. 2010, 11:89.
47. Yue Z., Jin S., Yang C., Levine A.J., Heintz N. Beclin 1, an autophagy gene essential for early embryonic development, is a haploinsufficient tumor suppressor. Proc. Natl. Acad. Sci. USA 2003, 100:15077-15082.
48. Zhou F., Yang Y., Xing D. Bcl-2 and Bcl-xL play important roles in the crosstalk between autophagy and apoptosis. FEBS J. 2011, 278:403-413.
49. Zhou Q., Lui V.W., Lau C.P., Cheng S.H., Ng M.H., Cai Y., Chan S.L., Yeo W. Sustained antitumor activity by co-targeting mTOR and the microtubule with temsirolimus/vinblastine combination in hepatocellular carcinoma. Biochem. Pharmacol. 2012, 83:1146-1158.
50. Zolnik B.S., Stern S.T., Kaiser J.M., Heakal Y., Clogston J.D., Kester M., McNeil S.E. Rapid distribution of liposomal short-chain ceramide in vitro and in vivo. Drug Metab. Dispos.: Biol. Fate Chem. 2008, 36:1709-1715.