Autophagy inhibition sensitizes colon cancer cells to antiangiogenic and cytotoxic therapy

Clinical Cancer Research

Volumn 19, Issue 11, 2013, Pages 2995-3007

  Selvakumaran, Muthu ^a   Amaravadi, Ravi K ^a   Vasilevskaya, Irina A ^a   O'Dwyer, Peter J ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOPHAGY PROTEIN 5; BECLIN 1; BEVACIZUMAB; CHLOROQUINE; OXALIPLATIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIANGIOGENIC THERAPY; ARTICLE; AUTOPHAGY; CANCER CELL; CANCER CHEMOTHERAPY; CANCER CONTROL; CANCER INHIBITION; CELL PROTECTION; COLON CANCER; CONTROLLED STUDY; CYTOTOXICITY; DNA DAMAGE; DRUG EFFICACY; ENZYME ACTIVITY; ENZYME REGULATION; HUMAN; HUMAN CELL; HYPOXIA; IN VITRO STUDY; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; SENSITIZATION; TREATMENT DURATION; TREATMENT RESPONSE; TUMOR XENOGRAFT;

ANGIOGENESIS INHIBITORS; ANIMALS; ANTIBODIES, MONOCLONAL, HUMANIZED; ANTINEOPLASTIC AGENTS; APOPTOSIS REGULATORY PROTEINS; AUTOPHAGY; CELL HYPOXIA; CELL LINE, TUMOR; CHLOROQUINE; COLONIC NEOPLASMS; DRUG RESISTANCE, NEOPLASM; FEMALE; GENE KNOCKDOWN TECHNIQUES; HT29 CELLS; HUMANS; MEMBRANE PROTEINS; MICE; ORGANOPLATINUM COMPOUNDS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84878992314     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-12-1542     Document Type: Article

References (50)

1. Saltz LB, Cox JV, Blanke C, Rosen LS, Fehrenbacher L, Moore MJ, et al. Irinotecan plus fluorouracil and leucovorin for metastatic colorectal cancer. N Engl J Med 2000;343:905-14.
2. Goldberg RM, Sargent DJ, Morton RF, Fuchs CS, Ramanathan RK, Williamson SK, et al., A randomized controlled trial of fluorouracil plus leucovorin, irinotecan, and oxaliplatin combinations in patients with previously untreated metastatic colorectal cancer. J Clin Oncol 2004;22:23-30. (Pubitemid 41095110)
3. Hurwitz H, Fehrenbacher L, Novotny W, Cartwright T, Hainsworth J, Heim W, et al. Bevacizumab plus irinotecan, fluorouracil, and leucovorin for metastatic colorectal cancer.NEngl J Med 2004;350:2335-42. (Pubitemid 38702844)
4. Giantonio BJ, Catalano PJ, Meropol NJ, O'Dwyer PJ, Mitchell EP, Alberts SR, et al. Bevacizumab in combination with oxaliplatin, fluorouracil, and leucovorin (FOLFOX4) for previously treated metastatic colorectal cancer: results from the Eastern Cooperative Oncology Group Study E3200. J Clin Oncol 2007;25:1539-44. (Pubitemid 46733080)
5. Vaupel P, Kallinowski F, Okunief F. Blood flow, oxygen and nutrient supply, and metabolic microenvironment of human tumors: a review. Cancer Res 1989;49:6449-65. (Pubitemid 20008770)
6. Cao D, Hou M, Guan YS, Jiang M, Yang Y, Gou HF. Expression of HIF-1alpha and VEGF in colorectal cancer: association with clinical outcomes and prognostic implications. BMC Cancer 2009;9:432-40.
7. DeBerardinis RJ, Lum JJ, Hatzivassiliou G, Thompson CB. The biology of cancer: metabolic reprogramming fuels cell growth and proliferation. Cell Metab 2008;7:11-20.
8. Tennant DA, Durán RV, Gottlieb E. Targeting metabolic transformation for cancer therapy. Nat Rev Cancer 2010;10:267-77.
9. Willett CG, Boucher Y, di Tomaso E, Duda DG, Munn LL, Tong RT, et al. Direct evidence that the VEGF-specific antibody bevacizumab has antivascular effects in human rectal cancer. Nat Med 2004;10:145-7. (Pubitemid 38524883)
10. Yao K, Gietema JA, Shida S, Selvakumaran M, Fonrose X, Haas NB, et al. In vitro hypoxia-conditioned colon cancer cell lines derived from HCT116 and HT29 exhibit altered apoptosis susceptibility and a more angiogenic profile in vivo. Br J Cancer 2005;93:1356-63. (Pubitemid 41752862)
11. Selvakumaran M, Yao KS, Feldman MD, O'Dwyer PJ. Antitumor effect of the angiogenesis inhibitor bevacizumab is dependent on susceptibility of tumors to hypoxia-induced apoptosis. Biochem Pharmacol 2008;75:627-38.
12. Ebos JM, Lee CR, Cruz-Munoz W, Bjarnason GA, Christensen JG, Kerbel RS. Accelerated metastasis after short-term treatment with a potent inhibitor of tumor angiogenesis. Cancer Cell 2009;15:232-9.
13. Yoo YG, Christensen J, Gu J, Huang LE. HIF-1alpha mediates tumor hypoxia to confer a perpetual mesenchymal phenotype for malignant progression. Sci Signal 2011;4:pt4.
14. Reynolds TY, Rockwell S, Glazer PM. Genetic instability induced by the tumor microenvironment. Cancer Res 1996;56:5754-7. (Pubitemid 26422184)
15. Graeber TG, Osmanian C, Jacks T, Housman DE, Koch CJ, Lowe SW, et al. Hypoxia-mediated selection of cells with diminished apoptotic potential in solid tumours. Nature 1996;379:88-91. (Pubitemid 26008141)
16. Esumi H, Izuishi K, Kato K, Hashimoto K, Kurashima Y, Kishimoto A, et al. Hypoxia and nitric oxide treatment confer tolerance to glucose starvation in a 5′-AMP-activated protein kinase-dependent manner. J Biol Chem 2002;277:32791-8. (Pubitemid 34984788)
17. Levine B, Kroemer G. Autophagy in the pathogenesis of disease. Cell 2008;132:27-42.
18. Xie Z, Klionsky DJ. Autophagosome formation: core machinery and adaptations. Nat Cell Biol 2007;9:1102-9. (Pubitemid 47500484)
19. Nakatogawa H, Ichimura Y, Ohsumi Y. Atg8, a ubiquitin-like protein required for autophagosome formation, mediates membrane tethering and hemifusion. Cell 2007;130:165-78. (Pubitemid 47031316)
20. Nakatogawa H, Suzuki K, Kamada Y, Ohsumi Y. Dynamics and diversity in autophagy mechanisms: lessons from yeast. Nat Rev Mol Cell Biol 2009;10:458-67.
21. Mathew R, Karp CM, Beaudoin B, Vuong N, Chen G, Chen HY, et al. Autophagy suppresses tumorigenesis through elimination of p62. Cell 2009;137:1062-75.
22. Matthew R, Karantza-Wadsworth V, White E. Role of autophagy in cancer. Nat Rev Cancer 2007;7:961-7. (Pubitemid 350165856)
23. Amaravadi RK, Yu D, Lun JJ, Bui T, Christophorou MA, Evan GI, et al. Autophagy inhibition enhances therapy-induced apoptosis in a Myc-induced model of lymphoma. J Clin Invest 2007;117:326-36. (Pubitemid 46203961)
24. Degenhardt K, Mathew R, Beaudoin B, Bray K, Anderson D, Chen G, et al. Autophagy promotes tumor cell survival and restricts necrosis, inflammation, and tumorigenesis. Cancer Cell 2006;10:51-64.
25. Karantza-Wadsworth V, Patel S, Kravchuk O, Chen G, Mathew R, Jin S, et al. Autophagy mitigates metabolic stress and genome damage in mammary tumorigenesis. Genes Dev 2007;21:1621-35. (Pubitemid 47026367)
26. Mathew R, Kongara S, Beaudoin B, Karp CM, Bray K, Degenhardt K, et al. Autophagy suppresses tumor progression by limiting chromosomal instability. Genes Dev 2007;21:1367-81. (Pubitemid 46871040)
27. Azad MB, Chen Y, Henson ES, Cizeau J, McMillan-Ward E, Israels SJ, et al. Hypoxia induces autophagic cell death in apoptosis-competent cells through a mechanism involving BNIP3. Autophagy 2008;16:195- 204.
28. Bellot G, Garcia-Medina R, Gounon P, Chiche J, Roux D, Pouyssegur J, et al. Hypoxia-induced autophagy is mediated through hypoxia-inducible factor induction of BNIP3 and BNIP3L via their BH3 domains. Mol Cell Biol 2009;10:2570-81.
29. Hu Y-L, DeLay M, Jahangiri A, Molinaro AM, Rose SD, Carbonell WS, et al. Hypoxia-induced autophagy promotes tumor cell survival and adaptation to antiangiogenic treatment in glioblastoma. Cancer Res 2012;72:1773-83.
30. Bacon AL, Fox S, Turley H, Harris AL. Selective silencing of the hypoxia-inducible 1 target gene BNIP3 by histone deacetylation and methylation in colorectal cancer. Oncogene 2007;26:132-41. (Pubitemid 46067338)
31. Song J, Qu Z, Guo X, Zhao X, Gao L, Sun K, et al. Hypoxia-induced autophagy contributes to the chemoresistance of hepatocellular carcinoma cells. Autophagy 2009;5:1131-44.
32. Amaravadi RK, Thompson CB. The roles of therapy-induced autophagy and necrosis in cancer treatment. Clin Cancer Res 2007;15:7271-9.
33. Chou T-C. Theoretical basis, experimental design and computerized simulation of synergism and antagonism in drug combination studies. Pharmacol Rev 2006;58:621-81. (Pubitemid 44403686)
34. Chou T-C, Martin N. CompuSyn software for drug combinations and for general dose-effect analysis, and user's guide. Paramus, NJ: ComboSyn, Inc.; 2007. Available from: www.combosyn.com.
35. Yang S, Wang X, Contino G, Liesa M, Sahin E, Ying H, et al. Pancreatic cancers require autophagy for tumor growth. Genes Dev 2011;25:717-29.
36. Dikov DI, Auriault ML, Boivin JF, Sarafian VS, Papadimitriou JC. Hyaline globules (thanatosomes) in gastrointestinal epithelium: pathophysiologic correlations. Am J Clin Pathol 2007;127:792-9.
37. Ramakrishnan S, Nguyen TM, Subramanian IV, Kelekar A. Autophagy and angiogenesis inhibition. Autophagy 2007;3:512-5. (Pubitemid 47293743)
38. Lee S-J, Kim HP, Jin Y, Choi AMK, Ryter SW. Beclin 1 deficiency is associated with increased hypoxia-induced angiogenesis. Autophagy 2011;7:829-39.
39. Du J, Teng RJ, Guan T, Eis A, Kaul S, Konduri GG, et al. Role of autophagy in angiogenesis in aortic endothelial cells. Am J Physiol Cell Physiol 2012;302:C383-91.
40. Rouschop KM, van den Beucken T, Dubois L, Niessen H, Bussink J, Savelkouls K, et al. The unfolded protein response protects human tumor cells during hypoxia through regulation of the autophagy genes MAP1LC3B and ATG5. J Clin Invest 2010;120:127-41.
41. Shi YH, Ding ZB, Zhou J, Hui B, Shi GM, Ke AW, et al. Targeting autophagy enhances sorafenib lethality for hepatocellular carcinoma via ER stress-related apoptosis. Autophagy 2011;7:1159-72.
42. Rakitina T, Vasilevskaya IV, O'Dwyer PJ. Inhibition of G1/S transition potentiates oxaliplatin-induced cell death in colon cancer cell lines. Biochem Pharmacol 2007;73:1715-26. (Pubitemid 46601405)
43. Vasilevskaya IA, Selvakumaran M, O'Dwyer PJ. Signaling through MKK7 is required for oxaliplatin-induced cell death in hypoxic colon adenocarcinoma cell lines. Mol Pharmacol 2008;74:246-54. (Pubitemid 351872175)
44. Frezza C, Zheng L, Tennant DA, Papkovsky DB, Hedley BA, Kalna G, et al. Metabolic profiling of hypoxic cells revealed a catabolicv signature required for cell survival. PLoS ONE 2011;6:e24411.
45. Zhang H, Bosch-Marce M, Shimoda LA, Tan YS, Baek JH, Wesley JB, et al. Mitochondrial autophagy is an HIF-1-dependent adaptive metabolic response to hypoxia. J Biol Chem 2008;283:10892-903.
46. Mazure NM, Pouysségur J. Atypical BH3-domains of BNIP3 and BNIP3L lead to autophagy in hypoxia. Autophagy 2009;5:868-9.
47. Murai M, Toyota M, Suzuki H, Satoh A, Sasaki Y, Akino K, et al. Aberrant methylation and silencing of the BNIP3 gene in colorectal and gastric cancer. Clin Cancer Res 2005;11:1021-7. (Pubitemid 40175749)
48. Goel S, Duda DG, Xu L, Munn LL, Boucher Y, Fukumura D, et al. Normalization of the vasculature for treatment of cancer and other diseases. Physiol Rev 2011;91:1071-121.
49. Matsumoto S, Batra S, Saito K, Yasui H, Choudhuri R, Gadisetti C, et al. Antiangiogenic agent sunitinib transiently increases tumor oxygenation and suppresses cycling hypoxia. Cancer Res 2011;71:6350-9.
50. Sorensen AG, Emblem KE, Polaskova P, Jennings D, Kim H, Ancukiewicz M, et al. Increased survival of glioblastoma patients who respond to antiangiogenic therapy with elevated blood perfusion. Cancer Res 2012;72:402-7. Cancer Institute/National Institutes of Health Cancer Institute/National Institutes of Health