Blocking hypoxia-induced autophagy in tumors restores cytotoxic T-cell activity and promotes regression

Cancer Research

Volumn 71, Issue 18, 2011, Pages 5976-5986

  Noman, Muhammad Zaeem ^a   Janji, Bassam ^b   Kaminska, Bozena ^c   Van Moer, Kris ^b   Pierson, Sandrine ^b   Przanowski, Piotr ^c   Buart, Stéphanie ^a   Berchem, Guy ^b   Romero, Pedro ^d   Mami Chouaib, Fathia ^a   Chouaib, Salem ^a  

^a INSTITUT GUSTAVE ROUSSY   (France)

^b LUXEMBOURG INSTITUTE OF HEALTH   (Luxembourg)

^c NENCKI INSTITUTE OF EXPERIMENTAL BIOLOGY   (Poland)

^d UNIVERSITY OF LAUSANNE   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOPHAGY PROTEIN 5; BECLIN 1; CPG OLIGODEOXYNUCLEOTIDE; HYDROXYCHLOROQUINE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; JANUS KINASE; MICROTUBULE ASSOCIATED PROTEIN; PROTEASOME; PROTEIN BCL 2; PROTEIN BNIP3; PROTEIN P62; PROTEIN TYROSINE KINASE; SMALL INTERFERING RNA; STAT3 PROTEIN; TYROSINASE RELATED PROTEIN 2; UBIQUITIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; CANCER INHIBITION; CANCER SUSCEPTIBILITY; CONTROLLED STUDY; CYTOLYSIS; CYTOTOXIC T LYMPHOCYTE; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME REGULATION; HUMAN; HUMAN CELL; HYPOXIA; IN VIVO STUDY; LUNG TUMOR; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN TARGETING; RNA INTERFERENCE; TUMOR CELL; TUMOR GROWTH; TUMOR IMMUNITY; TUMOR REGRESSION; UBIQUITINATION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; AUTOPHAGY; CELL HYPOXIA; CELL LINE, TUMOR; HEAT-SHOCK PROTEINS; HUMANS; LUNG NEOPLASMS; MELANOMA, EXPERIMENTAL; MICE; MICE, INBRED C57BL; PHOSPHORYLATION; PROTEASOME ENDOPEPTIDASE COMPLEX; SRC-FAMILY KINASES; STAT3 TRANSCRIPTION FACTOR; T-LYMPHOCYTES, CYTOTOXIC; UBIQUITIN;

EID: 80052806536     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-11-1094     Document Type: Article

References (44)

1. Wouters BG, van den Beucken T, Magagnin MG, Lambin P, Koumenis C. Targeting hypoxia tolerance in cancer. Drug Resist Updat 2004;7:25-40. (Pubitemid 38453834)
2. Rosenberg SA. Progress in the development of immunotherapy for the treatment of patients with cancer. J Intern Med 2001;250:462-75. (Pubitemid 34013510)
3. Markiewicz MA, Gajewski TF. The immune system as anti-tumor sentinel: molecular requirements for an anti-tumor immune response. Crit Rev Oncog 1999;10:247-60. (Pubitemid 29395170)
4. Chouaib S, Asselin-Paturel C, Mami-Chouaib F, Caignard A, Blay JY. The host-tumor immune conflict: from immunosuppression to resistance and destruction. Immunol Today 1997;18:493-7. (Pubitemid 27441593)
5. Chouaib S. Integrating the quality of the cytotoxic response and tumor susceptibility into the design of protective vaccines in tumor immunotherapy. J Clin Invest 2003;111:595-7. (Pubitemid 36278575)
6. Hamai A, Benlalam H, Meslin F, Hasmim M, Carre T, Akalay I, et al. Immune surveillance of human cancer: if the cytotoxic T-lymphocytes play the music, does the tumoral system call the tune? Tissue Antigens 2010;75:1-8.
7. Semenza GL. Chairman's summary: mechanisms of oxygen homeostasis, circa 1999. Adv Exp Med Biol 2000;475:303-10. (Pubitemid 32197735)
8. Lukashev D, Klebanov B, Kojima H, Grinberg A, Ohta A, Berenfeld L, et al. Cutting edge: hypoxia-inducible factor 1alpha and its activation-inducible short isoform I.1 negatively regulate functions of CD4+ and CD8+ T lymphocytes. J Immunol 2006;177:4962-5. (Pubitemid 44527564)
9. Aebersold DM, Burri P, Beer KT, Laissue J, Djonov V, Greiner RH, et al. Expression of hypoxia-inducible factor-1alpha: a novel predictive and prognostic parameter in the radiotherapy of oropharyngeal cancer. Cancer Res 2001;61:2911-6. (Pubitemid 32691934)
10. Giaccia A, Siim BG, Johnson RS. HIF-1 as a target for drug development. Nat Rev Drug Discov 2003;2:803-11. (Pubitemid 37361812)
11. Semenza GL. HIF-1 inhibitors for cancer therapy: from gene expression to drug discovery. Curr Pharm Des 2009;15:3839-43.
12. Xu Q, Briggs J, Park S, Niu G, Kortylewski M, Zhang S, et al. Targeting Stat3 blocks both HIF-1 and VEGF expression induced by multiple oncogenic growth signaling pathways. Oncogene 2005;24:5552-60. (Pubitemid 43119350)
13. Wenger RH, Stiehl DP, Camenisch G. Integration of oxygen signaling at the consensus HRE. Sci STKE 2005;2005:re12.
14. Bromberg JF, Wrzeszczynska MH, Devgan G, Zhao Y, Pestell RG, Albanese C, et al. Stat3 as an oncogene. Cell 1999;98:295-303. (Pubitemid 29380565)
15. Huang S. Regulation of metastases by signal transducer and activator of transcription 3 signaling pathway: clinical implications. Clin Cancer Res 2007;13:1362-6. (Pubitemid 46450423)
16. Levine B, Kroemer G. Autophagy in the pathogenesis of disease. Cell 2008;132:27-42.
17. Lavieu G, Scarlatti F, Sala G, Levade T, Ghidoni R, Botti J, et al. Is autophagy the key mechanism by which the sphingolipid rheostat controls the cell fate decision? Autophagy 2007;3:45-7.
18. Munz C. Enhancing immunity through autophagy. Annu Rev Immunol 2009;27:423-49.
19. Amaravadi RK, Yu D, Lum 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)
20. 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.
21. 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;29:2570-81.
22. Mazure NM, Pouyssegur J. Hypoxia-induced autophagy: cell death or cell survival?Curr Opin Cell Biol 2010;22:177-80.
23. Noman MZ, Buart S, Van Pelt J, Richon C, Hasmim M, Leleu N, et al. The cooperative induction of hypoxia-inducible factor-1 alpha and STAT3 during hypoxia induced an impairment of tumor susceptibility to CTL-mediated cell lysis. J Immunol 2009;182:3510-21.
24. Magnon C, Opolon P, Ricard M, Connault E, Ardouin P, Galaup A, et al. Radiation and inhibition of angiogenesis by canstatin synergize to induce HIF-1alpha-mediated tumor apoptotic switch. J Clin Invest 2007;117:1844-55. (Pubitemid 47036318)
25. Korolchuk VI, Menzies FM, Rubinsztein DC. Mechanisms of cross-talk between the ubiquitin-proteasome and autophagy-lysosome systems. FEBS Lett 2010;584:1393-8.
26. Pursiheimo JP, Rantanen K, Heikkinen PT, Johansen T, Jaakkola PM. Hypoxia-activated autophagy accelerates degradation of SQSTM1/p62. Oncogene 2009;28:334-44.
27. Kochenderfer JN, Chien CD, Simpson JL, Gress RE. Synergism between CpG-containing oligodeoxynucleotides and IL-2 causes dramatic enhancement of vaccine-elicited CD8+ T cell responses. J Immunol 2006;177:8860-73. (Pubitemid 44893853)
28. Lisanti MP, Martinez-Outschoorn UE, Chiavarina B, Pavlides S, Whitaker-Menezes D, Tsirigos A, et al. Understanding the "lethal" drivers of tumor-stroma co-evolution: emerging role(s) for hypoxia, oxidative stress and autophagy/mitophagy in the tumor micro-environment. Cancer Biol Ther 2010;10:537-42.
29. Ding WX, Ni HM, Gao W, Yoshimori T, Stolz DB, Ron D, et al. Linking of autophagy to ubiquitin-proteasome system is important for the regulation of endoplasmic reticulum stress and cell viability. Am J Pathol 2007;171:513-24. (Pubitemid 47344684)
30. Bech-Otschir D, Kraft R, Huang X, Henklein P, Kapelari B, Pollmann C, et al. COP9 signalosome-specific phosphorylation targets p53 to degradation by the ubiquitin system. EMBO J 2001;20:1630-9. (Pubitemid 32299400)
31. Brand C, Horovitz-Fried M, Inbar A, Tamar Brutman B, Brodie C, Sampson SR. Insulin stimulation of PKCdelta triggers its rapid degradation via the ubiquitin-proteasome pathway. Biochim Biophys Acta 2010;1803:1265-75.
32. Korolchuk VI, Mansilla A, Menzies FM, Rubinsztein DC. Autophagy inhibition compromises degradation of ubiquitin-proteasome pathway substrates. Mol Cell 2009;33:517-27.
33. Rosenberg SA, Yang JC, Schwartzentruber DJ, Hwu P, Marincola FM, Topalian SL, et al. Immunologic and therapeutic evaluation of a synthetic peptide vaccine for the treatment of patients with metastatic melanoma. Nat Med 1998;4:321-7. (Pubitemid 28144091)
34. Rosenberg SA, Yang JC, Restifo NP. Cancer immunotherapy: moving beyond current vaccines. Nat Med 2004;10:909-15. (Pubitemid 39273730)
35. Song J, Qu Z, Guo X, Zhao Q, Zhao X, Gao L, et al. Hypoxia-induced autophagy contributes to the chemoresistance of hepatocellular carcinoma cells. Autophagy 2009;5:1131-44.
36. Cho HI, Celis E. Optimized peptide vaccines eliciting extensive CD8 T-cell responses with therapeutic antitumor effects. Cancer Res 2009;69:9012-9.
37. Fan C, Wang W, Zhao B, Zhang S, Miao J. Chloroquine inhibits cell growth and induces cell death in A549 lung cancer cells. Bioorg Med Chem 2006;14:3218-22.
38. Zheng Y, Zhao YL, Deng X, Yang S, Mao Y, Li Z, et al. Chloroquine inhibits colon cancer cell growth in vitro and tumor growth in vivo via induction of apoptosis. Cancer Invest 2009;27:286-92.
39. Rubinsztein DC, Gestwicki JE, Murphy LO, Klionsky DJ. Potential therapeutic applications of autophagy. Nat Rev Drug Discov 2007;6:304-12. (Pubitemid 46505881)
40. Dalby KN, Tekedereli I, Lopez-Berestein G, Ozpolat B. Targeting the prodeath and prosurvival functions of autophagy as novel therapeutic strategies in cancer. Autophagy 2010;6:322-9.
41. Sasaki K, Tsuno NH, Sunami E, Tsurita G, Kawai K, Okaji Y, et al. Chloroquine potentiates the anti-cancer effect of 5-fluorouracil on colon cancer cells. BMC Cancer 2010;10:370.
42. Vucicevic L, Misirkic M, Janjetovic K, Vilimanovich U, Sudar E, Isenovic E, et al. Compound C induces protective autophagy in cancer cells through AMPK inhibition-independent blockade of Akt/mTOR pathway. Autophagy 2011;7:40-50.
43. Sotelo J, Briceno E, Lopez-Gonzalez MA. Adding chloroquine to conventional treatment for glioblastoma multiforme: a randomized, double-blind, placebo-controlled trial. Ann Intern Med 2006;144:337-43. (Pubitemid 46768188)
44. Available from: http://clinicaltrials.gov/ct2/results?term=chloroquine.