When cells suffocate: Autophagy in cancer and immune cells under low oxygen

International Journal of Cell Biology

Volumn , Issue , 2011, Pages

  Schlie, Katrin ^a   Spowart, Jaeline E ^a,b   Hughson, Luke R K ^a,b   Townsend, Katelin N ^a,b   Lum, Julian J ^a,b  

^a BRITISH COLUMBIA CANCER AGENCY   (Canada)

^b UNIVERSITY OF VICTORIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE MONOPHOSPHATE ACTIVATED PROTEIN KINASE; ADENOSINE TRIPHOSPHATE; ANTINEOPLASTIC AGENT; BORTEZOMIB; FENRETINIDE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; PROTEIN KINASE; PROTEIN P53; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG;

ADAPTIVE IMMUNITY; ANAEROBIC METABOLISM; AUTOPHAGY; CANCER CELL; CANCER GROWTH; CANCER RADIOTHERAPY; CANCER RESISTANCE; CELL HYPOXIA; CELL SURVIVAL; CELLULAR IMMUNITY; DRUG CYTOTOXICITY; DRUG POTENCY; ENZYME ACTIVITY; FIBROBLAST; HUMAN; IMMUNOCOMPETENT CELL; IMMUNOMODULATION; IMMUNOSURVEILLANCE; INNATE IMMUNITY; INTRACELLULAR SIGNALING; MITOPHAGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN FOLDING; RADIOSENSITIVITY; REVIEW; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; TUMOR IMMUNITY; TUMOR MICROENVIRONMENT; UNFOLDED PROTEIN RESPONSE; UPREGULATION;

EID: 84855605176     PISSN: 16878876     EISSN: 16878884     Source Type: Journal    
DOI: 10.1155/2011/470597     Document Type: Review

References (103)

1. Helmlinger G., Yuan F., Dellian M., Jain R. K., Interstitial pH and pO2 gradients in solid tumors in vivo: high-resolution measurements reveal a lack of correlation Nature Medicine 1997 3 2 177 182 (Pubitemid 27064702)
2. Vaupel P., Hckel M., Mayer A., Detection and characterization of tumor hypoxia using pO2 histography Antioxidants and Redox Signaling 2007 9 8 1221 1235 (Pubitemid 47080831)
3. Matsumoto S., Yasui H., Mitchell J. B., Krishna M. C., Imaging cycling tumor hypoxia Cancer Research 2010 70 24 10019 10023
4. Yasui H., Matsumoto S., Devasahayam N., Munasinghe J. P., Choudhuri R., Saito K., Subramanian S., Mitchell J. B., Krishna M. C., Low-field magnetic resonance imaging to visualize chronic and cycling hypoxia in tumor-bearing mice Cancer Research 2010 70 16 6427 6436
5. Semenza G. L., Hypoxia-inducible factor 1: master regulator of O2 homeostasis Current Opinion in Genetics and Development 1998 8 5 588 594 (Pubitemid 28477364)
6. Mizushima N., Yamamoto A., Matsui M., Yoshimori T., Ohsumi Y., In vivo analysis of autophagy in response to nutrient starvation using transgenic mice expressing a fluorescent autophagosome marker Molecular Biology of the Cell 2004 15 3 1101 1111 (Pubitemid 38316219)
7. Lum J. J., Bauer D. E., Kong M., Harris M. H., Li C., Lindsten T., Thompson C. B., Growth factor regulation of autophagy and cell survival in the absence of apoptosis Cell 2005 120 2 237 248 (Pubitemid 40174766)
8. Bellot G., Garcia-Medina R., Gounon P., Chiche J., Roux D., Pouysségur J., Mazure N. M., Hypoxia-induced autophagy is mediated through hypoxia-inducible factor induction of BNIP3 and BNIP3L via their BH3 domains Molecular and Cellular Biology 2009 29 10 2570 2581
9. Bursch W., Ellinger A., Kienzl H., Torok L., Pandey S., Sikorska M., Walker R., Hermann R. S., Active cell death induced by the anti-estrogens tamoxifen and ICI 164 384 in human mammary carcinoma cells (MCF-7) in culture: the role of autophagy Carcinogenesis 1996 17 8 1595 1607 (Pubitemid 26280381)
10. Yang Z., Klionsky D. J., Eaten alive: a history of macroautophagy Nature Cell Biology 2010 12 9 814 822
11. Rabinowitz J. D., White E., Autophagy and metabolism Science 2010 330 6009 1344 1348
12. Shang L., Wang X., AMPK and mTOR coordinate the regulation of Ulk1 and mammalian autophagy initiation Autophagy 2011 7 8 924 926
13. Wang S. Y., Yu Q. J., Zhang R. D., Liu B., Core signaling pathways of survival/death in autophagy-related cancer networks International Journal of Biochemistry and Cell Biology 2011 43 9 1263 1266
14. Papandreou I., Lim A. L., Laderoute K., Denko N. C., Hypoxia signals autophagy in tumor cells via AMPK activity, independent of HIF-1, BNIP3, and BNIP3L Cell Death and Differentiation 2008 15 10 1572 1581
15. Zhang R., Zhu F., Ren J., Huang L., Liu P., Wu G., Beclin1/PI3K-mediated autophagy prevents hypoxia-induced apoptosis in EAhy926 cell line Cancer Biotherapy and Radiopharmaceuticals 2011 26 3 335 343
16. Sivridis E., Koukourakis M. I., Mendrinos S. E., Karpouzis A., Fiska A., Kouskoukis C., Giatromanolaki A., Beclin-1 and LC3A expression in cutaneous malignant melanomas: a biphasic survival pattern for beclin-1 Melanoma Research 2011 21 3 188 195
17. Yoo B. H., Wu X., Derouet M., Haniff M., Eskelinen E. L., Rosen K., Hypoxia-induced downregulation of autophagy mediator beclin 1 reduces the susceptibility of malignant intestinal epithelial cells to hypoxia-dependent apoptosis Autophagy 2009 5 8 1166 1179
18. Yousefi S., Perozzo R., Schmid I., Ziemiecki A., Schaffner T., Scapozza L., Brunner T., Simon H. U., Calpain-mediated cleavage of Atg5 switches autophagy to apoptosis Nature Cell Biology 2006 8 10 1124 1132 (Pubitemid 44473608)
19. Gozuacik D., Kimchi A., Autophagy as a cell death and tumor suppressor mechanism Oncogene 2004 23 16 2891 2906 (Pubitemid 38638851)
20. Kroemer G., Levine B., Autophagic cell death: the story of a misnomer Nature Reviews Molecular Cell Biology 2008 9 12 1004 1010
21. Ali S., Ahmad M., Lynam J., Rees R. C., Brown N., Trafficking of tumor peptide-specific cytotoxic T lymphocytes into the tumor microcirculation Journal International du Cancer 2004 110 2 239 244 (Pubitemid 38580397)
22. Rosenberg S. A., Yang J. C., Sherry R. M., Kammula U. S., Hughes M. S., Phan G. Q., Citrin D. E., Restifo N. P., Robbins P. F., Wunderlich J. R., Morton K. E., Laurencot C. M., Steinberg S. M., White D. E., Dudley M. E., Durable complete responses in heavily pretreated patients with metastatic melanoma using T cell transfer immunotherapy Clinical Cancer Research 2011 17 13 4550 4557
23. Yang T., Wall E. M., Milne k., Theiss P., Watson P., Nelson B. H., CD8+ T cells induce complete regression of advanced ovarian cancers by an interleukin (IL)-2/IL-15 dependent mechanism Clinical Cancer Research 2007 13 23 7172 7180 (Pubitemid 350276904)
24. Menrad H., Werno C., Schmid T., Copanaki E., Deller T., Dehne N., Brne B., Roles of hypoxia-inducible factor-1alpha (HIF-1alpha) versus HIF-2alpha in the survival of hepatocellular tumor spheroids Hepatology 2010 51 6 2183 2192
25. Tasdemir E., Maiuri M. C., Galluzzi L., Vitale I., Djavaheri-Mergny M., D'Amelio M., Criollo A., Morselli E., Zhu C., Harper F., Nannmark U., Samara C., Pinton P., Vicencio J. M., Carnuccio R., Moll U. M., Madeo F., Paterlini-Brechot P., Rizzuto R., Szabadkai G., Pierron G., Blomgren K., Tavernarakis N., Codogno P., Cecconi F., Kroemer G., Regulation of autophagy by cytoplasmic p53 Nature Cell Biology 2008 10 6 676 687 (Pubitemid 351772933)
26. Azad M. B., Chen Y., Henson E. S., Cizeau J., McMillan-Ward E., Israels S. J., Gibson S. B., Hypoxia induces autophagic cell death in apoptosis-competent cells through a mechanism involving BNIP3 Autophagy 2008 4 2 195 204 (Pubitemid 351231183)
27. Zhang H., Bosch-Marce M., Shimoda L. A., Yee S. T., Jin H. B., Wesley J. B., Gonzalez F. J., Semenza G. L., Mitochondrial autophagy is an HIF-1-dependent adaptive metabolic response to hypoxia Journal of Biological Chemistry 2008 283 16 10892 10903
28. Rzymski T., Milani M., Pike L., Buffa F., Mellor H. R., Winchester L., Pires I., Hammond E., Ragoussis I., Harris A. L., Regulation of autophagy by ATF4 in response to severe hypoxia Oncogene 2010 29 31 4424 4435
29. Rouschop K. M. A., van den Beucken T., Dubois L., Niessen H., Bussink J., Savelkouls K., Keulers T., Mujcic H., Landuyt W., Voncken J. W., Lambin P., Van Der Kogel A. J., Koritzinsky M., Wouters B. G., The unfolded protein response protects human tumor cells during hypoxia through regulation of the autophagy genes MAP1LC3B and ATG5 Journal of Clinical Investigation 2010 120 1 127 141
30. Wirawan E., Walle L. V., Kersse K., Cornelis S., Claerhout S., Vanoverberghe I., Roelandt R., De Rycke R., Verspurten J., Declercq W., Agostinis P., Berghe T. V., Lippens S., Vandenabeele P., Caspase-mediated cleavage of Beclin-1 inactivates Beclin-1-induced autophagy and enhances apoptosis by promoting the release of proapoptotic factors from mitochondria Cell Death and Disease 2010 1, article e18
31. Wilkinson S., O'Prey J., Fricker M., Ryan K. M., Hypoxia-selective macroautophagy and cell survival signaled by autocrine PDGFR activity Genes Development 2009 23 11 1283 1288
32. Graeber T. G., Osmanian C., Jacks T., Housman D. E., Koch C. J., Lowe S. W., Giaccia A. J., Hypoxia-mediated selection of cells with diminished apoptotic potential in solid tumours Nature 1996 379 6560 88 91 (Pubitemid 26008141)
33. Rzymski T., Milani M., Singleton D. C., Harris A. L., Role of ATF4 in regulation of autophagy and resistance to drugs and hypoxia Cell Cycle 2009 8 23 3838 3847
34. Tsukamoto S., Kuma A., Murakami M., Kishi C., Yamamoto A., Mizushima N., Autophagy is essential for preimplantation development of mouse embryos Science 2008 321 5885 117 120 (Pubitemid 351956245)
35. Kuma A., Hatano M., Matsui M., Yamamoto A., Nakaya H., Yoshimori T., Ohsumi Y., Tokuhisa T., Mizushima N., The role of autophagy during the early neonatal starvation period Nature 2004 432 7020 1032 1036 (Pubitemid 40052234)
36. Guo J. Y., Chen H. Y., Mathew R., Fan J., Strohecker A. M., Karsli-Uzunbas G., Kamphorst J. J., Chen G., Lemons J. M.S., Karantza V., Coller H. A., DiPaola R. S., Gelinas C., Rabinowitz J. D., White E., Activated Ras requires autophagy to maintain oxidative metabolism and tumorigenesis Genes and Development 2011 25 5 460 470
37. Amaravadi R. K., Yu D., Lum J. J., Bui T., Christophorou M. A., Evan G. I., Thomas-Tikhonenko A., Thompson C. B., Autophagy inhibition enhances therapy-induced apoptosis in a Myc-induced model of lymphoma Journal of Clinical Investigation 2007 117 2 326 336 (Pubitemid 46203961)
38. Gupta A., Roy S., Lazar A. J. F., Wang W. L., McAuliffe J. C., Reynoso D., McMahon J., Taguchi T., Floris G., Debiec-Rychter M., Schoffski P., Trent J. A., Debnath J., Rubin B. P., Autophagy inhibition and antimalarials promote cell death in gastrointestinal stromal tumor (GIST) Proceedings of the National Academy of Sciences of the United States of America 2010 107 32 14333 14338
39. Li J., Hou N., Faried A., Tsutsumi S., Kuwano H., Inhibition of autophagy augments 5-fluorouracil chemotherapy in human colon cancer in vitro and in vivo model European Journal of Cancer 2010 46 10 1900 1909
40. Wan X. B., Fan X. J., Chen M. Y., Xiang J., Huang P. Y., Guo L., Wu X. Y., Xu J., Long Z. J., Zhao Y., Zhou W. H., Mai H. Q., Liu Q., Hong M. H., Elevated Beclin 1 expression is correlated with HIF-1alpha in predicting poor prognosis of nasopharyngeal carcinoma Autophagy 2010 6 3 395 404
41. Koukourakis M. I., Giatromanolaki A., Sivridis E., Pitiakoudis M., Gatter K. C., Harris A. L., Beclin 1 over- and underexpression in colorectal cancer: distinct patterns relate to prognosis and tumour hypoxia British Journal of Cancer 2010 103 8 1209 1214
42. Yousefi S., Simon H. U., Apoptosis regulation by autophagy gene 5 Critical Reviews in Oncology/Hematology 2007 63 3 241 244 (Pubitemid 47126867)
43. Djavaheri-Mergny M., Maiuri M. C., Kroemer G., Cross talk between apoptosis and autophagy by caspase-mediated cleavage of Beclin 1 Oncogene 2010 29 12 1717 1719
44. Kang R., Zeh H. J., Lotze M. T., Tang D., The Beclin 1 network regulates autophagy and apoptosis Cell Death and Differentiation 2011 18 4 571 580
45. Wilson W. R., Hay M. P., Targeting hypoxia in cancer therapy Nature Reviews Cancer 2011 11 393 410
46. Song J., Qu Z., Guo X., Zhao Q., Xue Z., Lu G., Kai S., Feng S., Mengchao W., Lixin W., Hypoxia-induced autophagy contributes to the chemoresistance of hepatocellular carcinoma cells Autophagy 2009 5 8 1131 1144
47. Liu X. W., Su Y., Zhu H., Cao J., Ding W. J., Zhao Y. C., He Q. J., Yang B., HIF-1alpha-dependent autophagy protects HeLa cells from fenretinide (4-HPR)-induced apoptosis in hypoxia Pharmacological Research 2010 62 5 416 425
48. Fels D. R., Ye J., Segan A. T., Kridel S. J., Spiotto M., Olson M., Koong A. C., Koumenis C., Preferential cytotoxicity of bortezomib toward hypoxic tumor cells via overactivation of endoplasmic reticulum stress pathways Cancer Research 2008 68 22 9323 9330
49. Levine B., Mizushima N., Virgin H. W., Autophagy in immunity and inflammation Nature 2011 469 323 335
50. Saitoh T., Akira S., Regulation of innate immune responses by autophagy-related proteins Journal of Cell Biology 2010 189 6 925 935
51. Hoskin D. W., Mader J. S., Furlong S. J., Conrad D. M., Blay J., Inhibition of T cell and natural killer cell function by adenosine and its contribution to immune evasion by tumor cells (Review) International Journal of Oncology 2008 32 3 527 535 (Pubitemid 351330458)
52. Singer K., Gottfried E., Kreutz M., Mackensen A., Suppression of T cell responses by tumor metabolites Cancer Immunology, Immunotherapy 2011 60 3 425 431
53. Vesely M. D., Kershaw M. H., Schreiber R. D., Smyth M. J., Natural innate and adaptive immunity to cancer Annual Review of Immunology 2011 29 235 271
54. Vyas J. M., Van der Veen A. G., Ploegh H. L., The known unknowns of antigen processing and presentation Nature Reviews Immunology 2008 8 8 607 618
55. Coussens L. M., Werb Z., Inflammation and cancer Nature 2002 420 6917 860 867 (Pubitemid 36019639)
56. Kumar V., Sharma A., Neutrophils: cinderella of innate immune system International Immunopharmacology 2010 10 11 1325 1334
57. Walmsley S. R., Print C., Farahi N., Peyssonnaux C., Johnson R. S., Cramer T., Sobolewski A., Condliffe A. M., Cowburn A. S., Johnson N., Chilvers E. R., Hypoxia-induced neutrophil survival is mediated by HIF-1alpha-dependent NF-kappaB activity Journal of Experimental Medicine 2005 201 1 105 115 (Pubitemid 40130088)
58. Mihalache C. C., Yousefi S., Conus S., Villiger P. M., Schneider E. M., Simon H. U., Inflammation-associated autophagy-related programmed necrotic death of human neutrophils characterized by organelle fusion events Journal of Immunology 2011 186 11 6532 6542
59. Lewis J. S., Lee J. A., Underwood J. C. E., Harris A. L., Lewis C. E., Macrophage responses to hypoxia: relevance to disease mechanisms Journal of Leukocyte Biology 1999 66 6 889 900 (Pubitemid 30010512)
60. Mancino A., Schioppa T., Larghi P., Pasqualini F., Nebuloni M., Chen I. H., Sozzani S., Austyn J. M., Mantovani A., Sica A., Divergent effects of hypoxia on dendritic cell functions Blood 2008 112 9 3723 3734
61. Futalan D., Huang C. T., Schmidt-Wolf I. G., Larsson M., Messmer D., Effect of oxygen levels on the physiology of dendritic cells: implications for adoptive cell therapy Molecular Medicine 2011 17 9-10 910 916
62. Yang M., Ma C., Liu S., Sun J., Shao Q., Gao W., Zhang Y., Li Z., Xie Q., Dong Z., Qu X., Hypoxia skews dendritic cells to a T helper type 2-stimulating phenotype and promotes tumour cell migration by dendritic cell-derived osteopontin Immunology 2009 128 1 e237 e249
63. Naldini A., Morena E., Pucci A., Hypoxia affects dendritic cell survival: role of the hypoxia-inducible factor-1alpha and lipopolysaccharide. Journal of Cellular Physiology. In press
64. Shi C. S., Kehrl J. H., MyD88 and Trif target Beclin 1 to trigger autophagy in macrophages Journal of Biological Chemistry 2008 283 48 33175 33182
65. Xu Y., Jagannath C., Liu X. D., Sharafkhaneh A., Kolodziejska K. E., Eissa N. T., Toll-like receptor 4 is a sensor for autophagy associated with innate immunity Immunity 2007 27 1 135 144 (Pubitemid 47089027)
66. Sanjuan M. A., Dillon C. P., Tait S. W. G., Moshiach S., Dorsey F., Connell S., Komatsu M., Tanaka K., Cleveland J. L., Withoff S., Green D. R., Toll-like receptor signalling in macrophages links the autophagy pathway to phagocytosis Nature 2007 450 7173 1253 1257
67. Lee H. K., Mattei L. M., Steinberg B. E., Alberts P., Lee Y. H., Chervonsky A., Mizushima N., Grinstein S., Iwasaki A., In vivo requirement for Atg5 in antigen presentation by dendritic cells Immunity 2010 32 2 227 239
68. Zhang Y., Pfannenstiel L. W., Bolesta E. B., Interleukin-7 inhibits tumor-induced CD27-CD28- suppressor T cells: implications for cancer immunotherapy Clinical Cancer Research 2011 17 15 4968 4975
69. Mackall C. L., Fry T. J., Gress R. E., Harnessing the biology of IL-7 for therapeutic application Nature Reviews Immunology 2011 11 5 330 342
70. McDermott D. F., Regan M. M., Clark J. I., Flaherty L. E., Weiss G. R., Logan T. F., Kirkwood J. M., Gordon M. S., Sosman J. A., Ernstoff M. S., Tretter C. P. G., Urba W. J., Smith J. W., Margolin K. A., Mier J. W., Gollob J. A., Dutcher J. P., Atkins M. B., Randomized phase III trial of high-dose interleukin-2 versus subcutaneous interleukin-2 and interferon in patients with metastatic renal cell carcinoma Journal of Clinical Oncology 2005 23 1 133 141 (Pubitemid 41702632)
71. Cameron F., Whiteside G., Perry C., Ipilimumab: first global approval Drugs 2011 71 8 1093 1104
72. Tamas P., Hawley S. A., Clarke R. G., Mustard K. J., Green K., Hardie D. G., Cantrell D. A., Regulation of the energy sensor AMP-activated protein kinase by antigen receptor and Ca2+ in T lymphocytes Journal of Experimental Medicine 2006 203 7 1665 1670 (Pubitemid 44036271)
73. Larbi A., Zelba H., Goldeck D., Pawelec G., Induction of HIF-1 alpha and the glycolytic pathway alters apoptotic and differentiation profiles of activated human T cells Journal of Leukocyte Biology 2010 87 2 265 273
74. Inoki K., Zhu T., Guan K. L., TSC2 mediates cellular energy response to control cell growth and survival Cell 2003 115 5 577 590 (Pubitemid 37506046)
75. Gwinn D. M., Shackelford D. B., Egan D. F., Mihaylova M. M., Mery A., Vasquez D. S., Turk B. E., Shaw R. J., AMPK phosphorylation of raptor mediates a metabolic checkpoint Molecular Cell 2008 30 2 214 226 (Pubitemid 351626684)
76. Salmond R. J., Emery J., Okkenhaug K., Zamoyska R., MAPK, phosphatidylinositol 3-kinase, and mammalian target of rapamycin pathways converge at the level of ribosomal protein S6 phosphorylation to control metabolic signaling in CD8 T cells Journal of Immunology 2009 183 11 7388 7397
77. Nakamura H., Makino Y., Okamoto K., Poellinger L., Ohnuma K., Morimoto C., Tanaka H., TCR engagement increases hypoxia-inducible factor-1 alpha protein synthesis via rapamycin-sensitive pathway under hypoxic conditions in human peripheral T cells Journal of Immunology 2005 174 12 7592 7599 (Pubitemid 40806263)
78. Fox C. J., Hammerman P. S., Thompson C. B., Fuel feeds function: energy metabolism and the T cell response Nature Reviews Immunology 2005 5 11 844 852 (Pubitemid 41581666)
79. Dvel K., Yecies J. L., Menon S., Raman P., Lipovsky A. I., Souza A. L., Triantafellow E., Ma Q., Gorski R., Cleaver S., Heiden M. G. V., MacKeigan J. P., Finan P. M., Clish C. B., Murphy L. O., Manning B. D., Activation of a metabolic gene regulatory network downstream of mTOR complex 1 Molecular Cell 2010 39 2 171 183
80. Zuckerberg A. L., Goldberg L. I., Lederman H. M., Effects of hypoxia on interleukin-2 mRNA expression by T lymphocytes Critical Care Medicine 1994 22 2 197 203 (Pubitemid 24061640)
81. Lukashev D., Klebanov B., Kojima H., Grinberg A., Ohta A., Berenfeld L., Wenger R. H., Ohta A., Sitkovsky M., Cutting edge: hypoxia-inducible factor 1alpha and its activation-inducible short isoform I.1 negatively regulate functions of CD4+ and CD8+ T lymphocytes Journal of Immunology 2006 177 8 4962 4965 (Pubitemid 44527564)
82. Robbins J. R., Lee S. M., Filipovich A. H., Szigligeti P., Neumeier L., Petrovic M., Conforti L., Hypoxia modulates early events in T cell receptor-mediated activation in human T lymphocytes via Kv1.3 channels Journal of Physiology 2005 564 1 131 143 (Pubitemid 40542193)
83. Neumann A. K., Yang J., Biju M. P., Joseph S. K., Johnson R. S., Haase V. H., Freedman B. D., Turka L. A., Hypoxia inducible factor 1 alpha regulates T cell receptor signal transduction Proceedings of the National Academy of Sciences of the United States of America 2005 102 47 17071 17076 (Pubitemid 41692685)
84. Ben-Shoshan J., Maysel-Auslender S., Mor A., Keren G., George J., Hypoxia controls CD4+ CD25+ regulatory T cell homeostasis via hypoxia-inducible factor-1alpha European Journal of Immunology 2008 38 9 2412 2418
85. Shi L. Z., Wang R., Huang G., HIF1{alpha}-dependent glycolytic pathway orchestrates a metabolic checkpoint for the differentiation of TH17 and Treg cells Journal of Experimental Medicine 2011 208 7 1367 1376
86. Hori S., Nomura T., Sakaguchi S., Control of regulatory T cell development by the transcription factor Foxp3 Science 2003 299 5609 1057 1061 (Pubitemid 36222930)
87. Schabowsky R. H., Madireddi S., Sharma R., Yolcu E. S., Shirwan H., Targeting CD4+CD25+FoxP3+ regulatory T cells for the augmentation of cancer immunotherapy Current Opinion in Investigational Drugs 2007 8 12 1002 1008 (Pubitemid 350224326)
88. Makino Y., Nakamura H., Ikeda E., Ohnuma K., Yamauchi K., Yabe Y., Poellinger L., Okada Y., Morimoto C., Tanaka H., Hypoxia-inducible factor regulates survival of antigen receptor-driven T cells Journal of Immunology 2003 171 12 6534 6540 (Pubitemid 37532083)
89. Tabbekh M., Franciszkiewicz K., Haouas H., Lecluse Y., Benihoud K., Raman C., Mami-Chouaib F., Rescue of tumor-infiltrating lymphocytes from activation-induced cell death enhances the antitumor CTL response in CD5-deficient mice Journal of Immunology 2011 187 1 102 109
90. Bell B. D., Leverrier S., Weist B. M., Newton R. H., Arechiga A. F., Luhrs K. A., Morrissette N. S., Walsh C. M., FADD and caspase-8 control the outcome of autophagic signaling in proliferating T cells Proceedings of the National Academy of Sciences of the United States of America 2008 105 43 16677 16682
91. Pua H. H., Dzhagalov I., Chuck M., Mizushima N., He Y. W., A critical role for the autophagy gene Atg5 in T cell survival and proliferation Journal of Experimental Medicine 2007 204 1 25 31 (Pubitemid 46148752)
92. Hubbard V. M., Valdor R., Patel B., Singh R., Cuervo A. M., Macian F., Macroautophagy regulates energy metabolism during effector T cell activation Journal of Immunology 2010 185 12 7349 7357
93. Araki K., Turner A. P., Shaffer V. O., Gangappa S., Keller S. A., Bachmann M. F., Larsen C. P., Ahmed R., mTOR regulates memory CD8 T cell differentiation Nature 2009 460 7251 108 112
94. Rao R. R., Li Q., Odunsi K., Shrikant P. A., The mTOR kinase determines effector versus memory CD8+ T cell fate by regulating the expression of transcription factors T-bet and Eomesodermin Immunity 2010 32 1 67 78
95. He S., Kato K., Jiang J., Wahl D. R., Mineishi S., Fisher E. M., Murasko D. M., Glick G. D., Zhang Y., Characterization of the metabolic phenotype of rapamycin-treated CD8+ T cells with augmented ability to generate long-lasting memory cells PLoS One 2011 6 5, article e20107
96. Jubb A. M., Harris A. L., Biomarkers to predict the clinical efficacy of bevacizumab in cancer The Lancet Oncology 2010 11 12 1172 1183
97. Rizzieri D. A., Feldman E., Dipersio J. F., Gabrail N., Stock W., Strair R., Rivera V. M., Albitar M., Bedrosian C. L., Giles F. J., A phase 2 clinical trial of deforolimus (AP23573, MK-8669), a novel mammalian target of rapamycin inhibitor, in patients with relapsed or refractory hematologic malignancies Clinical Cancer Research 2008 14 9 2756 2762
98. Chan S., Scheulen M. E., Johnston S., Mross K., Cardoso F., Dittrich C., Eiermann W., Hess D., Morant R., Semiglazov V., Borner M., Salzberg M., Ostapenko V., Illiger H. J., Behringer D., Bardy-Bouxin N., Boni J., Kong S., Cincotta M., Moore L., Phase II study of temsirolimus (CCI-779), a novel inhibitor of mTOR, in heavily pretreated patients with locally advanced or metastatic breast cancer Journal of Clinical Oncology 2005 23 23 5314 5322 (Pubitemid 46206985)
99. 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 Clinical Cancer Research 2011 17 4 654 666
100. Chen N., Karantza-Wadsworth V., Role and regulation of autophagy in cancer Biochimica et Biophysica Acta 2009 1793 9 1516 1523
101. Egan D. F., Shackelford D. B., Mihaylova M. M., Phosphorylation of ULK1 (hATG1) by AMP-activated protein kinase connects energy sensing to mitophagy Science 2011 331 6016 456 461
102. Kim S. Y., Choi Y. J., Joung S. M., Lee B. H., Jung Y. S., Lee J. Y., Hypoxic stress up-regulates the expression of Toll-like receptor 4 in macrophages via hypoxia-inducible factor Immunology 2010 129 4 516 524
103. Kepp O., Galluzzi L., Martins I., Schlemmer F., Adjemian S., Michaud M., Sukkurwala A. Q., Menger L., Zitvogel L., Kroemer G., Molecular determinants of immunogenic cell death elicited by anticancer chemotherapy Cancer and Metastasis Reviews 2011 30 1 61 69