Glucose-starved cells do not engage in prosurvival autophagy

Journal of Biological Chemistry

Volumn 288, Issue 42, 2013, Pages 30387-30398

  Ramírez Peinado, Silvia ^a   León Annicchiarico, Clara Lucía ^a   Galindo Moreno, Javier ^a   Iurlaro, Raffaella ^a   Caro Maldonado, Alfredo ^a,d   Prehn, Jochen H M ^b   Ryan, Kevin M ^c   Muñoz Pinedo, Cristina ^a  

^a BELLVITGE BIOMEDICAL RESEARCH INSTITUTE IDIBELL   (Spain)

^b Department of Physiology and Medical Physics ^*  (Ireland)

^c BEATSON INSTITUTE FOR CANCER RESEARCH   (United Kingdom)

^d DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APOPTOTIC; AUTOPHAGY; GLUCOSE DEPRIVATION; MAMMALIAN CELLS; NECROTIC CELL DEATHS; NUTRIENT DEPRIVATION;

CELL DEATH; CHEMICAL COMPOUNDS;

GLUCOSE;

3 METHYLADENINE; AUTOPHAGY PROTEIN 7; BECLIN 1; CELL PROTEIN; CHLOROQUINE; DEOXYGLUCOSE; GLUCOSE; MAMMALIAN TARGET OF RAPAMYCIN; PROTEIN BAX; PROTEIN P62; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; ATG7 GENE; AUTOPHAGY; BECLIN 1 GENE; CELL STRAIN; CELL SURVIVAL; CONTROLLED STUDY; FIBROBLAST; GENE; GENE SILENCING; GLUCOSE DEPRIVATION; HELA CELL; HUMAN; HUMAN CELL; P62 GENE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; STARVATION;

APOPTOSIS; AUTOPHAGY; GLUCOSE; MTOR; NECROSIS (NECROTIC DEATH);

ADENINE; ANIMALS; ANTIMETABOLITES; APOPTOSIS REGULATORY PROTEINS; AUTOPHAGY; CELL SURVIVAL; CYSTEINE ENDOPEPTIDASES; DEOXYGLUCOSE; FIBROBLASTS; GLUCOSE; HELA CELLS; HUMANS; MEMBRANE PROTEINS; MICE; MICROTUBULE-ASSOCIATED PROTEINS; RNA-BINDING PROTEINS; SWEETENING AGENTS; TOR SERINE-THREONINE KINASES; TRANSCRIPTION FACTORS; UBIQUITIN-ACTIVATING ENZYMES;

EID: 84886883442     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.490581     Document Type: Article

References (37)

1. Singh, R., and Cuervo, A. M. (2011) Autophagy in the cellular energetic balance. Cell Metab. 13, 495-504
2. Mizushima, N., Yoshimori, T., and Ohsumi, Y. (2011) The role of Atg proteins in autophagosome formation. Annu. Rev. Cell Dev. Biol. 27, 107-132
3. Boya, P., Gonźlez-Polo, R. A., Casares, N., Perfettini, J. L., Dessen, P., Larochette, N., Métivier, D., Meley, D., Souquere, S., Yoshimori, T., Pierron, G., Codogno, P., and Kroemer, G. (2005) Inhibition of macroautophagy triggers apoptosis. Mol. Cell Biol. 25, 1025-1040
4. DiPaola, R. S., Dvorzhinski, D., Thalasila, A., Garikapaty, V., Doram, D., May, M., Bray, K., Mathew, R., Beaudoin, B., Karp, C., Stein, M., Foran, D. J., and White, E. (2008) Therapeutic starvation and autophagy in prostate cancer: A new paradigm for targeting metabolism in cancer therapy. Prostate 68, 1743-1752
5. Xi, H., Kurtoglu, M., Liu, H., Wangpaichitr, M., You, M., Liu, X., Savaraj, N., and Lampidis, T. (2011) 2-Deoxy-D-glucose activates autophagy via endoplasmic reticulum stress rather than ATP depletion. Cancer Chemother. Pharmacol. 67, 899-910
6. Altman, B. J., Jacobs, S. R., Mason, E. F., Michalek, R. D., MacIntyre, A. N., Coloff, J. L., Ilkayeva, O., Jia, W., He, Y. W., and Rathmell, J. C. (2011) Autophagy is essential to suppress cell stress and to allow BCR-Abl-mediated leukemogenesis. Oncogene 30, 1855-1867
7. Ramírez-Peinado, S., Alćzar-Limones, F., Lagares-Tena, L., El Mjiyad, N., Caro-Maldonado, A., Tirado, O. M., and Muñoz-Pinedo, C. (2011) 2-deoxyglucose induces noxa-dependent apoptosis in alveolar rhabdomyosarcoma. Cancer Res. 71, 6796-6806
8. Kurtoglu, M., Gao, N., Shang, J., Maher, J. C., Lehrman, M. A., Wangpaichitr, M., Savaraj, N., Lane, A. N., and Lampidis, T. J. (2007) Under normoxia, 2-deoxy-D-glucose elicits cell death in select tumor types not by inhibition of glycolysis but by interfering withN-linked glycosylation. Mol. Cancer Ther. 6, 3049-3058
9. Egan, D. F., Shackelford, D. B., Mihaylova, M. M., Gelino, S., Kohnz, R. A., Mair, W., Vasquez, D. S., Joshi, A., Gwinn, D. M., Taylor, R., Asara, J. M., Fitzpatrick, J., Dillin, A., Viollet, B., Kundu, M., Hansen, M., and Shaw, R. J. (2011) Phosphorylation of ULK1 (hATG1) by AMP-activated protein kinase connects energy sensing to mitophagy. Science 331, 456-461
10. Kim, J., Kundu, M., Viollet, B., and Guan, K. L. (2011) AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nat. Cell Biol. 13, 132-141
11. Degenhardt, K., Mathew, R., Beaudoin, B., Bray, K., Anderson, D., Chen, G., Mukherjee, C., Shi, Y., Gélinas, C., Fan, Y., Nelson, D. A., Jin, S., and White, E. (2006) Autophagy promotes tumor cell survival and restricts necrosis, inflammation, and tumorigenesis. Cancer Cell 10, 51-64
12. El Mjiyad, N., Caro-Maldonado, A., Ramírez-Peinado, S., and Muñoz-Pinedo, C. (2011) Sugar-free approaches to cancer cell killing. Oncogene 30, 253-264
13. Caro-Maldonado, A., and Munoz-Pinedo, C. (2011) Dying for something to eat: how cells respond to starvation. Open Cell Signal J. 3, 42-51
14. Wei, M. C., Zong, W. X., Cheng, E. H., Lindsten, T., Panoutsakopoulou, V., Ross, A. J., Roth, K. A., MacGregor, G. R., Thompson, C. B., and Korsmeyer, S. J. (2001) Proapoptotic BAX and BAK: A Requisite Gateway to Mitochondrial Dysfunction and Death. Science 292, 727-730
15. Sanjuan, M. A., Dillon, C. P., Tait, S. W., Moshiach, S., Dorsey, F., Connell, S., Komatsu, M., Tanaka, K., Cleveland, J. L., Withoff, S., and Green, D. R. (2007) Toll-like receptor signalling in macrophages links the autophagy pathway to phagocytosis. Nature 450, 1253-1257
16. Kimura, S., Noda, T., and Yoshimori, T. (2007) Dissection of the autophagosome maturation process by a novel reporter protein, tandem fluorescent- tagged LC3. Autophagy 3, 452-460
17. Caro-Maldonado, A., Tait, S. W., Ramírez-Peinado, S., Ricci, J. E., Fabregat, I., Green, D. R., and Muñoz-Pinedo, C. (2010) Glucose deprivation induces an atypical form of apoptosis mediated by caspase-8 in Bax-, Bakdeficient cells. Cell Death Differ. 17, 1335-1344
18. Wang, Y., Singh, R., Massey, A. C., Kane, S. S., Kaushik, S., Grant, T., Xiang, Y., Cuervo, A. M., and Czaja, M. J. (2008) Loss of macroautophagy promotes or prevents fibroblast apoptosis depending on the death stimulus. J. Biol. Chem. 283, 4766-4777
19. Fujita, N., Hayashi-Nishino, M., Fukumoto, H., Omori, H., Yamamoto, A., Noda, T., and Yoshimori, T. (2008) An Atg4B mutant hampers the lipidation of LC3 paralogues and causes defects in autophagosome closure. Mol. Biol. Cell 19, 4651-4659
20. Ullman, E., Fan, Y., Stawowczyk, M., Chen, H. M., Yue, Z., and Zong, W. X. (2008) Autophagy promotes necrosis in apoptosis-deficient cells in response to ER stress. Cell Death Differ. 15, 422-425
21. Matsui, Y., Takagi, H., Qu, X., Abdellatif, M., Sakoda, H., Asano, T., Levine, B., and Sadoshima, J. (2007) Distinct roles of autophagy in the heart during ischemia and reperfusion: roles of AMP-activated protein kinase and beclin 1 in mediating autophagy. Circ. Res. 100, 914-922
22. Germain, M., Nguyen, A. P., Le Grand, J. N., Arbour, N., Vanderluit, J. L., Park, D. S., Opferman, J. T., and Slack, R. S. (2011) MCL-1 is a stress sensor that regulates autophagy in a developmentally regulated manner.EMBOJ. 30, 395-407
23. Cheong, H., Lindsten, T., Wu, J., Lu, C., and Thompson, C. B. (2011) Ammonia-induced autophagy is independent of ULK1/ULK2 kinases. Proc. Natl. Acad. Sci. U.S.A. 108, 11121-11126
24. Kim, J., Kim, Y. C., Fang, C., Russell, R. C., Kim, J. H., Fan, W., Liu, R., Zhong, Q., and Guan, K. L. (2013) Differential regulation of distinct Vps34 complexes by AMPK in nutrient stress and autophagy. Cell 152, 290-303
25. Liu, T. J., Koul, D., LaFortune, T., Tiao, N., Shen, R. J., Maira, S. M., Garcia-Echevrria, C., and Yung, W. K. (2009) NVP-BEZ235, a novel dual phosphatidylinositol 3-kinase/mammalian target of rapamycin inhibitor, elicits multifaceted antitumor activities in human gliomas. Mol. Cancer Ther. 8, 2204-2210
26. Aki, T., Yamaguchi, K., Fujimiya, T., and Mizukami, Y. (2003) Phosphoinositide 3-kinase accelerates autophagic cell death during glucose deprivation in the rat cardiomyocyte-derived cell line H9c2. Oncogene 22, 8529-8535
27. Sato, K., Tsuchihara, K., Fujii, S., Sugiyama, M., Goya, T., Atomi, Y., Ueno, T., Ochiai, A., and Esumi, H. (2007) Autophagy is activated in colorectal cancer cells and contributes to the tolerance to nutrient deprivation. Cancer Res. 67, 9677-9684
28. Ezaki, J., Matsumoto, N., Takeda-Ezaki, M., Komatsu, M., Takahashi, K., Hiraoka, Y., Taka, H., Fujimura, T., Takehana, K., Yoshida, M., Iwata, J., Tanida, I., Furuya, N., Zheng, D. M., Tada, N., Tanaka, K., Kominami, E., and Ueno, T. (2011) Liver autophagy contributes to the maintenance of blood glucose and amino acid levels. Autophagy 7, 727-736
29. Efeyan, A., Zoncu, R., Chang, S., Gumper, I., Snitkin, H., Wolfson, R. L., Kirak, O., Sabatini, D. D., and Sabatini, D. M. (2013) Regulation of mTORC1 by the Rag GTPases is necessary for neonatal autophagy and survival. Nature 493, 679-683
30. Kuma, A., Hatano, M., Matsui, M., Yamamoto, A., Nakaya, H., Yoshimori, T., Ohsumi, Y., Tokuhisa, T., and Mizushima, N. (2004) The role of autophagy during the early neonatal starvation period. Nature 432, 1032-1036
31. McAlpine, F., Williamson, L. E., Tooze, S. A., and Chan, E. Y. (2013) Regulation of nutrient-sensitive autophagy by uncoordinated 51-like kinases 1 and 2. Autophagy 9, 361-373
32. Xi, H., Barredo, J. C., Merchan, J. R., and Lampidis, T. J. (2013) Endoplasmic reticulum stress induced by 2-deoxyglucose but not glucose starvation activates AMPK through CaMKK leading to autophagy. Biochem. Pharmacol. 85, 1463-1477
33. Moruno-Manchón, J. F., Pérez-Jiménez, E., and Knecht, E. (2013) Glucose induces autophagy under starvation conditions by a p38 MAPK-dependent pathway. Biochem. J. 449, 497-506
34. Ravikumar, B., Stewart, A., Kita, H., Kato, K., Duden, R., and Rubinsztein, D. C. (2003) Raised intracellular glucose concentrations reduce aggregation and cell death caused by mutant huntingtin exon 1 by decreasing mTOR phosphorylation and inducing autophagy. Hum. Mol. Genet. 12, 985-994
35. Decuypere, J. P., Kindt, D., Luyten, T., Welkenhuyzen, K., Missiaen, L., De Smedt, H., Bultynck, G., and Parys, J. B. (2013) mTOR-controlled autophagy requires intracellular Ca2 signaling. PLoS One 8, e61020
36. Rodríguez-Vargas, J. M., Ruiz-Magaña, M. J., Ruiz-Ruiz, C., Majuelos- Melguizo, J., Peralta-Leal, A., Rodríguez, M. I., Muñoz-Ǵmez, J. A., de Almodóvar, M. R., Siles, E., Rivas, A. L., Jäättela, M., and Oliver, F. J. (2012) ROS-induced DNA damage and PARP-1 are required for optimal induction of starvation-induced autophagy. Cell Res. 22, 1181-1198
37. Puyal, J., Vaslin, A., Mottier, V., and Clarke, P. G. (2009) Postischemic treatment of neonatal cerebral ischemia should target autophagy. Ann. Neurol. 66, 378-389