Inhibition of macroautophagy triggers apoptosis

Molecular and Cellular Biology

Volumn 25, Issue 3, 2005, Pages 1025-1040

  Boya, Patricia ^a,e   González Polo, Rosa Ana ^a   Casares, Noelia ^a   Perfettini, Jean Luc ^a   Dessen, Philippe ^a   Larochette, Nathanael ^a   Métivier, Didier ^a   Meley, Daniel ^b   Souquere, Sylvie ^b   Yoshimori, Tamotsu ^c   Pierron, Gérard ^b   Codogno, Patrice ^b   Kroemer, Guido ^a,d  

^a INSTITUT GUSTAVE ROUSSY   (France)

^b INSTITUT ANDRÉ LWOFF   (France)

^c NATIONAL INSTITUTE OF GENETICS   (Japan)

^d CNRS   (France)

^e CSIC   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

3 METHYLADENINE; BAFILOMYCIN A1; HYDROXYCHLOROQUINE; MONENSIN; SMALL INTERFERING RNA;

APOPTOSIS; ARTICLE; ATG10 GENE; ATG12 GENE; ATG5 GENE; ATG6 GENE; AUTOPHAGY; BECLIN 1 1 GENE; CELL CULTURE; CELL PROTECTION; CELL STRUCTURE; CELL ULTRASTRUCTURE; CELL VACUOLE; CONTROLLED STUDY; ENZYME INHIBITION; GENE TARGETING; HUMAN; HUMAN CELL; LYSOSOME; MEMBRANE POTENTIAL; MITOCHONDRIAL MEMBRANE; MOLECULAR INTERACTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PHAGOSOME; PRIORITY JOURNAL; REGULATOR GENE;

CYTOMEGALOVIRUS; MAMMALIA;

EID: 19944434059     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.25.3.1025-1040.2005     Document Type: Article

References (77)

1. Adams, J. M. 2003. Ways of dying: multiple pathways to apoptosis. Genes Dev. 17:2481-2495.
2. Beers, M. F. 1996. Inhibition of cellular processing of surfactant protein C by drugs affecting intracellular pH gradients. J. Biol. Chem. 271:14361-14370.
3. Belzacq, A. S., C. El Hamel, H. L. A. Vieira, I. Cohen, D. Haouzi, D. Métivier, P. Marchetti, V. Goldmacher, C. Brenner, and G. Kroemer. 2001. The adenine nucleotide translocator mediates the mitochondrial membrane permeabilization induced by lonidamine, arsenite and CD437. Oncogene 20:7579-7587.
4. Blommaart, E. F., U. Krause, J. P. Schellens, H. Vreeling-Sindelarova, and A. J. Meijer. 1997. The phosphatidylinositol 3-kinase inhibitors wortmannin and LY294002 inhibit autophagy in isolated rat hepatocytes. Eur. J. Biochem. 243:240-246.
5. Bowman, E. J., A. Siebers, and K. Altendorf. 1988. Bafilomycins: a class of inhibitors of membrane ATPases from microorganisms, animal cells, and plant cells. Proc. Natl. Acad. Sci. USA 85:7972-7976.
6. Boya, P., K. Andreau, D. Poncet, N. Zamzami, J.-L. Perfettini, D. Métivier, D. M. Ojcius, M. Jaattela, and G. Kroemer. 2003. Lysosomal membrane permeabilization induces cell death in a mitochondrion-dependent fashion. J. Exp. Med. 197:1323-1334.
7. Boya, P., R.-A. Gonzalez-Polo, D. Poncet, K. Andreau, T. Roumier, J.-L. Perfettini, and G. Kroemer. 2003. Mitochondrial membrane permeabilization is a critical step of lysosome-initiated apoptosis induced by hydroxychloroquine. Oncogene 22:3927-3936.
8. Boya, P., M. C. Morales, R.-A. González-Polo, K. Andreau, I. Gourdier, J.-L. Perfettini, N. Larochette, A. Deniaud, F. Baran-Marszak, R. Fagard, J. Feuillard, A. Asumendi, M. Raphael, B. Pau, C. Brenner, and G. Kroemer. 2003. The chemopreventive agent 4-hydroxyphenylretinamide induces apoptosis through a mitochondrial pathway regulated by proteins from the Bcl-2 family. Oncogene 22:6220-6230.
9. Bursch, W. 2001. The autophagosomal-lysosomal compartment in programmed cell death. Cell Death Differ. 8:569-581.
10. Castedo, M., K. Ferri, T. Roumier, D. Métivier, N. Zamzami, and G. Kroemer. 2002. Quantitation of mitochondrial alterations associated with apoptosis. J. Immunol. Methods 265:39-47.
11. 1 arrest and apoptosis in human Jurkat T cells by pentagalloylglucose through inhibiting proteasome activity and elevating p27Kip1, p21Cip1/WAF1, and Bax proteins. J. Biol. Chem. 279:13496-13505.
12. Cregan, S. P., A. Fortin, J. G. MacLaurin, S. M. Callaghan, F. Cecconi, D. S. Park, T. M. Dawson, G. Kroemer, and R. S. Slack. 2002. Apoptosis-inducing factor is involved in the regulation of caspase-independent neuronal cell death. J. Cell Biol. 158:507-517.
13. Edinger, A. L., and C. B. Thompson. 2003. Defective autophagy leads to cancer. Cancer Cell 4:422-424.
14. Elmore, S. P., T. Quian, S. F. Grissom, and J. J. Lemasters. 2002. The mitochondrial permeability transition initiates autophagy in rat hepatocytes. FASEB J. 15:2286-2287.
15. Ferri, K. F., E. Jacotot, J. Blanco, J. A. Esté, A. Zamzami, S. A. Susin, G. Brothers, J. C. Reed, J. M. Penninger, and G. Kroemer. 2000. Apoptosis control in syncytia induced by the HIV type 1-envelope glycoprotein complex: role of mitochondria and caspases. J. Exp. Med. 192:1081-1092.
16. Ferri, K. F., and G. K. Kroemer. 2001. Organelle-specific initiation of cell death pathways. Nat. Cell Biol. 3:E255-E263.
17. Fletcher, G. C., L. Xue, S. K. Passingham, and A. M. Tolkovsky. 2000. Death commitment is advanced by axotomy in sympathetic neurons. J. Cell Biol. 150:741-754.
18. Fuller, K. M., and E. A. Arriaga. 2003. Analysis of individual acidic organelles by capillary electrophoresis with laser-induced fluorescence detection facilitated by the endocytosis of fluorescently labeled microspheres. Anal. Chem. 75:2123-2130.
19. Goldmacher, V. S., L. M. Bartle, S. Skletskaya, C. A. Dionne, N. L. Kedersha, C. A. Vater, J. W. Han, R. J. Lutz, S. Watanabe, E. D. C. McFarland, E. D. Kieff, E. S. Mocarski, and T. Chittenden. 1999. A cytomegalovirus-encoded mitochondria-localized inhibitor of apoptosis structurally unrelated to Bcl-2. Proc. Natl. Acad. Sci. USA 96:12536-12541.
20. Gorski, S. M., S. Chittaranjan, E. D. Pleasance, J. D. Freeman, C. L. Anderson, R. J. Varhol, S. M. Coughlin, S. D. Zuyderduyn, S. J. Jones, and M. A. Marra. 2003. A SAGE approach to discovery of genes involved in autophagic cell death. Curr. Biol. 13:358-363.
21. Green, D. R., and G. Kroemer. 1998. The central executioner of apoptosis: mitochondria or caspases? Trends Cell Biol. 8:267-271.
22. Green, D. R., and J. C. Reed. 1998. Mitochondria and apoptosis. Science 281:1309-1312.
23. Grinde, B. 1983. Effect of carboxylic ionophores on lysosomal protein degradation in rat hepatocytes. Exp. Cell Res. 149:27-35.
24. Guimaraes, C. A., M. Benchimol, G. P. Amarante-Mendes, and R. Linden. 2003. Alternative programs of cell death in developing retinal tissue. J. Biol. Chem. 278:41938-41946.
25. Harborth, J., S. M. Elbashir, K. Bechert, T. Tuschl, and K. Weber. 2001. Identification of essential genes in cultured mammalian cells using small interfering RNAs. J. Cell Sci. 114:4557-4565.
26. Hernandez, L. D., M. Pypaert, R. A. Flavell, and J. E. Galán. 2003. A Salmonella protein causes macrophage cell death by inducing autophagy. J. Cell Biol. 163:1123-1131.
27. Inbal, B., S. Bialik, I. Sabanay, G. Shani, and A. Kimchi. 2002. DAP kinase and DRP-1 mediate membrane blebbing and the formation of autophagic vesicles during programmed cell death. J. Cell Biol. 157:455-468.
28. Jesenberger, V., and S. Jentsch. 2002. Deadly encounter: ubiquitin meets apoptosis. Nat. Rev. Mol. Cell Biol. 3:112-121.
29. Kabeya, Y., N. Mizushima, T. Ueno, A. Yamamoto, T. Kirisako, T. Noda, E. Kominami, Y. Ohsumi, and T. Yoshimori. 2000. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J. 19:5720-5728.
30. Kanzawa, T., I. M. Germano, T. Komata, H. Iton, Y. Kondo, and S. Kondo. 2004. Role of autophagy in temozolomide-induced cytotoxicity for malignant glioma cells. Cell Death Differ. 11:448-457.
31. Kanzawa, T., Y. Kondo, H. Ito, S. Kondo, and I. Germano. 2003. Induction of autophagic cell death in malignant glioma cells by arsenic trioxide. Cancer Res. 63:2103-2108.
32. Kerr, J. F. R., A. H. Wyllie, and A. R. Currie. 1972. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br. J. Cancer 26:239-257.
33. Kihara, A., Y. Kabeya, Y. Ohsumi, and T. Yoshimori. 2001. Beclin-phosphatidylinositol 3-kinase complex functions at the trans-Golgi network. EMBO Rep. 2:330-335.
34. Kim, J., and D. J. Klionsky. 2000. Autophagy, cytoplasm-to-vacuole targeting pathway, and pexophagy in yeast and mammalian cells. Annu. Rev. Biochem. 69:303-342.
35. Kimchi, A. 2001. A cell death-promoting kinase. Nat. Struct. Biol. 8:824-826.
36. Klionsky, D. J., J. M. Cregg, W. A. J. Dunn, Jr., S. D. Emr, Y. Sakai, I. V. Sandoval, A. Sibirny, S. Subramani, M. Thumm, M. Veenhuis, and Y. Ohsumi. 2003. A unified nomenclature for yeast autophagy-related genes. Dev. Cell 5:539-545.
37. Klionsky, D. J., and S. D. Emr. 2000. Autophagy as a regulated pathway of cellular degradation. Science 290:1717-1721.
38. Kroemer, G., and J. C. Reed. 2000. Mitochondrial control of cell death. Nat. Med. 6:513-519.
39. Larsen, K. E., E. A. Fon, T. G. Hastings, R. H. Edwards, and D. Sulzer. 2002. Methamphetamine-induced degeneration of dopaminergic neurons involves autophagy and upregulation of dopamine synthesis. J. Neurosci. 22:8951-8960.
40. Lassus, P., X. Opitz-Araya, and Y. Lazebnik. 2002. Requirement for caspase-2 in stress-induced apoptosis before mitochondrial permeabilization. Science 297:1352-1354.
41. Lee, C. Y., E. A. Clough, P. Yellon, T. M. Teslovich, D. A. Stephan, and E. H. Baehrecke. 2003. Genome-wide analyses of steroid- and radiation-triggered programmed cell death in Drosophila. Curr. Biol. 13:350-357.
42. Leist, M., and M. Jaattela. 2001. Four deaths and a funeral: from caspases to alternative mechanisms. Nat. Rev. Mol. Cell Biol. 2:589-598.
43. Lemasters, J. J., A.-L. Nieminen, T. Qian, L. C. Trost, S. P. Elmore, Y. Nishimura, R. A. Crowe, W. E. Cascio, C. A. Bradham, D. A. Brenner, and B. Herman. 1998. The mitochondrial permeability transition in cell death: a common mechanism in necrosis, apoptosis and autophagy. Biochim. Biophys. Acta 1366:177-196.
44. Leverkus, M., M. R. Sprick, T. Wachter, T. Mengling, B. Baumann, E. Serfling, E.-B. Bröcker, M. Goebeler, M. Neumann, and H. Walczak. 2003. Proteasome inhibition results in TRAIL sensitization of primary keratinocytes by removing the resistance-mediating block of effector caspase maturation. Mol. Cell. Biol. 23:777-790.
45. Liang, X. H., S. Jackson, M. Seaman, K. Brown, B. Kempkes, H. Hibshoosh, and B. Levine. 1999. Induction of autophagy and inhibition of tumorigenesis by beclin 1. Nature 402:672-676.
46. Liang, X. H., L. K. Kleeman, H. H. Jiang, G. Gordon, J. E. Goldman, G. Berry, B. Herman, and B. Levine. 1998. Protection against fatal Sindbis virus encephalitis by beclin, a novel Bcl-2-interacting protein. J. Virol. 72:8586-8596.
47. Lockshin, R. A., and Z. Zakeri. 2002. Caspase-independent cell deaths. Curr. Opin. Cell Biol. 14:727-733.
48. Martin, D. N., and E. H. Baehrecke. 2004. Caspases function in autophagic programmed cell death in Drosophila. Development 131:275-284.
49. Martinez, I., S. Chakrabarti, T. Hellevik, J. Morehead, K. Fowler, and N. W. Andrews. 2000. Synaptotagmin VII regulates Ca(2+)-dependent exocytosis of lysosomes in fibroblasts. J. Cell Biol. 148:1141-1149.
50. Mitsiades, N., C. S. Mitsiades, V. Poulaki, D. Chauhan, G. Fanourakis, X. Gu, C. Bailey, M. Joseph, T. A. Libermann, S. P. Treon, N. C. Munshi, P. G. Richardson, T. Hideshima, and K. C. Anderson. 2002. Molecular sequelae of proteasome inhibition in human multiple myeloma cells. Proc. Natl. Acad. Sci. USA 99:14374-14379.
51. Mizushima, N., A. Yamamoto, M. Hatano, Y. Kobayashi, Y. Kabeya, K. Suzuki, T. Tokuhisa, Y. Ohsumi, and T. Yoshimori. 2001. Dissection of autophagosome formation using Apg5-deficient mouse embryonic stem cells. J. Cell Biol. 152:657-668.
52. Nakagawa, T., H. Zhu, N. Morishima, E. Li, J. Xu, B. A. Yankner, and J. Yuan. 2000. Caspase-12 mediates endoplasmic-reticulum-specific apoptosis and cytotoxicity by amyloid-beta. Nature 403:98-103.
53. Nemoto, T., I. Tanida, E. Tanida-Miyake, N. Minematsu-Ikeguchi, M. Yokota, M. Ohsumi, T. Ueno, and E. Kominami. 2003. The mouse APG10 homologue, an authentic E2-like enzyme for Apg12p conjugation, facilitates MAP-LC3 modification. J. Biol. Chem. 278:39517-39526.
54. Ogier-Denis, E., J. J. Houri, C. Bauvy, and P. Codogno. 1996. Guanine nucleotide exchange on heterotrimeric Gi3 protein controls autophagic sequestration in HT-29 cells. J. Biol. Chem. 271:28593-28600.
55. Opipari, A. W. J., L. Tan, A. E. Boitano, D. R. Sorenson, A. Aurora, and J. R. Liu. 2004. Resveratrol-induced autophagocytosis in ovarian cancer cells. Cancer Res. 64:696-703.
56. Paglin, S., T. Hollister, T. Delohery, N. Hackett, M. McMahill, E. Sphicas, D. Domingo, and J. Yahalom. 2001. A novel response of cancer cells to radiation involves autophagy and formation of acidic vesicles. Cancer Res. 61:439-444.
57. Patterson, G. H., and J. Lippincott-Schwartz. 2002. A photoactivatable GFP for selective photolabeling of proteins and cells. Science 297:1873-1877.
58. Pattingre, S., C. Bauvy, and P. Codogno. 2003. Amino acids interfere with the ERK1/2-dependent control of macroautophagy by controlling the activation of Raf-1 in human colon cancer HT-29 cells. J. Biol. Chem. 278:16667-16674.
59. Plas, D. R., and C. B. Thompson. 2002. Cell metabolism in the regulation of programmed cell death. Trends Endocrinol. Metab. 13:75-78.
60. Qu, X., J. Yu, G. Bhagat, N. Furuya, H. Hibshoosh, A. Troxel, J. Rosen, E. L. Eskelinen, N. Mizushima, Y. Ohsumi, G. Cattoretti, and B. Levine. 2003. Promotion of tumorigenesis by heterozygous disruption of the beclin 1 autophagy gene. J. Clin. Investig. 112:1809-1820.
61. Reggiori, F., and D. J. Klionsky. 2002. Autophagy in the eukaryotic cell. Eukaryot. Cell 1:11-21.
62. Saeki, K., A. Yuo, E. Okuma, Y. Yazaki, S. A. Susin, G. Kroemer, and F. Takaku. 2000. Bcl-2 down-regulation causes autophagy in a caspase-independent manner in human leukemic HL60 cells. Cell Death Differ. 7:1263-1269.
63. Seglen, P. O., and P. B. Gordon. 1982. 3-Methyladenine: specific inhibitor of autophagic/lysosomal protein degradation in isolated rat hepatocytes. Proc. Natl. Acad. Sci. USA 79:1889-1892.
64. Sullivan, P. G., N. B. Dragicevic, J. H. Deng, Y. Bai, E. Dimayuga, Q. Ding, Q. Chen, A. J. Bruce-Keller, and J. N. Keller. 2004. Proteasome inhibition alters neural mitochondrial homeostasis and mitochondria turnover. J. Biol. Chem. 279:20699-20707.
65. Tanaka, Y., G. Guhde, A. Suter, E. L. Eskelinen, D. Hartmann, R. Lullmann-Rauch, P. M. Janssen, J. Blanz, K. von Figura, and P. Saftig. 2000. Accumulation of autophagic vacuoles and cardiomyopathy in LAMP-2-deficient mice. Nature 406:902-906.
66. Tsukada, M., and Y. Ohsumi. 1993. Isolation and characterization of autophagy-defective mutants of Saccharomyces cerevisiae. FEBS Lett. 333:169-174.
67. Voorhees, P. M., E. C. Dees, B. O'Neil, and R. Z. Orlowski. 2003. The proteasome as a target for cancer therapy. Clin. Cancer Res. 9:6316-6325.
68. Wang, X. 2002. The expanding role of mitochondria in apoptosis. Genes Dev. 15:2922-2933.
69. Wei, M. C., W.-X. Zong, E. H.-Y. Cheng, T. Lindsten, V. Panoutsakopoulou, A. J. Ross, K. A. Roth, G. R. MacGregor, C. B. Thompson, and S. J. Korsmeyer. 2001. Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death. Science 292:727-730.
70. Xue, L., G. C. Fletcher, and A. M. Tolkovsky. 2001. Mitochondria are selectively eliminated from eukaryotic cells after blockade of caspases during apoptosis. Curr. Biol. 6:361-365.
71. Yamamoto, A., Y. Tagawa, T. Yoshimori, Y. Moriyama, R. Masaki, and Y. Tashiro. 1998. Bafilomycin A1 prevents maturation of autophagic vacuoles by inhibiting fusion between autophagosomes and lysosomes in rat hepatoma cell line, H-4-II-E cells. Cell Struct. Funct. 23:33-42.
72. Yanagisawa, H., T. Miyashita, Y. Nakano, and D. Yamamoto. 2003. HSpin1, a transmembrane protein interacting with Bcl-2/Bcl-xL, induces a caspase-independent autophagic cell death. Cell Death Differ. 10:798-807.
73. Yoshimori, T. 2004. Autophagy: a regulated bulk degradation process inside cells. Biochem. Biophys. Res. Commun. 313:453-458.
74. Yoshimori, T., A. Yamamoto, Y. Moriyama, M. Futai, and Y. Tashiro. 1991. Bafilomycin A1, a specific inhibitor of vacuolar-type H(+)-ATPase. inhibits acidification and protein degradation in lysosomes of cultured cells. J. Biol. Chem. 266:17707-17712.
75. Yue, Z., A. Horton, M. Bravin, P. L. DeJager, F. Selimi, and N. Heintz. 2002. A novel protein complex linking the δ2 glutamate receptor and autophagy: implications for neurodegeneration in lurcher mice. Neuron 35:921-933.
76. Yue, Z., S. Jin, C. Yang, A. J. Levine, and N. Heintz. 2003. Beclin 1, an autophagy gene essential for early embryonic development, is a haploinsufficient tumor suppressor. Proc. Natl. Acad. Sci. USA 100:15077-15082.
77. Zamzami, N., D. Métivier, and G. Kroemer. 2000. Quantitation of the mitochondrial transmembrane potential in cells and in isolated mitochondria. Methods Enzymol. 322:208-213.