Functional and physical interaction between Bcl-XL and a BH3-like domain in Beclin-1

EMBO Journal

Volumn 26, Issue 10, 2007, Pages 2527-2539

  Maiuri, M Chiara ^a,b,c,d   Le Toumelin, Gaëtane ^e   Criollo, Alfredo ^a,b,c   Rain, Jean Christophe ^f   Gautier, Fabien ^g   Juin, Philippe ^g   Tasdemir, Ezgi ^a,b,c   Pierron, Gérard ^h   Troulinaki, Kostoula ⁱ   Tavernarakis, Nektarios ⁱ   Hickman, John A ^e   Geneste, Olivier ^e   Kroemer, Guido ^a,b,c  

^a Institut Gustave Roussy   (France)

^b INSTITUT GUSTAVE ROUSSY   (France)

^c UNIVERSITÉ PARIS SACLAY   (France)

^d UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^e INSTITUT DE RECHERCHES INTERNATIONALES SERVIER   (France)

^f Hybrigenics SA   (France)

^g UNIVERSITÉ DE NANTES   (France)

^h CNRS   (France)

ⁱ INSTITUTE OF COMPUTER SCIENCE   (Greece)

Author keywords

Apoptosis; Autophagy; Bax; Bcl 2; Mitochondria

Indexed keywords

4 [4 (4' CHLORO 2 BIPHENYLYLMETHYL) 1 PIPERAZINYL] N [4 [3 DIMETHYLAMINO 1 (PHENYLTHIOMETHYL)PROPYLAMINO] 3 NITROBENZENESULFONYL]BENZAMIDE; BECLIN 1; BH3 PROTEIN; ISOPROTEIN; PROTEIN; PROTEIN BAD; PROTEIN BCL 2; PROTEIN BCL XL; PROTEIN EGL1; UNCLASSIFIED DRUG;

ARTICLE; AUTOPHAGY; CONTROLLED STUDY; EMBRYO; GENE DELETION; HUMAN; HUMAN CELL; MOLECULAR DYNAMICS; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEOMICS;

ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; AUTOPHAGY; BCL-X PROTEIN; BLOTTING, WESTERN; CELLS, CULTURED; FIBROBLASTS; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; HELA CELLS; HUMANS; MEMBRANE PROTEINS; MICE; MUTATION; PRECIPITIN TESTS; PROTEIN STRUCTURE, TERTIARY; PROTEINS; RNA INTERFERENCE; TWO-HYBRID SYSTEM TECHNIQUES;

CAENORHABDITIS ELEGANS;

EID: 34248998801     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/sj.emboj.7601689     Document Type: Article

References (45)

1. Boya P, Gonzalez-Polo R-A, Casares N, Perfettini J-L, Dessen P, Larochette N, Metivier D, Meley D, Souquere S, Pierron G, Ohsumi Y, Codogno P, Kroemer G (2005) Inhibition of macroautophagy triggers apoptosis. Mol Cell Biol 25: 1025-1040
2. Brenner S (1974) The genetics of Caenorhabditis elegans. Genetics 77: 71-94
3. Byfield MP, Murray JT, Backer JM (2005) hVps34 is a nutrientregulated lipid kinase required for activation of p70 S6 kinase. J Biol Chem 280: 33076-33082
4. Chen R, Valencia I, Zhong F, McColl KS, Roderick HL, Bootman MD, Berridge MJ, Conway SJ, Holmes AB, Mignery GA, Velez P, Distelhorst CW (2004) Bcl-2 functionally interacts with inositol 1,4,5-trisphosphate receptors to regulate calcium release from the ER in response to inositol 1,4,5-trisphosphate. J Cell Biol 166: 193-203
5. Conradt B, Horvitz HR (1998) The C. elegans protein EGL-1 is required for programmed cell death and interacts with the Bcl-2-like protein CED-9. Cell 93: 519-529
6. Conradt B, Horvitz HR (1999) The TRA-1A sex determination protein of C. elegans regulates sexually dimorphic cell deaths by repressing the egl-1 cell death activator gene. Cell 98: 317-327
7. Criollo A, Maiuri MC, Tasdemir E, Vitale I, Fiebig AA, Andrews D, Molgo J, Diaz J, Lavandero S, Harper F, Pierron G, Di Stefano D, Rizzuto R, Szabadkai G, Kroemer G (2007) Regulation of autophagy by the inositol trisphosphate receptor. Cell Death Diff (in press)
8. Danial NN, Korsmeyer S (2004) Cell death: critical control points. Cell 116: 205-219
9. Fromont-Racine M, Rain JC, Legrain P (2002) Building protein-protein networks by two-hybrid mating strategy. Methods Enzymol 350: 513-524
10. Germain M, Shore GC (2003) Cellular distribution of Bcl-2 family proteins. Sci STKE 2003: pe10
11. Gonzalez-Polo RA, Boya P, Paulau A-L, Jalil A-A, Larochette N, Souquere S, Eskelinen EL, Pierron G, Saftig P, Kroemer G (2005) The apoptosis/autophagy paradox. Accumulation of autophagic vacuoles triggers apoptosis. J Cell Sci 118: 3091-3102
12. Gozuacik D, Kimchi A (2004) Autophagy as a cell death and tumor suppressor mechanism. Oncogene 23: 2891-2906
13. Harborth J, Elbashir SM, Bechert K, Tuschl T, Weber K (2001) Identification of essential genes in cultured mammalian cells using small interfering RNAs. J Cell Science 114: 4557-4565
14. Hoyer-Hansen M, Bastholm L, Mathiasen IS, Elling F, Jaattela M (2005) Vitamin D analog EB1089 triggers dramatic lysosomal changes and Beclin 1-mediated autophagic cell death. Cell Death Differ 12: 1297-1309
15. Jin Z, Gao F, Flagg T, Deng X (2004) Nicotine induces multi-site phosphorylation of Bad in association with suppression of apoptosis. J Biol Chem 279: 23837-23844
16. Kabeya Y, Mizushima N, Ueno T, Yamamoto A, Kirisako T, Noda T, Kominami E, Ohsumi Y, Yoshimori T (2000) LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J 19: 5720-5728
17. Konopleva M, Contractor R, Tsao T, Samudio I, Ruvolo PP, Kitada S, Deng X, Zhai D, Shi Y-X, Sneed T, Verhaegen M, Soengas M, Ruvolo VR, McQueen T, Schober WD, Watt JC, Jiffar T, Ling X, Marini FC, Harris D, Dietrich M, Estrov Z, McCubrey J, Stratford May W, Reed JC, Andreeff M (2006) Mechanisms of apoptosis sensitivity and resistance to the BH3 mimetic ABT-737 in acute myeloid leukemia. Cancer Cell 10: 375-388
18. Kroemer G, Jaattela M (2005) Lysosomes and autophagy in cell death control. Nat Rev Cancer 5: 886-897
19. Letai A, Bassik MC, Walensky LD, Sorcinelli MD, Weiler S, Korsmeyer SJ (2002) Distinct BH3 domains either sensitize or activate mitochondrial apoptosis, serving as prototype cancer therapeutics. Cancer Cell 2: 183-192
20. Liang XH, Jackson S, Seaman M, Brown K, Kempkes B, Hibshoosh H, Levine B (1999) Induction of autophagy and inhibition of tumorigenesis by beclin 1. Nature 402: 672-676
21. Lum JJ, Bauer DE, Kong M, Harris HM, Li C, Lindsten T, Thompson CB (2005) Growth factor regulation of autophagy and cell survival in the absence of apoptosis. Cell 120: 237-248
22. Melendez A, Talloczy Z, Seaman M, Eskelinen EL, Hall DH, Levine B (2003) Autophagy genes are essential for dauer development and life-span extension in C. elegans. Science 301: 1387-1391
23. Mizushima N, Yamamoto A, Matsui M, Yoshimori T, Ohsumi Y (2004) In vivo analysis of autophagy in response to nutrient starvation using transgenic mice expressing a fluorescent autophagosome marker. Mol Biol Cell 15: 1101-1111
24. Nobukuni T, Joaquin M, Roccio M, Dann SG, Kim SY, Gulati P, Byfield MP, Backer JM, Natt F, Bos JL, Zwartkruis FJ, Thomas G (2005) Amino acids mediate mTOR/raptor signaling through activation of class 3 phosphatidylinositol 3OH-kinase. Proc Natl Acad Sci USA 102: 14238-14243
25. Obeid M, Tesniere A, Ghiringhelli F, Fimia GM, Apetoh L, Perfettini JL, Castedo M, Mignot G, Panaretakis T, Casares N, Metivier D, Larochette N, van Endert P, Ciccosanti F, Piacentini M, Zitvogel L, Kroemer G (2007) Calreticulin exposure dictates the immunogenicity of cancer cell death. Nat Med 13: 54-61
26. L-beclin 1 peptide complex: Beclin 1 is a novel BH3-only protein. J Biol Chem [E-pub ahead of print]
27. Oltersdorf T, Elmore SW, Shoemaker AR, Armstrong RC, Augeri DJ, Belli BA, Bruncko M, Deckwerth TL, Dinges J, Hajduk PJ, Joseph MK, Kitada S, Korsmeyer SJ, Kunzer AR, Letai A, Li C, Mitten MJ, Nettesheim DG, Ng S, Nimmer PM, O'Connor JM, Oleksijew A, Petros AM, Reed JC, Shen W, Tahir SK, Thompson CB, Tomaselli KJ, Wang B, Wendt MD, Zhang H, Fesik SW, Rosenberg SH (2005) An inhibitor of Bcl-2 family proteins induces regression of solid tumours. Nature 435: 677-681
28. Ottilie S, Diaz JL, Chang J, Wilson G, Tuffo KM, Weeks S, McConnell M, Wang Y, Oltersdorf T, Fritz LC (1997) Structural and functional complementation of an inactive Bcl-2 mutant by Bax truncation. J Biol Chem 272: 16955-16961
29. Pattingre S, Tassa A, Qu X, Garuti R, Liang XH, Mizushima N, Packer M, Schneider MD, Levine B (2005) Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell 122: 927-939
30. Qu X, Yu J, Bhagat G, Furuya N, Hibshoosh H, Troxel A, Rosen J, Eskelinen EL, Mizushima N, Ohsumi Y, Cattoretti G, Levine B (2003) Promotion of tumorigenesis by heterozygous disruption of the beclin 1 autophagy gene. J Clin Invest 112: 1809-1820
31. Ranger AM, Zha J, Harada H, Datta SR, Danial NN, Gilmore AP, Kutok JL, Le Beau MM, Greenberg ME, Korsmeyer SJ (2003) Bad-deficient mice develop diffuse large B cell lymphoma. Proc Natl Acad Sci USA 100: 9324-9329
32. Ruvolo PP, Deng X, Carr BK, Stratford May W (1998) A functional role for mitochondrial protein kinase Cα in Bcl-2 phosphorylation and suppression of apoptosis. J Biol Chem 278: 25436-25442
33. Sarbassovdos D, Ali SM, Sabatini DM (2005) Growing roles for the mTOR pathway. Curr Opin Cell Biol 17: 596-603
34. Sarkar S, Floto RA, Berger Z, Imarisio S, Cordenier A, Pasco M, Cook LJ, Rubinsztein DC (2005) Lithium induces autophagy by inhibiting inositol monophosphatase. J Cell Biol 170: 1101-1111
35. Shimizu S, Kanaseki T, Mizushima N, Mizuta T, Arakawa-Kobayashi S, Thompson CB, Korsmeyer SJ, Tsujimoto Y (2004) A role of Bcl-2 family of proteins in non-apoptotic programmed cell death dependent on autophagy genes. Nature Cell Biology 6: 1221-1228
36. Shimizu S, Narita M, Tsujimoto Y (1999) Bcl-2 family proteins regulate the release of apoptogenic cytochrome c by the mitochondrial channel VDAC. Nature 399: 411-412
37. Shintani T, Klionsky DJ (2004) Autophagy in health and disease: a double-edged sword. Science 306: 990-995
38. Takacs-Vellai K, Vellai T, Puoti A, Passannante M, Wicky C, Streit A, Kovacs AL, Muller F (2005) Inactivation of the autophagy gene bec-1 triggers apoptotic cell death in C. elegans. Curr Biol 15: 1513-1517
39. Vahsen N, Cande C, Briere J-J, Benit P, Joza N, Mastroberardini PG, Pequignot M, Casares N, Larochette N, Metivier D, Feraud O, Debili N, Piacentini M, Penninger JM, Rustin P, Kroemer G (2004) AIF deficiency compromises oxidative phosphorylation. EMBO J 23: 4679-4689
40. Van Delft MF, Wei AH, Mason KD, Vandenberg CJ, Chen L, Czabotar PE, Willis SN, Scott CL, Day CL, Cory S, Adams JM, Roberts AW, Huang DCS (2006) The BH3 mimetic ABT-737 targets selective Bcl-2 proteins and efficiently induces apoptosis via Bak/Bax if Mcl-1 is neutralised. Cancer Cell 10: 389-399
41. Wei MC, Zong W-X, Cheng EH-Y, Lindsten T, Panoutsakopoulou V, Ross AJ, Roth KA, MacGregor GR, Thompson CB, Korsmeyer SJ (2001) Proapoptotic BAX and BAK: A requisite gateway to mitochondrial dysfunction and death. Science 292: 727-730
42. Yu L, Alva A, Su H, Dutt P, Freundt E, Welsh S, Baehrecke EH, Lenardo MJ (2004) Regulation of an ATG7-beclin 1 program of autophagic cell death by caspase-8. Science 304: 1500-1502
43. Yue Z, Jin S, Yang C, Levine AJ, Heintz N (2003) Beclin 1, an autophagy gene essential for early embryonic development, is a haploinsufficient tumor suppressor. Proc Natl Acad Sci USA 100: 15077-15082
44. Zeng X, Overmeyer JH, Maltese WA (2006) Functional specificity of the mammalian Beclin-Vps34 PI 3-kinase complex in macroautophagy versus endocytosis and lysosomal enzyme trafficking. J Cell Sci 119: 259-270
45. Zhu W, Cowie A, Wasfy GW, Penn LZ, Leber B, Andrews DW (1996) Bcl-2 mutants with restricted subcellular location reveal spatially distinct pathways for apoptosis in different cell types. EMBO J 15: 4130-4141