Interaction of Bcl-2 with the autophagy-related GABAA receptor-associated protein (GABARAP): Biophysical characterization and functional implications

Journal of Biological Chemistry

Volumn 288, Issue 52, 2013, Pages 37204-37215

  Ma, Peixiang ^a,b   Schwarten, Melanie ^a,b   Schneider, Lars ^c   Boeske, Alexandra ^a   Henke, Nadine ^c   Lisak, Dmitrij ^c   Weber, Stephan ^a   Mohrlüder, Jeannine ^a   Stoldt, Matthias ^a,b   Strodel, Birgit ^a   Methner, Axel ^b,c   Hoffmann, Silke ^a   Weiergräber, Oliver H ^a   Willbold, Dieter ^a,b  

^a FORSCHUNGSZENTRUM JÜLICH   (Germany)

^b HEINRICH HEINE UNIVERSITY   (Germany)

^c UNIVERSITY MEDICAL CENTER MAINZ   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOPHAGY; BIOPHYSICAL CHARACTERIZATION; CANCER THERAPY; DOWN-REGULATION; LIPIDATION; RECEPTOR-ASSOCIATED PROTEINS;

BIOCHEMISTRY; BIOLOGY;

CELL DEATH;

4 AMINOBUTYRIC ACID RECEPTOR; AUTOPHAGY RELATED 4 AMINOBUTYRIC ACID RECEPTOR ASSOCIATED PROTEIN; AUTOPHAGY RELATED PROTEIN 8; CELL PROTEIN; GLANDULAR EPITHELIAL CELL PROTEIN 1; PROTEIN BCL 2; UBIQUITIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; AUTOPHAGOSOME; BINDING AFFINITY; CONTROLLED STUDY; EMBRYO; HYDROPHOBICITY; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS INHIBITION; RAT;

EID: 84891448023     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.528067     Document Type: Article

References (64)

1. Mizushima, N., Levine, B., Cuervo, A. M., and Klionsky, D. J. (2008) Autophagy fights disease through cellular self-digestion. Nature 451, 1069-1075
2. Tanida, I., Ueno, T., and Kominami, E. (2004) LC3 conjugation system in mammalian autophagy. Int. J. Biochem. Cell Biol. 36, 2503-2518
3. Ichimura, Y., Kirisako, T., Takao, T., Satomi, Y., Shimonishi, Y., Ishihara, N., Mizushima, N., Tanida, I., Kominami, E., Ohsumi, M., Noda, T., and Ohsumi, Y. (2000) A ubiquitin-like system mediates protein lipidation. Nature 408, 488-492
4. Kirisako, T., Baba, M., Ishihara, N., Miyazawa, K., Ohsumi, M., Yoshimori, T., Noda, T., and Ohsumi, Y. (1999) Formation process of autophagosome is traced with Apg8/Aut7p in yeast. J. Cell Biol. 147, 435-446
5. Kabeya, Y., Mizushima, N., Yamamoto, A., Oshitani-Okamoto, S., Ohsumi, Y., and Yoshimori, T. (2004) LC3, GABARAP and GATE16 localize to autophagosomal membrane depending on form-II formation. J. Cell Sci. 117, 2805-2812
6. Weidberg, H., Shvets, E., Shpilka, T., Shimron, F., Shinder, V., and Elazar, Z. (2010) LC3 and GATE-16/GABARAP subfamilies are both essential yet act differently in autophagosome biogenesis. EMBO J. 29, 1792-1802
7. Mohrlüder, J., Schwarten, M., and Willbold, D. (2009) Structure and potential function of γ-aminobutyrate type A receptor-associated protein. FEBS J. 276, 4989-5005
8. Klebig, C., Seitz, S., Arnold, W., Deutschmann, N., Pacyna-Gengelbach, M., Scherneck, S., and Petersen, I. (2005) Characterization of γ-aminobutyric acid type A receptor-associated protein, a novel tumor suppressor, showing reduced expression in breast cancer. Cancer Res. 65, 394-400
9. Roberts, S. S., Mendonça-Torres, M. C., Jensen, K., Francis, G. L., and Vasko, V. (2009) GABA receptor expression in benign and malignant thyroid tumors. Pathol. Oncol. Res. 15, 645-650
10. Mohrlüder, J., Hoffmann, Y., Stangler, T., Hänel, K., and Willbold, D. (2007) Identification of clathrin heavy chain as a direct interaction partner for the γ-aminobutyric acid type A receptor associated protein. Biochemistry 46, 14537-14543
11. Mohrlüder, J., Stangler, T., Hoffmann, Y., Wiesehan, K., Mataruga, A., and Willbold, D. (2007) Identification of calreticulin as a ligand of GABARAP by phage display screening of a peptide library. FEBS J. 274, 5543-5555
12. A receptorassociated protein. J. Mol. Biol. 381, 1320-1331
13. Thielmann, Y., Weiergräber, O. H., Mohrlüder, J., and Willbold, D. (2009) Structural framework of the GABARAP-calreticulin interface. Implications for substrate binding to endoplasmic reticulum chaperones. FEBS J. 276, 1140-1152
14. Thielmann, Y., Weiergräber, O. H., Mohrlüder, J., and Willbold, D. (2009) Structural characterization of GABARAP-ligand interactions. Mol. Biosyst. 5, 575-579
15. Ma, P., Mohrlüder, J., Schwarten, M., Stoldt, M., Singh, S. K., Hartmann, R., Pacheco, V., and Willbold, D. (2010) Preparation of a functional GABARAP-lipid conjugate in nanodiscs and its investigation by solution NMR spectroscopy. Chem Bio Chem 11, 1967-1970
16. Schwarten, M., Mohrlüder, J., Ma, P., Stoldt, M., Thielmann, Y., Stangler, T., Hersch, N., Hoffmann, B., Merkel, R., and Willbold, D. (2009) Nix directly binds to GABARAP. As possible crosstalk between apoptosis and autophagy. Autophagy 5, 690-698
17. Imazu, T., Shimizu, S., Tagami, S., Matsushima, M., Nakamura, Y., Miki, T., Okuyama, A., and Tsujimoto, Y. (1999) Bcl-2/E1B 19 kDa-interacting protein 3-like protein (Bnip3L) interacts with bcl-2/Bcl-xL and induces apoptosis by altering mitochondrial membrane permeability. Oncogene 18, 4523-4529
18. L and induces cell death independent of a Bcl-2 homology 3 (BH3) domain at both mitochondrial and nonmitochondrial sites. J. Biol. Chem. 275, 1439-1448
19. Novak, I., Kirkin, V., McEwan, D. G., Zhang, J., Wild, P., Rozenknop, A., Rogov, V., Löhr, F., Popovic, D., Occhipinti, A., Reichert, A. S., Terzic, J., Dötsch, V., Ney, P. A., and Dikic I. (2010) Nix is a selective autophagy receptor for mitochondrial clearance. EMBO Rep. 11, 45-51
20. 15N resonance assignments of human GABA receptor associated protein. J. Biomol. NMR 21, 183-184
21. Opferman, J. T., Letai, A., Beard, C., Sorcinelli, M. D., Ong, C. C., and Korsmeyer, S. J. (2003) Development and maintenance of B and T lymphocytes requires antiapoptotic MCL-1. Nature 426, 671-676
22. Petros, A. M., Medek, A., Nettesheim, D. G., Kim, D. H., Yoon, H. S., Swift, K., Matayoshi, E. D., Oltersdorf, T., and Fesik, S. W. (2001) Solution structure of the antiapoptotic protein bcl-2. Proc. Natl. Acad. Sci. U.S.A. 98, 3012-3017
23. Conus, S., Kaufmann, T., Fellay, I., Otter, I., Rossé, T., and Borner, C. (2000) Bcl-2 is a monomeric protein. Prevention of homodimerization by structural constraints. EMBO J. 19, 1534-1544
24. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J., and Bax, A. (1995) NMRPipe. A multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 6, 277-293
25. Johnson, B. A., and Blevins, R. A. (1994) NMR view. A computer program for the visualization and analysis of NMR data. J. Biomol. NMR4, 603-614
26. Vranken, W. F., Boucher, W., Stevens, T. J., Fogh, R. H., Pajon, A., Llinas, M., Ulrich, E. L., Markley, J. L., Ionides, J., and Laue, E. D. (2005) The CCPN data model for NMR spectroscopy. Development of a software pipeline. Proteins 59, 687-696
27. Lescop, E., Schanda, P., and Brutscher, B. (2007) A set of BEST tripleresonance experiments for time-optimized protein resonance assignment. J. Magn. Reson. 187, 163-169
28. Grzesiek, S., and Bax, A. (1992) Improved 3D triple resonance NMR techniques applied to a 31 kDa protein. J. Magn. Reson. 96, 432-440
29. Keller, R. (2004) The Computer-Aided Resonance Assignment Tutorial, CANTINA Verlag, Goldau
30. Dominguez, C., Boelens, R., and Bonvin, A. M. (2003) HADDOCK. A protein-protein docking approach based on biochemical or biophysical information. J. Am. Chem. Soc. 125, 1731-1737
31. de Vries, S. J., van Dijk, A. D., Krzeminski, M., van Dijk, M., Thureau, A., Hsu, V., Wassenaar, T., and Bonvin, A. M. (2007) HADDOCK versus HADDOCK. New features and performance of HADDOCK2.0 on the CAPRI targets. Proteins 69, 726-733
32. Wales, D. J., and Doye, J. P. K. (1997) Global optimization by basin-hopping and the lowest energy structures of Lennard-Jones clusters containing up to 110 atoms. J. Phys. Chem. A 101, 5111-5116
33. Wales, D. J. (2003) Energy Landscapes, Cambridge University Press, Cambridge
34. MacKerell, A. D., Bashford, D., Bellott, M., Dunbrack, R. L., Evanseck, J. D., Field, M. J., Fischer, S., Gao, J., Guo, H., Ha, S., Joseph-McCarthy, D., Kuchnir, L., Kuczera, K., Lau, F. T. K., Mattos, C., Michnick, S., Ngo, T., Nguyen, D. T., Prodhom, B., Reiher, W. E., Roux, B., Schlenkrich, M., Smith, J. C., Stote, R., Straub, J., Watanabe, M., Wiorkiewicz-Kuczera, J., Yin, D., and Karplus, M. (1998) All-atom empirical potential for molecular modeling and dynamics studies of proteins. J. Phys. Chem. B 102, 3586-3616
35. Trisciuoglio, D., De Luca, T., Desideri, M., Passeri, D., Gabellini, C., Scarpino, S., Liang, C., Orlandi, A., and Del Bufalo, D. (2013) Removal of the BH4 domain from Bcl-2 protein triggers an autophagic process that impairs tumor growth. Neoplasia 15, 315-327
36. Singh R., Kaushik, S., Wang, Y., Xiang, Y., Novak, I., Komatsu, M., Tanaka, K., Cuervo, A. M., and Czaja, M. J. (2009) Autophagy regulates lipid metabolism. Nature 458, 1131-1135
37. A receptor-associated protein GABARAP. Implications for biological function and its regulation. J. Biol. Chem. 277, 13363-13366
38. Thielmann, Y., Mohrlüder, J., Koenig, B. W., Stangler, T., Hartmann, R., Becker, K., Höltje, H. D., and Willbold, D. (2008) An indole-binding site is a major determinant of the ligand specificity of the GABA type Areceptorassociated protein GABARAP. Chem Bio Chem 9, 1767-1775
39. Li, Z., and Scheraga, H. A. (1987) Monte Carlo-minimization approach to the multiple-minima problem in protein folding. Proc. Natl. Acad. Sci. U.S.A. 84, 6611-6615
40. Gotow, T., Shibata, M., Kanamori, S., Tokuno, O., Ohsawa, Y., Sato, N., Isahara, K., Yayoi, Y., Watanabe, T., Leterrier, J. F., Linden, M., Kominami, E., and Uchiyama, Y. (2000) Selective localization of Bcl-2 to the inner mitochondrial and smooth endoplasmic reticulum membranes in mammalian cells. Cell Death Differ. 7, 666-674
41. Otter, I., Conus, S., Ravn, U., Rager, M., Olivier, R., Monney, L., Fabbro, D., and Borner, C. (1998) The binding properties and biological activities of Bcl-2 and Bax in cells exposed to apoptotic stimuli. J. Biol. Chem. 273, 6110-6120
42. Levine, B., Sinha, S., and Kroemer, G. (2008) Bcl-2 family members. Dual regulators of apoptosis and autophagy. Autophagy 4, 600-606
43. Pattingre, S., Tassa, A., Qu, X., Garuti, R., Liang, X. H., Mizushima, N., Packer, M., Schneider, M. D., and Levine, B. (2005) Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell 122, 927-939
44. Pankiv, S., Clausen, T. H., Lamark, T., Brech, A., Bruun, J. A., Outzen, H., Øvervatn, A., Bjørkøy, G., and Johansen, T. (2007) p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J. Biol. Chem. 282, 24131-24145
45. Noda, N. N., Ohsumi, Y., and Inagaki, F. (2010) Atg8-family interacting motif crucial for selective autophagy. FEBS Lett. 584, 1379-1385
46. Thielmann, Y., Weiergräber, O. H., Ma, P., Schwarten, M., Mohrlüder, J., and Willbold, D. (2009) Comparative modeling of human NSF reveals a possible binding mode of GABARAP and GATE-16. Proteins 77, 637-646
47. Souers, A. J., Leverson, J. D., Boghaert, E. R., Ackler, S. L., Catron, N. D., Chen, J., Dayton, B. D., Ding, H., Enschede, S. H., Fairbrother, W. J., Huang, D. C., Hymowitz, S. G., Jin, S., Khaw, S. L., Kovar, P. J., Lam, L. T., Lee, J., Maecker, H. L., Marsh, K. C., Mason, K. D., Mitten, M. J., Nimmer, P. M., Oleksijew, A., Park, C. H., Park, C. M., Phillips, D. C., Roberts, A. W., Sampath, D., Seymour, J. F., Smith, M. L., Sullivan, G. M., Tahir, S. K., Tse, C., Wendt, M. D., Xiao, Y., Xue, J. C., Zhang, H., Humerickhouse, R. A., Rosenberg, S. H., and Elmore, S. W. (2013) ABT-199, a potent and selective BCL-2 inhibitor, achieves antitumor activity while sparing platelets. Nat. Med. 19, 202-208
48. L, but not Bcl-2, to the mitochondrial outer membrane. J. Cell Biol. 160, 53-64
49. Wang, N. S., Unkila, M. T., Reineks, E. Z., and Distelhorst, C. W. (2001) Transient expression of wild-type or mitochondrially targeted Bcl-2 induces apoptosis, whereas transient expression of endoplasmic reticulumtargeted Bcl-2 is protective against Bax-induced cell death. J. Biol. Chem. 276, 44117-44128
50. A receptor-associated protein-phospholipid conjugates. J. Biol. Chem. 279, 36268-36276
51. Noda, T., Fujita, N., and Yoshimori, T. (2009) The late stages of autophagy. How does the end begin? Cell Death Differ. 16, 984-990
52. Li, M., Hou, Y., Wang, J., Chen, X., Shao, Z. M., and Yin, X. M. (2011) Kinetics comparisons of mammalian Atg4 homologues indicate selective preferences toward diverse Atg8 substrates. J. Biol. Chem. 286, 7327-7338
53. Hemelaar, J., Lelyveld, V. S., Kessler, B. M., and Ploegh, H. L. (2003) A single protease, Apg4B, is specific for the autophagy-related ubiquitin-like proteins GATE-16, MAP1-LC3, GABARAP, and Apg8L. J. Biol. Chem. 278, 51841-51850
54. Satoo, K., Noda, N. N., Kumeta, H., Fujioka, Y., Mizushima, N., Ohsumi, Y., and Inagaki, F. (2009) The structure of Atg4B-LC3 complex reveals the mechanism of LC3 processing and delipidation during autophagy. EMBO J. 28, 1341-1350
55. Noda, N. N., Satoo, K., Fujioka, Y., Kumeta, H., Ogura, K., Nakatogawa, H., Ohsumi, Y., and Inagaki, F. (2011) Structural basis of Atg8 activation by a homodimeric E1, Atg7. Mol. Cell 44, 462-475
56. Criollo, A., Maiuri, M. C., Tasdemir, E., Vitale, I., Fiebig, A. A., Andrews, D., Molgó, J., Díaz, J., Lavandero, S., Harper, F., Pierron, G., di Stefano, D., Rizzuto, R., Szabadkai, G., and Kroemer, G. (2007) Regulation of autophagy by the inositol trisphosphate receptor. Cell Death Differ. 14, 1029-1039
57. Wei, Y., Sinha, S., and Levine, B. (2008) Dual role of JNK1-mediated phosphorylation of Bcl-2 in autophagy and apoptosis regulation. Autophagy 4, 949-951
58. 2 homeostasis and apoptosis. EMBO J. 23, 1207-1216
59. Wei, Y., Pattingre, S., Sinha, S., Bassik, M., and Levine, B. (2008) JNK1-mediated phosphorylation of Bcl-2 regulates starvation-induced autophagy. Mol. Cell 30, 678-688
60. Wild, P., Farhan, H., McEwan, D. G., Wagner, S., Rogov, V. V., Brady, N. R., Richter, B., Korac, J., Waidmann, O., Choudhary, C., Dötsch, V., Bumann, D., and Dikic, I. (2011) Phosphorylation of the autophagy receptor optineurin restricts Salmonella growth. Science 333, 228-233
61. Zhu, Y., Massen, S., Terenzio, M., Lang, V., Chen-Lindner, S., Eils, R., Novak, I., Dikic, I., Hamacher-Brady, A., and Brady, N. R. (2013) Modulation of serines 17 and 24 in the LC3-interacting region of Bnip3 determines pro-survival mitophagy versus apoptosis. J. Biol. Chem. 288, 1099-1113
62. Stehmeier, P., and Muller, S. (2009) Phospho-regulated SUMO interaction modules connect the SUMO system to CK2 signaling. Mol. Cell 33, 400-409
63. Hallin, U., Kondo, E., Ozaki, Y., Hagberg, H., Shibasaki, F., and Blomgren, K. (2006) Bcl-2 phosphorylation in the BH4 domain precedes caspase-3 activation and cell death after neonatal cerebral hypoxic-ischemic injury. Neurobiol. Dis. 21, 478-486
64. Oh, S., Xiaofei, E., Ni, D., Pirooz, S. D., Lee, J. Y., Lee, D., Zhao, Z., Lee, S., Lee, H., Ku, B., Kowalik, T., Martin, S. E., Oh, B. H., Jung, J. U., and Liang, C. (2011) Downregulation of autophagy by Bcl-2 promotes MCF7 breast cancer cell growth independent of its inhibition of apoptosis. Cell Death Differ. 18, 452-464