Bcl2-associated athanogene 3 interactome analysis reveals a new role in modulating proteasome activity

Molecular and Cellular Proteomics

Volumn 12, Issue 10, 2013, Pages 2804-2819

  Chen, Ying ^a,b   Yang, Li Na ^b,c,d   Cheng, Li ^c,d   Tu, Shun ^c,d   Guo, Shu Juan ^c,d   Le, Huang Ying ^c   Xiong, Qian ^a   Mo, Ran ^a,b   Li, Chong Yang ^a,b   Jeong, Jun Seop ^e   Jiang, Lizhi ^e   Blackshaw, Seth ^e   Bi, Li Jun ^f   Zhu, Heng ^e   Tao, Sheng Ce ^c,d,g   Ge, Feng ^a  

^a INSTITUTE OF HYDROBIOLOGY   (China)

^b INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

^c Chinese National Human Genome Center at Shanghai   (China)

^d School of Medicine   (China)

^e JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f INSTITUTE OF BIOPHYSICS   (China)

^g SHANGHAI JIAO TONG UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BCL2 ASSOCIATED ATHANOGENE 3 PROTEIN; CHAPERONE; NUCLEIC ACID BINDING PROTEIN; PROTEASOME; PROTEIN BCL 2; TRANSCRIPTION FACTOR; TRANSFERASE; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; AUTOPHAGY; CELL FUNCTION; CELL MATURATION; CELL SURVIVAL; CONTROLLED STUDY; ENZYME ACTIVITY; FEMALE; GENE SILENCING; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN MICROARRAY; PROTEIN PROTEIN INTERACTION; QUANTITATIVE ANALYSIS; SIGNAL TRANSDUCTION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; APOPTOSIS REGULATORY PROTEINS; CELL LINE, TUMOR; HUMANS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN ARRAY ANALYSIS; PROTEIN INTERACTION MAPPING; PROTEOME;

EID: 84885154570     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M112.025882     Document Type: Article

References (75)

1. Doong, H., Vrailas, A., and Kohn, E. C. (2002) What's in the "BAG"?- A functional domain analysis of the BAG-family proteins. Cancer Lett. 188, 25-32
2. Kabbage, M., and Dickman, M. B. (2008) The BAG proteins: a ubiquitous family of chaperone regulators. Cell. Mol. Life Sci. 65, 1390-1402
3. Rosati, A., Graziano, V., De Laurenzi, V., Pascale, M., and Turco, M. C. (2011) BAG3: a multifaceted protein that regulates major cell pathways. Cell Death Dis. 2, e141
4. Doong, H., Rizzo, K., Fang, S., Kulpa, V., Weissman, A. M., and Kohn, E. C. (2003) CAIR-1/BAG-3 abrogates heat shock protein-70 chaperone complex-mediated protein degradation: accumulation of poly-ubiquitinated Hsp90 client proteins. J. Biol. Chem. 278, 28490-28500
5. Hishiya, A., Kitazawa, T., and Takayama, S. (2010) BAG3 and Hsc70 interact with actin capping protein CapZ to maintain myofibrillar integrity under mechanical stress. Circ. Res. 107, 1220-1231
6. Doong, H., Price, J., Kim, Y. S., Gasbarre, C., Probst, J., Liotta, L. A., Blanchette, J., Rizzo, K., and Kohn, E. (2000) CAIR-1/BAG-3 forms an EGF-regulated ternary complex with phospholipase C-gamma and Hsp70/Hsc70. Oncogene 19, 4385-4395
7. Lee, J. H., Takahashi, T., Yasuhara, N., Inazawa, J., Kamada, S., and Tsujimoto, Y. (1999) Bis, a Bcl-2-binding protein that synergizes with Bcl-2 in preventing cell death. Oncogene 18, 6183-6190
8. Behl, C. (2011) BAG3 and friends: co-chaperones in selective autophagy during aging and disease. Autophagy 7, 795-798
9. Gamerdinger, M., Hajieva, P., Kaya, A. M., Wolfrum, U., Hartl, F. U., and Behl, C. (2009) Protein quality control during aging involves recruitment of the macroautophagy pathway by BAG3. EMBO J. 28, 889-901
10. Kyratsous, C. A., and Silverstein, S. J. (2008) The co-chaperone BAG3 regulates Herpes Simplex Virus replication. Proc. Natl. Acad. Sci. U. S. A. 105, 20912-20917
11. Kyratsous, C. A., and Silverstein, S. J. (2007) BAG3, a host cochaperone, facilitates varicella-zoster virus replication. J. Virol. 81, 7491-7503
12. Baud, V., and Karin, M. (2009) Is NF-kappaB a good target for cancer therapy? Hopes and pitfalls. Nat. Rev. Drug Discov. 8, 33-40
13. Zhang, L., Zhang, Z. P., Zhang, X. E., Lin, F. S., and Ge, F. (2010) Quantitative proteomics analysis reveals BAG3 as a potential target to suppress severe acute respiratory syndrome coronavirus replication. J. Virol. 84, 6050-6059
14. Selbach, M., and Mann, M. (2006) Protein interaction screening by quantitative immunoprecipitation combined with knockdown (QUICK). Nat. Methods 3, 981-983
15. Ge, F., Li, W. L., Bi, L. J., Tao, S. C., Zhang, Z. P., and Zhang, X. E. (2010) Identification of novel 14-3-3zeta interacting proteins by quantitative immunoprecipitation combined with knockdown (QUICK). J. Proteome Res. 9, 5848-5858
16. Meixner, A., Boldt, K., Van Troys, M., Askenazi, M., Gloeckner, C. J., Bauer, M., Marto, J. A., Ampe, C., Kinkl, N., and Ueffing, M. (2011) A QUICK screen for Lrrk2 interaction partners-leucine-rich repeat kinase 2 is involved in actin cytoskeleton dynamics. Mol. Cell. Proteomics 10, M110.001172
17. Zheng, P., Zhong, Q., Xiong, Q., Yang, M., Zhang, J., Li, C., Bi, L. J., and Ge, F. (2012) QUICK identification and SPR validation of signal transducers and activators of transcription 3 (Stat3) interacting proteins. J. Proteomics 75, 1055-1066
18. Chen, C. S., Korobkova, E., Chen, H., Zhu, J., Jian, X., Tao, S. C., He, C., and Zhu, H. (2008) A proteome chip approach reveals new DNA damage recognition activities in Escherichia coli. Nat. Methods 5, 69-74
19. Tao, S. C., Chen, C. S., and Zhu, H. (2007) Applications of protein microarray technology. Comb. Chem. High Throughput Screen. 10, 706-718
20. Zhu, H., Bilgin, M., Bangham, R., Hall, D., Casamayor, A., Bertone, P., Lan, N., Jansen, R., Bidlingmaier, S., Houfek, T., Mitchell, T., Miller, P., Dean, R. A., Gerstein, M., and Snyder, M. (2001) Global analysis of protein activities using proteome chips. Science 293, 2101-2105
21. Yang, L., Guo, S., Li, Y., Zhou, S., and Tao, S. (2011) Protein microarrays for systems biology. Acta Biochim. Biophys. Sin. (Shanghai) 43, 161-171
22. Jeong, J. S., Rho, H. S., and Zhu, H. (2011) A functional protein microarray approach to characterizing posttranslational modifications on lysine residues. Methods Mol. Biol. 723, 213-223
23. Lin, Y. Y., Lu, J. Y., Zhang, J., Walter, W., Dang, W., Wan, J., Tao, S. C., Qian, J., Zhao, Y., Boeke, J. D., Berger, S. L., and Zhu, H. (2009) Protein acetylation microarray reveals that NuA4 controls key metabolic target regulating gluconeogenesis. Cell 136, 1073-1084
24. Jeong, J. S., Jiang, L., Albino, E., Marrero, J., Rho, H. S., Hu, J., Hu, S., Vera, C., Bayron-Poueymiroy, D., Rivera-Pacheco, Z. A., Ramos, L., Torres-Castro, C., Qian, J., Bonaventura, J., Boeke, J. D., Yap, W. Y., Pino, I., Eichinger, D. J., Zhu, H., and Blackshaw, S. (2012) Rapid identification of monospecific monoclonal antibodies using a human proteome microarray. Mol. Cell. Proteomics 11, O111.016253
25. Schnack, C., Danzer, K. M., Hengerer, B., and Gillardon, F. (2008) Protein array analysis of oligomerization-induced changes in alpha-synuclein protein-protein interactions points to an interference with Cdc42 effector proteins. Neuroscience 154, 1450-1457
26. Virok, D. P., Simon, D., Bozso, Z., Rajko, R., Datki, Z., Balint, E., Szegedi, V., Janaky, T., Penke, B., and Fulop, L. (2011) Protein array based interactome analysis of amyloid-beta indicates an inhibition of protein translation. J. Proteome Res. 10, 1538-1547
27. Haas, W., Faherty, B. K., Gerber, S. A., Elias, J. E., Beausoleil, S. A., Bakalarski, C. E., Li, X., Villen, J., and Gygi, S. P. (2006) Optimization and use of peptide mass measurement accuracy in shotgun proteomics. Mol. Cell. Proteomics 5, 1326-1337
28. Park, S. K., Venable, J. D., Xu, T., and Yates, J. R., 3rd (2008) A quantitative analysis software tool for mass spectrometry-based proteomics. Nat. Methods 5, 319-322
29. Mi, H., Guo, N., Kejariwal, A., and Thomas, P. D. (2007) PANTHER version 6: protein sequence and function evolution data with expanded representation of biological pathways. Nucleic Acids Res. 35, D247-D252
30. Yu, X., Ivanic, J., Memisevic, V., Wallqvist, A., and Reifman, J. (2011) Categorizing biases in high-confidence high-throughput protein-protein interaction data sets. Mol. Cell. Proteomics 10, M111.012500
31. Ashburner, M., Ball, C. A., Blake, J. A., Botstein, D., Butler, H., Cherry, J. M., Davis, A. P., Dolinski, K., Dwight, S. S., Eppig, J. T., Harris, M. A., Hill, D. P., Issel-Tarver, L., Kasarskis, A., Lewis, S., Matese, J. C., Richardson, J. E., Ringwald, M., Rubin, G. M., and Sherlock, G. (2000) Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat. Genet. 25, 25-29
32. Kanehisa, M., and Goto, S. (2000) KEGG: Kyoto Encyclopedia of Genes and Genomes. Nucleic Acids Res. 28, 27-30
33. Finn, R. D., Tate, J., Mistry, J., Coggill, P. C., Sammut, S. J., Hotz, H. R., Ceric, G., Forslund, K., Eddy, S. R., Sonnhammer, E. L., and Bateman, A. (2008) The Pfam protein families database. Nucleic Acids Res. 36, D281-D288
34. Huang da, W., Sherman, B. T., and Lempicki, R. A. (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4, 44-57
35. Huang da, W., Sherman, B. T., and Lempicki, R. A. (2009) Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res. 37, 1-13
36. Maere, S., Heymans, K., and Kuiper, M. (2005) BiNGO: a Cytoscape plugin to assess overrepresentation of gene ontology categories in biological networks. Bioinformatics 21, 3448-3449
37. Jensen, L. J., Kuhn, M., Stark, M., Chaffron, S., Creevey, C., Muller, J., Doerks, T., Julien, P., Roth, A., Simonovic, M., Bork, P., and von Mering, C. (2009) STRING 8- A global view on proteins and their functional interactions in 630 organisms. Nucleic Acids Res. 37, D412-D416
38. Bader, G. D., and Hogue, C. W. (2003) An automated method for finding molecular complexes in large protein interaction networks. BMC Bioinformatics 4, 2
39. Shannon, P., Markiel, A., Ozier, O., Baliga, N. S., Wang, J. T., Ramage, D., Amin, N., Schwikowski, B., and Ideker, T. (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 13, 2498-2504
40. Adams, J. (2003) The proteasome: structure, function, and role in the cell. Cancer Treat. Rev. 29 Suppl 1, 3-9
41. Glas, R., Bogyo, M., McMaster, J. S., Gaczynska, M., and Ploegh, H. L. (1998) A proteolytic system that compensates for loss of proteasome function. Nature 392, 618-622
42. Grune, T., Reinheckel, T., Joshi, M., and Davies, K. J. (1995) Proteolysis in cultured liver epithelial cells during oxidative stress. Role of the multicatalytic proteinase complex, proteasome. J. Biol. Chem. 270, 2344-2351
43. Wang, X., Hessner, M. J., Wu, Y., Pati, N., and Ghosh, S. (2003) Quantitative quality control in microarray experiments and the application in data filtering, normalization and false positive rate prediction. Bioinformatics 19, 1341-1347
44. Fontanella, B., Birolo, L., Infusini, G., Cirulli, C., Marzullo, L., Pucci, P., Turco, M. C., and Tosco, A. (2010) The co-chaperone BAG3 interacts with the cytosolic chaperonin CCT: new hints for actin folding. Int. J. Biochem. Cell Biol. 42, 641-650
45. Fuchs, M., Poirier, D. J., Seguin, S. J., Lambert, H., Carra, S., Charette, S. J., and Landry, J. (2010) Identification of the key structural motifs involved in HspB8/HspB6-Bag3 interaction. Biochem. J. 425, 245-255
46. Jiang, D., Jia, Y., and Jarrett, H. W. (2011) Transcription factor proteomics: identification by a novel gel mobility shift-three-dimensional electrophoresis method coupled with southwestern blot and high-performance liquid chromatography-electrospray-mass spectrometry analysis. J. Chromatogr. A 1218, 7003-7015
47. McCollum, A. K., Casagrande, G., and Kohn, E. C. (2010) Caught in the middle: the role of Bag3 in disease. Biochem. J. 425, e1-e3
48. von Mering, C., Huynen, M., Jaeggi, D., Schmidt, S., Bork, P., and Snel, B. (2003) STRING: a database of predicted functional associations between proteins. Nucleic Acids Res. 31, 258-261
49. Matta, A., Siu, K. M., and Ralhan, R. (2012) 14-3-3 zeta as novel molecular target for cancer therapy. Expert Opin. Ther. Targets epub pubmed/22512284
50. Besteiro, S., Brooks, C. F., Striepen, B., and Dubremetz, J. F. (2011) Autophagy protein Atg3 is essential for maintaining mitochondrial integrity and for normal intracellular development of Toxoplasma gondii tachyzoites. PLoS Pathog. 7, e1002416
51. Keutgens, A., Zhang, X., Shostak, K., Robert, I., Olivier, S., Vanderplasschen, A., Chapelle, J. P., Viatour, P., Merville, M. P., Bex, F., Gothot, A., and Chariot, A. (2010) BCL-3 degradation involves its polyubiquitination through a FBW7-independent pathway and its binding to the proteasome subunit PSMB1. J. Biol. Chem. 285, 25831-25840
52. Sebolt-Leopold, J. S., and Herrera, R. (2004) Targeting the mitogen-activated protein kinase cascade to treat cancer. Nat. Rev. Cancer 4, 937-947
53. Whitesell, L., and Lindquist, S. (2009) Inhibiting the transcription factor HSF1 as an anticancer strategy. Expert Opin. Ther. Targets 13, 469-478
54. Du, Z. X., Zhang, H. Y., Meng, X., Gao, Y. Y., Zou, R. L., Liu, B. Q., Guan, Y., and Wang, H. Q. (2009) Proteasome inhibitor MG132 induces BAG3 expression through activation of heat shock factor 1. J. Cell. Physiol. 218, 631-637
55. Wang, H. Q., Liu, H. M., Zhang, H. Y., Guan, Y., and Du, Z. X. (2008) Transcriptional upregulation of BAG3 upon proteasome inhibition. Biochem. Biophys. Res. Commun. 365, 381-385
56. Ge, F., Bi, L. J., Tao, S. C., Xu, X. D., Zhang, Z. P., Kitazato, K., and Zhang, X. E. (2011) Proteomic analysis of multiple myeloma: current status and future perspectives. Proteomics Clin. Appl. 5, 30-37
57. Elliott, M. H., Smith, D. S., Parker, C. E., and Borchers, C. (2009) Current trends in quantitative proteomics. J. Mass Spectrom. 44, 1637-1660
58. Yu, X., Ivanic, J., Memisevic, V., Wallqvist, A., and Reifman, J. (2011) Categorizing biases in high-confidence high-throughput protein-protein interaction data sets. Mol. Cell. Proteomics, M111.012500
59. Guerrero, C., Tagwerker, C., Kaiser, P., and Huang, L. (2006) An integrated mass spectrometry-based proteomic approach: quantitative analysis of tandem affinity-purified in vivo cross-linked protein complexes (QTAX) to decipher the 26 S proteasome-interacting network. Mol. Cell. Proteomics 5, 366-378
60. Zong, C., Gomes, A. V., Drews, O., Li, X., Young, G. W., Berhane, B., Qiao, X., French, S. W., Bardag-Gorce, F., and Ping, P. (2006) Regulation of murine cardiac 20S proteasomes: role of associating partners. Circ. Res. 99, 372-380
61. Bousquet-Dubouch, M. P., Baudelet, E., Guerin, F., Matondo, M., Uttenweiler-Joseph, S., Burlet-Schiltz, O., and Monsarrat, B. (2009) Affinity purification strategy to capture human endogenous proteasome complexes diversity and to identify proteasome-interacting proteins. Mol. Cell. Proteomics 8, 1150-1164
62. Huang, L, and Burlingame, A. L. (2005) Comprehensive mass spectrometric analysis of the 20S proteasome complex. Methods Enzymol. 405, 187-236
63. Aiken, C. T., Kaake, R. M., Wang, X., and Huang, L. (2011) Oxidative stress-mediated regulation of proteasome complexes. Mol. Cell. Proteomics 10, R110.006924
64. Guerrero, C, Milenkovic, T., Przulj, N., Kaiser, P., and Huang, L. (2008) Characterization of the proteasome interaction network using a QTAX-based tag-team strategy and protein interaction network analysis. Proc. Natl. Acad. Sci. U. S. A. 105, 13333-13338
65. Kwak, J., Workman, J. L, and Lee, D. (2011) The proteasome and its regulatory roles in gene expression. Biochim. Biophys. Acta 1809, 88-96
66. Driscoll, J. J., Minter, A., Driscoll, D. A., and Burris, J. K. (2011) The ubiquitin+proteasome protein degradation pathway as a therapeutic strategy in the treatment of solid tumor malignancies. Anticancer Agents Med. Chem. 11, 242-246
67. Ruschak, A. M., Slassi, M., Kay, L. E., and Schimmer, A. D. (2011) Novel proteasome inhibitors to overcome bortezomib resistance. J. Natl. Cancer Inst. 103, 1007-1017
68. Calderwood, S. K., Khaleque, M. A., Sawyer, D. B., and Ciocca, D. R. (2006) Heat shock proteins in cancer: chaperones of tumorigenesis. Trends Biochem. Sci. 31, 164-172
69. Richter, K., Haslbeck, M., and Buchner, J. (2010) The heat shock response: life on the verge of death. Mol. Cell 40, 253-266
70. Lanneau, D., Brunet, M., Frisan, E., Solary, E., Fontenay, M., and Garrido, C. (2008) Heat shock proteins: essential proteins for apoptosis regulation. J. Cell. Mol. Med. 12, 743-761
71. Gentilella, A., and Khalili, K. (2011) BAG3 expression in glioblastoma cells promotes accumulation of ubiquitinated clients in an Hsp70-dependent manner. J. Biol. Chem. 286, 9205-9215
72. Yang, Z., and Klionsky, D. J. (2010) Eaten alive: a history of macroautophagy. Nat. Cell Biol. 12, 814-822
73. Xie, Z., and Klionsky, D. J. (2007) Autophagosome formation: core machinery and adaptations. Nat. Cell Biol. 9, 1102-1109
74. Carra, S. (2009) The stress-inducible HspB8-Bag3 complex induces the eIF2alpha kinase pathway: implications for protein quality control and viral factory degradation? Autophagy 5, 428-429
75. Carra, S., Brunsting, J. F., Lambert, H., Landry, J., and Kampinga, H. H. (2009) HspB8 participates in protein quality control by a non-chaperonelike mechanism that requires eIF2{alpha} phosphorylation. J. Biol. Chem. 284, 5523-5532