Structural analysis of the Sil1-Bip complex reveals the mechanism for Sil1 to function as a nucleotide-exchange factor

Biochemical Journal

Volumn 438, Issue 3, 2011, Pages 447-455

  Yan, Ming ^a   Li, Jingzhi ^a   Sha, Bingdong ^a  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

Bip; Crystal structure; Heat shock protein of 70 Da (Hsp70); Nucleotide exchange factor (NEF); Sil1

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATASE; GLUCOSE REGULATED PROTEIN 78; GUANINE NUCLEOTIDE EXCHANGE FACTOR; MULTIPROTEIN COMPLEX; MUTANT PROTEIN; NUCLEOTIDE BINDING PROTEIN; PROTEIN SIL1; SIL1 BIP COMPLEX PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; BINDING SITE; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME ACTIVITY; HYDROGEN BOND; MOLECULE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN STRUCTURE; STRUCTURE ANALYSIS;

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATASES; AMINO ACID SEQUENCE; BINDING SITES; FUNGAL PROTEINS; HSP70 HEAT-SHOCK PROTEINS; MEMBRANE TRANSPORT PROTEINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; PROTEIN CONFORMATION; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EUKARYOTA;

EID: 80052177927     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20110500     Document Type: Article

References (50)

1. Wickner, W. and Schekman, R. (2005) Protein translocation across biological membranes. Science 310, 1452-1456 (Pubitemid 41746334)
2. Shan, S. O. and Walter, P. (2005) Co-translational protein targeting by the signal recognition particle. FEBS Lett. 579, 921-926
3. Osborne, A. R., Rapoport, T. A. and van den Berg, B. (2005) Protein translocation by the Sec61/SecY channel. Annu. Rev. Cell Dev. Biol. 21, 529-550
4. Kramer, G., Boehringer, D., Ban, N. and Bukau, B. (2009) The ribosome as a platform for co-translational processing, folding and targeting of newly synthesized proteins. Nat. Struct. Mol. Biol. 16, 589-597
5. Schroder, M., Clark, R., Liu, C. Y. and Kaufman, R. J. (2004) The unfolded protein response represses differentiation through the RPD3-SIN3 histone deacetylase. EMBO J. 23, 2281-2292 (Pubitemid 38833237)
6. Bukau, B. and Horwich, A. L. (1998) The Hsp70 and Hsp60 chaperone machines. Cell 92, 351-366
7. Hartl, F. U. and Hayer-Hartl, M. (2009) Converging concepts of protein folding in vitro and in vivo. Nat. Struct. Mol. Biol. 16, 574-581
8. Ni, M. and Lee, A. S. (2007) ER chaperones in mammalian development and human diseases. FEBS Lett. 581, 3641-3651 (Pubitemid 47082516)
9. Weitzmann, A., Baldes, C., Dudek, J. and Zimmermann, R. (2007) The heat shock protein 70 molecular chaperone network in the pancreatic endoplasmic reticulum - a quantitative approach. FEBS J. 274, 5175-5187 (Pubitemid 47485662)
10. Hellman, R., Vanhove, M., Lejeune, A., Stevens, F. J. and Hendershot, L. M. (1999) The in vivo association of BiP with newly synthesized proteins is dependent on the rate and stability of folding and not simply on the presence of sequences that can bind to BiP. J. Cell Biol. 144, 21-30
11. Fewell, S. W., Travers, K. J., Weissman, J. S. and Brodsky, J. L. (2001) The action of molecular chaperones in the early secretory pathway. Annu. Rev. Genet. 35, 149-191
12. Ron, D. and Walter, P. (2007) Signal integration in the endoplasmic reticulum unfolded protein response. Nat. Rev. Mol. Cell Biol. 8, 519-529
13. Malhotra, J. D. and Kaufman, R. J. (2007) The endoplasmic reticulum and the unfolded protein response. Semin. Cell Dev. Biol. 18, 716-731
14. Flaherty, K. M., DeLuca-Flaherty, C. and McKay, D. B. (1990) Three-dimensional structure of the ATPase fragment of a 70K heat-shock cognate protein. Nature 346, 623-628
15. Zhu, X., Zhao, X., Burkholder, W. F., Gragerov, A., Ogata, C. M., Gottesman, M. E. and Hendrickson, W. A. (1996) Structural analysis of substrate binding by the molecular chaperone DnaK. Science 272, 1606-1614
16. Jiang, J., Prasad, K., Lafer, E. M. and Sousa, R. (2005) Structural basis of interdomain communication in the Hsc70 chaperone. Mol. Cell 20, 513-524 (Pubitemid 41668637)
17. Schuermann, J. P., Jiang, J., Cuellar, J., Llorca, O., Wang, L., Gimenez, L. E., Jin, S., Taylor, A. B., Demeler, B., Morano, K. A. et al. (2008) Structure of the Hsp110:Hsc70 nucleotide exchange machine. Mol. Cell 31, 232-243
18. Polier, S., Dragovic, Z., Hartl, F. U. and Bracher, A. (2008) Structural basis for the cooperation of Hsp70 and Hsp110 chaperones in protein folding. Cell 133, 1068-1079 (Pubitemid 351787748)
19. Gething, M. J. and Sambrook, J. (1992) Protein folding in the cell. Nature 355, 33-45
20. Glover, J. R. and Lindquist, S. (1998) Hsp104, Hsp70, and Hsp40: a novel chaperone system that rescues previously aggregated proteins. Cell 94, 73-82
21. Li, J., Qian, X. and Sha, B. (2009) Heat shock protein 40: structural studies and their functional implications. Protein Pept. Lett. 16, 606-612
22. Briknarova, K., Takayama, S., Brive, L., Havert, M. L., Knee, D. A., Velasco, J., Homma, S., Cabezas, E., Stuart, J., Hoyt, D. W. et al. (2001) Structural analysis of BAG1 cochaperone and its interactions with Hsc70 heat shock protein. Nat. Struct. Biol. 8, 349-352
23. Shomura, Y., Dragovic, Z., Chang, H. C., Tzvetkov, N., Young, J. C., Brodsky, J. L., Guerriero, V., Hartl, F. U. and Bracher, A. (2005) Regulation of Hsp70 function by HspBP1: structural analysis reveals an alternate mechanism for Hsp70 nucleotide exchange. Mol. Cell 17, 367-379 (Pubitemid 40193308)
24. Sondermann, H., Scheufler, C., Schneider, C., Hohfeld, J., Hartl, F. U. and Moarefi, I. (2001) Structure of a Bag/Hsc70 complex: convergent functional evolution of Hsp70 nucleotide exchange factors. Science 291, 1553-1557 (Pubitemid 32179223)
25. Dragovic, Z., Broadley, S. A., Shomura, Y., Bracher, A. and Hartl, F. U. (2006) Molecular chaperones of the Hsp110 family act as nucleotide exchange factors of Hsp70s. EMBO J. 25, 2519-2528
26. Raviol, H., Sadlish, H., Rodriguez, F., Mayer, M. P. and Bukau, B. (2006) Chaperone network in the yeast cytosol: Hsp110 is revealed as an Hsp70 nucleotide exchange factor. EMBO J. 25, 2510-2518 (Pubitemid 44012233)
27. Harrison, C. J., Hayer-Hartl, M., Di Liberto, M., Hartl, F. and Kuriyan, J. (1997) Crystal structure of the nucleotide exchange factor GrpE bound to the ATPase domain of the molecular chaperone DnaK. Science 276, 431-435 (Pubitemid 27180708)
28. Xu, Z., Page, R. C., Gomes, M. M., Kohli, E., Nix, J. C., Herr, A. B., Patterson, C. and Misra, S. (2008) Structural basis of nucleotide exchange and client binding by the Hsp70 cochaperone Bag2. Nat. Struct. Mol. Biol. 15, 1309-1317
29. Shida, M., Arakawa, A., Ishii, R., Kishishita, S., Takagi, T., Kukimoto-Niino, M., Sugano, S., Tanaka, A., Shirouzu, M. and Yokoyama, S. (2010) Direct inter-subdomain interactions switch between the closed and open forms of the Hsp70 nucleotide-binding domain in the nucleotide-free state. Acta Crystallogr. Sect. D Biol. Crystallogr. 66, 223-232
30. Arakawa, A., Handa, N., Ohsawa, N., Shida, M., Kigawa, T., Hayashi, F., Shirouzu, M. and Yokoyama, S. (2010) The C-terminal BAG domain of BAG5 induces conformational changes of the Hsp70 nucleotide-binding domain for ADP-ATP exchange. Structure 18, 309-319
31. Briknarova, K., Takayama, S., Homma, S., Baker, K., Cabezas, E., Hoyt, D. W., Li, Z., Satterthwait, A. C. and Ely, K. R. (2002) BAG4/SODD protein contains a short BAG domain. J. Biol. Chem. 277, 31172-31178
32. Hale, S. J., Lovell, S. C., de Keyzer, J. and Stirling, C. J. (2010) Interactions between Kar2p and its nucleotide exchange factors Sil1p and Lhs1p are mechanistically distinct. J. Biol. Chem. 285, 21600-21606
33. Tyson, J. R. and Stirling, C. J. (2000) LHS1 and SIL1 provide a lumenal function that is essential for protein translocation into the endoplasmic reticulum. EMBO J. 19, 6440-6452
34. Chung, K. T., Shen, Y. and Hendershot, L. M. (2002) BAP, a mammalian BiP-associated protein, is a nucleotide exchange factor that regulates the ATPase activity of BiP. J. Biol. Chem. 277, 47557-47563
35. Steel, G. J., Fullerton, D. M., Tyson, J. R. and Stirling, C. J. (2004) Coordinated activation of Hsp70 chaperones. Science 303, 98-101 (Pubitemid 38055780)
36. Kabani, M., McLellan, C., Raynes, D. A., Guerriero, V. and Brodsky, J. L. (2002) HspBP1, a homologue of the yeast Fes1 and Sls1 proteins, is an Hsc70 nucleotide exchange factor. FEBS Lett. 531, 339-342
37. Travers, K. J., Patil, C. K., Wodicka, L., Lockhart, D. J., Weissman, J. S. and Walter, P. (2000) Functional and genomic analyses reveal an essential coordination between the unfolded protein response and ER-associated degradation. Cell 101, 249-258
38. Zhao, L., Longo-Guess, C., Harris, B. S., Lee, J. W. and Ackerman, S. L. (2005) Protein accumulation and neurodegeneration in the woozy mutant mouse is caused by disruption of SIL1, a cochaperone of BiP. Nat. Genet. 37, 974-979
39. Senderek, J., Krieger, M., Stendel, C., Bergmann, C., Moser, M., Breitbach-Faller, N., Rudnik-Schoneborn, S., Blaschek, A., Wolf, N. I., Harting, I. et al. (2005) Mutations in SIL1 cause Marinesco-Sjogren syndrome, a cerebellar ataxia with cataract and myopathy. Nat. Genet. 37, 1312-1314
40. Anttonen, A. K., Mahjneh, I., Hamalainen, R. H., Lagier-Tourenne, C., Kopra, O., Waris, L., Anttonen, M., Joensuu, T., Kalimo, H., Paetau, A. et al. (2005) The gene disrupted in Marinesco-Sjogren syndrome encodes SIL1, an HSPA5 cochaperone. Nat. Genet. 37, 1309-1311
41. Sakai, K., Tada, M., Yonemochi, Y., Nakajima, T., Onodera, O., Takahashi, H. and Kakita, A. (2008) Marinesco-Sjogren syndrome with atrophy of the brain stem tegmentum and dysplastic cytoarchitecture in the cerebral cortex. Neuropathology 28, 541-546
42. Riazuddin, S. A., Amiri-Kordestani, L., Kaul, H., Butt, T., Jiao, X., Riazuddin, S. and Hejtmancik, J. F. (2009) Novel SIL1 mutations in consanguineous Pakistani families mapping to chromosomes 5q31. Mol. Vis. 15, 1050-1056
43. Terwilliger, T. C. and Berendzen, J. (1999) Automated MAD and MIR structure solution. Acta Crystallogr. Sect. D Biol. Crystallogr. 55, 849-861
44. Terwilliger, T. C. (2000) Maximum-likelihood density modification. Acta Crystallogr. Sect. D Biol. Crystallogr. 56, 965-972
45. Emsley, P. and Cowtan, K. (2004) COOT: model-building tools for molecular graphics. Acta Crystallogr. Sect. D Biol. Crystallogr. 60, 2126-2132
46. Brunger, A. T., Adams, P. D., Clore, G. M., DeLano, W. L., Gros, P., Grosse-Kunstleve, R. W., Jiang, J. S., Kuszewski, J., Nilges, M., Pannu, N. S. et al. (1998) Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. Sect. D Biol. Crystallogr. 54, 905-921
47. Lanzetta, P. A., Alvarez, L. J., Reinach, P. S. and Candia, O. A. (1979) An improved assay for nanomole amounts of inorganic phosphate. Anal. Biochem. 100, 95-97
48. Hale, S. J., Lovell, S. C., de Keyzer, J. and Stirling, C. J. (2010) Interactions between Kar2p and its nucleotide exchange factors Sil1p and Lhs1p are mechanistically distinct. J. Biol. Chem. 285, 21600-21606
49. Jiang, J., Maes, E. G., Taylor, A. B., Wang, L., Hinck, A. P., Lafer, E. M. and Sousa, R. (2007) Structural basis of J cochaperone binding and regulation of Hsp70. Mol. Cell 28, 422-433
50. Liu, Q. and Hendrickson, W. A. (2007) Insights into Hsp70 chaperone activity from a crystal structure of the yeast Hsp110 Sse1. Cell 131, 106-120