The DNAJA2 substrate release mechanism is essential for chaperone-mediated folding

Journal of Biological Chemistry

Volumn 287, Issue 50, 2012, Pages 41939-41954

  Baaklini, Imad ^a   Wong, Michael J H ^a   Hantouche, Christine ^a   Patel, Yogita ^a   Shrier, Alvin ^a   Young, Jason C ^a  

^a MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ATP HYDROLYSIS; CONFORMATIONAL DIFFERENCES; EXPRESSION LEVELS; FOLDING MECHANISM; FUNCTIONAL MECHANISMS; LIMITED PROTEOLYSIS; PURIFIED PROTEIN; RELEASE MECHANISM; SPECIFIC ACTIVITY; WILD TYPES; ZINC FINGER MOTIFS;

ETHERS; GENE EXPRESSION; PROTEOLYSIS;

SUBSTRATES;

ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; CHAPERONE; DJA1 PROTEIN; DJA2 PROTEIN; DNAJS2 PROTEIN; HEAT SHOCK COGNATE PROTEIN 70; LUCIFERASE; UNCLASSIFIED DRUG; ZINC FINGER PROTEIN;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DIMERIZATION; ENZYME SUBSTRATE; GENE EXPRESSION; GENE MUTATION; GENE REPRESSION; HERG GENE; HUMAN; HUMAN CELL; HYDROLYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN MOTIF; WILD TYPE;

ETHER-A-GO-GO POTASSIUM CHANNELS; HEK293 CELLS; HELA CELLS; HSC70 HEAT-SHOCK PROTEINS; HSP40 HEAT-SHOCK PROTEINS; HUMANS; MUTATION; PROTEIN FOLDING; PROTEIN TRANSPORT; PROTEOLYSIS; ZINC FINGERS;

EID: 84871314516     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.413278     Document Type: Article

References (42)

1. 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
2. Kampinga, H. H., and Craig, E. A. (2010) The HSP70 chaperone machinery. J proteins as drivers of functional specificity. Nat. Rev. Mol. Cell Biol. 11, 579-592
3. Mayer, M. P., and Bukau, B. (2005) Hsp70 chaperones: cellular functions and molecular mechanism. Cell. Mol. Life Sci. 62, 670-684
4. 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)
5. Daugaard, M., Rohde, M., and Jäättelä, M. (2007) The heat shock protein 70 family. Highly homologous proteins with overlapping and distinct functions. FEBS Lett. 581, 3702-3710 (Pubitemid 47081009)
6. Swain, J. F., Dinler, G., Sivendran, R., Montgomery, D. L., Stotz, M., and Gierasch, L. M. (2007) Hsp70 chaperone ligands control domain association via an allosteric mechanism mediated by the interdomain linker. Mol. Cell 26, 27-39 (Pubitemid 46550933)
7. Bertelsen, E. B., Chang, L., Gestwicki, J. E., and Zuiderweg, E. R. (2009) Solution conformation of wild-type E. coli Hsp70 (DnaK) chaperone complexed with ADP and substrate. Proc. Natl. Acad. Sci. U.S.A. 106, 8471-8476
8. Young, J. C. (2010) Mechanisms of the Hsp70 chaperone system. Biochem. Cell Biol. 88, 291-300
9. Qiu, X. B., Shao, Y. M., Miao, S., and Wang, L. (2006) The diversity of the DnaJ/Hsp40 family, the crucial partners for Hsp70 chaperones. Cell. Mol. Life Sci. 63, 2560-2570 (Pubitemid 44800711)
10. Terada, K., and Mori, M. (2000) Human DnaJ homologs dj2 and dj3 and bag-1 are positive cochaperones of hsc70. J. Biol. Chem. 275, 24728-24734 (Pubitemid 30626575)
11. Terada, K., and Oike, Y. (2010) Multiple molecules of Hsc70 and a dimer of DjA1 independently bind to an unfolded protein. J. Biol. Chem. 285, 16789-16797
12. Hageman, J., van Waarde, M. A., Zylicz, A., Walerych, D., and Kampinga, H. H. (2011) The diverse members of the mammalian HSP70 machine show distinct chaperone-like activities. Biochem. J. 435, 127-142
13. Bhangoo, M. K., Tzankov, S., Fan, A. C., Dejgaard, K., Thomas, D. Y., and Young, J. C. (2007) Multiple 40-kDa heat-shock protein chaperones function in Tom70-dependent mitochondrial import. Mol. Biol. Cell 18, 3414-3428 (Pubitemid 47378681)
14. Tzankov, S., Wong, M. J., Shi, K., Nassif, C., and Young, J. C. (2008) Functional divergence between co-chaperones of Hsc70. J. Biol. Chem. 283, 27100-27109
15. Johnson, J. L., and Craig, E. A. (2001) An essential role for the substrate-binding region of Hsp40s in Saccharomyces cerevisiae. J. Cell Biol. 152, 851-856 (Pubitemid 34280169)
16. Fan, C. Y., Ren, H. Y., Lee, P., Caplan, A. J., and Cyr, D. M. (2005) The type I Hsp40 zinc finger-like region is required for Hsp70 to capture non-native polypeptides from Ydj1. J. Biol. Chem. 280, 695-702 (Pubitemid 40165037)
17. Banecki, B., Liberek, K., Wall, D., Wawrzynów, A., Georgopoulos, C., Bertoli, E., Tanfani, F., and Zylicz, M. (1996) Structure-function analysis of the zinc finger region of the DnaJ molecular chaperone. J. Biol. Chem. 271, 14840-14848 (Pubitemid 26194966)
18. Linke, K., Wolfram, T., Bussemer, J., and Jakob, U. (2003) The roles of the two zinc-binding sites in DnaJ. J. Biol. Chem. 278, 44457-44466 (Pubitemid 37377197)
19. Li, J., Qian, X., and Sha, B. (2003) The crystal structure of the yeast Hsp40 Ydj1 complexed with its peptide substrate. Structure 11, 1475-1483 (Pubitemid 37510348)
20. Wu, Y., Li, J., Jin, Z., Fu, Z., and Sha, B. (2005) The crystal structure of the C-terminal fragment of yeast Hsp40 Ydj1 reveals novel dimerization motif for Hsp40. J. Mol. Biol. 346, 1005-1011 (Pubitemid 40215525)
21. Kota, P., Summers, D. W., Ren, H. Y., Cyr, D. M., and Dokholyan, N. V. (2009) Identification of a consensus motif in substrates bound by a type I Hsp40. Proc. Natl. Acad. Sci. U.S.A. 106, 11073-11078
22. Borges, J. C., Fischer, H., Craievich, A. F., and Ramos, C. H. (2005) Low resolution structural study of two human HSP40 chaperones in solution. DJA1 from subfamily A and DJB4 from subfamily B have different quaternary structures. J. Biol. Chem. 280, 13671-13681 (Pubitemid 40517262)
23. Ramos, C. H., Oliveira, C. L., Fan, C. Y., Torriani, I. L., and Cyr, D. M. (2008) Conserved central domains control the quaternary structure of type I and type II Hsp40 molecular chaperones. J. Mol. Biol. 383, 155-166
24. Jin, Y., Awad, W., Petrova, K., and Hendershot, L. M. (2008) Regulated release of ERdj3 from unfolded proteins by BiP. EMBO J. 27, 2873-2882
25. Petrova, K., Oyadomari, S., Hendershot, L. M., and Ron, D. (2008) Regulated association of misfolded endoplasmic reticulum lumenal proteins with P58/DNAJc3. EMBO J. 27, 2862-2872
26. Walker, V. E., Wong, M. J., Atanasiu, R., Hantouche, C., Young, J. C., and Shrier, A. (2010) Hsp40 chaperones promote degradation of the HERG potassium channel. J. Biol. Chem. 285, 3319-3329
27. Milarski, K. L., and Morimoto, R. I. (1989) Mutational analysis of the human HSP70 protein. Distinct domains for nucleolar localization and adenosine triphosphate binding. J. Cell Biol. 109, 1947-1962 (Pubitemid 19282585)
28. O'Brien, M. C., Flaherty, K. M., and McKay, D. B. (1996) Lysine 71 of the chaperone protein Hsc70 Is essential for ATP hydrolysis. J. Biol. Chem. 271, 15874-15878 (Pubitemid 26236194)
29. Schneider, C., Sepp-Lorenzino, L., Nimmesgern, E., Ouerfelli, O., Danishefsky, S., Rosen, N., and Hartl, F. U. (1996) Pharmacologic shifting of a balance between protein refolding and degradation mediated by Hsp90. Proc. Natl. Acad. Sci. U.S.A. 93, 14536-14541 (Pubitemid 26419002)
30. Kapust, R. B., Tözsér, J., Fox, J. D., Anderson, D. E., Cherry, S., Copeland, T. D., and Waugh, D. S. (2001) Tobacco etch virus protease: mechanism of autolysis and rational design of stable mutants with wild-type catalytic proficiency. Protein Eng. 14, 993-1000 (Pubitemid 34137240)
31. Fewell, S. W., Smith, C. M., Lyon, M. A., Dumitrescu, T. P., Wipf, P., Day, B. W., and Brodsky, J. L. (2004) Small molecule modulators of endogenous and co-chaperone-stimulated Hsp70 ATPase activity. J. Biol. Chem. 279, 51131-51140 (Pubitemid 40017855)
32. Michels, A. A., Kanon, B., Konings, A. W., Ohtsuka, K., Bensaude, O., and Kampinga, H. H. (1997) Hsp70 and Hsp40 chaperone activities in the cytoplasm and the nucleus of mammalian cells. J. Biol. Chem. 272, 33283-33289 (Pubitemid 28023677)
33. Akhavan, A., Atanasiu, R., Noguchi, T., Han, W., Holder, N., and Shrier, A. (2005) Identification of the cyclic nucleotide binding domain as a conserved determinant of ion-channel cell-surface localization. J. Cell Sci. 118, 2803-2812 (Pubitemid 41136358)
34. Walker, V. E., Atanasiu, R., Lam, H., and Shrier, A. (2007) Co-chaperone FKBP38 promotes HERG trafficking. J. Biol. Chem. 282, 23509-23516 (Pubitemid 47311946)
35. Flom, G. A., Lemieszek, M., Fortunato, E. A., and Johnson, J. L. (2008) Farnesylation of Ydj1 is required for in vivo interaction with Hsp90 client proteins. Mol. Biol. Cell 19, 5249-5258
36. Summers, D. W., Douglas, P. M., Ren, H. Y., and Cyr, D. M. (2009) The type I Hsp40 Ydj1 utilizes a farnesyl moiety and zinc finger-like region to suppress prion toxicity. J. Biol. Chem. 284, 3628-3639
37. Arnold, K., Bordoli, L., Kopp, J., and Schwede, T. (2006) The SWISS-MODEL workspace. A web-based environment for protein structure homology modelling. Bioinformatics 22, 195-201 (Pubitemid 43205406)
38. Ficker, E., Dennis, A. T., Wang, L., and Brown, A. M. (2003) Role of the cytosolic chaperones Hsp70 and Hsp90 in maturation of the cardiac potassium channel HERG. Circ. Res. 92, e87-100
39. Smith, C. A., and Rayment, I. (1996) X-ray structure of the magnesium(II)·ADP·vanadate complex of the Dictyostelium discoideum myosin motor domain to 1.9 Å resolution. Biochemistry 35, 5404-5417
40. Inobe, T., Kikushima, K., Makio, T., Arai, M., and Kuwajima, K. (2003) The allosteric transition of GroEL induced by metal fluoride-ADP complexes. J. Mol. Biol. 329, 121-134 (Pubitemid 36555170)
41. Okiyoneda, T., Barrière, H., Bagdány, M., Rabeh, W. M., Du, K., Höhfeld, J., Young, J. C., and Lukacs, G. L. (2010) Peripheral protein quality control removes unfolded CFTR from the plasma membrane. Science 329, 805-810
42. Rosales-Hernandez, A., Beck, K. E., Zhao, X., Braun, A. P., and Braun, J. E. (2009) RDJ2 (DNAJA2) chaperones neural G protein signaling pathways. Cell Stress Chaperones 14, 71-82