Hsp70 Forms Antiparallel Dimers Stabilized by Post-translational Modifications to Position Clients for Transfer to Hsp90

Cell Reports

Volumn 11, Issue 5, 2015, Pages 759-769

  Morgner, Nina ^a   Schmidt, Carla ^a   Beilsten Edmands, Victoria ^a   Ebong, Ima Obong ^a   Patel, Nisha A ^a   Clerico, Eugenia M ^b   Kirschke, Elaine ^c   Daturpalli, Soumya ^d   Jackson, Sophie E ^d   Agard, David ^c   Robinson, Carol V ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF MASSACHUSETTS   (United States)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^d UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; GLUCOCORTICOID RECEPTOR; HEAT SHOCK PROTEIN 40; HEAT SHOCK PROTEIN 70; HEAT SHOCK PROTEIN 90; PROTEIN HOP; PROTEIN P23; UNCLASSIFIED DRUG; PROTEIN BINDING; RECOMBINANT PROTEIN; SACCHAROMYCES CEREVISIAE PROTEIN;

ARTICLE; CATALYSIS; COMPLEX FORMATION; CONTROLLED STUDY; DIMERIZATION; MASS SPECTROMETRY; PRIORITY JOURNAL; PROTEIN CROSS LINKING; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; BIOSYNTHESIS; CHEMISTRY; ESCHERICHIA COLI; GENETICS; HUMAN; ISOLATION AND PURIFICATION; METABOLISM; PROTEIN FOLDING; PROTEIN MULTIMERIZATION; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE;

EUKARYOTA;

DIMERIZATION; ESCHERICHIA COLI; HSP40 HEAT-SHOCK PROTEINS; HSP70 HEAT-SHOCK PROTEINS; HSP90 HEAT-SHOCK PROTEINS; HUMANS; PROTEIN BINDING; PROTEIN FOLDING; PROTEIN MULTIMERIZATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, GLUCOCORTICOID; RECOMBINANT PROTEINS; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84933675876     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2015.03.063     Document Type: Article

References (70)

1. Alvira S., Cuéllar J., Röhl A., Yamamoto S., Itoh H., Alfonso C., Rivas G., Buchner J., Valpuesta J.M. Structural characterization of the substrate transfer mechanism in Hsp70/Hsp90 folding machinery mediated by Hop. Nat. Commun. 2014, 5:5484.
2. Aprile F.A., Dhulesia A., Stengel F., Roodveldt C., Benesch J.L., Tortora P., Robinson C.V., Salvatella X., Dobson C.M., Cremades N. Hsp70 oligomerization is mediated by an interaction between the interdomain linker and the substrate-binding domain. PLoS ONE 2013, 8:e67961.
3. Barrott J.J., Haystead T.A. Hsp90, an unlikely ally in the war on cancer. FEBS J. 2013, 280:1381-1396.
4. Beltrao P., Albanèse V., Kenner L.R., Swaney D.L., Burlingame A., Villén J., Lim W.A., Fraser J.S., Frydman J., Krogan N.J. Systematic functional prioritization of protein posttranslational modifications. Cell 2012, 150:413-425.
5. Benaroudj N., Batelier G., Triniolles F., Ladjimi M.M. Self-association of the molecular chaperone HSC70. Biochemistry 1995, 34:15282-15290.
6. Benesch J.L., Aquilina J.A., Ruotolo B.T., Sobott F., Robinson C.V. Tandem mass spectrometry reveals the quaternary organization of macromolecular assemblies. Chem. Biol. 2006, 13:597-605.
7. Bertelsen E.B., Chang L., Gestwicki J.E., Zuiderweg E.R. Solution conformation of wild-type E. coli Hsp70 (DnaK) chaperone complexed with ADP and substrate. Proc. Natl. Acad. Sci. USA 2009, 106:8471-8476.
8. Bledsoe R.K., Montana V.G., Stanley T.B., Delves C.J., Apolito C.J., McKee D.D., Consler T.G., Parks D.J., Stewart E.L., Willson T.M., et al. Crystal structure of the glucocorticoid receptor ligand binding domain reveals a novel mode of receptor dimerization and coactivator recognition. Cell 2002, 110:93-105.
9. Brychzy A., Rein T., Winklhofer K.F., Hartl F.U., Young J.C., Obermann W.M. Cofactor Tpr2 combines two TPR domains and a J domain to regulate the Hsp70/Hsp90 chaperone system. EMBO J. 2003, 22:3613-3623.
10. Chang Y.W., Sun Y.J., Wang C., Hsiao C.D. Crystal structures of the 70-kDa heat shock proteins in domain disjoining conformation. J.Biol. Chem. 2008, 283:15502-15511.
11. Chen S., Smith D.F. Hop as an adaptor in the heat shock protein 70 (Hsp70) and hsp90 chaperone machinery. J.Biol. Chem. 1998, 273:35194-35200.
12. Cuéllar J., Perales-Calvo J., Muga A., Valpuesta J.M., Moro F. Structural insights into the chaperone activity of the 40-kDa heat shock protein DnaJ: binding and remodeling of a native substrate. J.Biol. Chem. 2013, 288:15065-15074.
13. Cyr D.M., Douglas M.G. Differential regulation of Hsp70 subfamilies by the eukaryotic DnaJ homologue YDJ1. J.Biol. Chem. 1994, 269:9798-9804.
14. Dittmar K.D., Demady D.R., Stancato L.F., Krishna P., Pratt W.B. Folding of the glucocorticoid receptor by the heat shock protein (hsp) 90-based chaperone machinery. The role of p23 is to stabilize receptor.hsp90 heterocomplexes formed by hsp90.p60.hsp70. J.Biol. Chem. 1997, 272:21213-21220.
15. Dutta A., Girotra M., Merchant N., Nair P., Dutta S.K. Evidence of multimeric forms of HSP70 with phosphorylation on serine and tyrosine residues-implications for roles of HSP70 in detection of GI cancers. Asian Pac. J. Cancer Prev. 2013, 14:5741-5745.
16. Ebong I.O., Morgner N., Zhou M., Saraiva M.A., Daturpalli S., Jackson S.E., Robinson C.V. Heterogeneity and dynamics in the assembly of the heat shock protein 90 chaperone complexes. Proc. Natl. Acad. Sci. USA 2011, 108:17939-17944.
17. Heck A.J. Native mass spectrometry: a bridge between interactomics and structural biology. Nat. Methods 2008, 5:927-933.
18. Hennessy F., Nicoll W.S., Zimmermann R., Cheetham M.E., Blatch G.L. Not all J domains are created equal: implications for the specificity of Hsp40-Hsp70 interactions. Protein Sci. 2005, 14:1697-1709.
19. Hernández H., Robinson C.V. Determining the stoichiometry andinteractions of macromolecular assemblies from mass spectrometry. Nat. Protoc. 2007, 2:715-726.
20. Hernández M.P., Chadli A., Toft D.O. HSP40 binding is the first step in the HSP90 chaperoning pathway for the progesterone receptor. J.Biol. Chem. 2002, 277:11873-11881.
21. Hilton G.R., Benesch J.L. Two decades of studying non-covalent biomolecular assemblies by means of electrospray ionization mass spectrometry. J.R. Soc. Interface 2012, 9:801-816.
22. Jackson S.E. Hsp90: structure and function. Top. Curr. Chem. 2013, 328:155-240.
23. Jiang J., Prasad K., Lafer E.M., Sousa R. Structural basis of interdomain communication in the Hsc70 chaperone. Mol. Cell 2005, 20:513-524.
24. Jiang J., Maes E.G., Taylor A.B., Wang L., Hinck A.P., Lafer E.M., Sousa R. Structural basis of J cochaperone binding and regulation of Hsp70. Mol. Cell 2007, 28:422-433.
25. Kampinga H.H., Craig E.A. The HSP70 chaperone machinery: J proteins as drivers of functional specificity. Nat. Rev. Mol. Cell Biol. 2010, 11:579-592.
26. King C., Eisenberg E., Greene L.E. Interaction between Hsc70 and DnaJ homologues: relationship between Hsc70 polymerization and ATPase activity. Biochemistry 1999, 38:12452-12459.
27. Kirschke E., Goswami D., Southworth D., Griffin P.R., Agard D.A. Glucocorticoid receptor function regulated by coordinated action of the Hsp90 and Hsp70 chaperone cycles. Cell 2014, 157:1685-1697.
28. Kityk R., Kopp J., Sinning I., Mayer M.P. Structure and dynamics of the ATP-bound open conformation of Hsp70 chaperones. Mol. Cell 2012, 48:863-874.
29. Kundrat L., Regan L. Balance between folding and degradation for Hsp90-dependent client proteins: a key role for CHIP. Biochemistry 2010, 49:7428-7438.
30. Laufen T., Mayer M.P., Beisel C., Klostermeier D., Mogk A., Reinstein J., Bukau B. Mechanism of regulation of hsp70 chaperones by DnaJ cochaperones. Proc. Natl. Acad. Sci. USA 1999, 96:5452-5457.
31. Li J., Qian X., Sha B. The crystal structure of the yeast Hsp40 Ydj1 complexed with its peptide substrate. Structure 2003, 11:1475-1483.
32. Li J., Wu Y., Qian X., Sha B. Crystal structure of yeast Sis1 peptide-binding fragment and Hsp70 Ssa1 C-terminal complex. Biochem. J. 2006, 398:353-360.
33. Li J., Richter K., Buchner J. Mixed Hsp90-cochaperone complexes are important for the progression of the reaction cycle. Nat. Struct. Mol. Biol. 2011, 18:61-66.
34. Liu Q., Hendrickson W.A. Insights into Hsp70 chaperone activity from a crystal structure of the yeast Hsp110 Sse1. Cell 2007, 131:106-120.
35. Mapa K., Sikor M., Kudryavtsev V., Waegemann K., Kalinin S., Seidel C.A., Neupert W., Lamb D.C., Mokranjac D. The conformational dynamics of the mitochondrial Hsp70 chaperone. Mol. Cell 2010, 38:89-100.
36. Marty M.T., Baldwin A.J., Marklund E.G., Hochberg G.K., Benesch J.L., Robinson C.V. Bayesian Deconvolution of Mass and Ion Mobility Spectra: From Binary Interactions to Polydisperse Ensembles. Anal. Chem. 2015, Published online March 23, 2015. 10.1021/acs.analchem.5b00140.
37. Mayer M.P., Bukau B. Hsp70 chaperones: cellular functions and molecular mechanism. Cell. Mol. Life Sci. 2005, 62:670-684.
38. Mayer M.P., Schröder H., Rüdiger S., Paal K., Laufen T., Bukau B. Multistep mechanism of substrate binding determines chaperone activity of Hsp70. Nat. Struct. Biol. 2000, 7:586-593.
39. McLaughlin S.H., Sobott F., Yao Z.P., Zhang W., Nielsen P.R., Grossmann J.G., Laue E.D., Robinson C.V., Jackson S.E. The co-chaperone p23 arrests the Hsp90 ATPase cycle to trap client proteins. J.Mol. Biol. 2006, 356:746-758.
40. Morgner N., Robinson C.V. Massign: an assignment strategy formaximizing information from the mass spectra of heterogeneous protein assemblies. Anal. Chem. 2012, 84:2939-2948.
41. Picard D., Khursheed B., Garabedian M.J., Fortin M.G., Lindquist S., Yamamoto K.R. Reduced levels of hsp90 compromise steroid receptor action invivo. Nature 1990, 348:166-168.
42. Pratt W.B., Dittmar K.D. Studies with purified chaperones advance the understanding of the mechanism of glucocorticoid receptor-hsp90 heterocomplex assembly. Trends Endocrinol. Metab. 1998, 9:244-252.
43. Pratt W.B., Toft D.O. Steroid receptor interactions with heat shock protein and immunophilin chaperones. Endocr. Rev. 1997, 18:306-360.
44. Prodromou C. The 'active life' of Hsp90 complexes. Biochim. Biophys. Acta 2012, 1823:614-623.
45. Qi R., Sarbeng E.B., Liu Q., Le K.Q., Xu X., Xu H., Yang J., Wong J.L., Vorvis C., Hendrickson W.A., et al. Allosteric opening of the polypeptide-binding site when an Hsp70 binds ATP. Nat. Struct. Mol. Biol. 2013, 20:900-907.
46. Richter K., Muschler P., Hainzl O., Reinstein J., Buchner J. Sti1 is a non-competitive inhibitor of the Hsp90 ATPase. Binding prevents the N-terminal dimerization reaction during the atpase cycle. J.Biol. Chem. 2003, 278:10328-10333.
47. Rohrer K.M., Haug M., Schwörer D., Kalbacher H., Holzer U. Mutations in the substrate binding site of human heat-shock protein 70 indicate specific interaction with HLA-DR outside the peptide binding groove. Immunology 2014, 142:237-247.
48. Sanchez E.R. Chaperoning steroidal physiology: lessons from mouse genetic models of Hsp90 and its cochaperones. Biochim. Biophys. Acta 2012, 1823:722-729.
49. Sarbeng E.B., Liu Q., Tian X., Yang J., Li H., Wong J.L., Zhou L., Liu Q. A functional DnaK dimer is essential for the efficient interaction with heat shock protein 40kDa (Hsp40). J.Biol. Chem. 2015, 290:8849-8862.
50. Schaffar G., Breuer P., Boteva R., Behrends C., Tzvetkov N., Strippel N., Sakahira H., Siegers K., Hayer-Hartl M., Hartl F.U. Cellular toxicity of polyglutamine expansion proteins: mechanism of transcription factor deactivation. Mol. Cell 2004, 15:95-105.
51. Scheufler C., Brinker A., Bourenkov G., Pegoraro S., Moroder L., Bartunik H., Hartl F.U., Moarefi I. Structure of TPR domain-peptide complexes: critical elements in the assembly of the Hsp70-Hsp90 multichaperone machine. Cell 2000, 101:199-210.
52. Schmid A.B., Lagleder S., Gräwert M.A., Röhl A., Hagn F., Wandinger S.K., Cox M.B., Demmer O., Richter K., Groll M., et al. The architecture of functional modules in the Hsp90 co-chaperone Sti1/Hop. EMBO J. 2012, 31:1506-1517.
53. Schmidt C., Robinson C.V. A comparative cross-linking strategy to probe conformational changes in protein complexes. Nat. Protoc. 2014, 9:2224-2236.
54. Schmidt C., Zhou M., Marriott H., Morgner N., Politis A., Robinson C.V. Comparative cross-linking and mass spectrometry of an intact F-type ATPase suggest a role for phosphorylation. Nat. Commun. 2013, 4:1985.
55. Shevchenko A., Wilm M., Vorm O., Mann M. Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal. Chem. 1996, 68:850-858.
56. Smith D.F. Dynamics of heat shock protein 90-progesterone receptor binding and the disactivation loop model for steroid receptor complexes. Mol. Endocrinol. 1993, 7:1418-1429.
57. Sobott F., Hernández H., McCammon M.G., Tito M.A., Robinson C.V. A tandem mass spectrometer for improved transmission and analysis of large macromolecular assemblies. Anal. Chem. 2002, 74:1402-1407.
58. Southworth D.R., Agard D.A. Client-loading conformation of the Hsp90 molecular chaperone revealed in the cryo-EM structure of the human Hsp90:Hop complex. Mol. Cell 2011, 42:771-781.
59. Stengel F., Baldwin A.J., Painter A.J., Jaya N., Basha E., Kay L.E., Vierling E., Robinson C.V., Benesch J.L. Quaternary dynamics and plasticity underlie small heat shock protein chaperone function. Proc. Natl. Acad. Sci. USA 2010, 107:2007-2012.
60. Swain J.F., Dinler G., Sivendran R., Montgomery D.L., Stotz M., Gierasch L.M. Hsp70 chaperone ligands control domain association via an allosteric mechanism mediated by the interdomain linker. Mol. Cell 2007, 26:27-39.
61. Taipale M., Jarosz D.F., Lindquist S. HSP90 at the hub of protein homeostasis: emerging mechanistic insights. Nat. Rev. Mol. Cell Biol. 2010, 11:515-528.
62. Thompson A.D., Bernard S.M., Skiniotis G., Gestwicki J.E. Visualization and functional analysis of the oligomeric states of Escherichia coli heat shock protein 70 (Hsp70/DnaK). Cell Stress Chaperones 2012, 17:313-327.
63. Tsutsumi S., Mollapour M., Prodromou C., Lee C.T., Panaretou B., Yoshida S., Mayer M.P., Neckers L.M. Charged linker sequence modulates eukaryotic heat shock protein 90 (Hsp90) chaperone activity. Proc. Natl. Acad. Sci. USA 2012, 109:2937-2942.
64. van Noort V., Seebacher J., Bader S., Mohammed S., Vonkova I., Betts M.J., Kühner S., Kumar R., Maier T., O'Flaherty M., et al. Cross-talk between phosphorylation and lysine acetylation in a genome-reduced bacterium. Mol. Syst. Biol. 2012, 8:571.
65. Wu C.C., Naveen V., Chien C.H., Chang Y.W., Hsiao C.D. Crystal structure of DnaK protein complexed with nucleotide exchange factor GrpE in DnaK chaperone system: insight into intermolecular communication. J.Biol. Chem. 2012, 287:21461-21470.
66. Wyttenbach T., Bowers M.T. Intermolecular interactions in biomolecular systems examined by mass spectrometry. Annu. Rev. Phys. Chem. 2007, 58:511-533.
67. Young J.C. Mechanisms of the Hsp70 chaperone system. Biochem. Cell Biol. 2010, 88:291-300.
68. Young J.C., Obermann W.M., Hartl F.U. Specific binding of tetratricopeptide repeat proteins to the C-terminal 12-kDa domain of hsp90. J.Biol. Chem. 1998, 273:18007-18010.
69. Young J.C., Moarefi I., Hartl F.U. Hsp90: a specialized but essential protein-folding tool. J.Cell Biol. 2001, 154:267-273.
70. Zhuravleva A., Clerico E.M., Gierasch L.M. An interdomain energetic tug-of-war creates the allosterically active state in Hsp70 molecular chaperones. Cell 2012, 151:1296-1307.