The molecular chaperone Hsp70 activates protein phosphatase 5 (PP5) by binding the tetratricopeptide repeat (TPR) domain

Journal of Biological Chemistry

Volumn 289, Issue 5, 2014, Pages 2908-2917

  Connarn, Jamie N ^a   Assimon, Victoria A ^a   Reed, Rebecca A ^a   Tse, Eric ^a,b   Southworth, Daniel R ^a,b   Zuiderweg, Erik R P ^b   Gestwicki, Jason E ^a,b   Sun, Duxin ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CANCER SIGNALING; CO-CHAPERONES; HEAT SHOCK PROTEIN 70; HSP90; NMR; PEPTIDES; PROTEIN PHOSPHATASE; PROTEIN-PROTEIN INTERACTIONS; SPLIT LUCIFERASE; TETHERED BINDING;

ENZYME ACTIVATION; GLYCOPROTEINS; HEK293 CELLS; HSC70 HEAT-SHOCK PROTEINS; HSP90 HEAT-SHOCK PROTEINS; HUMANS; LUCIFERASES; MODELS, CHEMICAL; MOLECULAR CHAPERONES; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN STRUCTURE, TERTIARY; SIGNAL TRANSDUCTION;

EID: 84893493799     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.519421     Document Type: Article

References (41)

1. Zuo, Z., Urban, G., Scammell, J. G., Dean, N. M., McLean, T. K., Aragon, I., and Honkanen, R. E. (1999) Ser/Thr protein phosphatase type 5 (PP5) is a negative regulator of glucocorticoid receptor-mediated growth arrest. Biochemistry 38, 8849-8857
2. Morita, K., Saitoh, M., Tobiume, K., Matsuura, H., Enomoto, S., Nishitoh, H., and Ichijo, H. (2001) Negative feedback regulation of ASK1 by protein phosphatase 5 (PP5) in response to oxidative stress. EMBO J. 20, 6028-6036
3. Ali, A., Zhang, J., Bao, S., Liu, I., Otterness, D., Dean, N. M., Abraham, R. T., and Wang, X. F. (2004) Requirement of protein phosphatase 5 in DNA-damage-induced ATM activation. Genes Dev. 18, 249-254
4. Chen, M. X., and Cohen, P. T. (1997) Activation of protein phosphatase 5 by limited proteolysis or the binding of polyunsaturated fatty acids to the TPR domain. FEBS Lett. 400, 136-140
5. Zhou, G., Golden, T., Aragon, I. V., and Honkanen, R. E. (2004) Ser/Thr protein phosphatase 5 inactivates hypoxia-induced activation of an apoptosis signal-regulating kinase 1/MKK-4/JNK signaling cascade. J. Biol. Chem. 279, 46595-46605
6. Zuo, Z., Dean, N. M., and Honkanen, R. E. (1998) Serine/threonine protein phosphatase type 5 acts upstream of p53 to regulate the induction of p21 (WAF1/Cip1) and mediate growth arrest. J. Biol. Chem. 273, 12250-12258
7. Chen, M. S., Silverstein, A. M., Pratt, W. B., and Chinkers, M. (1996) The tetratricopeptide repeat domain of protein phosphatase 5 mediates binding to glucocorticoid receptor heterocomplexes and acts as a dominant negative mutant. J. Biol. Chem. 271, 32315-32320
8. Golden, T., Aragon, I. V., Rutland, B., Tucker, J. A., Shevde, L. A., Samant, R. S., Zhou, G., Amable, L., Skarra, D., and Honkanen, R. E. (2008) Elevated levels of Ser/Thr protein phosphatase 5 (PP5) in human breast cancer. Biochim. Biophys. Acta 1782, 259-270
9. Golden, T., Swingle, M., and Honkanen, R. E. (2008) The role of serine/threonine protein phosphatase type 5 (PP5) in the regulation of stressinduced signaling networks and cancer. Cancer Metastasis Rev. 27, 169-178
10. McConnell, J. L., and Wadzinski, B. E. (2009) Targeting protein serine/threonine phosphatases for drug development. Mol. Pharmacol. 75, 1249-1261
11. Bollen, M., and Stalmans, W. (1992) The structure, role, and regulation of type-1 protein phosphatases. Crit. Rev. Biochem. Mol. Biol 27, 227-281
12. Cohen, P. T. (1997) Novel protein serine/threonine phosphatases: Variety is the spice of life. Trends Biochem. Sci. 22, 245-251
13. Zhang, M. H., Windheim, M., Roe, S. M., Peggie, M., Cohen, P., Prodromou, C, and Pearl, L. H. (2005) Chaperoned ubiquitylation - crystal structures of the CHIPU box E3 ubiquitin ligase and a CHIP-Ubc13-Uev1a complex. Mol. Cell 20, 525-538
14. Yang, J., Roe, S. M., Cliff, M. J., Williams, M. A., Ladbury, J. E., Cohen, P. T., and Barford, D. (2005) Molecular basis for TPR domain-mediated regulation of protein phosphatase. EMBOJ. 24, 1-10
15. Wang, L., Liu, Y. T., Hao, R., Chen, L., Chang, Z., Wang, Z. X., Wang, H. R., and Wu, J. W. (2011) Molecular mechanism of the negative regulation of Smad1/5 protein by carboxyl terminus of Hsc70-interacting protein (CHIP). J. Biol. Chem. 286, 15883-15894
16. Scheufler, C, Brinker, A., Bourenkov, G., Pegoraro, S., Moroder, L., Bartunik, H., Hartl, F. U., and Moarefi, I. (2000) Structure of TPR domainpeptide complexes: Critical elements in the assembly of the Hsp70-Hsp90 multichaperone machine. Cell 101, 199-210
17. Chen, L., Qi, H., Korenberg, J., Garrow, T. A., Choi, Y. J., and Shane, B. (1996) Purification and properties of human cytosolic folylpoly-7-glutamate synthetase and organization, localization, and differential splicing of its gene. J. Biol. Chem. 271, 13077-13087
18. Silverstein, A. M., Galigniana, M. D., Chen, M. S., Owens-Grillo, J. K., Chinkers, M., and Pratt, W. B. (1997) Protein phosphatase 5 is a major component of glucocorticoid receptor. hsp90 complexes with properties of an FK506-binding immunophilin. J. Biol. Chem. 272, 16224-16230
19. Cliff, M. J., Harris, R., Barford, D., Ladbury, J. E., and Williams, M. A. (2006) Conformational diversity in the TPR domain-mediated interaction of protein phosphatase 5 with Hsp90. Structure 14, 415-426
20. Cliff, M. J., Williams, M. A., Brooke-Smith, J., Barford, D., and Ladbury, J. E. (2005) Molecular recognition via coupled folding and binding in a TPR domain. J. Mol. Biol. 346, 717-732
21. Zeke, T., Morrice, N., Vazquez-Martin, C, and Cohen, P. T. (2005) Human protein phosphatase 5 dissociates from heat-shock proteins and is proteolytically activated in response to arachidonic acid and the microtubule-depolymerizing drug nocodazole. Biochem. J. 385, 45-56
22. Hohfeld, J., Cyr, D. M., and Patterson, C. (2001) From the cradle to the grave: molecular chaperones that may choose between folding and degradation. EMBORep. 2, 885-890
23. Mayer, M. P., and Bukau, B. (2005) Hsp70 chaperones: Cellular functions and molecular mechanism. Cell Mol. Life Sci. 62, 670-684
24. Connell, P., Ballinger, C. A., Jiang, J., Wu, Y., Thompson, L. J., Hohfeld, J., and Patterson, C (2001) The co-chaperone CHIP regulates protein triage decisions mediated by heat-shock proteins. Nat. Cell Biol. 3, 93-96
25. Qian, S. B., McDonough, H, Boellmann, F., Cyr, D. M., and Patterson, C. (2006) CHIP-mediated stress recovery by sequential ubiquitination of substrates and Hsp70. Nature 440, 551-555
26. Chen, S., and Smith, D. F. (1998) Hop as an adaptor in the heat shock protein 70 (Hsp70) and Hsp90 chaperone machinery. J. Biol. Chem. 273, 35194-35200
27. Heinlein, C. A., and Chang, C. (2001) Role of chaperones in nuclear translocation and transactivation of steroid receptors. Endocrine 14, 143-149
28. Paulmurugan, R., Massoud, T. F., Huang, J., and Gambhir, S. S. (2004) Molecular imaging of drug-modulated protein-protein interactions in living subjects. Cancer Res. 64, 2113-2119
29. Chang, L., Thompson, A. D., Ung, P., Carlson, H. A., and Gestwicki, J. E. (2010) Mutagenesis reveals the complex relationships between ATPase rate and the chaperone activities of Escherichia coli heat shock protein 70 (Hsp70/DnaK). J. Biol. Chem. 285, 21282-21291
30. Amblard, M., Fehrentz, J. A., Martinez, J., and Subra, G. (2006) Methods and protocols of modern solid phase peptide synthesis. Mol. Biotechnol. 33, 239-254
31. Jiang, Y., Bernard, D., Yu, Y., Xie, Y., Zhang, T., Li, Y., Burnett, J. P., Fu, X., Wang, S., and Sun, D. (2010) Split Renilla luciferase protein fragmentassisted complementation (SRL-PFAC) to characterize Hsp90-Cdc37 complex and identify critical residues in protein/protein interactions. J. Biol. Chem. 285, 21023-21036
32. Wu, S. J., Liu, F. H., Hu, S. M., and Wang, C. (2001) Different combinations of the heat-shock cognate protein 70 (hsc70) C-terminal functional groups are utilized to interact with distinct tetratricopeptide repeat-containing proteins. Biochem. J. 359, 419-426
33. Liu, F. H., Wu, S. J., Hu, S. M., Hsiao, C. D., and Wang, C. (1999) Specific interaction of the 70-kDa heat shock cognate protein with the tetratricopeptide repeats. J. Biol. Chem. 274, 34425-34432
34. Russell, L. C., Whitt, S. R., Chen, M. S., and Chinkers, M. (1999) Identification of conserved residues required for the binding of a tetratricopeptide repeat domain to heat shock protein 90. J. Biol. Chem. 274, 20060-20063
35. Southworth, D. R., and Agard, D. A. (2011) Client-loading conformation of the Hsp90 molecular chaperone revealed in the cryo-EM structure of the human Hsp90:Hop complex. Mol. Cell. 42, 771-781
36. Revington, M., Zhang, Y., Yip, G. N., Kurochkin, A. V., and Zuiderweg, E. R. (2005) NMR investigations of allosteric processes in a two-domain Thermus thermophilus Hsp70 molecular chaperone. J. Mol. Biol. 349, 163-183
37. Krukenberg, K. A., Street, T. O., Lavery, L. A., and Agard, D. A. (2011) Conformational dynamics of the molecular chaperone Hsp90. Q. Rev. Biophys. 44, 229-255
38. Smith, M. C., Scaglione, K. M., Assimon, V. A., Patury, S., Thompson, A. D., Dickey, C. A., Southworth, D. R., Paulson, H. L., Gestwicki, J. E., and Zuiderweg, E. R. (2013) The E3 ubiquitin ligase CHIP and the molecular chaperone Hsc70 form a dynamic, tethered complex. Biochemistry 52, 5354-5364
39. 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
40. Bertelsen, E. B., Chang, L., Gestwicki, J. E., and Zuiderweg, E. R. (2009) Solution conformation of wild-type E. coliHsp70 (DnaK) chaperone complexed with ADP and substrate. Proc. Natl. Acad. Sci. U. S. A. 106, 8471-8476
41. Zuiderweg, E. R., Bertelsen, E. B., Rousaki, A., Mayer, M. P., Gestwicki, J. E., and Ahmad, A. (2013) Allostery in the Hsp70 chaperone proteins. Top Curr. Chem. 328, 99-153