Phosphorylated and unphosphorylated serine 13 of CDC37 stabilize distinct interactions between its client and HSP90 binding domains

Biochemistry

Volumn 54, Issue 7, 2015, Pages 1493-1504

  Liu, Wenjun ^a   Landgraf, Ralf ^a,b  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MIAMI   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; ENZYMES; PEPTIDES; PROTEINS;

COMPACT STRUCTURES; INDUCED TRANSITIONS; INTRAMOLECULAR CHAPERONE; MOLECULAR PROPERTIES; PROTEIN KINASE CK2; SECONDARY STRUCTURES; STABILIZING PROPERTIES; STRUCTURE DETERMINATION;

PHOSPHORYLATION;

8 ANILINO 1 NAPHTHALENESULFONIC ACID; CASEIN KINASE II; CELL CYCLE PROTEIN 37; EPIDERMAL GROWTH FACTOR RECEPTOR; HEAT SHOCK PROTEIN 90; PHOSPHOSERINE; SERINE; THREONINE; CDC37 PROTEIN, HUMAN; CELL CYCLE PROTEIN; CHAPERONIN; PROTEIN BINDING;

ALGORITHM; AMINO ACID SUBSTITUTION; AMINO TERMINAL SEQUENCE; ARTICLE; BINDING SITE; CELL LYSATE; CELL SURFACE; CIRCULAR DICHROISM; CONTROLLED STUDY; DIMERIZATION; ESCHERICHIA COLI; FLUORESCENCE; GENE OVEREXPRESSION; HUMAN; MCF 7 CELL LINE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEPHOSPHORYLATION; PROTEIN PHOSPHORYLATION; PROTEIN SECONDARY STRUCTURE; PROTEIN STABILITY; QUANTITATIVE ANALYSIS; TEMPERATURE STRESS; WESTERN BLOTTING; WILD TYPE; CHEMISTRY; METABOLISM; PHOSPHORYLATION; PROTEIN MULTIMERIZATION; PROTEIN TERTIARY STRUCTURE;

EUKARYOTA;

CELL CYCLE PROTEINS; CHAPERONINS; HSP90 HEAT-SHOCK PROTEINS; HUMANS; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY; SERINE;

EID: 84923351259     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi501129g     Document Type: Article

References (74)

1. Pearl, L. H. and Prodromou, C. (2001) Structure, function, and mechanism of the Hsp90 molecular chaperone Adv. Protein Chem. 59, 157-186
2. Loo, M. A., Jensen, T. J., Cui, L., Hou, Y., Chang, X. B., and Riordan, J. R. (1998) Perturbation of Hsp90 interaction with nascent CFTR prevents its maturation and accelerates its degradation by the proteasome EMBO J. 17, 6879-6887
3. Wang, X., Venable, J., LaPointe, P., Hutt, D. M., Koulov, A. V., Coppinger, J., Gurkan, C., Kellner, W., Matteson, J., Plutner, H., Riordan, J. R., Kelly, J. W., Yates, J. R., III, and Balch, W. E. (2006) Hsp90 cochaperone Aha1 downregulation rescues misfolding of CFTR in cystic fibrosis Cell 127, 803-815
4. Miyata, Y. (2009) Protein kinase CK2 in health and disease: CK2: the kinase controlling the Hsp90 chaperone machinery Cell. Mol. Life Sci. 66, 1840-1849
5. Taipale, M., Krykbaeva, I., Koeva, M., Kayatekin, C., Westover, K. D., Karras, G. I., and Lindquist, S. (2012) Quantitative analysis of HSP90-client interactions reveals principles of substrate recognition Cell 150, 987-1001
6. Lee, P., Rao, J., Fliss, A., Yang, E., Garrett, S., and Caplan, A. J. (2002) The Cdc37 protein kinase-binding domain is sufficient for protein kinase activity and cell viability J. Cell Biol. 159, 1051-1059
7. Tatebe, H. and Shiozaki, K. (2003) Identification of Cdc37 as a novel regulator of the stress-responsive mitogen-activated protein kinase Mol. Cell. Biol. 23, 5132-5142
8. Rao, J., Lee, P., Benzeno, S., Cardozo, C., Albertus, J., Robins, D. M., and Caplan, A. J. (2001) Functional interaction of human Cdc37 with the androgen receptor but not with the glucocorticoid receptor J. Biol. Chem. 276, 5814-5820
9. Wang, X., Grammatikakis, N., and Hu, J. (2002) Role of p50/CDC37 in hepadnavirus assembly and replication J. Biol. Chem. 277, 24361-24367
10. Wu, F., Peacock, S. O., Rao, S., Lemmon, S. K., and Burnstein, K. L. (2013) Novel interaction between the co-chaperone Cdc37 and Rho GTPase exchange factor Vav3 promotes androgen receptor activity and prostate cancer growth J. Biol. Chem. 288, 5463-5474
11. Smith, J. R. and Workman, P. (2009) Targeting CDC37: an alternative, kinase-directed strategy for disruption of oncogenic chaperoning Cell Cycle 8, 362-372
12. Smith, J. R., Clarke, P. A., de Billy, E., and Workman, P. (2009) Silencing the cochaperone CDC37 destabilizes kinase clients and sensitizes cancer cells to HSP90 inhibitors Oncogene 28, 157-169
13. Gray, P. J., Jr., Stevenson, M. A., and Calderwood, S. K. (2007) Targeting Cdc37 inhibits multiple signaling pathways and induces growth arrest in prostate cancer cells Cancer Res. 67, 11942-11950
14. Stepanova, L., Yang, G., DeMayo, F., Wheeler, T. M., Finegold, M., Thompson, T. C., and Harper, J. W. (2000) Induction of human Cdc37 in prostate cancer correlates with the ability of targeted Cdc37 expression to promote prostatic hyperplasia Oncogene 19, 2186-2193
15. Siligardi, G., Panaretou, B., Meyer, P., Singh, S., Woolfson, D. N., Piper, P. W., Pearl, L. H., and Prodromou, C. (2002) Regulation of Hsp90 ATPase activity by the co-chaperone Cdc37p/p50cdc37 J. Biol. Chem. 277, 20151-20159
16. Mayer, M. P., Prodromou, C., and Frydman, J. (2009) The Hsp90 mosaic: a picture emerges Nat. Struct. Mol. Biol. 16, 2-6
17. Vaughan, C. K., Gohlke, U., Sobott, F., Good, V. M., Ali, M. M., Prodromou, C., Robinson, C. V., Saibil, H. R., and Pearl, L. H. (2006) Structure of an Hsp90-Cdc37-Cdk4 complex Mol. Cell 23, 697-707
18. Vaughan, C. K., Mollapour, M., Smith, J. R., Truman, A., Hu, B., Good, V. M., Panaretou, B., Neckers, L., Clarke, P. A., Workman, P., Piper, P. W., Prodromou, C., and Pearl, L. H. (2008) Hsp90-dependent activation of protein kinases is regulated by chaperone-targeted dephosphorylation of Cdc37 Mol. Cell 31, 886-895
19. Grammatikakis, N., Lin, J. H., Grammatikakis, A., Tsichlis, P. N., and Cochran, B. H. (1999) p50(cdc37) acting in concert with Hsp90 is required for Raf-1 function Mol. Cell. Biol. 19, 1661-1672
20. Shao, J., Irwin, A., Hartson, S. D., and Matts, R. L. (2003) Functional dissection of Cdc37: characterization of domain structure and amino acid residues critical for protein kinase binding Biochemistry 42, 12577-12588
21. Roe, S. M., Ali, M. M., Meyer, P., Vaughan, C. K., Panaretou, B., Piper, P. W., Prodromou, C., and Pearl, L. H. (2004) The mechanism of Hsp90 regulation by the protein kinase-specific cochaperone p50(Cdc37) Cell 116, 87-98
22. Shao, J., Grammatikakis, N., Scroggins, B. T., Uma, S., Huang, W., Chen, J. J., Hartson, S. D., and Matts, R. L. (2001) Hsp90 regulates p50(cdc37) function during the biogenesis of the activeconformation of the heme-regulated eIF2 alpha kinase J. Biol. Chem. 276, 206-214
23. Zhang, W., Hirshberg, M., McLaughlin, S. H., Lazar, G. A., Grossmann, J. G., Nielsen, P. R., Sobott, F., Robinson, C. V., Jackson, S. E., and Laue, E. D. (2004) Biochemical and structural studies of the interaction of Cdc37 with Hsp90 J. Mol. Biol. 340, 891-907
24. Bandhakavi, S., McCann, R. O., Hanna, D. E., and Glover, C. V. (2003) A positive feedback loop between protein kinase CKII and Cdc37 promotes the activity of multiple protein kinases J. Biol. Chem. 278, 2829-2836
25. Mandal, A. K., Lee, P., Chen, J. A., Nillegoda, N., Heller, A., DiStasio, S., Oen, H., Victor, J., Nair, D. M., Brodsky, J. L., and Caplan, A. J. (2007) Cdc37 has distinct roles in protein kinase quality control that protect nascent chains from degradation and promote posttranslational maturation J. Cell Biol. 176, 319-328
26. Sreeramulu, S., Jonker, H. R., Langer, T., Richter, C., Lancaster, C. R., and Schwalbe, H. (2009) The human Cdc37·Hsp90 complex studied by heteronuclear NMR spectroscopy J. Biol. Chem. 284, 3885-3896
27. Dunker, A. K., Cortese, M. S., Romero, P., Iakoucheva, L. M., and Uversky, V. N. (2005) Flexible nets. The roles of intrinsic disorder in protein interaction networks FEBS J. 272, 5129-5148
28. Dyson, H. J. and Wright, P. E. (2005) Intrinsically unstructured proteins and their functions Nat. Rev. Mol. Cell Biol. 6, 197-208
29. Babu, M. M., Kriwacki, R. W., and Pappu, R. V. (2012) Structural biology. Versatility from protein disorder Science 337, 1460-1461
30. Espinoza-Fonseca, L. M. (2009) Reconciling binding mechanisms of intrinsically disordered proteins Biochem. Biophys. Res. Commun. 382, 479-482
31. Ward, J. J., Sodhi, J. S., McGuffin, L. J., Buxton, B. F., and Jones, D. T. (2004) Prediction and functional analysis of native disorder in proteins from the three kingdoms of life J. Mol. Biol. 337, 635-645
32. Dunker, A. K., Lawson, J. D., Brown, C. J., Williams, R. M., Romero, P., Oh, J. S., Oldfield, C. J., Campen, A. M., Ratliff, C. M., Hipps, K. W., Ausio, J., Nissen, M. S., Reeves, R., Kang, C., Kissinger, C. R., Bailey, R. W., Griswold, M. D., Chiu, W., Garner, E. C., and Obradovic, Z. (2001) Intrinsically disordered protein J. Mol. Graphics Modell. 19, 26-59
33. Kussie, P. H., Gorina, S., Marechal, V., Elenbaas, B., Moreau, J., Levine, A. J., and Pavletich, N. P. (1996) Structure of the MDM2 oncoprotein bound to the p53 tumor suppressor transactivation domain Science 274, 948-953
34. Kar, S., Sakaguchi, K., Shimohigashi, Y., Samaddar, S., Banerjee, R., Basu, G., Swaminathan, V., Kundu, T. K., and Roy, S. (2002) Effect of phosphorylation on the structure and fold of transactivation domain of p53 J. Biol. Chem. 277, 15579-15585
35. Lum, J. K., Neuweiler, H., and Fersht, A. R. (2012) Long-range modulation of chain motions within the intrinsically disordered transactivation domain of tumor suppressor p53 J. Am. Chem. Soc. 134, 1617-1622
36. McDowell, C., Chen, J., and Chen, J. (2013) Potential conformational heterogeneity of p53 bound to S100B(betabeta) J. Mol. Biol. 425, 999-1010
37. Rajagopalan, S., Jaulent, A. M., Wells, M., Veprintsev, D. B., and Fersht, A. R. (2008) 14-3-3 activation of DNA binding of p53 by enhancing its association into tetramers Nucleic Acids Res. 36, 5983-5991
38. van Dieck, J., Teufel, D. P., Jaulent, A. M., Fernandez-Fernandez, M. R., Rutherford, T. J., Wyslouch-Cieszynska, A., and Fersht, A. R. (2009) Posttranslational modifications affect the interaction of S100 proteins with tumor suppressor p53 J. Mol. Biol. 394, 922-930
39. Iakoucheva, L. M., Brown, C. J., Lawson, J. D., Obradovic, Z., and Dunker, A. K. (2002) Intrinsic disorder in cell-signaling and cancer-associated proteins J. Mol. Biol. 323, 573-584
40. Xie, H., Vucetic, S., Iakoucheva, L. M., Oldfield, C. J., Dunker, A. K., Uversky, V. N., and Obradovic, Z. (2007) Functional anthology of intrinsic disorder. 1. Biological processes and functions of proteins with long disordered regions J. Proteome Res. 6, 1882-1898
41. Ou, L., Waddell, M. B., and Kriwacki, R. W. (2012) Mechanism of cell cycle entry mediated by the intrinsically disordered protein p27(Kip1) ACS Chem. Biol. 7, 678-682
42. Peng, Z., Xue, B., Kurgan, L., and Uversky, V. N. (2013) Resilience of death: intrinsic disorder in proteins involved in the programmed cell death Cell Death Differ. 20, 1257-1267
43. Kovacs, D. and Tompa, P. (2012) Diverse functional manifestations of intrinsic structural disorder in molecular chaperones Biochem. Soc. Trans. 40, 963-968
44. Bardwell, J. C. and Jakob, U. (2012) Conditional disorder in chaperone action Trends Biochem. Sci. 37, 517-525
45. Tompa, P. and Kovacs, D. (2010) Intrinsically disordered chaperones in plants and animals Biochem. Cell Biol. 88, 167-174
46. Iakoucheva, L. M., Radivojac, P., Brown, C. J., OConnor, T. R., Sikes, J. G., Obradovic, Z., and Dunker, A. K. (2004) The importance of intrinsic disorder for protein phosphorylation Nucleic Acids Res. 32, 1037-1049
47. Eisenhaber, B. and Eisenhaber, F. (2007) Posttranslational modifications and subcellular localization signals: indicators of sequence regions without inherent 3D structure? Curr. Protein Pept. Sci. 8, 197-203
48. Fukuchi, S., Hosoda, K., Homma, K., Gojobori, T., and Nishikawa, K. (2011) Binary classification of protein molecules into intrinsically disordered and ordered segments BMC Struct. Biol. 11, 29
49. Kurotani, A., Tokmakov, A. A., Kuroda, Y., Fukami, Y., Shinozaki, K., and Sakurai, T. (2014) Correlations between predicted protein disorder and post-translational modifications in plants Bioinformatics 30, 1095-1103
50. Bozoky, Z., Krzeminski, M., Chong, P. A., and Forman-Kay, J. D. (2013) Structural changes of CFTR R region upon phosphorylation: a plastic platform for intramolecular and intermolecular interactions FEBS J. 280, 4407-4416
51. Chen, L., Brown, J. W., Mok, Y. F., Hatters, D. M., and McKnight, C. J. (2013) The allosteric mechanism induced by protein kinase A (PKA) phosphorylation of dematin (band 4.9) J. Biol. Chem. 288, 8313-8320
52. Chen, Y. X., Du, J. T., Zhou, L. X., Liu, X. H., Zhao, Y. F., Nakanishi, H., and Li, Y. M. (2006) Alternative O-GlcNAcylation/O-phosphorylation of Ser16 induce different conformational disturbances to the N terminus of murine estrogen receptor beta Chem. Biol. 13, 937-944
53. Jones, D. T. (1999) Protein secondary structure prediction based on position-specific scoring matrices J. Mol. Biol. 292, 195-202
54. Buchan, D. W., Minneci, F., Nugent, T. C., Bryson, K., and Jones, D. T. (2013) Scalable web services for the PSIPRED protein analysis workbench Nucleic Acids Res. 41, W349-357
55. Xue, B., Dunbrack, R. L., Williams, R. W., Dunker, A. K., and Uversky, V. N. (2010) PONDR-FIT: a meta-predictor of intrinsically disordered amino acids Biochim. Biophys. Acta 1804, 996-1010
56. Radivojac, P., Obradovic, Z., Brown, C. J., and AK, D. (2003) Prediction of boundaries between intrinsically ordered and disordered protein regions Pac. Symp. Biocomput. 216-227
57. Romero, O. and Dunker, K. (1997) Sequence data analysis for long disordered regions prediction in the calcineurin family Genome Inf. Ser. 8, 110-124
58. Romero, P., Obradovic, Z., Li, X., Garner, E. C., Brown, C. J., and Dunker, A. K. (2001) Sequence complexity of disordered protein Proteins 42, 38-48
59. Li, X., Romero, P., Rani, M., Dunker, A. K., and Obradovic, Z. (1999) Predicting protein disorder for N-, C-, and internal regions Genome Inf. Ser. 10, 30-40
60. Miyata, Y. and Nishida, E. (2007) Analysis of the CK2-dependent phosphorylation of serine 13 in Cdc37 using a phospho-specific antibody and phospho-affinity gel electrophoresis FEBS J. 274, 5690-5703
61. Miyata, Y. and Nishida, E. (2004) CK2 controls multiple protein kinases by phosphorylating a kinase-targeting molecular chaperone, Cdc37 Mol. Cell. Biol. 24, 4065-4074
62. Gerbin, C. S. and Landgraf, R. (2010) Geldanamycin selectively targets the nascent form of ERBB3 for degradation Cell Stress Chaperones 15, 529-544
63. Xu, W., Mimnaugh, E., Rosser, M. F., Nicchitta, C., Marcu, M., Yarden, Y., and Neckers, L. (2001) Sensitivity of mature Erbb2 to geldanamycin is conferred by its kinase domain and is mediated by the chaperone protein Hsp90 J. Biol. Chem. 276, 3702-3708
64. Alimandi, M., Romano, A., Curia, M. C., Muraro, R., Fedi, P., Aaronson, S. A., Di Fiore, P. P., and Kraus, M. H. (1995) Cooperative signaling of ErbB3 and ErbB2 in neoplastic transformation and human mammary carcinomas Oncogene 10, 1813-1821
65. Kraus, M. H., Popescu, N. C., Amsbaugh, S. C., and King, C. R. (1987) Overexpression of the EGF receptor-related proto-oncogene erbB-2 in human mammary tumor cell lines by different molecular mechanisms EMBO J. 6, 605-610
66. Sreerama, N. and Woody, R. W. (2000) Estimation of protein secondary structure from circular dichroism spectra: comparison of CONTIN, SELCON, and CDSSTR methods with an expanded reference set Anal. Biochem. 287, 252-260
67. Fink, A. L., Calciano, L. J., Goto, Y., Kurotsu, T., and Palleros, D. R. (1994) Classification of acid denaturation of proteins: intermediates and unfolded states Biochemistry 33, 12504-12511
68. Eilers, M. and Schatz, G. (1986) Binding of a specific ligand inhibits import of a purified precursor protein into mitochondria Nature 322, 228-232
69. Xu, W., Mollapour, M., Prodromou, C., Wang, S., Scroggins, B. T., Palchick, Z., Beebe, K., Siderius, M., Lee, M. J., Couvillon, A., Trepel, J. B., Miyata, Y., Matts, R., and Neckers, L. (2012) Dynamic tyrosine phosphorylation modulates cycling of the HSP90-P50(CDC37)-AHA1 chaperone machine Mol. Cell 47, 434-443
70. Zetina, C. R. (2001) A conserved helix-unfolding motif in the naturally unfolded proteins Proteins 44, 479-483
71. Smart, J. L. and McCammon, J. A. (1999) Phosphorylation stabilizes the N-termini of alpha-helices Biopolymers 49, 225-233
72. Szilak, L., Moitra, J., Krylov, D., and Vinson, C. (1997) Phosphorylation destabilizes alpha-helices Nat. Struct. Biol. 4, 112-114
73. Pinna, L. A. (2002) Protein kinase CK2: a challenge to canons J. Cell Sci. 115, 3873-3878
74. Shao, J., Prince, T., Hartson, S. D., and Matts, R. L. (2003) Phosphorylation of serine 13 is required for the proper function of the Hsp90 co-chaperone, Cdc37 J. Biol. Chem. 278, 38117-38120