The co-chaperone Cdc37 regulates the rabies virus phosphoprotein stability by targeting to Hsp90AA1 machinery

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Xu, Yunbin ^a,b   Liu, Fei ^c   Liu, Juan ^a,b   Wang, Dandan ^a   Yan, Yan ^a,b   Ji, Senlin ^c   Zan, Jie ^a,b   Zhou, Jiyong ^a,b,c  

^a ZHEJIANG UNIVERSITY   (China)

^b ZHEJIANG UNIVERSITY   (China)

^c NANJING AGRICULTURAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CDC37 PROTEIN, MOUSE; CELL CYCLE PROTEIN; CHAPERONE; HEAT SHOCK PROTEIN 90; P PHOSPHOPROTEIN, RABIES VIRUS; PHOSPHOPROTEIN; PROTEIN BINDING; VIRAL PROTEIN;

ALLOSTERISM; ANIMAL; CELL LINE; CHEMISTRY; GENE EXPRESSION REGULATION; METABOLISM; MOUSE; PATHOGENICITY; PHOSPHORYLATION; PROTEIN CONFORMATION; PROTEIN STABILITY; RABIES; RABIES VIRUS; VIROLOGY;

ALLOSTERIC REGULATION; ANIMALS; CELL CYCLE PROTEINS; CELL LINE; GENE EXPRESSION REGULATION; HSP90 HEAT-SHOCK PROTEINS; MICE; MOLECULAR CHAPERONES; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN STABILITY; RABIES; RABIES VIRUS; VIRAL STRUCTURAL PROTEINS;

EID: 84973364581     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep27123     Document Type: Article

References (48)

1. Fu, Z. F. Genetic comparison of the rhabdoviruses from animals and plants. Curr Top Microbiol Immunol 292, 1-24, doi: 10.1007/3-540-27485-5-1 (2005).
2. Lafon, M. Evasive strategies in rabies virus infection. Adv Virus Res 79, 33-53, doi: 10.1016/B978-0-12-387040-7.00003-2 (2011).
3. Lahaye, X. et al. Functional characterization of Negri bodies (NBs) in rabies virus-infected cells: Evidence that NBs are sites of viral transcription and replication. J Virol 83, 7948-7958, doi: 10.1128/JVI.00554-09 (2009).
4. Menager, P. et al. Toll-like receptor 3 (TLR3) plays a major role in the formation of rabies virus Negri Bodies. PLoS Pathog 5, e1000315, doi: 10.1371/journal.ppat.1000315 (2009).
5. Lahaye, X., Vidy, A., Fouquet, B. & Blondel, D. Hsp70 protein positively regulates rabies virus infection. J Virol 86, 4743-4751, doi: 10.1128/JVI.06501-11 (2012).
6. Zhang, J. et al. Cellular chaperonin CCTgamma contributes to rabies virus replication during infection. J Virol 87, 7608-7621, doi: 10.1128/JVI.03186-12 (2013).
7. Kopito, R. R. Aggresomes, inclusion bodies and protein aggregation. Trends Cell Biol 10, 524-530, doi: 10.1016/S0962- 8924(00)01852-3 (2000).
8. Borkovich, K. A., Farrelly, F. W., Finkelstein, D. B., Taulien, J. & Lindquist, S. hsp82 is an essential protein that is required in higher concentrations for growth of cells at higher temperatures. Mol Cell Biol 9, 3919-3930, doi: 10.1128/MCB.9.9.3919 (1989).
9. Taipale, M., Jarosz, D. F. & Lindquist, S. HSP90 at the hub of protein homeostasis: emerging mechanistic insights. Nat Rev Mol Cell Biol 11, 515-528, doi: 10.1038/nrm2918 (2010).
10. Didenko, T., Duarte, A. M., Karagoz, G. E. & Rudiger, S. G. Hsp90 structure and function studied by NMR spectroscopy. Biochim Biophys Acta 1823, 636-647, doi: 10.1016/j.bbamcr.2011.11.009 (2012).
11. Prodromou, C. et al. The ATPase cycle of Hsp90 drives a molecular 'clamp' via transient dimerization of the N-terminal domains. EMBO J 19, 4383-4392, doi: 10.1093/emboj/19.16.4383 (2000).
12. Young, J. C., Moarefi, I. & Hartl, F. U. Hsp90: a specialized but essential protein-folding tool. J Cell Biol 154, 267-273, doi: 10.1083/jcb.200104079 (2001).
13. Grenert, J. P. et al. The amino-terminal domain of heat shock protein 90 (hsp90) that binds geldanamycin is an ATP/ADP switch domain that regulates hsp90 conformation. J Biol Chem 272, 23843-23850, doi: 10.1074/jbc.272.38.23843 (1997).
14. Prodromou, C. et al. Identification and structural characterization of the ATP/ADP-binding site In the Hsp90 molecular chaperone Cell 90, 65-75, doi: 10.1016/S0092-8674(00)80314-1 (1997).
15. Stebbins, C. E. et al. Crystal structure of an Hsp90-geldanamycin complex: targeting of a protein chaperone by an antitumor agent. Cell 89, 239-250, doi: 10.1016/S0092-8674(00)80203-2 (1997).
16. Stepanova, L., Leng, X., Parker, S. B. & Harper, J. W. Mammalian p50Cdc37 is a protein kinase-targeting subunit of Hsp90 that binds and stabilizes Cdk4. Genes Dev 10, 1491-1502, doi: 10.1101/gad.10.12.1491 (1996).
17. Roe, S. M. et al. The Mechanism of Hsp90 regulation by the protein kinase-specific cochaperone p50(cdc37). Cell 116, 87-98, doi: 10.1016/S0092-8674(03)01027-4 (2004).
18. Grammatikakis, N., Lin, J. H., Grammatikakis, A., Tsichlis, P. N. & Cochran, B. H. p50(cdc37) acting in concert with Hsp90 is required for Raf-1 function. Mol Cell Biol 19, 1661-1672, doi: 10.1128/MCB.19.3.1661 (1999).
19. Rao, J. et al. Functional interaction of human Cdc37 with the androgen receptor but not with the glucocorticoid receptor. J Biol Chem 276, 5814-5820, doi: 10.1074/jbc.M007385200 (2001).
20. Shao, J. et al. Hsp90 regulates p50(cdc37) function during the biogenesis of the activeconformation of the heme-regulated eIF2 alpha kinase. J Biol Chem 276, 206-214, doi: 10.1074/jbc.M007583200 (2001).
21. Zhang, T. et al. A novel Hsp90 inhibitor to disrupt Hsp90/Cdc37 complex against pancreatic cancer cells. Mol Cancer Ther 7, 162-170, doi: 10.1158/1535-7163.MCT-07-0484 (2008).
22. Zhang, T. et al. Characterization of celastrol to inhibit hsp90 and cdc37 interaction. J Biol Chem 284, 35381-35389, doi: 10.1074/jbc. M109.051532 (2009).
23. Smith, J. R. et al. Restricting direct interaction of CDC37 with HSP90 does not compromise chaperoning of client proteins. Oncogene 34, 15-26, doi: 10.1038/onc.2013.519 (2013).
24. Nomura, N., Nomura, M., Newcomb, E. W. & Zagzag, D. Geldanamycin induces G2 arrest in U87MG glioblastoma cells through downregulation of Cdc2 and cyclin B1. Biochem Pharmacol 73, 1528-1536, doi: 10.1016/j.bcp.2007.01.022 (2007).
25. Sun, X. et al. Hsp90 inhibitors block outgrowth of EBV-infected malignant cells in vitro and in vivo through an EBNA1-dependent mechanism. Proc Natl Acad Sci USA 107, 3146-3151, doi: 10.1073/pnas.0910717107 (2010).
26. Qing, G., Yan, P. & Xiao, G. Hsp90 inhibition results in autophagy-mediated proteasome-independent degradation of IkappaB kinase (IKK). Cell Res 16, 895-901, doi: 10.1038/sj.cr.7310109 (2006).
27. Miyata, Y. & Nishida, E. CK2 controls multiple protein kinases by phosphorylating a kinase-targeting molecular chaperone, Cdc37. Mol Cell Biol 24, 4065-4074, doi: 10.1128/MCB.24.9.4065-4074.2004 (2004).
28. Shao, J., Prince, T., Hartson, S. D. & Matts, R. L. Phosphorylation of serine 13 is required for the proper function of the Hsp90 cochaperone, Cdc37. J Biol Chem 278, 38117-38120, doi: 10.1074/jbc.C300330200 (2003).
29. Taipale, M. et al. Quantitative analysis of HSP90-client interactions reveals principles of substrate recognition. Cell 150, 987-1001, doi: 10.1016/j.cell.2012.06.047(2012).
30. Geller, R., Taguwa, S. & Frydman, J. Broad action of Hsp90 as a host chaperone required for viral replication. Biochim Biophys Acta 1823, 698-706, doi: 10.1016/j.bbamcr.2011.11.007 (2012).
31. Hu, J., Flores, D., Toft, D., Wang, X. & Nguyen, D. Requirement of Heat Shock Protein 90 for Human Hepatitis B Virus Reverse Transcriptase Function. J Virol 78, 13122-13131, doi: 10.1128/JVI.78.23.13122-13131.2004 (2004).
32. Naito, T., Momose, F., Kawaguchi, A. & Nagata, K. Involvement of Hsp90 in assembly and nuclear import of influenza virus RNA polymerase subunits. J Virol 81, 1339-1349, doi: 10.1128/JVI.01917-06 (2007).
33. Chase, G. et al. Hsp90 inhibitors reduce influenza virus replication in cell culture. Virology 377, 431-439, doi: 10.1016/j. virol.2008.04.040 (2008).
34. Wang, X., Grammatikakis, N. & Hu, J. Role of p50/CDC37 in hepadnavirus assembly and replication. J Biol Chem 277, 24361-24367, doi: 10.1074/jbc.M202198200 (2002).
35. Sun, X. et al. Hsp90 inhibitor 17-DMAG decreases expression of conserved herpesvirus protein kinases and reduces virus production in Epstein-Barr virus-infected cells. J Virol 87, 10126-10138, doi: 10.1128/JVI.01671-13 (2013).
36. Gupta, A. K., Blondel, D., Choudhary, S. & Banerjee, A. K. The phosphoprotein of rabies virus is phosphorylated by a unique cellular protein kinase and specific isomers of protein kinase C. J Virol 74, 91-98, doi: 10.1128/JVI.74.1.91-98.2000 (2000).
37. MacLean, M. & Picard, D. Cdc37 goes beyond Hsp90 and kinases. Cell Stress Chaperones 8, 114-119, doi: 10.1379/1466- 1268(2003)008 〈0114:CGBHAK〉 2.0.CO;2:14627196 (2003).
38. Miyata, Y. & Nishida, E. CK2 binds, phosphorylates, and regulates its pivotal substrate Cdc37, an Hsp90-cochaperone. Mol Cell Biochem 274, 171-179, doi: 10.1007/s11010-005-2949-8 (2005).
39. Mavrakis, M. et al. Rabies virus chaperone: identification of the phosphoprotein peptide that keeps nucleoprotein soluble and free from non-specific RNA. Virology 349, 422-429, doi: 10.1016/j.virol.2006.01.030 (2006).
40. Green, T. J. & Luo, M. Structure of the Vesicular Stomatitis Virus Nucleocapsid in Complex with the Nucleocapsid-Binding Domain of the Small Polymerase Cofactor, P. Proc Natl Acad Sci USA 106, 11713-11718, doi: 10.1073/pnas.0903228106 (2009).
41. Pasdeloup, D. et al. Nucleocytoplasmic shuttling of the rabies virus P protein requires a nuclear localization signal and a CRM1- dependent nuclear export signal. Virology 334, 284-293, doi: 10.1016/j.virol.2005.02.005 (2005).
42. Raux, H., Flamand, A. & Blondel, D. Interaction of the rabies virus P protein with the LC8 dynein light chain. J Virol 74, 10212-10216, doi: 10.1128/JVI.74.21.10212-10216.2000 (2000).
43. Brzozka, K., Finke, S. & Conzelmann, K. K. Identification of the rabies virus alpha/beta interferon antagonist: phosphoprotein P interferes with phosphorylation of interferon regulatory factor 3. J Virol 79, 7673-7681, doi: 10.1128/JVI.79.12.7673-7681.2005 (2005).
44. Brzozka, K., Finke, S. & Conzelmann, K. K. Inhibition of interferon signaling by rabies virus phosphoprotein P: activationdependent binding of STAT1 and STAT2. J Virol 80, 2675-2683, doi: 10.1128/JVI.80.6.2675-2683.2006 (2006).
45. Lieu, K. G. et al. The rabies virus interferon antagonist P protein interacts with activated STAT3 and inhibits Gp130 receptor signaling. J Virol 87, 8261-8265, doi: 10.1128/JVI.00989-13JVI.00 989-13 (2013).
46. Zhang, J. et al. Efficient generation of monoclonal antibodies against major structural proteins of rabies virus with suckling mouse brain antigen. Monoclon Antib Immunodiagn Immunother 33, 94-100, doi: 10.1089/mab.2013.0087 (2014).
47. Cao, J. et al. Circovirus transport proceeds via direct interaction of the cytoplasmic dynein IC1 subunit with the viral capsid protein. J Virol 89, 2777-2791, doi: 10.1128/JVI.03117-14JVI.03117-14 (2015).
48. Zhang, X. et al. Differential proteome analysis of host cells infected with porcine circovirus type 2. J Proteome Res 8, 5111-5119, doi: 10.1021/pr900488q (2009).