An Acetylation Site in the Middle Domain of Hsp90 Regulates Chaperone Function

Molecular Cell

Volumn 25, Issue 1, 2007, Pages 151-159

  Scroggins, Bradley T ^a   Robzyk, Kenneth ^b   Wang, Dongxia ^c   Marcu, Monica G ^a   Tsutsumi, Shinji ^a   Beebe, Kristin ^a   Cotter, Robert J ^c   Felts, Sara ^d,e   Toft, David ^d,e   Karnitz, Larry ^d,e   Rosen, Neal ^b   Neckers, Len ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^c JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d MAYO GRADUATE SCHOOL   (United States)

^e MAYO CLINIC   (United States)

Author keywords

PROTEINS

Indexed keywords

HEAT SHOCK PROTEIN 90; HISTONE DEACETYLASE 6; HISTONE DEACETYLASE INHIBITOR; LYSINE;

ACETYLATION; ANIMAL CELL; ARTICLE; DEACETYLATION; ENZYME INHIBITION; HUMAN; HUMAN CELL; MALIGNANT TRANSFORMATION; MUTATION; NONHUMAN; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROCESSING; SIGNAL TRANSDUCTION;

ACETYLATION; AMINO ACID SEQUENCE; ANIMALS; CERCOPITHECUS AETHIOPS; COS CELLS; HSP90 HEAT-SHOCK PROTEINS; HUMANS; LYSINE; MICE; MOLECULAR SEQUENCE DATA; MUTANT PROTEINS; MUTATION; NIH 3T3 CELLS; PROTEIN BINDING; PROTEIN KINASES; PROTEIN STRUCTURE, TERTIARY; SACCHAROMYCES CEREVISIAE;

EID: 33846014703     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2006.12.008     Document Type: Article

References (36)

1. Ali M.M., Roe S.M., Vaughan C.K., Meyer P., Panaretou B., Piper P.W., Prodromou C., and Pearl L.H. Crystal structure of an Hsp90-nucleotide-p23/Sba1 closed chaperone complex. Nature 440 (2006) 1013-1017
2. Arlander S.J., Felts S.J., Wagner J.M., Stensgard B., Toft D.O., and Karnitz L.M. Chaperoning checkpoint kinase 1 (Chk1), an Hsp90 client, with purified chaperones. J. Biol. Chem. 281 (2006) 2989-2998
3. Bali P., Pranpat M., Bradner J., Balasis M., Fiskus W., Guo F., Rocha K., Kumaraswamy S., Boyapalle S., Atadja P., et al. Inhibition of histone deacetylase 6 acetylates and disrupts the chaperone function of heat shock protein 90: a novel basis for antileukemia activity of histone deacetylase inhibitors. J. Biol. Chem. 280 (2005) 26729-26734
4. Bali P., Pranpat M., Swaby R., Fiskus W., Yamaguchi H., Balasis M., Rocha K., Wang H.G., Richon V., and Bhalla K. Activity of suberoylanilide hydroxamic acid against human breast cancer cells with amplification of her-2. Clin. Cancer Res. 11 (2005) 6382-6389
5. Blagg B.S., and Kerr T.D. Hsp90 inhibitors: small molecules that transform the Hsp90 protein folding machinery into a catalyst for protein degradation. Med. Res. Rev. 26 (2006) 310-338
6. Blagosklonny M.V., Robey R., Sackett D.L., Du L., Traganos F., Darzynkiewicz Z., Fojo T., and Bates S.E. Histone deacetylase inhibitors all induce p21 but differentially cause tubulin acetylation, mitotic arrest, and cytotoxicity. Mol. Cancer Ther. 1 (2002) 937-941
7. Chadli A., Bouhouche I., Sullivan W., Stensgard B., McMahon N., Catelli M.G., and Toft D.O. Dimerization and N-terminal domain proximity underlie the function of the molecular chaperone heat shock protein 90. Proc. Natl. Acad. Sci. USA 97 (2000) 12524-12529
8. Furumai R., Matsuyama A., Kobashi N., Lee K.H., Nishiyama M., Nakajima H., Tanaka A., Komatsu Y., Nishino N., Yoshida M., and Horinouchi S. FK228 (depsipeptide) as a natural prodrug that inhibits class I histone deacetylases. Cancer Res. 62 (2002) 4916-4921
9. Hartson S.D., Thulasiraman V., Huang W., Whitesell L., and Matts R.L. Molybdate inhibits hsp90, induces structural changes in its C-terminal domain, and alters its interactions with substrates. Biochemistry 38 (1999) 3837-3849
10. Huai Q., Wang H., Liu Y., Kim H.Y., Toft D., and Ke H. Structures of the N-terminal and middle domains of E. coli Hsp90 and conformation changes upon ADP binding. Structure 13 (2005) 579-590
11. Isaacs J.S., Jung Y.J., Mimnaugh E.G., Martinez A., Cuttitta F., and Neckers L.M. Hsp90 regulates a von Hippel Lindau-independent hypoxia-inducible factor-1 alpha-degradative pathway. J. Biol. Chem. 277 (2002) 29936-29944
12. Kim M.Y., Woo E.M., Chong Y.T., Homenko D.R., and Kraus W.L. Acetylation of estrogen receptor alpha by p300 at lysines 266 and 268 enhances the DNA binding and transactivation activities of the receptor. Mol. Endocrinol. 20 (2006) 1479-1493 10.1210/me.2005-0531 Published online February 23, 2006
13. Kovacs J.J., Murphy P.J., Gaillard S., Zhao X., Wu J.T., Nicchitta C.V., Yoshida M., Toft D.O., Pratt W.B., and Yao T.P. HDAC6 regulates Hsp90 acetylation and chaperone-dependent activation of glucocorticoid receptor. Mol. Cell 18 (2005) 601-607
14. Louvion J.F., Abbas-Terki T., and Picard D. Hsp90 is required for pheromone signaling in yeast. Mol. Biol. Cell 9 (1998) 3071-3083
15. MacLean M.J., Llordella M.M., Bot N., and Picard D. A yeast-based assay reveals a functional defect of the Q488H polymorphism in human Hsp90alpha. Biochem. Biophys. Res. Commun. 337 (2005) 133-137
16. Meyer P., Prodromou C., Liao C., Hu B., Mark Roe S., Vaughan C.K., Vlasic I., Panaretou B., Piper P.W., and Pearl L.H. Structural basis for recruitment of the ATPase activator Aha1 to the Hsp90 chaperone machinery. EMBO J. 23 (2004) 511-519
17. Mimnaugh E.G., Worland P.J., Whitesell L., and Neckers L.M. Possible role for serine/threonine phosphorylation in the regulation of the heteroprotein complex between the hsp90 stress protein and the pp60v-src tyrosine kinase. J. Biol. Chem. 270 (1995) 28654-28659
18. Murphy P.J., Morishima Y., Kovacs J.J., Yao T.P., and Pratt W.B. Regulation of the dynamics of hsp90 action on the glucocorticoid receptor by acetylation/deacetylation of the chaperone. J. Biol. Chem. 280 (2005) 33792-33799
19. Nathan D.F., and Lindquist S. Mutational analysis of Hsp90 function: interactions with a steroid receptor and a protein kinase. Mol. Cell. Biol. 15 (1995) 3917-3925
20. Nemoto T., Sato N., Iwanari H., Yamashita H., and Takagi T. Domain structures and immunogenic regions of the 90-kDa heat-shock protein (HSP90). Probing with a library of anti-HSP90 monoclonal antibodies and limited proteolysis. J. Biol. Chem. 272 (1997) 26179-26187
21. Nimmanapalli R., Fuino L., Bali P., Gasparetto M., Glozak M., Tao J., Moscinski L., Smith C., Wu J., Jove R., et al. Histone deacetylase inhibitor LAQ824 both lowers expression and promotes proteasomal degradation of Bcr-Abl and induces apoptosis of imatinib mesylate-sensitive or -refractory chronic myelogenous leukemia-blast crisis cells. Cancer Res. 63 (2003) 5126-5135
22. Ogiso H., Kagi N., Matsumoto E., Nishimoto M., Arai R., Shirouzu M., Mimura J., Fujii-Kuriyama Y., and Yokoyama S. Phosphorylation analysis of 90 kDa heat shock protein within the cytosolic arylhydrocarbon receptor complex. Biochemistry 43 (2004) 15510-15519
23. Picard D., Khursheed B., Garabedian M.J., Fortin M.G., Lindquist S., and Yamamoto K.R. Reduced levels of hsp90 compromise steroid receptor action in vivo. Nature 348 (1990) 166-168
24. Piper P.W., Panaretou B., Millson S.H., Trumana A., Mollapour M., Pearl L.H., and Prodromou C. Yeast is selectively hypersensitised to heat shock protein 90 (Hsp90)-targetting drugs with heterologous expression of the human Hsp90beta, a property that can be exploited in screens for new Hsp90 chaperone inhibitors. Gene 302 (2003) 165-170
25. Rose A.B., and Broach J.R. Propagation and expression of cloned genes in yeast: 2-microns circle-based vectors. Methods Enzymol. 185 (1990) 234-279
26. Sartor O., McLellan C.A., and Chiueh T. Comparison of src-family cDNAs reveals distinct mechanisms underlying focus formation in transfected fibroblasts. J. Biol. Chem. 267 (1992) 21044-21051
27. Sato S., Fujita N., and Tsuruo T. Modulation of Akt kinase activity by binding to Hsp90. Proc. Natl. Acad. Sci. USA 97 (2000) 10832-10837
28. Sikorski R.S., and Hieter P. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122 (1989) 19-27
29. Tzahar E., Waterman H., Chen X., Levkowitz G., Karunagaran D., Lavi S., Ratzkin B.J., and Yarden Y. A hierarchical network of interreceptor interactions determines signal transduction by Neu differentiation factor/neuregulin and epidermal growth factor. Mol. Cell. Biol. 16 (1996) 5276-5287
30. Wandinger S.K., Suhre M.H., Wegele H., and Buchner J. The phosphatase Ppt1 is a dedicated regulator of the molecular chaperone Hsp90. EMBO J. 25 (2006) 367-376
31. Wang Y.H., Tsay Y.G., Tan B.C., Lo W.Y., and Lee S.C. Identification and characterization of a novel p300-mediated p53 acetylation site, lysine 305. J. Biol. Chem. 278 (2003) 25568-25576
32. Whitesell L., Mimnaugh E.G., De Costa B., Myers C.E., and Neckers L.M. Inhibition of heat shock protein HSP90-pp60v-src heteroprotein complex formation by benzoquinone ansamycins: essential role for stress proteins in oncogenic transformation. Proc. Natl. Acad. Sci. USA 91 (1994) 8324-8328
33. Xu Y., and Lindquist S. Heat-shock protein hsp90 governs the activity of pp60v-src kinase. Proc. Natl. Acad. Sci. USA 90 (1993) 7074-7078
34. Xu W., Marcu M., Yuan X., Mimnaugh E., Patterson C., and Neckers L. Chaperone-dependent E3 ubiquitin ligase CHIP mediates a degradative pathway for c-ErbB2/Neu. Proc. Natl. Acad. Sci. USA 99 (2002) 12847-12852
35. Yu X., Guo Z.S., Marcu M.G., Neckers L., Nguyen D.M., Chen G.A., and Schrump D.S. Modulation of p53, ErbB1, ErbB2, and Raf-1 expression in lung cancer cells by depsipeptide FR901228. J. Natl. Cancer Inst. 94 (2002) 504-513
36. Zhao Y.G., Gilmore R., Leone G., Coffey M.C., Weber B., and Lee P.W. Hsp90 phosphorylation is linked to its chaperoning function. Assembly of the reovirus cell attachment protein. J. Biol. Chem. 276 (2001) 32822-32827