Tosylcyclonovobiocic acids promote cleavage of the hsp90-associated cochaperone p23

Biochemical and Biophysical Research Communications

Volumn 379, Issue 2, 2009, Pages 514-518

  Radanyi, Christine ^a   Le Bras, Gaëlle ^a   Bouclier, Céline ^a   Messaoudi, Samir ^a   Peyrat, Jean François ^a   Brion, Jean Daniel ^a   Alami, Mouâd ^a   Renoir, Jack Michel ^a  

^a UNIVERSITÉ PARIS SACLAY   (France)

Author keywords

Apoptosis; Cell cycle; ER stress; Heat shock protein 90; hsp90; hsp90 inhibitors; Molecular cochaperone; Novobiocin; p23; RNA interference

Indexed keywords

BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; CHAPERONE; COCHAPERONE P23; HEAT SHOCK PROTEIN 90; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; NOVOBIOCIN; SMALL INTERFERING RNA; TOSYLCYCLONOVOBIOCIC ACID; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CELL CYCLE ARREST; CELL DEATH; CELL STRAIN MCF 7; COLON CANCER; CONTROLLED STUDY; ENZYME ACTIVATION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PROCESSING; WESTERN BLOTTING;

EID: 58249122591     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2008.12.102     Document Type: Article

References (40)

1. Pratt W.B., and Toft D.O. Regulation of signaling protein function and trafficking by the hsp90/hsp70-based chaperone machinery. Exp. Biol. Med. 228 (2003) 111-133
2. Bishop S.C., Burlison J.A., and Blagg B.S. Hsp90: a novel target for the disruption of multiple signaling cascades. Curr. Cancer Drug Targets 7 (2007) 369-388
3. Workman P., Burrows F., Neckers L., and Rosen N. Drugging the cancer chaperone HSP90, combinatorial therapeutic exploitation of oncogene addiction ant tumor stress. Ann. N. Y. Acad. Sci. 1113 (2007) 202-216
4. Xu W., and Neckers L. Targeting the molecular chaperone heat shock protein 90 provides a multifaceted effect on diverse cell signaling pathways of cancer cells. Clin. Cancer Res. 13 (2007) 1625-1629
5. Solit D.B., and Chiosis G. Development and application of Hsp90 inhibitors. Drug Discov. Today 13 (2008) 38-43
6. Sullivan W.P., Owen B.A., and Toft D.O. The influence of ATP and p23 on the conformation of hsp90. J. Biol. Chem. 277 (2002) 45942-45948
7. Pearl L.H., and Prodromou C. Structure and mechanism of the hsp90 molecular chaperone machinery. Annu. Rev. Biochem. 75 (2006) 271-294
8. Smith D.F., Faber L.E., and Toft D.O. Purification of unactivated progesterone receptor and identification of novel receptor-associated proteins. J. Biol. Chem. 265 (1990) 3996-4003
9. Johnson J.L., and Toft D.O. Binding of p23 and hsp90 during assembly with the progesterone receptor. Mol. Endocrinol. 9 (1995) 670-678
10. 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
11. McLaughlin S.H., Sobott F., Yao Z.-P., Zhang W., Nielsen P.R., Grossmann J.G., Laue E.D., Robinson C.V., and Jackson S.E. The co-chaperone p23 arrests the hsp90 ATPase cycle to trap client proteins. J. Mol. Biol. 356 (2006) 746-758
12. Marcu M.G., Chadli A., Bouhouche I., Catelli M., and Neckers L.M. The heat shock protein 90 antagonist novobiocin interacts with a previously unrecognized ATP-binding domain in the carboxyl terminus of the chaperone. J. Biol. Chem. 275 (2000) 37181-37186
13. Yun B.-G., Huang W., Leach N., Hartson S.D., and Matts R.L. Novobiocin induces a distinct conformation of hsp90 and alters hsp90-cochaperone-client interactions. Biochemistry 43 (2004) 8217-8229
14. 2 biosynthesis. J. Biol. Chem. 275 (2000) 32775-32782
15. 2 synthase by 90-kDa heat shock protein. Biochem. Biophys. Res. Commun. 303 (2003) 1018-1023
16. Mollerup J., Krogh T.N., Nielsen P.F., and Berchtold M.W. Properties of the co-chaperone protein p23 erroneously attributed to ALG-2 (apoptosis-linked gene 2). FEBS Lett. 555 (2003) 478-482
17. Jung Y.-S., Kim K.-S., Kim K.D., Lin J.-S., Kim J.-W., and Kim E. Apoptosis-linked gene 2 binds to the death domain of Fas and dissociates from Fas during Fas-mediated apoptosis in Jurkat cells. Biochem. Biophys. Res. Commun. 288 (2001) 420-426
18. Gausdal G., Gjertsen B.T., Fladmark K.E., Demol H., Vandekerckhove J., and Døskeland S.-O. Caspase-dependent, geldanamycin-enhanced cleavage of co-chaperone p23 in leukemic apoptosis. Leukemia 18 (2004) 1989-1996
19. Mollerup J., and Berchtold M.W. The co-chaperone p23 is degraded by caspases and the proteasome during apoptosis. FEBS Lett. 579 (2005) 4187-4192
20. Rao R.V., Niazi K., Mollahan P., Mao X., Crippen D., Poksay K.S., Chen S., and Bredesen D.E. Coupling endoplasmic reticulum stress to the cell-death program: a novel hsp90-independent role for the small chaperone protein p23. Cell Death Differ. 13 (2005) 415-425
21. Bakhshi J., Weinstein L., Poksay K.S., Nishinaga B., Bredesen D.E., and Rao R.V. Coupling endoplasmic reticulum stress to the cell death program in mouse melanoma cells: effect of curcumin. Apoptosis 13 (2008) 904-914
22. Le Bras G., Radanyi C., Peyrat J.-F., Brion J.-D., Alami M., Marsaud V., Stella B., and Renoir J.-M. New novobiocin analogues as antiproliferative agents in breast cancer cells and potential inhibitors of heat shock protein 90. J. Med. Chem. 50 (2007) 6189-6200
23. Radanyi C., Le Bras G., Marsaud V., Peyrat J.-F., Messaoudi S., Catelli M.-G., Brion J.-D., Alami M., and Renoir J.-M. Antiproliferative and apoptotic activities of tosylcyclonovobiocic acids as potent heat shock protein 90 inhibitors in human cancer cells. Cancer Lett. 274 (2009) 88-94
24. Walsh J.G., Cullen S.P., Sheridan C., Lüthi A.U., Gerner C., and Martin S.J. Executioner caspase-3 and caspase-7 are functionally distinct proteases. Proc. Natl. Acad. Sci. USA 105 (2008) 12815-12819
25. Jänicke R.U., Sprengart M.L., Wati M.R., and Porter A.G. Caspase-3 is required for DNA fragmentation and morphological changes associated with apoptosis. J. Biol. Chem. 273 (1998) 9357-9360
26. Mimnaugh E.G., Xu W., Vos M., Yuan X., Isaacs J.S., Bisht K.S., Gius D., and Neckers L. Simultaneous inhibition of hsp90 and the proteasome promotes protein ubiquitination, causes endoplasmic reticulum-derived cytosolic vacuolization, and enhances antitumor activity. Mol. Cancer Ther. 3 (2004) 551-566
27. Sun X.-M., Butterworth M., MacFarlane M., Dubiel W., Ciechanover A., and Cohen G.M. Caspase activation inhibits proteasome function during apoptosis. Mol. Cell 14 (2004) 81-93
28. Lee A.S. The glucose-regulated proteins: stress induction and clinical applications. Trends Biochem. Sci. 26 (2001) 504-510
29. Lawson B., Brewer J.W., and Hendershot L.M. Geldanamycin, an hsp90/GRP94-binding drug, induces increased transcription of endoplasmic reticulum (ER) chaperones via the ER stress pathway. J. Cell. Physiol. 174 (1998) 170-178
30. Li J., and Lee A.S. Stress induction of GRP78/BiP and its role in cancer. Curr. Mol. Med. 6 (2006) 45-54
31. Weikl T., Abelmann K., and Buchner J. An unstructured C-terminal region of the hsp90 co-chaperone p23 is important for its chaperone function. J. Mol. Biol. 293 (1999) 685-691
32. Berry N.B., Fan M., and Nephew K.P. Estrogen receptor-α hinge region lysines 302 and 303 regulate receptor degradation by the proteasome. Mol. Endocrinol. 22 (2008) 1535-1551
33. Oxelmark E., Roth J.M., Brooks P.C., Braunstein S.E., Schneider R.J., and Garabedian M.J. The cochaperone p23 differentially regulates estrogen receptor target genes and promote tumor cell adhesion and invasion. Mol. Cell. Biol. 26 (2006) 5205-5213
34. 2+-binding modulator protein involved in cell proliferation and in cell death. Biochim. Biophys. Acta 1600 (2002) 68-73
35. Forafonov F., Toogun O.A., Grad I., Suslova E., Freeman B.C., and Picard D. p23/Sba1p protects against hsp90 inhibitors independently of its intrinsic chaperone activity. Mol. Cell. Biol. 28 (2008) 3446-3456
36. Knoblauch R., and Garabedian M.J. Role for Hsp90-associated cochaperone p23 in estrogen receptor signal transduction. Mol. Cell. Biol. 19 (1999) 3748-3759
37. Freeman B.C., Felts S.J., Toft D.O., and Yamamoto K.R. The p23 molecular chaperones act at a late step in intracellular receptor action to differentially affect ligand efficacies. Genes Dev. 14 (2000) 422-434
38. Toogun O.A., Zeiger W., and Freeman B.C. The p23 molecular chaperone promotes functional telomerase complexes through DNA dissociation. Proc. Natl. Acad. Sci. USA 104 (2007) 5765-5770
39. Elmore L.W., Forsythe R., Forsythe H., Bright A.T., Nasim S., Endo K., and Holt S.E. Overexpression of telomerase-associated chaperone proteins in prostatic intraepithelial neoplasia and carcinomas. Oncol. Rep. 20 (2008) 613-617
40. Shay J.W., and Bacchetti S. A survey of telomerase activity in human cancer. Eur. J. Cancer 33 (1997) 787-791