Celastrol analogues as inducers of the heat shock response. Design and synthesis of affinity probes for the identification of protein targets

ACS Chemical Biology

Volumn 7, Issue 5, 2012, Pages 928-937

  Klaić, Lada ^a   Morimoto, Richard I ^a   Silverman, Richard B ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMIDE; BETA TUBULIN; CARBOXYLIC ACID; CELASTROL; HEAT SHOCK PROTEIN 90; LIPOCORTIN 2;

ALKYLATION; AMINO ACID SEQUENCE; ANTIOXIDANT RESPONSIVE ELEMENT; ARTICLE; BINDING AFFINITY; BIOAVAILABILITY; CELL ACTIVITY; CELL LYSATE; CLICK CHEMISTRY; CONTROLLED STUDY; ENZYME INHIBITION; ESTERIFICATION; GENE EXPRESSION; HEAT SHOCK RESPONSE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMAN CELL; HYDROGEN BOND; HYDROLYSIS; HYDROPHOBICITY; IN VITRO STUDY; IN VIVO STUDY; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN MODIFICATION; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; PROTEIN TARGETING; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STRUCTURE ACTIVITY RELATION;

ANTIOXIDANTS; BIOTINYLATION; CELASTRACEAE; CELL LINE; CELL LINE, TUMOR; DRUG DESIGN; HEAT-SHOCK RESPONSE; HSP90 HEAT-SHOCK PROTEINS; HUMANS; TRITERPENES;

EID: 84862093085     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/cb200539u     Document Type: Article

References (57)

1. Gunatilaka, A. A. (1996) Triterpenoid Quinonemethides and Realted Compounds (Celastroloids), Vol. 67, Springer, Wien, New York.
2. Figueiredo, J. N., Raz, B, and Sequin, U. (1998) Novel quinone methides from Salacia kraussii with in vitro antimalarial activity J. Nat. Prod. 61, 718-723 (Pubitemid 28317130)
3. Sassa, H, Kogure, K, Takaishi, Y, and Terada, H. (1994) Structural basis of potent antiperoxidation activity of the triterpene celastrol in mitochondria: effect of negative membrane surface charge on lipid peroxidation Free Radical Biol. Med. 17, 201-207 (Pubitemid 24269672)
4. Huang, F. C., Chan, W. K., Moriarty, K. J., Zhang, D. C., Chang, M. N., He, W, Yu, K. T., and Zilberstein, A. (1998) Novel cytokine release inhibitors. Part I: Triterpenes Bioorg. Med. Chem. Lett. 8, 1883-1886 (Pubitemid 28338334)
5. He, W, Huang, F. C., Gavai, A, Chan, W. K., Amato, G, Yu, K. T., and Zilberstein, A. (1998) Novel cytokine release inhibitors. Part III: Truncated analogs of tripterine Bioorg. Med. Chem. Lett. 8, 3659-3664 (Pubitemid 29012596)
6. Jin, H. Z., Hwang, B. Y., Kim, H. S., Lee, J. H., Kim, Y. H., and Lee, J. J. (2002) Antiinflammatory constituents of Celastrus orbiculatus inhibit the NF-kappaB activation and NO production J. Nat. Prod. 65, 89-91
7. Ngassapa, O, Soejarto, D. D., Pezzuto, J. M., and Farnsworth, N. R. (1994) Quinone-methide triterpenes and salaspermic acid from Kokoona ochracea J. Nat. Prod. 57, 1-8 (Pubitemid 24076888)
8. Chang, F. R., Hayashi, K, Chen, I. H., Liaw, C. C., Bastow, K. F., Nakanishi, Y, Nozaki, H, Cragg, G. M., Wu, Y. C., and Lee, K. H. (2003) Antitumor agents. 228. five new agarofurans, Reissantins A-E, and cytotoxic principles from Reissantia buchananii J. Nat. Prod. 66, 1416-1420 (Pubitemid 37490387)
9. Abbas, S, Bhoumik, A, Dahl, R, Vasile, S, Krajewski, S, Cosford, N. D., and Ronai, Z. A. (2007) Preclinical studies of celastrol and acetyl isogambogic acid in melanoma Clin. Cancer Res. 13, 6769-6778 (Pubitemid 350206815)
10. Yang, H, Chen, D, Cui, Q. C., Yuan, X, and Dou, Q. P. (2006) Celastrol, a triterpene extracted from the Chinese "Thunder of God Vine", is a potent proteasome inhibitor and suppresses human prostate cancer growth in nude mice Cancer Res. 66, 4758-4765
11. Huang, Y, Zhou, Y, Fan, Y, and Zhou, D. (2008) Celastrol inhibits the growth of human glioma xenografts in nude mice through suppressing VEGFR expression Cancer Lett. 264, 101-106
12. Westerheide, S. D., Bosman, J. D., Mbadugha, B. N., Kawahara, T. L., Matsumoto, G, Kim, S, Gu, W, Devlin, J. P., Silverman, R. B., and Morimoto, R. I. (2004) Celastrols as inducers of the heat shock response and cytoprotection J. Biol. Chem. 279, 56053-56060 (Pubitemid 40066613)
13. Mu, T. W., Ong, D. S., Wang, Y. J., Balch, W. E., Yates, J. R., 3rd, Segatori, L, and Kelly, J. W. (2008) Chemical and biological approaches synergize to ameliorate protein-folding diseases Cell 134, 769-781
14. Trott, A, West, J. D., Klaic, L, Westerheide, S. D., Silverman, R. B., Morimoto, R. I., and Morano, K. A. (2008) Activation of heat shock and antioxidant responses by the natural product celastrol: transcriptional signatures of a thiol-targeted molecule Mol. Biol. Cell 19, 1104-1112 (Pubitemid 351481823)
15. Klaic, L, Trippier, P. C., Mishra, R. K., Morimoto, R. I., and Silverman, R. B. (2011) Remarkable stereospecific conjugate additions to the Hsp90 inhibitor celastrol J. Am. Chem. Soc. 133, 19634-19637
16. Sreeramulu, S, Gande, S. L., Gobel, M, and Schwalbe, H. (2009) Molecular mechanism of inhibition of the human protein complex Hsp90-Cdc37, a kinome chaperone-cochaperone, by triterpene celastrol Angew. Chem., Int. Ed. 48, 5853-5855
17. Lee, J. H., Koo, T. H., Yoon, H, Jung, H. S., Jin, H. Z., Lee, K, Hong, Y. S., and Lee, J. J. (2006) Inhibition of NF-kappa B activation through targeting I kappa B kinase by celastrol, a quinone methide triterpenoid Biochem. Pharmacol. 72, 1311-1321 (Pubitemid 44572192)
18. Seo, H. R., Seo, W. D., Pyun, B. J., Lee, B. W., Jin, Y. B., Park, K. H., Seo, E. K., Lee, Y. J., and Lee, Y. S. (2011) Radiosensitization by celastrol is mediated by modification of antioxidant thiol molecules Chem. Biol. Interact. 193, 34-42
19. Zhang, T, Li, Y, Yu, Y, Zou, P, Jiang, Y, and Sun, D. (2009) Characterization of celastrol to inhibit hsp90 and cdc37 interaction J. Biol. Chem. 284, 35381-35389
20. Chadli, A, Felts, S. J., Wang, Q, Sullivan, W. P., Botuyan, M. V., Fauq, A, Ramirez-Alvarado, M, and Mer, G (2010) Celastrol inhibits Hsp90 chaperoning of steroid receptors by inducing fibrillization of the co-chaperone p23 J. Biol. Chem. 285, 4224-4231
21. Akerfelt, M, Morimoto, R. I., and Sistonen, L. (2010) Heat shock factors: integrators of cell stress, development and lifespan Nat. Rev. Mol. Cell Biol. 11, 545-555
22. Bjork, J. K. and Sistonen, L. (2010) Regulation of the members of the mammalian heat shock factor family FEBS J. 277, 4126-4139
23. Wu, C. (1995) Heat shock transcription factors: structure and regulation Annu. Rev. Cell Dev. Biol. 11, 441-469 (Pubitemid 26019611)
24. Sarge, K. D., Murphy, S. P., and Morimoto, R. I. (1993) Activation of heat shock gene transcription by heat shock factor 1 involves oligomerization, acquisition of DNA-binding activity, and nuclear localization and can occur in the absence of stress Mol. Cell. Biol. 13, 1392-1407 (Pubitemid 23068075)
25. Holmberg, C. I., Hietakangas, V, Mikhailov, A, Rantanen, J. O., Kallio, M, Meinander, A, Hellman, J, Morrice, N, MacKintosh, C, Morimoto, R. I., Eriksson, J. E., and Sistonen, L. (2001) Phosphorylation of serine 230 promotes inducible transcriptional activity of heat shock factor 1 EMBO J. 20, 3800-3810 (Pubitemid 32691791)
26. Morimoto, R. I. (1998) Regulation of the heat shock transcriptional response: cross talk between a family of heat shock factors, molecular chaperones, and negative regulators Genes Dev. 12, 3788-3796 (Pubitemid 29024840)
27. Lindquist, S and Craig, E. A. (1988) The heat-shock proteins Annu. Rev. Genet. 22, 631-677 (Pubitemid 19156675)
28. Ellis, R. J. and Hartl, F. U. (1999) Principles of protein folding in the cellular environment Curr. Opin. Struct. Biol. 9, 102-110 (Pubitemid 29471981)
29. Ellis, R. J. and Minton, A. P. (2006) Protein aggregation in crowded environments Biol. Chem. 387, 485-497 (Pubitemid 44071450)
30. Minton, A. P. (2006) Macromolecular crowding Curr. Biol. 16, R269-271
31. Muchowski, P. J., Schaffar, G, Sittler, A, Wanker, E. E., Hayer-Hartl, M. K., and Hartl, F. U. (2000) Hsp70 and hsp40 chaperones can inhibit self-assembly of polyglutamine proteins into amyloid-like fibrils Proc. Natl. Acad. Sci. U.S.A. 97, 7841-7846 (Pubitemid 30460735)
32. Magrane, J, Smith, R. C., Walsh, K, and Querfurth, H. W. (2004) Heat shock protein 70 participates in the neuroprotective response to intracellularly expressed beta-amyloid in neurons J. Neurosci. 24, 1700-1706 (Pubitemid 38240967)
33. Auluck, P. K. and Bonini, N. M. (2002) Pharmacological prevention of Parkinson disease in Drosophila Nat. Med. 8, 1185-1186 (Pubitemid 35373534)
34. Takeuchi, H, Kobayashi, Y, Yoshihara, T, Niwa, J, Doyu, M, Ohtsuka, K, and Sobue, G. (2002) Hsp70 and Hsp40 improve neurite outgrowth and suppress intracytoplasmic aggregate formation in cultured neuronal cells expressing mutant SOD1 Brain Res. 949, 11-22 (Pubitemid 35246172)
35. Drummond, J. T. and Johnson, G. (1988) Convenient procedure for the preparation of alkyl and aryl substituted N-(aminoalkylacyl)sulfonamides Tetrahedron Lett. 29, 1653-1656
36. Carpino, L. A. and El-Faham, A. (1995) Tetramethylfluoroformamidinium hexafluorophosphate: a rapid-acting peptide coupling reagent for solution and solid phase peptide synthesis J. Am. Chem. Soc. 117, 5401-5402
37. Grant, P. K., Johnson, A. W., Juby, P. F., and King, T. J. (1960) Pristimerin. III. Modified structure for the chromophore J. Chem. Soc. 549-555
38. Shibata, T, Yamada, T, Ishii, T, Kumazawa, S, Nakamura, H, Masutani, H, Yodoi, J, and Uchida, K. (2003) Thioredoxin as a molecular target of cyclopentenone prostaglandins J. Biol. Chem. 278, 26046-26054 (Pubitemid 36835372)
39. Ioakimidis, L, Thoukydidis, L, Mirza, A, Naeem, S, and Reynisson, J. (2008) Benchmarking the reliability of QikProp. Correlation between experimental and predicted values QSAR Comb. Sci. 27, 445-456
40. Szalecki, W. (1996) Synthesis of norbiotinamine and its derivatives Bioconjugate Chem. 7, 271-273 (Pubitemid 126639657)
41. Saxon, E, Armstrong, J. I., and Bertozzi, C. R. (2000) A "traceless" Staudinger ligation for the chemoselective synthesis of amide bonds Org. Lett. 2, 2141-2143
42. Saxon, E and Bertozzi, C. R. (2000) Cell surface engineering by a modified Staudinger reaction Science 287, 2007-2010 (Pubitemid 30158675)
43. Kolb, H. C. and Sharpless, K. B. (2003) The growing impact of click chemistry on drug discovery Drug Discovery Today 8, 1128-1137 (Pubitemid 37547919)
44. Hur, W and Gray, N. S. (2011) Small molecule modulators of antioxidant response pathway Curr. Opin. Chem. Biol. 15, 162-173
45. Wang, X. J., Hayes, J. D., and Wolf, C. R. (2006) Generation of a stable antioxidant response element-driven reporter gene cell line and its use to show redox-dependent activation of nrf2 by cancer chemotherapeutic agents Cancer Res. 66, 10983-10994 (Pubitemid 44876998)
46. Hieronymus, H, Lamb, J, Ross, K. N., Peng, X. P., Clement, C, Rodina, A, Nieto, M, Du, J, Stegmaier, K, Raj, S. M., Maloney, K, Clardy, J, Hahn, W, Chiosis, G, and Golub, T. (2006) Gene expression signature-based chemical genomic prediction identifies a novel class of HSP90 pathway modulators Cancer Cell 10, 321-330 (Pubitemid 44512193)
47. Neckers, L. (2003) Development of small molecule Hsp90 inhibitors: utilizing both forward and reverse chemical genomics for drug identification Curr. Med. Chem. 10, 733-739 (Pubitemid 36443229)
48. Whitesell, L and Lindquist, S. L. (2005) HSP90 and the chaperoning of cancer Nat. Rev. Cancer 5, 761-772 (Pubitemid 41400776)
49. Zhang, T, Hamza, A, Cao, X, Wang, B, Yu, S, Zhan, C. G., and Sun, D. (2008) A novel Hsp90 inhibitor to disrupt Hsp90/Cdc37 complex against pancreatic cancer cells Mol. Cancer Ther. 7, 162-170
50. Calamini, B, Silva, M. C., Madoux, F, Hutt, D. M., Khanna, S, Chalfant, M. A., Saldanha, S. A., Hodder, P, Tait, B. D., Garza, D, Balch, W. E., and Morimoto, R. I. (2011) Small-molecule proteostasis regulators for protein conformational diseases Nat. Chem. Biol. 8, 185-196
51. Waisman, D. M. (1995) Annexin II tetramer: structure and function Mol. Cell. Biochem. 149-150, 301-322
52. Caplan, J. F., Filipenko, N. R., Fitzpatrick, S. L., and Waisman, D. M. (2004) Regulation of annexin A2 by reversible glutathionylation J. Biol. Chem. 279, 7740-7750 (Pubitemid 38294657)
53. Falsey, R. R., Marron, M. T., Gunaherath, G. M., Shirahatti, N, Mahadevan, D, Gunatilaka, A. A., and Whitesell, L. (2006) Actin microfilament aggregation induced by withaferin A is mediated by annexin II Nat. Chem. Biol. 2, 33-38
54. Mateyak, M. K. and Kinzy, T. G. (2010) eEF1A: thinking outside the ribosome J. Biol. Chem. 285, 21209-21213
55. Lau, J, Castelli, L. A., Lin, E. C., and Macaulay, S. L. (2006) Identification of elongation factor 1alpha as a potential associated binding partner for Akt2 Mol. Cell. Biochem. 286, 17-22
56. Jordan, M. A. and Wilson, L (2004) Microtubules as a target for anticancer drugs Nat. Rev. Cancer 4, 253-265 (Pubitemid 38525281)
57. Jo, H, Loison, F, Hattori, H, Silberstein, L. E., Yu, H, and Luo, H. R. (2010) Natural product Celastrol destabilizes tubulin heterodimer and facilitates mitotic cell death triggered by microtubule-targeting anti-cancer drugs PLoS One 5, e10318