A structurally simplified analogue of geldanamycin exhibits neuroprotective activity

ACS Medicinal Chemistry Letters

Volumn 4, Issue 10, 2013, Pages 953-957

  Madathil, Manikandadas M ^a   Khdour, Omar M ^a   Jaruvangsanti, Jennifer ^a   Hecht, Sidney M ^a  

^a ARIZONA STATE UNIVERSITY   (United States)

Author keywords

Geldanamycin; lipid peroxidation; mitochondria; oxidative stress

Indexed keywords

5 [N (3 CARBOXYPROPYL)AMINO] 2 HYDROXY 3 TRIDECYL 1,4 BENZOQUINONE DERIVATIVE; AMYLOID BETA PROTEIN; GELDANAMYCIN; HEAT SHOCK PROTEIN 90; NEUROPROTECTIVE AGENT; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG;

ARTICLE; CELL DAMAGE; CELL PROTECTION; CONTROLLED STUDY; CYTOTOXICITY; DOSE RESPONSE; DRUG SYNTHESIS; FRIEDREICH ATAXIA; LIPID MEMBRANE; LIPID PEROXIDATION; LYMPHOCYTE; MITOCHONDRIAL MEMBRANE POTENTIAL; NEUROPROTECTION; NEUROTOXICITY; PRIORITY JOURNAL;

EID: 84885442630     PISSN: None     EISSN: 19485875     Source Type: Journal    
DOI: 10.1021/ml400207m     Document Type: Article

References (46)

1. Bras, M.; Queenan, B.; Susin, S. A. Programmed cell death via mitochondria: different modes of dying Biochemistry (Moscow) 2005, 70, 231-239
2. McBride, H. M.; Neuspiel, M.; Wasiak, S. Mitochondria: more than just a powerhouse Curr. Biol. 2006, 16, R551-560
3. Cardoso, A. R.; Queliconi, B. B.; Kowaltowski, A. J. Mitochondrial ion transport pathways: role in metabolic diseases Biochim. Biophys. Acta, Bioenerg. 2010, 1797, 832-838
4. West, A. P.; Shadel, G. S.; Ghosh, S. Mitochondria in innate immune responses Nat. Rev. Immunol. 2011, 11, 389-402
5. Coskun, P.; Wyrembak, J.; Schriner, S. E.; Chen, H.-W.; Marciniack, C.; LaFerla, F.; Wallace, D. C. A mitochondrial etiology of Alzheimer and Parkinson disease Biochim. Biophys. Acta, Gen. Subj. 2012, 1820, 553-564
6. McCoy, M. K.; Cookson, M. R. Mitochondrial quality control and dynamics in Parkinson's disease Antioxid. Redox Signaling 2012, 16, 869-882
7. Mochel, F.; Haller, R. G. Energy deficit in Huntington disease: why it matters J. Clin. Invest. 2011, 121, 493-499
8. Armstrong, J. S.; Khdour, O.; Hecht, S. M. Does oxidative stress contribute to the pathology of Friedreich's ataxia? A radical question FASEB J. 2010, 24, 2152-2163
9. Lin, M. T.; Beal, M. F. Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases Nature 2006, 443, 787-795
10. Madathil, M. M.; Khdour, O. M.; Jaruvangsanti, J.; Hecht, S. M. Synthesis and biological activities of N -(3-carboxylpropyl)-5-amino-2-hydroxy-3- tridecyl-1,4-benzoquinone and analogues J. Nat. Prod. 2012, 75, 2209-2215
11. DeBoer, C.; Meulman, P. A.; Wnuk, R. J.; Peterson, D. H. Geldanamycin, a new antibiotic J. Antibiot. 1970, 23, 442-447
12. Stebbins, C. E.; Russo, A. A.; Schneider, C.; Rosen, N.; Hartl, F. U.; Pavletich, N. P. Crystal structure of an Hsp90-geldanamycin complex: targeting of a protein chaperone by an antitumor agent Cell 1997, 89, 239-250
13. v-src heteroprotein complex formation by benzoquinone ansamycins: essential role for stress proteins in oncogenic transformation Proc. Natl. Acad. Sci. U.S.A. 1994, 91, 8324-8328
14. Schneider, C.; Sepp-Lorenzino, L.; Nimmesgern, E.; Ouerfelli, O.; Danishefsky, S.; Rosen, N.; Hartl, F. U. Pharmacologic shifting of a balance between protein refolding and degradation mediated by Hsp90 Proc. Natl. Acad. Sci. U.S.A. 1996, 93, 14536-14541
15. bcr-abl and v-src proteins before their degradation by the proteasome Cell Growth Differ. 2000, 11, 355-360
16. Schulte, T. W.; Blagosklonny, M. V.; Ingui, C.; Neckers, L. Disruption of the Raf-1-Hsp90 molecular complex results in destabilization of Raf-1 and loss of Raf-1-Ras association J. Biol. Chem. 1995, 270, 24585-24588
17. Whitesell, L.; Shifrin, S. D.; Schwab, G.; Neckers, L. M. Benzoquinonoid ansamycins possess selective tumoricidal activity unrelated to src kinase inhibition Cancer Res. 1992, 52, 1721-1728
18. Clevenger, R. C.; Blagg, B. S. J. Design, synthesis, and evaluation of a radicicol and geldanamycin chimera, radamide Org. Lett. 2004, 6, 4459-4462
19. Wang, M.; Shen, G.; Blagg, B. S. J. Radanamycin, a macrocyclic chimera of radicicol and geldanamycin Bioorg. Med. Chem. Lett. 2006, 16, 2459-2462
20. Kuduk, S. D.; Zheng, F. F.; Sepp-Lorenzino, L.; Rosen, N.; Danishefsky, S. J. Synthesis and evaluation of geldanamycin-estradiol hybrids Bioorg. Med. Chem. Lett. 1999, 9, 1233-1238
21. Kuduk, S. D.; Harris, C. R.; Zheng, F. F.; Sepp-Lorenzino, L.; Ouerfelli, Q.; Rosen, N.; Danishefsky, S. J. Synthesis and evaluation of geldanamycin-testosterone hybrids Bioorg. Med. Chem. Lett. 2000, 10, 1303-1306
22. Zheng, F. F.; Kuduk, S. D.; Chiosis, G.; Munster, P. N.; Sepp-Lorenzino, L.; Danishefsky, S. J.; Rosen, N. Identification of a geldanamycin dimer that induces the selective degradation of HER-family tyrosine kinases Cancer Res. 2000, 60, 2090-2094
23. McErlean, C. S. P.; Proisy, N.; Davis, C. J.; Boland, N. A.; Sharp, S. Y.; Boxall, K.; Slawin, A. M. Z.; Workman, P.; Moody, C. J. Synthetic ansamycins prepared by a ring-expanding Claisen rearrangement. Synthesis and biological evaluation of ring and conformational analogues of the Hsp90 molecular chaperone inhibitor geldanamycin Org. Biomol. Chem. 2007, 5, 531-546
24. Kitson, R. R. A.; Chang, C.-H.; Xiong, R.; Williams, H. E. L.; Davis, A. L.; Lewis, W.; Dehn, D. L.; Siegel, D.; Roe, S. M.; Prodromou, C.; Ross, D.; Moody, C. J. Synthesis of 19-substituted geldanamycins with altered conformations and their binding to heat shock protein Hsp90 Nat. Chem. 2013, 5, 307-314
25. Shen, H.-Y.; He, J.-C.; Wang, Y.; Huang, Q.-Y.; Chen, J.-F. Geldanamycin induces heat shock protein 70 and protects against MPTP-induced dopaminergic neurotoxicity in mice J. Biol. Chem. 2005, 280, 39962-39969
26. Marcu, M. G.; Chadli, A.; Bouhouche, I.; Catelli, M.; 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. 2000, 275, 37181-37186
27. Ansar, S.; Burlison, J. A.; Hadden, M. K.; Yu, X. M.; Desino, K. E.; Bean, J.; Neckers, L.; Audus, K. L.; Michaelis, M. L.; Blagg, B. S. J. A non-toxic Hsp90 inhibitor protects neurons from Aβ-induced toxicity Bioorg. Med. Chem. Lett. 2007, 17, 1984-1990
28. Lu, Y.; Ansar, S.; Michaelis, M. L.; Blagg, B. S. J. Neuroprotective activity and evaluation of Hsp90 inhibitors in an immortalized neuronal cell line Bioorg. Med. Chem. 2009, 17, 1709-1715
29. Blagg, B.; Michaelis, M. L.; McIntosh, M. Preparation of novobiocin analogs useful for the treatment and/or prevention of neurodegenerative disorders, autoimmune disorders, and as antitumor agents. U. S. Patent 7,622,451, 24 Nov 2009.
30. Matsumoto, M.; Kobayashi, K.; Hotta, Y. Acid-catalyzed oxidation of benzaldehydes to phenols by hydrogen peroxide J. Org. Chem. 1984, 49, 4740-4741
31. Poigny, S.; Guyot, M.; Samadi, M. Total synthesis of maesanin and analogues Tetrahedron 1998, 54, 14791-14802
32. Chakraborti, A. K.; Gulhane, R. Perchloric acid adsorbed on silica gel as a new, highly efficient, and versatile catalyst for acetylation of phenols, thiols, alcohols, and amines Chem. Commun. 2003, 1896-1897
33. Gagne, M. R.; Stern, C. L.; Marks, T. J. Organolanthanide-catalyzed hydroamination. A kinetic, mechanistic, and diastereoselectivity study of the cyclization of N -unprotected amino olefins J. Am. Chem. Soc. 1992, 114, 275-294
34. Luly, J. R.; Rapoport, H. Routes to mitomycins. An improved synthesis of 7-methoxymitosene using palladium catalysis J. Org. Chem. 1984, 49, 1671-1672
35. Shen, G.; Wang, M.; Welch, T. R.; Blagg, B. S. J. Design, synthesis, and structure-activity relationships for chimeric inhibitors of Hsp90 J. Org. Chem. 2006, 71, 7618-7631
36. Armstrong, J. S.; Jones, D. P. Glutathione depletion enforces the mitochondrial permeability transition and causes cell death in HL60 cells that overexpress Bcl-2 FASEB J. 2002, 16, 1263-1265
37. 10 analog decylubiquinone inhibits the redox-activated mitochondrial permeability transition: Role of mitochondrial respiratory complex III J. Biol. Chem. 2003, 278, 49079-49084
38. Khdour, O.; Lu, J.; Hecht, S. M. An acetate prodrug of a pyridinol-based vitamin E analogue Pharm. Res. 2011, 28, 2896-2909
39. 581/591 FEBS Lett. 1999, 453, 278-282
40. 581/591, an oxidation-sensitive fluorescent lipid peroxidation probe: (micro)spectroscopic characterization and validation of methodology Free Radical Biol. Med. 2002, 33, 473-490
41. Miccadei, S.; Kyle, M. E.; Gilfor, D.; Farber, J. L. Toxic consequence of the abrupt depletion of glutathione in cultured rat hepatocytes Arch. Biochem. Biophys. 1988, 265, 311-320
42. Tirmenstein, M. A.; Nicholls-Grzemski, F. A.; Zhang, J. G.; Fariss, M. W. Glutathione depletion and the production of reactive oxygen species in isolated hepatocyte suspensions Chem.-Biol. Interact. 2000, 127, 201-217
43. Ehrenberg, B.; Montana, V.; Wei, M. D.; Wuskell, J. P.; Loew, L. M. Membrane potential can be determined in individual cells from the Nernstian distribution of cationic dyes Biophys. J. 1988, 53, 785-794
44. Griffith, O. W.; Meister, A. Potent and specific inhibition of glutathione synthesis by buthionine sulfoximine (S-n -butyl homocysteine sulfoximine) J. Biol. Chem. 1979, 254, 7558-7560
45. Smiley, S. T.; Reers, M.; Mottola-Hartshorn, C.; Lin, M.; Chen, A.; Smith, T. W.; Steele, G. D.; Chen, L. B. Intracellular heterogeneity in mitochondrial membrane potentials revealed by a J-aggregate-forming lipophilic cation JC-1 Proc. Natl. Acad. Sci. U.S.A. 1991, 88, 3671-3675
46. 10 on mitochondrial respiratory chain function and cytoprotection Bioorg. Med. Chem. 2013, 21, 2346-2354