Dihydroquinone ansamycins: Toward resolving the conflict between low in vitro affinity and high cellular potency of geldariamycin derivatives

Biochemistry

Volumn 45, Issue 17, 2006, Pages 5678-5685

  Maroney, Anna C ^a   Marugan, Juan J ^a   Mezzasalma, Tara M ^a   Barnakov, Alexander N ^a   Garrabrant, Thomas A ^a   Weaner, Larry E ^a   Jones, William J ^a   Barnakova, Ludmila A ^a   Koblish, Holly K ^a   Todd, Matthew J ^a   Masucci, John A ^a   Deckman, Ingrid C ^a   Galemmo Jr , Robert A ^a   Johnson, Dana L ^a  

^a JOHNSON AND JOHNSON PHARMACEUTICAL RESEARCH AND DEVELOPMENT   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELLS; COMPOSITION; DERIVATIVES; SOLUTIONS; TUMORS;

CELLULAR TRANSFORMATIONS; DIHYDROQUINONE ANSAMYCINS; HEAT SHOCK PROTEIN 90 (HSP90); ONCOGENESIS;

PROTEINS;

17 ALLYLAMINOGELDANAMYCIN; ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; ANSAMYCIN DERIVATIVE; CHAPERONE; DIHYDRO 17 ALLYLAMINOGELDANAMYCIN; DIHYDROGELDANAMYCIN; GELDANAMYCIN; HEAT SHOCK PROTEIN 90; HEAT SHOCK PROTEIN 90 INHIBITOR; HYDROQUINONE DERIVATIVE; RADICICOL; REDUCING AGENT; UNCLASSIFIED DRUG;

ANTINEOPLASTIC ACTIVITY; AQUEOUS SOLUTION; ARTICLE; BINDING AFFINITY; CANCER INHIBITION; CARCINOGENESIS; CELL PROLIFERATION; CELL SURVIVAL; CELL TRANSFORMATION; DRUG EFFICACY; DRUG POTENCY; DRUG PROTEIN BINDING; EPITHELIUM CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; OXIDATION; PRIORITY JOURNAL; TUMOR CELL;

ANTINEOPLASTIC AGENTS; BENZOQUINONES; CELL LINE, TUMOR; CELLS, CULTURED; DRUG STABILITY; HSP90 HEAT-SHOCK PROTEINS; HUMANS; LACTAMS, MACROCYCLIC; PROTEIN BINDING; QUINONES; REDUCING AGENTS; RIFABUTIN; SOLUBILITY;

EID: 33646345860     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi0524969     Document Type: Article

References (45)

1. Uehara, Y. (2003) Natural product origins of Hsp90 inhibitors, Curr. Cancer Drug Targets 3, 325-330.
2. Sausville, E. A., Tomaszewski, J. E., and Ivy, P. (2003) Clinical development of 17-allylamino, 17-demethoxygeldanamycin, Curr. Cancer Drug Targets 3, 377-383.
3. Neckers, L., and Neckers, K. (2005) Heat-shock protein 90 inhibitors as novel cancer chemotherapeutics-an update, Expert Opin. Emerging Drugs 10, 137-149.
4. Grem, J. L., Morrison, G., Guo, X. D., Agnew, E., Takimoto, C. H., Thomas, R., Szabo, E., Grochow, L., Grollman, F., Hamilton, J. M., Neckers, L., and Wilson, R. H. (2005) Phase I and pharmacologic study of 17-(allylamino)-17- demethoxygeldanamycin in adult patients with solid tumors, J. Clin. Oncol. 23, 1885-1893.
5. Goetz, M. P., Toft, D., Reid, J., Ames, M., Stensgard, B., Safgren, S., Adjei, A. A., Sloan, J., Atherton, P., Vasile, V., Salazaar, S., Adjei, A., Croghan, G., and Erlichman, C. (2005) Phase I trial of 17-allylamino-17- demethoxygeldanamycin in patients with advanced cancer, J. Clin. Oncol. 23, 1078-1087.
6. Stebbins, C. E., Russo, A. A., Schneider, C., Rosen, N., Hartl, F. U., and Pavletich, N. P. (1997) Crystal structure of an Hsp90-geldanamycin complex: targeting of a protein chaperone by an antitumor agent, Cell 89, 239-250.
7. Roe, S. M., Prodromou, C., O'Brien, R., Ladbury, J. E., Piper, P. W., and Pearl, L. H. (1999) Structural basis for inhibition of the Hsp90 molecular chaperone by the antitumor antibiotics radicicol and geldanamycin, J. Med. Chem. 42, 260-266.
8. Csermely, P., Schnaider, T., Soti, C., Prohaszka, Z., and Nardai, G. (1998) The 90-kDa molecular chaperone family: structure, function, and clinical applications. A comprehensive review, Pharmacol. Ther. 79, 129-168.
9. Prodromou, C., and Pearl, L. H. (2003) Structure and functional relationships of Hsp90, Curr. Cancer Drug Targets 3, 301-323.
10. Obermann, W. M. J., Sondermann, H., Russo, A. A., Pavletich, N. P., and Hartl, F. U. (1998) In vivo function of Hsp90 is dependent on ATP binding and ATP hydrolysis, J. Cell Biol. 143, 901-910.
11. Grenert, J. P., Johnson, B. D., and Toft, D. O. (1999) The importance of ATP binding and hydrolysis by hsp90 in formation and function of protein heterocomplexes, J. Biol. Chem. 274, 17525-17533.
12. Panaretou, B., Prodromou, C., Roe, S. M., O'Brien, R., Ladbury, J. E., Piper, P. W., and Pearl, L. H. (1998) ATP binding and hydrolysis are essential to the function of the Hsp90 molecular chaperone in vivo, EMBO J. 17, 4829-4836.
13. Sreedhar, A. S., Soti, C., and Csermely, P. (2004) Inhibition of Hsp90: a new strategy for inhibiting protein kinases, Biochim. Biophys. Acta 1697, 233-242.
14. Chiosis, G., Huezo, H., Rosen, N., Mimnaugh, E., Whitesell, L., and Neckers, L. (2003) 17AAG: low target binding affinity and potent cell activity-finding an explanation, Mol. Cancer Ther. 2, 123-129.
15. Tian, Z. Q., Liu, Y., Zhang, D., Wang, Z., Dong, S. D., Carreras, C. W., Zhou, Y., Rastelli, G., Santi, D. V., and Myles, D. C. (2004) Synthesis and biological activities of novel 17-aminogeldanamycin derivatives, Bioorg. Med. Chem. 12, 5317-5329.
16. Whitesell, L., Shifrin, S. D., Schwab, G., and Neckers, L. M. (1992) Benzoquinonoid ansamycins possess selective tumoricidal activity unrelated to src kinase inhibition, Cancer Res. 52, 1721-1728.
17. Kelland, L. R., Sharp, S. Y., Rogers, P. M., Myers, T. G., and Workman, P. (1999) DT-Diaphorase expression and tumor cell sensitivity to 17-allylamino, 17-demethoxygeldanamycin, an inhibitor of heat shock protein 90, J. Natl. Cancer Inst. 91, 1940-1949.
18. Kamal, A., Thao, L., Sensintaffar, J., Zhang, L., Boehm, M. F., Fritz, L. C., and Burrows, F. J. (2003) A high-affinity conformation of Hsp90 confers tumour selectivity on Hsp90 inhibitors, Nature 425, 407-410.
19. Vilenchik, M. S. D., Basso, A., Huezo, H., Lucas, B., He, H., Rosen, N., Spampinato, C., Modrich, P., Chiosis, G. (2004) Targeting wide-range oncogenic transformation via PU24FC1, a specific inhibitor of tumor Hsp90, Chem. Biol. 11, 787-797.
20. Xu, L., Eiseman, J. L., Egorin, M. J., and D'Argenio, D. Z. (2003) Physiologically-based pharmacokinetics and molecular pharmacodynamics of 17-(allylamino)-17-demethoxygeldanamycin and its active metabolite in tumor-bearing mice, J. Pharmacokinet. Pharmacodyn. 30, 185-219.
21. Eiseman, J. L., Lan, J., Lagattuta, T. F., Hamburger, D. R., Joseph, E., Covey, J. M., and Egorin, M. J. (2005) Pharmacokinetics and pharmacodynamics of 17-demethoxy 17-[[(2-dimethylamino)ethyl]-amino]geldanamycin (17DMAG, NSC 707545) in C.B-17 SCID mice bearing MDA-MB-231 human breast cancer xenografts, Cancer Chemother. Pharmacol. 55, 21-32.
22. Schnur, R. C., Corman, M. L., Gallaschun, R. J., Cooper, B. A., Dee, M. F., Doty, J. L., Muzzi, M. L., Moyer, J. D., DiOrio, C. I., Barbacci, E. G., et al. (1995) Inhibition of the oncogene product p185erbB-2 in vitro and in vivo by geldanamycin and dihydrogeldanamycin derivatives, J. Med. Chem. 38, 3806-3812.
23. Matulis, D., Kranz, J. K., Salemme, F. R., and Todd, M. J. (2005) Thermodynamic stability of carbonic anhydrase: measurements of binding affinity and stoichiometry using ThermoFluor, Biochemistry 44, 5258-5266.
24. Robertson, A. D., and Murphy, K. P. (1997) Protein structure and the energetics of protein stability, Chem. Rev. 97, 1251-1268.
25. Barnakov, A. N., Barnakova, L. A., and Hazelbauer, G. L. (2002) Allosteric enhancement of adaptational demethylation by a carboxyl-terminal sequence on chemoreceptors, J. Biol. Chem. 277, 42151-42156.
26. Patel, K., Piagentini, M., Rascher, A., Tian, Z.-Q., Buchanan, G. O., Regentin, R., Hu, Z., Hutchinson, C. R., and McDaniel, R. (2004) Engineered biosynthesis of geldanamycin analogs for Hsp90 inhibition, Chem. Biol. 11, 1625-1633.
27. Carreras, C. W., Schirmer, A., Zhong, Z., and Santi, D. V. (2003) Filter binding assay for the geldanamycin-heat shock protein 90 interaction, Anal. Biochem 317, 40-46.
28. Kim, J., Felts, S., Llauger, L., He, H., Huezo, H., Rosen, N., and Chiosis, G. (2004) Development of a fluorescence polarization assay for the molecular chaperone Hsp90, J. Biomol. Screening 9, 375-381.
29. Jez, J. M., Chen, J. C., Rastelli, G., Stroud, R. M., and Santi, D. V. (2003) Crystal structure and molecular modeling of 17-DMAG in complex with human Hsp90, Chem. Biol. 10, 361-368.
30. Neckers, L., Schulte, T. W., and Mimnaugh, E. (1999) Geldanamycin as a potential anti-cancer agent: Its molecular target and biochemical activity, Invest. New Drugs 17, 361-373.
31. McLaughlin, S. H., Ventouras, L. A., Lobbezoo, B., and Jackson, S. E. (2004) Independent ATPase activity of Hsp90 subunits creates a flexible assembly platform, J. Mol. Biol. 344, 813-826.
32. Agatsuma, T., Ogawa, H., Akasaka, K., Asai, A., Yamashita, Y., Mizukami, T., Akinaga, S., and Saitoh, Y. (2002) Halohydrin and oxime derivatives of radicicol: synthesis and antitumor activities, Bioorg. Med. Chem. 10, 3445-3454.
33. Gorre, M. E., Ellwood-Yen, K., Chiosis, G., Rosen, N., and Sawyers, C. L. (2002) BCR-ABL point mutants isolated from patients with imatinib mesylate-resistant chronic myeloid leukemia remain sensitive to inhibitors of the BCR-ABL chaperone heat shock protein 90, Blood 100, 3041-3044.
34. Nimmanapalli, R., O'Bryan, E., Huang, M., Bali, P., Burnette, P. K., Loughran, T., Tepperberg, J., Jove, R., and Bhalla, K. (2002) Molecular characterization and sensitivity of STI-571 (imatinib mesylate, Gleevec)-resistant, Bcr-Abl-positive, human acute leukemia cells to SRC kinase inhibitor PD180970 and 17-allylamino-17-demethoxygeldanamycin, Cancer Res. 62, 5761-5769.
35. Xie, Q., Gao, C. F., Shinomiya, N., Sausville, E., Hay, R., Gustafson, M., Shen, Y., Wenkert, D., and Woude, G. F. (2005) Geldanamycins exquisitely inhibit HGF/SF-mediated tumor cell invasion, Oncogene 24, 3697-3707.
36. Hollingshead, M., Alley, M., Burger, A. M., Borgel, S., Pacula-Cox, C., Fiebig, H.-H., and Sausville, E. A. (2005) In vivo antitumor efficacy of 17-DMAG (17-dimethylaminoethylamino-17-demethoxygeldanamycin hydrochloride), a water-soluble geldanamycin derivative, Cancer Chemother. Pharmacol. 56, 115-125.
37. Banerji, U., Walton, M., Raynaud, F., Grimshaw, R., Kelland, L., Valenti, M., Judson, I., and Workman, P. (2005) Pharmacokinetic-pharmacodynamic relationships for the heat shock protein 90 molecular chaperone inhibitor 17-allylamino, 17-demethoxygeldanamycin in human ovarian cancer xenograft models, Clin. Cancer Res. 11, 7023-7032.
38. Behrsing, H. P., Amin, K., Ip, C., Jimenez, L., and Tyson, C. A. (2005) In vitro detection of differential and cell-specific hepatobiliary toxicity induced by geldanamycin and 17-allylaminogeldanamycin in rats, Toxicol. in Vitro 19, 1079-1088.
39. Smith, V., Sausville, E. A., Camalier, R. F., Fiebig, H.-H., and Burger, A. M. (2005) Comparison of 17-dimethylaminoethyl-amino-17-demethoxy-geldanamycin (17DMAG) and 17-allylamino-17-demethoxygeldanamycin (17AAG) in vitro: effects on Hsp90 and client proteins in melanoma models, Cancer Chemother. Pharmacol. 56, 126-137.
40. Brown, J. M., and Wilson, W. R. (2004) Exploiting tumour hypoxia in cancer treatment, Nat. Rev. Cancer 4, 437-447.
41. Patterson, L. H., McKeown, S. R., Robson, T., Gallagher, R., Raleigh, S. M., and Orr, S. (1999) Antitumour prodrug development using cytochrome P450 (CYP) mediated activation, Anticancer Drug Des. 14, 473-486.
42. Guo, W., Reigan, P., Siegel, D., Zirrolli, J., Gustafson, D., and Ross, D. (2005) Formation of 17-allylamino-demethoxygeldanamycin (17-AAG) hydroquinone by NAD(P)H:quinone oxidoreductase 1: role of 17-AAG hydroquinone in heat shock protein 90 inhibition, Cancer Res. 65, 10006-10015.
43. Bello, R. I., Gomez-Diaz, C., Navarro, F., Alcain, F. J., and Villalba, J. M. (2001) Expression of NAD(P)H:quinone oxidoreductase 1 in HeLa cells: role of hydrogen peroxide and growth phase, J. Biol. Chem. 276, 44379-44384.
44. Phillips, R. M., de la Cruz, A., Traver, R. D., and Gibson, N. W. (1994) Increased activity and expression of NAD(P)H:quinone acceptor oxidoreductase in confluent cell cultures and within multicellular spheroids, Cancer Res. 54, 3766-3771.
45. Fisher, G. R., and Gutierrez, P. L. (1991) The reductive metabolism of diaziquone (AZQ) in the S9 fraction of MCF-7 cells: free radical formation and NAD(P)H:quinone-acceptor oxidoreductase (DT-diaphorase) activity, Free Radical Biol. Med. 10, 359-370.