Enzyme specific activation of benzoquinone ansamycin prodrugs using HuCC49ΔCH2-β-galactosidase conjugates

Journal of Medicinal Chemistry

Volumn 49, Issue 21, 2006, Pages 6290-6297

  Fang, Lanyan ^a   Battisti, Robert F ^a   Cheng, Hao ^a   Reigan, Philip ^b   Xin, Yan ^a   Shen, Jie ^a   Ross, David ^b   Chan, Kenneth K ^a   Martin Jr , Edward W ^a   Wang, Peng George ^a   Sun, Duxin ^a  

^a OHIO STATE UNIVERSITY   (United States)

^b UNIVERSITY OF COLORADO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

17 AMINO 17 DEMETHOXYGELDANAMYCIN; 17 AMINO 17 DEMETHOXYGELDANAMYCIN C2; 17 AMINO 17 DEMETHOXYGELDANAMYCIN C2 GALACTOSE; ANSAMYCIN DERIVATIVE; BENZOQUINONE DERIVATIVE; BETA GALACTOSIDASE; GELDANAMYCIN; HEAT SHOCK PROTEIN 90; HUMANIZED CC49 MONOCLONAL ANTIBODY DELTA CH2; MONOCLONAL ANTIBODY CC49; PRODRUG; PROTEIN KINASE B; TETRAZOLIUM; TETRAZOLIUM [3 (4,5 DIMETHYTHIAZOL 2 YL)] 5 (3 CARBOXYMETHOXYPHENYL) 2 (4 SULFOPHENYL) 2H TETRAZOLIUM; TUMOR ANTIGEN; TUMOR ANTIGEN 72; UNCLASSIFIED DRUG;

ANTINEOPLASTIC ACTIVITY; ARTICLE; BINDING AFFINITY; CONJUGATE; CONTROLLED STUDY; DRUG BINDING; DRUG CONJUGATION; DRUG SPECIFICITY; ENZYME ACTIVATION; ENZYME DEGRADATION; ENZYME SPECIFICITY; HUMAN; HUMAN CELL; HUMAN TISSUE; MASS SPECTROMETRY;

ANTIBODIES, MONOCLONAL; ANTIGENS, NEOPLASM; ANTINEOPLASTIC AGENTS; BENZOQUINONES; BETA-GALACTOSIDASE; CELL LINE, TUMOR; COLONIC NEOPLASMS; DRUG CARRIERS; DRUG DELIVERY SYSTEMS; GALACTOSIDES; GLYCOPROTEINS; HSP90 HEAT-SHOCK PROTEINS; HUMANS; INDICATORS AND REAGENTS; LACTAMS, MACROCYCLIC; MASS SPECTROMETRY; MODELS, MOLECULAR; PRODRUGS; PROTEIN BINDING; PROTO-ONCOGENE PROTEINS C-AKT; TETRAZOLIUM SALTS; THIAZOLES;

EID: 33750107199     PISSN: 00222623     EISSN: None     Source Type: Journal    
DOI: 10.1021/jm060647f     Document Type: Article

References (53)

1. Syrigos, K. N.; Epenetos, A. A. Antibody directed enzyme prodrug therapy (ADEPT): A review of the experimental and clinical considerations. Anticancer Res. 1999, 19, 605-613.
2. Denny, W. A.; Wilson, W. R. The design of selectively activated anti-cancer prodrugs for use in antibody-directed and gene-directed enzyme-prodrug therapies. J Pharm Pharmacol 1998, 50, 387-394.
3. Colcher, D.; Milenic, D.; Roselli, M.; Raubitschek, A.; Yarranton, G.; et al. Characterization and biodistribution of recombinant and recombinant/chimeric constructs of monoclonal antibody B72.3. Cancer Res. 1989, 49, 1738-1745.
4. Johnson, V. G.; Schlom, J.; Paterson, A. J.; Bennett, J.; Magnani, J. L.; et al. Analysis of a human tumor-associated glycoprotein (TAG-72) identified by monoclonal antibody B72.3. Cancer Res. 1986, 46, 850-857.
5. Colcher, D.; Minelli, M. F.; Roselli, M.; Muraro, R.; Simpson-Milenic, D.; et al. Radioimmunolocalization of human carcinoma xenografts with B72.3 s generation monoclonal antibodies. Cancer Res. 1988, 48, 4597-4603.
6. Alvarez, R. D.; Huh, W. K.; Khazaeli, M. B.; Meredith, R. F.; Partridge, E. E.; et al. A phase I study of combined modality (90)-yttrium-CC49 intraperitoneal radioimmunotherapy for ovarian cancer. Clin Cancer Res. 2002, 8, 2806-2811.
7. Slavin-Chiorini, D. C.; Kashmiri, S. V.; Schlom, J.; Calvo, B.; Shu, L. M.; et al. Biological properties of chimeric domain-deleted anticarcinoma immunoglobulins. Cancer Res. 1995, 55, 5957s-5967s.
8. Kashmiri, S. V.; Shu, L.; Padlan, E. A.; Milenic, D. E.; Schlom, J.; et al. Generation, characterization, and in vivo studies of humanized anticarcinoma antibody CC49. Hybridoma 1995, 14, 461-473.
9. Xiao, J.; Horst, S.; Hinkle, G.; Cao, X.; Kocak, E.; et al. Pharmacokinetics and clinical evaluation of 125I-radiolabeled humanized CC49 monoclonal antibody (HuCC49deltaC(H)2) in recurrent and metastatic colorectal cancer patients. Cancer Biother. Radiopharm. 2005, 20, 16-26.
10. Bertsch, D. J.; Burak, W. E., Jr.; Young, D. C.; Arnold, M. W.; Martin, E. W., Jr. Radioimmunoguided surgery system improves survival for patients with recurrent colorectal cancer. Surgery 1995, 118, 634-638; discussion 638-639.
11. Martin, E. W., Jr.; Carey, L. C. Second-look surgery for colorectal cancer. The second time around. Ann. Surg. 1991, 214, 321-325; discussion 326-327.
12. Martinez, D. A.; Barbera-Guillem, E.; LaValle, G. J.; Martin, E. W., Jr. Radioimmunoguided surgery for gastrointestinal malignancies: An analysis of 14 years of clinical experience. Cancer Control 1997, 4, 505-516.
13. Hine, K. R.; Dykes, P. W. Prospective randomised trial of early cytotoxic therapy for recurrent colorectal carcinoma detected by serum CEA. Gut 1984, 25, 682-688.
14. Ahn, J. H.; Kim, T. W.; Lee, J. H.; Min, Y. J.; Kim, J. G.; et al. Oral doxifluridine plus leucovorin in metastatic colorectal cancer: Randomized phase II trial with intravenous 5-fluorouracil plus leucovorin. Am. J. Clin. Oncol. 2003, 26, 98-102.
15. Fuchs, C. S.; Moore, M. R.; Harker, G.; Villa, L.; Rinaldi, D.; et al. Phase III comparison of two irinotecan dosing regimens in second-line therapy of metastatic colorectal cancer. J. Clin. Oncol. 2003, 21, 807-814.
16. Kabbinavar, F.; Hurwitz, H. I.; Fehrenbacher, L.; Meropol, N. J.; Novotny, W. F.; et al. Phase II, randomized trial comparing bevacizumab plus fluorouracil (FU)/leucovorin (LV) with FU/LV alone in patients with metastatic colorectal cancer. J. Clin. Oncol. 2003, 21, 60-65.
17. Workman, P. Altered states: Selectively drugging the Hsp90 cancer chaperone. Trends Mol. Med. 2004, 10, 47-51.
18. Workman, P. Combinatorial attack on multistep oncogenesis by inhibiting the Hsp90 molecular chaperone. Cancer Lett. 2004, 206, 149-157.
19. Workman, P. Auditing the pharmacological accounts for Hsp90 molecular chaperone inhibitors: Unfolding the relationship between pharmacokinetics and pharmacodynamics. Mol. Cancer Ther. 2003, 2, 131-138.
20. Ferrarini, M.; Heltai, S.; Zocchi, M. R.; Rugarli, C. Unusual expression and localization of heat-shock proteins in human tumor cells. Int. J. Cancer 1992, 51, 613-619.
21. Neckers, L. Hsp90 inhibitors as novel cancer chemotherapeutic agents. Trends Mol. Med. 2002, 8, S55-61.
22. Neckers, L. Development of small molecule Hsp90 inhibitors: Utilizing both forward and reverse chemical genomics for drug identification. Curr. Med. Chem. 2003, 10, 733-739.
23. Prodromou, C.; Roe, S. M.; O'Brien, R.; Ladbury, J. E.; Piper, P. W.; et al. Identification and structural characterization of the ATP/ADP-binding site in the Hsp90 molecular chaperone. Cell 1997, 90, 65-75.
24. Stebbins, C. E.; Russo, A. A.; Schneider, C.; Rosen, N.; Hartl, F. U.; et al. Crystal structure of an Hsp90-geldanamycin complex: Targeting of a protein chaperone by an antitumor agent. Cell 1997, 89, 239-250.
25. Panaretou, B.; Prodromou, C.; Roe, S. M.; O'Brien, R.; Ladbury, J. E.; et al. ATP binding and hydrolysis are essential to the function of the Hsp90 molecular chaperone in vivo. EMBO J. 1998, 17, 4829-4836.
26. Panaretou, B.; Siligardi, G.; Meyer, P.; Maloney, A.; Sullivan, J. K.; et al. Activation of the ATPase activity of hsp90 by the stress-regulated cochaperone aha1. Mol. Cell 2002, 10, 1307-1318.
27. Panaretou, B.; Sinclair, K.; Prodromou, C.; Johal, J.; Pearl, L.; et al. The Hsp90 of Candida albicans can confer Hsp90 functions in Saccharomyces cerevisiae: A potential model for the processes that generate immunogenic fragments of this molecular chaperone in C. albicans infections. Microbiology 1999, 145 (Pt 12), 3455-3463.
28. Miller, P.; Schnur, R. C.; Barbacci, E.; Moyer, M. P.; Moyer, J. D. Binding of benzoquinoid ansamycins to p 100 correlates with their ability to deplete the erbB2 gene product p185. Biochem. Biophys. Res. Commun. 1994, 201, 1313-1319.
29. Miller, P.; DiOrio, C.; Moyer, M.; Schnur, R. C.; Bruskin, A.; et al. Depletion of the erbB-2 gene product p185 by benzoquinoid ansamycins. Cancer Res. 1994, 54, 2724-2730.
30. Mimnaugh, E. G.; Chavany, C.; Neckers, L. Polyubiquitination and proteasomal degradation of the p185c-erbB-2 receptor protein-tyrosine kinase induced by geldanamycin. J. Biol. Chem. 1996, 271, 22796-22801.
31. Xu, W.; Mimnaugh, E. G.; Kim, J. S.; Trepel, J. B.; Neckers, L. M. Hsp90, not Grp94, regulates the intracellular trafficking and stability of nascent ErbB2. Cell Stress Chaperones 2002, 7, 91-96.
32. Xu, W.; Yuan, X.; Xiang, Z.; Mimnaugh, E.; Marcu, M.; et al. Surface charge and hydrophobicity determine ErbB2 binding to the Hsp90 chaperone complex. Nat. Struct. Mol. Biol. 2005, 12, 120-126.
33. Neckers, L.; Schulte, T. W.; Mimnaugh, E. Geldanamycin as a potential anticancer agent: Its molecular target and biochemical activity. Invest. New Drugs 1999, 17, 361-373.
34. Supko, J. G.; Hickman, R. L.; Grever, M. R.; Malspeis, L. Preclinical pharmacologic evaluation of geldanamycin as an antitumor agent. Cancer Chemother. Pharmacol. 1995, 36, 305-315.
35. Schnur, R. C.; Corman, M. L.; Gallaschun, R. J.; Cooper, B. A.; Dee, M. F.; et al. erbB-2 oncogene inhibition by geldanamycin derivatives: Synthesis, mechanism of action, and structure-activity relationships. J Med. Chem. 1995, 38, 3813-3820.
36. Schnur, R. C.; Corman, M. L.; Gallaschun, R. J.; Cooper, B. A.; Dee, M. F.; et al. Inhibition of the oncogene product p185erbB-2 in vitro and in vivo by geldanamycin and dihydrogeldanamycin derivatives. J Med. Chem. 1995, 38, 3806-3812.
37. 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.
38. Kuduk, S. D.; Harris, C. R.; Zheng, F. F.; Sepp-Lorenzino, L.; Ouerfelli, O.; et al. Synthesis and evaluation of geldanamycin-testosterone hybrids. Bioorg. Med. Chem. Lett. 2000, 10, 1303-1306.
39. Mandler, R.; Kobayashi, H.; Davis, M. Y.; Waldmann, T. A.; Brechbiel, M. W. Modifications in synthesis strategy improve the yield and efficacy of geldanamycin-herceptin immunoconjugates. Bioconjugate Chem. 2002, 13, 786-791.
40. Ramanathan, R. K.; Trump, D. L.; Eiseman, J. L.; Belani, C. P.; Agarwala, S. S.; et al. Phase I pharmacokinetic-pharmacodynamic study of 17-(allylamino)-17-demethoxygeldanamycin (17AAG, NSC 330507), a novel inhibitor of heat shock protein 90, in patients with refractory advanced cancers. Clin. Cancer Res. 2005, 11, 3385-3391.
41. Sausville, E. A.; Tomaszewski, J. E.; Ivy, P. Clinical development of 17-allylamino, 17-demethoxygeldanamycin. Curr. Cancer Drug Targets 2003, 3, 377-383.
42. Glaze, E. R.; Lambert, A. L.; Smith, A. C.; Page, J. G.; Johnson, W. D.; et al. Preclinical toxicity of a geldanamycin analog, 17- (dimethylaminoethylamino)-17-demethoxygeldanamycin (17-DMAG), in rats and dogs: Potential clinical relevance. Cancer Chemother. Pharmacol. 2005, 56, 637-647.
43. Eiseman, J. L.; Lan, J.; Lagattuta, T. F.; Hamburger, D. R.; Joseph, E.; et al. Pharmacokinetics and pharmacodynamics of 17-demethoxy 17-[[(2-dimethylamino)ethyl]amino]geldanamycin (17DMAG, NSC 707545) in CB-17 SCID mice bearing MDA-MB-231 human breast cancer xenografts. Cancer Chemother. Pharmacol. 2005, 55, 21-32.
44. Cheng, H.; Cao, X.; Xian, M.; Fang, L.; Cai, T. B.; et al. Synthesis and enzyme-specific activation of carbohydrate-geldanamycin conjugates with potent anticancer activity. J. Med Chem. 2005, 48, 645-652.
45. Xu, L.; Eiseman, J. L.; Egorin, M. J.; D'Argenio, D. Z. Physiologically based pharmacokinetics and molecular pharmacodynamics of 17-(allylamino)-17- demethoxygeldanamycin and its active metabolite in tumor-bearing mice. J. Pharmacokinet. Pharmacodyn. 2003, 30, 185-219.
46. Tian, Z. Q.; Liu, Y.; Zhang, D.; Wang, Z.; Dong, S. D.; et al. Synthesis and biological activities of novel 17-aminogeldanamycin derivatives. Bioorg. Med. Chem. 2004, 12, 5317-5329.
47. Schnur, R.; Corman, M. [3,3]-sigmatropic rearrangements in an ansamycin: Stereospecific conversion of an (S)-allylic alcohol to an (S)-allylic amine derivative. J. Org. Chem. 1994, 59, 2581-2584.
48. Luty, B. A.; Wasserman, Z. R.; Stouten, P. F. W.; Hodge, C. N.; Zacharias, M.; et al. A molecular mechanics/grid method for evaluation of ligand-receptor interactions. J. Comput. Chem. 1995, 16, 454-464.
49. Stouten, P. F. W.; Froemmel, C.; Nakamura, H.; Sander, C. Mol. Simul. 1993, 10, 97-120.
50. Dauber-Osguthorpe, P.; Roberts, V. A.; Osguthorpe, D. J.; Wolff, J.; Genest, M.; et al. Structure and energetics of ligand binding to proteins: Escherichia coli dihydrofolate reductase-trimethoprim, a drug-receptor system. Proteins 1988, 4, 31-47.
51. Brooks, B. R.; Bruccoleri, R. E.; Olafson, B. D.; States, D. J.; Swaminathan, S.; et al. CHARMM: A program for macromolecular energy, minimization, and dynamics calculations. J. Comput. Chem. 1983, 4, 187-217.
52. Morris, G. M.; Goodsell, D. S.; Halliday, R. S.; Huey, R.; Hart, W. E.; et al. Automated docking using a Lamarckian genetic algorithm and empirical binding free energy function. J. Comput. Chem. 1998, 19, 1639-1662.
53. Gasteiger, J.; Marsili, M. Iterative partial equalization of orbital electronegativity: A rapid access to atomic charges. Tetrahedron 1980, 36, 3219-3228.