A rat retinal damage model predicts for potential clinical visual disturbances induced by Hsp90 inhibitors

Toxicology and Applied Pharmacology

Volumn 273, Issue 2, 2013, Pages 401-409

  Zhou, Dan ^a   Liu, Yuan ^a   Ye, Josephine ^a   Ying, Weiwen ^a   Ogawa, Luisa Shin ^a   Inoue, Takayo ^a   Tatsuta, Noriaki ^a   Wada, Yumiko ^a   Koya, Keizo ^a   Huang, Qin ^b   Bates, Richard C ^a   Sonderfan, Andrew J ^a  

^a Synta Pharmaceuticals Corp   (United States)

^b VA BOSTON HEALTHCARE SYSTEM   (United States)

Author keywords

Drug safety assessment; Hsp90 inhibitors; Predictive toxicology; Retinal degeneration; Rodent model; Visual impairment

Indexed keywords

ALVESPIMYCIN; GANETESPIB; HEAT SHOCK PROTEIN 70; HEAT SHOCK PROTEIN 90; HEAT SHOCK PROTEIN 90 INHIBITOR; LUMINESPIB; TANESPIMYCIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; AREA UNDER THE CURVE; ARTICLE; BIOACCUMULATION; CELL DEATH; CONTROLLED STUDY; DRUG ACCUMULATION; DRUG BLOOD LEVEL; DRUG CLEARANCE; DRUG CYTOTOXICITY; DRUG DISTRIBUTION; DRUG ELIMINATION; DRUG EXPOSURE; DRUG HALF LIFE; DRUG RETENTION; DRUG SAFETY; EYE TOXICITY; HISTOPATHOLOGY; MALE; MAXIMUM PLASMA CONCENTRATION; MAXIMUM TOLERATED DOSE; NONHUMAN; PHOTORECEPTOR; PHOTORECEPTOR CELL; PLASMA CLEARANCE; PLASMA CONCENTRATION-TIME CURVE; PROTEIN EXPRESSION; RAT; RAT MODEL; RETINA; RETINA DEGENERATION; RETINA INJURY; TIME TO MAXIMUM PLASMA CONCENTRATION; VISUAL DISORDER;

DRUG SAFETY ASSESSMENT; HSP90 INHIBITORS; PREDICTIVE TOXICOLOGY; RETINAL DEGENERATION; RODENT MODEL; VISUAL IMPAIRMENT;

ANIMALS; BENZOQUINONES; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; HSP90 HEAT-SHOCK PROTEINS; LACTAMS, MACROCYCLIC; MALE; PHOTORECEPTOR CELLS; PREDICTIVE VALUE OF TESTS; RATS; RATS, LONG-EVANS; RATS, SPRAGUE-DAWLEY; RETINAL DEGENERATION;

RATTUS; RODENTIA;

EID: 84888204057     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2013.09.018     Document Type: Article

References (47)

1. al-Tweigeri T., Nabholtz J.M., Mackey J.R. Ocular toxicity and cancer chemotherapy. A review. Cancer 1996, 78:1359-1373.
2. Banerji U. Heat shock protein 90 as a drug target: some like it hot. Clin. Cancer Res. 2009, 15:9-14.
3. Banerji U., O'Donnell A., Scurr M., Pacey S., Stapleton S., Asad Y., Simmons L., Maloney A., Raynaud F., Campbell M., Walton M., Lakhani S., Kaye S., Workman P., Judson I. Phase I pharmacokinetic and pharmacodynamic study of 17-allylamino, 17-demethoxygeldanamycin in patients with advanced malignancies. J. Clin. Oncol. 2005, 23:4152-4161.
4. Barres B.A., Silverstein B.E., Corey D.P., Chun L.L.Y. Immunological, morphological, and electrophysiological variations among retinal ganglion cells purified by panning. Neuron 1988, 1:791-803.
5. Biamonte M.A., VandeWater R., Arndt J.W., Scannevin R.H., Perret D., Lee W.C. Heat shock protein 90: inhibitors in clinical trials. J. Med. Chem. 2010, 53:3-17.
6. Cho D.C., Heath E.I., Cleary J.M., Kwak E.L., Gandhi L., Lawrence D.P., Zack C., Teofilovici F., Bradley R., Karol M.D., Shapiro G., LoRusso P. A phase I dose-escalation study of the Hsp90 inhibitor ganetespib (STA-9090) administered twice weekly to patients with solid tumors: updated report. J. Clin. Oncol. 2011, 29:A13051.
7. Dean D.O., Tytell M. Hsp25 and -90 immunoreactivity in the normal rat eye. Invest. Ophthalmol. Vis. Sci. 2001, 42:3031-3040.
8. Demetri G.D., Heinrich M.C., Chimelowski B., Morgan J.A., George S., Bradley R., Blackman R.K., Teofilovici F., Fletcher J.A., Tap W., von Mehren M. An open-label phase II study of the Hsp90 inhibitor ganetespib (STA-9090) in patients (pts) with metastatic and/or unresectable GIST. J. Clin. Oncol. 2011, 29:A10011.
9. den Hollander A.I., Roepman R., Koenekoop R.K., Cremers F.P. Leber congenital amaurosis: genes, proteins and disease mechanisms. Prog. Retin. Eye Res. 2008, 27:391-419.
10. Dickson M.A., Okuno S.H., Keohan M.L., Maki R.G., D'Adamo D.R., Akhurst T.J., Antonescu C.R., Schwartz G.K. Phase II study of the HSP90-inhibitor BIIB021 in gastrointestinal stromal tumors. Ann. Oncol. 2013, 24:252-257.
11. Eccles S.A., Massey A., Raynaud F.I., Sharp S.Y., Box G., Valenti M., Patterson L., de Haven Brandon A., Gowan S., Boxall F., Aherne W., Rowlands M., Hayes A., Martins V., Urban F., Boxall K., Prodromou C., Pearl L., James K., Matthews T.P., Cheung K.M., Kalusa A., Jones K., McDonald E., Barril X., Brough P.A., Cansfield J.E., Dymock B., Drysdale M.J., Finch H., Howes R., Hubbard R.E., Surgenor A., Webb P., Wood M., Wright L., Workman P. NVP-AUY922: a novel heat shock protein 90 inhibitor active against xenograft tumor growth, angiogenesis, and metastasis. Cancer Res. 2008, 68:2850-2860.
12. Elfiky A., Saif M.W., Beeram M., O'Brien S., Lammanna N., Castro J.E., Woodworth J., Perea R., Storgard C., Von Hoff D.D. BIIB021, an oral, synthetic non-ansamycin Hsp90 inhibitor: phase I experience. J. Clin. Oncol. 2008, 26:2503.
13. Goldman J.W., Raju R.N., Gordon G.A., Vukovic V.M., Bradley R., Rosen L.S. A phase I dose-escalation study of the Hsp90 inhibitor STA-9090 administered once weekly in patients with solid tumors. J. Clin. Oncol. 2010, 28:A2529.
14. Hidalgo-de-Quintana J., Evans R.J., Cheetham M.E., van der Spuy J. The Leber congenital amaurosis protein AIPL1 functions as part of a chaperone heterocomplex. Invest. Ophthalmol. Vis. Sci. 2008, 49:2878-2887.
15. Kaarniranta K., Ryhanen T., Karjalainen H.M., Lammi M.J., Suuronen T., Huhtala A., Kontkanen M., Terasvirta M., Uusitalo H., Salminen A. Geldanamycin increases 4-hydroxynonenal (HNE)-induced cell death in human retinal pigment epithelial cells. Neurosci. Lett. 2005, 382:185-190.
16. Kim Y.S., Alarcon S.V., Lee S., Lee M.J., Giaccone G., Neckers L., Trepel J.B. Update on Hsp90 inhibitors in clinical trial. Curr. Top. Med. Chem. 2009, 9:1479-1492.
17. Kirschman L.T., Kolandaivelu S., Frederick J.M., Dang L., Goldberg A.F., Baehr W., Ramamurthy V. The Leber congenital amaurosis protein, AIPL1, is needed for the viability and functioning of cone photoreceptor cells. Hum. Mol. Genet. 2010, 19:1076-1087.
18. Kosmaoglou M., Schwarz N., Bett J.S., Cheetham M.E. Molecular chaperones and photoreceptor function. Prog. Retin. Eye Res. 2008, 27:434-449.
19. Kummar S., Gutierrez M.E., Gardner E.R., Chen X., Figg W.D., Zajac-Kaye M., Chen M., Steinberg S.M., Muir C.A., Yancey M.A., Horneffer Y.R., Juwara L., Melillo G., Ivy S.P., Merino M., Neckers L., Steeg P.S., Conley B.A., Giaccone G., Doroshow J.H., Murgo A.J. Phase I trial of 17-dimethylaminoethylamino-17-demethoxygeldanamycin (17-DMAG), a heat shock protein inhibitor, administered twice weekly in patients with advanced malignancies. Eur. J. Cancer 2010, 46:340-347.
20. Lanneau D., Wettstein G., Bonniaud P., Garrido C. Heat shock proteins: cell protection through protein triage. ScientificWorldJournal 2010, 10:1543-1552.
21. LaVail M.M., Lawson N.R. Development of a congenic strain of pigmented and albino rats for light damage studies. Exp. Eye Res. 1986, 43:867-869.
22. Leblanc B., Jezequel S., Davies T., Hanton G., Taradach C. Binding of drugs to eye melanin is not predictive of ocular toxicity. Regul. Toxicol. Pharmacol. 1998, 28:124-132.
23. Mayer M.P., Bukau B. Hsp70 chaperones: cellular functions and molecular mechanism. Cell. Mol. Life Sci. 2005, 62:670-684.
24. Pacey S., Wilson R.H., Walton M., Eatock M.M., Hardcastle A., Zetterlund A., Arkenau H.T., Moreno-Farre J., Banerji U., Roels B., Peachey H., Aherne W., de Bono J.S., Raynaud F., Workman P., Judson I. A phase I study of the heat shock protein 90 inhibitor alvespimycin (17-DMAG) given intravenously to patients with advanced solid tumors. Clin. Cancer Res. 2011, 17:1561-1570.
25. Peponis V., Kyttaris V.C., Chalkiadakis S.E., Bonovas S., Sitaras N.M. Ocular side effects of anti-rheumatic medications: what a rheumatologist should know. Lupus 2010, 19:675-682.
26. Rajan A., Kelly R.J., Trepel J.B., Kim Y.S., Alarcon S.V., Kummar S., Gutierrez M., Crandon S., Zein W.M., Jain L., Mannargudi B., Figg W.D., Houk B.E., Shnaidman M., Brega N., Giaccone G. A phase I study of PF-04929113 (SNX-5422), an orally bioavailable heat shock protein 90 inhibitor, in patients with refractory solid tumor malignancies and lymphomas. Clin. Cancer Res. 2011, 17:6831-6839.
27. Ramalingam S.S., Egorin M.J., Ramanathan R.K., Remick S.C., Sikorski R.P., Lagattuta T.F., Chatta G.S., Friedland D.M., Stoller R.G., Potter D.M., Ivy S.P., Belani C.P. A phase I study of 17-allylamino-17-demethoxygeldanamycin combined with paclitaxel in patients with advanced solid malignancies. Clin. Cancer Res. 2008, 14:3456-3461.
28. Ramanathan R.K., Trump D.L., Eiseman J.L., Belani C.P., Agarwala S.S., Zuhowski E.G., Lan J., Potter D.M., Ivy S.P., Ramalingam S., Brufsky A.M., Wong M.K., Tutchko S., Egorin M.J. 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.
29. Ramanathan R.K., Egorin M.J., Eiseman J.L., Ramalingam S., Friedland D., Agarwala S.S., Ivy S.P., Potter D.M., Chatta G., Zuhowski E.G., Stoller R.G., Naret C., Guo J., Belani C.P. Phase I and pharmacodynamic study of 17-(allylamino)-17-demethoxygeldanamycin in adult patients with refractory advanced cancers. Clin. Cancer Res. 2007, 13:1769-1774.
30. Renouf D.J., Velazquez-Martin J.P., Simpson R., Siu L.L., Bedard P.L. Ocular toxicity of targeted therapies. J. Clin. Oncol. 2012, 30:3277-3286.
31. Samuel T.A., Sessa C., Britten C., Milligan K.S., Mita M.M., Banerji U., Pluard T.J., Stiegler P., Quadt C., Shapiro G. AUY922, a novel HSP90 inhibitor: final results of a first-in-human study in patients with advanced solid malignancies. J. Clin. Oncol. 2010, 28(15s):2528.
32. Sato S., Fujita N., Tsuruo T. Modulation of Akt kinase activity by binding to Hsp90. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:10832-10837.
33. Shahinfar S., Edward D.P., Tso M.O. A pathologic study of photoreceptor cell death in retinal photic injury. Curr. Eye Res. 1991, 10:47-59.
34. Shapiro G., Kwak E.L., Dezube B.J., Lawrence D.P., Cleary J.M., Lewis S., Squires M., Lock V., Lyons J.F., Yule M. Phase I pharmacokinetic and pharmacodynamic study of the heat shock protein 90 inhibitor AT13387 in patients with refractory solid tumors. J. Clin. Oncol. 2010, 28(15s):3069.
35. Sohocki M.M., Perrault I., Leroy B.P., Payne A.M., Dharmaraj S., Bhattacharya S.S., Kaplan J., Maumenee I.H., Koenekoop R., Meire F.M., Birch D.G., Heckenlively J.R., Daiger S.P. Prevalence of AIPL1 mutations in inherited retinal degenerative disease. Mol. Genet. Metab. 2000, 70:142-150.
36. Solit D.B., Ivy S.P., Kopil C., Sikorski R., Morris M.J., Slovin S.F., Kelly W.K., DeLaCruz A., Curley T., Heller G., Larson S., Schwartz L., Egorin M.J., Rosen N., Scher H.I. Phase I trial of 17-allylamino-17-demethoxygeldanamycin in patients with advanced cancer. Clin. Cancer Res. 2007, 13:1775-1782.
37. Taipale M., Jarosz D.F., Lindquist S. HSP90 at the hub of protein homeostasis: emerging mechanistic insights. Nat. Rev. Mol. Cell Biol. 2010, 11:515-528.
38. Taldone T., Gozman A., Maharaj R., Chiosis G. Targeting Hsp90: small-molecule inhibitors and their clinical development. Curr. Opin. Pharmacol. 2008, 8:370-374.
39. Trepel J., Mollapour M., Giaccone G., Neckers L. Targeting the dynamic HSP90 complex in cancer. Nat. Rev. Cancer 2010, 10:537-549.
40. Whitesell L., Lindquist S.L. HSP90 and the chaperoning of cancer. Nat. Rev. Cancer 2005, 5:761-772.
41. Whitesell L., Bagatell R., Falsey R. The stress response: implications for the clinical development of hsp90 inhibitors. Curr. Cancer Drug Targets 2003, 3:349-358.
42. Williams T.P., Howell W.L. Action spectrum of retinal light-damage in albino rats. Invest. Ophthalmol. Vis. Sci. 1983, 24:285-287.
43. Wong K., Koczywas M., Goldman J.W., Paschold E.H., Horn R.L., Blackman R.K., Teofilovici F., Shapiro G., Socinski M.A. An open-label phase II study of the Hsp90 inhibitor ganetespib (STA-9090) as monotherapy in patients with advanced non-small cell lung cancer (NSCLC). J. Clin. Oncol. 2011, 29:A7500.
44. Wu W.C., Wu M.H., Chang Y.C., Hsieh M.C., Wu H.J., Cheng K.C., Lai Y.H., Kao Y.H. Geldanamycin and its analog induce cytotoxicity in cultured human retinal pigment epithelial cells. Exp. Eye Res. 2010, 91:211-219.
45. Yao J.Q., Liu Q.H., Chen X., Yang Q., Xu Z.Y., Hu F., Wang L., Li J.M. Hsp90 inhibitor 17-allylamino-17-demethoxygeldanamycin inhibits the proliferation of ARPE-19 cells. J. Biomed. Sci. 2010, 17:30.
46. Ying W., Du Z., Sun L., Foley K.P., Proia D.A., Blackman R.K., Zhou D., Inoue T., Tatsuta N., Sang J., Ye S., Acquaviva J., Ogawa L.S., Wada Y., Barsoum J., Koya K. Ganetespib, a unique triazolone-containing Hsp90 inhibitor, exhibits potent antitumor activity and a superior safety profile for cancer therapy. Mol. Cancer Ther. 2012, 11:475-484.
47. Youssef P.N., Sheibani N., Albert D.M. Retinal light toxicity. Eye (Lond.) 2011, 25:1-14.