Hsp90 inhibition protects against inherited retinal degeneration

Human Molecular Genetics

Volumn 23, Issue 8, 2014, Pages 2164-2175

  Aguilà, Mònica ^a   Bevilacqua, Dalila ^a   Mcculley, Caroline ^a   Schwarz, Nele ^a   Athanasiou, Dimitra ^a   Kanuga, Naheed ^a   Novoselov, Sergey S ^a   Lange, Clemens A K ^a,c   Ali, Robin R ^a   Bainbridge, James W ^a   Gias, Carlos ^a   Coffey, Peter J ^a   Garriga, Pere ^b   Cheetham, Michael E ^a  

^a UCLInstitute of Ophthalmology ^*  (United Kingdom)

^b UNIVERSITAT POLITÈCNICA DE CATALUNYA   (Spain)

^c UNIVERSITY OF FREIBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 90 INHIBITOR; HEAT SHOCK TRANSCRIPTION FACTOR 1; PHOSPHODIESTERASE VI; RETINA S ANTIGEN; RHODOPSIN; RHODOPSIN KINASE; SCOTOPSIN; TANESPIMYCIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL MIGRATION; CONTROLLED STUDY; DRUG MECHANISM; EYE PROTECTION; IN VIVO STUDY; MOUSE; NONHUMAN; PHENOTYPE; PHOTOTRANSDUCTION; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; RAT; RETINA DEGENERATION; VISION; WILD TYPE;

ANIMALS; BLOTTING, WESTERN; CELLS, CULTURED; ELECTRORETINOGRAPHY; FEMALE; G-PROTEIN-COUPLED RECEPTOR KINASE 1; GENES, DOMINANT; GENETIC PREDISPOSITION TO DISEASE; HSP90 HEAT-SHOCK PROTEINS; IMMUNOENZYME TECHNIQUES; MICE; MICE, INBRED C57BL; MUTATION; PYRIDONES; PYRIMIDINES; RATS; RATS, SPRAGUE-DAWLEY; RATS, TRANSGENIC; REAL-TIME POLYMERASE CHAIN REACTION; RETINA; RETINITIS PIGMENTOSA; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RHODOPSIN; RNA, MESSENGER; TOMOGRAPHY, OPTICAL COHERENCE; VISION, OCULAR;

EID: 84897585126     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddt613     Document Type: Article

References (48)

1. Taipale, M., Jarosz, D.F. and Lindquist, S. (2010) HSP90 at the hub of protein homeostasis: emerging mechanistic insights. Nat. Rev. Mol. Cell Biol., 11, 515-528.
2. Li, J. and Buchner, J. (2013) Structure, function and regulation of the hsp90 machinery. Biomed. J., 36, 106-117.
3. Pearl, L.H., Prodromou, C. and Workman, P. (2008) The Hsp90 molecular chaperone: an open and shut case for treatment. Biochem. J., 410, 439-453.
4. Walton-Diaz, A., Khan, S., Bourboulia, D., Trepel, J.B., Neckers, L. and Mollapour, M. (2013) Contributions of co-chaperones and post-translational modifications towards Hsp90 drug sensitivity. Future Med. Chem., 5, 1059-1071.
5. Zou, J., Guo, Y., Guettouche, T., Smith, D.F. and Voellmy, R. (1998) Repression of heat shock transcription factor HSF1 activation by HSP90 (HSP90 complex) that forms a stress-sensitive complex with HSF1. Cell, 94, 471-480.
6. Sittler, A., Lurz, R., Lueder, G., Priller, J., Lehrach, H., Hayer-Hartl, M.K., Hartl, F.U. and Wanker, E.E. (2001) Geldanamycin activates a heat shock response and inhibits huntingtin aggregation in a cell culture model of Huntington's disease. Hum. Mol. Genet., 10, 1307-1315.
7. Waza, M., Adachi, H., Katsuno, M., Minamiyama, M., Tanaka, F. and Sobue, G. (2006) Alleviating neurodegeneration by an anticancer agent: an Hsp90 inhibitor (17-AAG). Ann. N. Y. Acad. Sci., 1086, 21-34.
8. Labbadia, J., Cunliffe, H., Weiss, A., Katsyuba, E., Sathasivam, K., Seredenina, T., Woodman, B., Moussaoui, S., Frentzel, S., Luthi-Carter, R. et al. (2011) Altered chromatin architecture underlies progressive impairment of the heat shock response in mouse models of Huntington disease. J. Clin. Invest., 121, 3306-3319.
9. Hartong, D.T., Berson, E.L. and Dryja, T.P. (2006) Retinitis pigmentosa. Lancet, 368, 1795-1809.
10. Dryja, T.P., McGee, T.L., Reichel, E., Hahn, L.B., Cowley, G.S., Yandell, D.W., Sandberg, M.A. and Berson, E.L. (1990) A point mutation of the rhodopsin gene in one form of retinitis pigmentosa. Nature, 343, 364-366.
11. Mendes, H.F., van der Spuy, J., Chapple, J.P. and Cheetham, M.E. (2005) Mechanisms of cell death in rhodopsin retinitis pigmentosa: implications for therapy. Trends Mol. Med., 11, 177-185.
12. Mendes, H.F. and Cheetham, M.E. (2008) Pharmacological manipulation of gain-of-function and dominant-negative mechanisms in rhodopsin retinitis pigmentosa. Hum. Mol. Genet., 17, 3043-3054.
13. Athanasiou, D., Aguila, M., Bevilacqua, D., Novoselov, S.S., Parfitt, D.A. and Cheetham, M.E. (2013) The cell stress machinery and retinal degeneration. FEBS Lett., 587, 2008-2017.
14. Chuang, J.Z., Vega, C., Jun, W. and Sung, C.H. (2004) Structural and functional impairment of endocytic pathways by retinitis pigmentosa mutant rhodopsin-arrestin complexes. J. Clin. Invest., 114, 131-140.
15. Iannaccone, A., Man, D., Waseem, N., Jennings, B.J., Ganapathiraju, M., Gallaher, K., Reese, E., Bhattacharya, S.S. and Klein-Seetharaman, J. (2006) Retinitis pigmentosa associated with rhodopsin mutations: Correlation between phenotypic variability and molecular effects. Vision Res., 46, 4556-4567.
16. Shi, W., Sports, C.D., Raman, D., Shirakawa, S., Osawa, S. and Weiss, E.R. (1998) Rhodopsin arginine-135 mutants are phosphorylated by rhodopsin kinase and bind arrestin in the absence of 11-cis-retinal. Biochemistry, 37, 4869-4874.
17. Tam, L.C., Kiang, A.S., Campbell, M., Keaney, J., Farrar, G.J., Humphries, M.M., Kenna, P.F. and Humphries, P. (2010) Prevention of autosomal dominant retinitis pigmentosa by systemic drug therapy targeting heat shock protein 90 (Hsp90). Hum. Mol. Genet., 19, 4421-4436.
18. Pennesi, M.E., Nishikawa, S., Matthes, M.T., Yasumura, D. and LaVail, M.M. (2008) The relationship of photoreceptor degeneration to retinal vascular development and loss in mutant rhodopsin transgenic and RCS rats. Exp. Eye Res., 87, 561-570.
19. Saliba, R.S., Munro, P.M., Luthert, P.J. and Cheetham, M.E. (2002) The cellular fate of mutant rhodopsin: quality control, degradation and aggresome formation. J. Cell Sci., 115, 2907-2918.
20. Noorwez, S.M., Malhotra, R., McDowell, J.H., Smith, K.A., Krebs, M.P. and Kaushal, S. (2004) Retinoids assist the cellular folding of the autosomal dominant retinitis pigmentosa opsin mutant P23H. J. Biol. Chem., 279, 16278-16284.
21. Tam, B.M. and Moritz, O.L. (2009) The role of rhodopsin glycosylation in protein folding, trafficking, and light-sensitive retinal degeneration. J. Neurosci., 29, 15145-15154.
22. McMillan, D.R., Xiao, X., Shao, L., Graves, K. and Benjamin, I.J. (1998) Targeted disruption of heat shock transcription factor 1 abolishes thermotolerance and protection against heat-inducible apoptosis. J. Biol. Chem., 273, 7523-7528.
23. Luo, J. and Benovic, J.L. (2003) G protein-coupled receptor kinase interaction with Hsp90 mediates kinase maturation. J. Biol. Chem., 278, 50908-50914.
24. Matsuda, T. and Cepko, C.L. (2007) Controlled expression of transgenes introduced by in vivo electroporation. Proc. Natl. Acad. Sci. USA, 104, 1027-1032.
25. 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. et al. (2010) 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, 46, 340-347.
26. Pacey, S., Wilson, R.H., Walton, M., Eatock, M.M., Hardcastle, A., Zetterlund, A., Arkenau, H.T., Moreno-Farre, J., Banerji, U., Roels, B. et al. (2011) 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., 17, 1561-1570.
27. Sessa, C., Shapiro, G.I., Bhalla, K.N., Britten, C., Jacks, K.S., Mita, M., Papadimitrakopoulou, V., Pluard, T., Samuel, T.A., Akimov, M. et al. (2013) First-in-human phase I dose-escalation study of the HSP90 inhibitor AUY922 in patients with advanced solid tumors. Clin. Cancer Res., 19, 3671-3680.
28. Lin, J.H., Li, H., Yasumura, D., Cohen, H.R., Zhang, C., Panning, B., Shokat, K.M., Lavail, M.M. and Walter, P. (2007) IRE1 signaling affects cell fate during the unfolded protein response. Science, 318, 944-949.
29. Lobanova, E.S., Finkelstein, S., Skiba, N.P. and Arshavsky, V.Y. (2013) Proteasome overload is acommonstress factor in multiple forms of inherited retinal degeneration. Proc. Natl. Acad. Sci. USA, 110, 9986-9991.
30. Gorbatyuk, M.S., Knox, T., LaVail, M.M., Gorbatyuk, O.S., Noorwez, S.M., Hauswirth, W.W., Lin, J.H., Muzyczka, N. and Lewin, A.S. (2010) Restoration of visual function in P23H rhodopsin transgenic rats by gene delivery of BiP/Grp78. Proc. Natl. Acad. Sci. USA, 107, 5961-5966.
31. Athanasiou, D., Kosmaoglou, M., Kanuga, N., Novoselov, S.S., Paton, A.W., Paton, J.C., Chapple, J.P. and Cheetham, M.E. (2012) BiP prevents rod opsin aggregation. Mol. Biol. Cell, 23, 3522-3531.
32. Vasireddy, V., Chavali, V.R., Joseph, V.T., Kadam, R., Lin, J.H., Jamison, J.A., Kompella, U.B., Reddy, G.B. and Ayyagari, R. (2011) Rescue of photoreceptor degeneration by curcumin in transgenic rats with P23H rhodopsin mutation. PLoS ONE, 6, e21193.
33. Fernandez-Sanchez, L., Lax, P., Pinilla, I., Martin-Nieto, J. and Cuenca, N. (2011) Tauroursodeoxycholic acid prevents retinal degeneration in transgenic P23H rats. Invest. Ophthalmol. Vis. Sci., 52, 4998-5008.
34. Palczewski, K. and Saari, J.C. (1997) Activation and inactivation steps in the visual transduction pathway. Curr. Opin. Neurobiol., 7, 500-504.
35. Chen, J., Shi, G., Concepcion, F.A., Xie, G., Oprian, D. and Chen, J. (2006) Stable rhodopsin/arrestin complex leads to retinal degeneration in a transgenic mouse model of autosomal dominant retinitis pigmentosa. J. Neurosci., 26, 11929-11937.
36. Moaven, H., Koike, Y., Jao, C.C., Gurevich, V.V., Langen, R. and Chen, J. (2013) Visual arrestin interaction with clathrin adaptor AP-2 regulates photoreceptor survival in the vertebrate retina. Proc. Natl. Acad. Sci. USA, 110, 9463-9468.
37. Alloway, P.G., Howard, L. and Dolph, P.J. (2000) The formation of stable rhodopsin-arrestin complexes induces apoptosis and photoreceptor cell degeneration. Neuron, 28, 129-138.
38. Fuchs, S., Nakazawa, M., Maw, M., Tamai, M., Oguchi, Y. and Gal, A. (1995) A homozygous 1-base pair deletion in the arrestin gene is a frequent cause of Oguchi disease in Japanese. Nat. Genet., 10, 360-362.
39. Yamamoto, S., Sippel, K.C., Berson, E.L. and Dryja, T.P. (1997) Defects in the rhodopsin kinase gene in the Oguchi form of stationary night blindness. Nat. Genet., 15, 175-178.
40. Caplan, A.J., Mandal, A.K. and Theodoraki, M.A. (2007) Molecular chaperones and protein kinase quality control. Trends Cell Biol., 17, 87-92.
41. Sohocki, M.M., Bowne, S.J., Sullivan, L.S., Blackshaw, S., Cepko, C.L., Payne, A.M., Bhattacharya, S.S., Khaliq, S., Qasim Mehdi, S., Birch, D.G. et al. (2000) Mutations in a new photoreceptor-pineal gene on 17p cause Leber congenital amaurosis. Nat. Genet., 24, 79-83.
42. Liu, X., Bulgakov, O.V., Wen, X.H., Woodruff, M.L., Pawlyk, B., Yang, J., Fain, G.L., Sandberg, M.A., Makino, C.L. and Li, T. (2004) AIPL1, the protein that is defective in Leber congenital amaurosis, is essential for the biosynthesis of retinal rod cGMP phosphodiesterase. Proc. Natl. Acad. Sci. USA, 101, 13903-8.
43. Ramamurthy, V., Niemi, G.A., Reh, T.A. and Hurley, J.B. (2004) Leber congenital amaurosis linked to AIPL1: a mouse model reveals destabilization of cGMP phosphodiesterase. Proc. Natl. Acad. Sci. USA, 101, 13897-13902.
44. Hidalgo-de-Quintana, J., Evans, R.J., Cheetham, M.E. and van der Spuy, J. (2008) The Leber congenital amaurosis protein AIPL1 functions as part of a chaperone heterocomplex. Invest. Ophthalmol. Vis. Sci., 49, 2878-2887.
45. Kosmaoglou, M. and Cheetham, M.E. (2008) Calnexin is not essential for mammalian rod opsin biogenesis. Mol. Vis., 14, 2466-2474.
46. Coffey, P.J., Gias, C., McDermott, C.J., Lundh, P., Pickering, M.C., Sethi, C., Bird, A., Fitzke, F.W., Maass, A., Chen, L.L. et al. (2007) Complement factor H deficiency in aged mice causes retinal abnormalities and visual dysfunction. Proc. Natl. Acad. Sci. USA, 104, 16651-6.
47. Matsuda, T.C. and Cepko, C.L. (2008) Analysis of Gene Function in the Retina. Methods Mol. Biol., 423, 259-278.
48. Peirson, S.N., Butler, J.N. and Foster, R.G. (2003) Experimental validation of novel and conventional approaches to quantitative real-time PCR data analysis. Nucleic Acids Res., 31, e73.