Unfolding the therapeutic potential of chemical chaperones for age-related macular degeneration

References

• Friedman DS, O’Colmain BJ, Munoz B et al. Prevalence of age-related macular degeneration in the United States. Arch. Ophthalmol.122, 564–572 (2004).
   PubMed Web of Science ®Google Scholar
• de Jong, P. T. Age-related macular degeneration. N. Engl. J. Med.355, 1474–1485 (2006).
   PubMed Web of Science ®Google Scholar
• Olsen TW, Feng X. The Minnesota grading system of eye bank eyes for age-related macular degeneration. Invest. Ophthalmol. Vis. Sci.45, 4484–4490 (2004).
   PubMed Web of Science ®Google Scholar
• Ambati J, Ambati BK, Yoo SH, Ianchulev S, Adamis AP. Age-related macular degeneration: etiology, pathogenesis, and therapeutic strategies. Surv. Ophthalmol.48, 257–293 (2003).
   PubMed Web of Science ®Google Scholar
• Schmidt-Erfurth UM, Pruente C. Management of neovascular age-related macular degeneration. Prog. Retin. Eye Res.26, 437–451 (2007).
   PubMedGoogle Scholar
• van LR, Boekhoorn S, Vingerling JR et al. Dietary intake of antioxidants and risk of age-related macular degeneration. JAMA294, 3101–3107 (2005).
   PubMed Web of Science ®Google Scholar
• Sangiovanni JP, Chew EY, Clemons TE et al. The relationship of dietary lipid intake and age-related macular degeneration in a case-control study: AREDS Report No. 20. Arch. Ophthalmol.125, 671–679 (2007).
   PubMed Web of Science ®Google Scholar
• Petrukhin K. New therapeutic targets in atrophic age-related macular degeneration. Expert Opin. Ther. Targets11, 625–639 (2007).
   PubMed Web of Science ®Google Scholar
• Age-Related Eye Disease Study Research Group. A randomized, placebo-controlled, clinical trial of high-dose supplementation with vitamins C and E, β carotene, and zinc for age-related macular degeneration and vision loss: AREDS report no. 8. Arch. Ophthalmol.119, 1417–1436 (2001).
   PubMed Web of Science ®Google Scholar
• Liang FQ, Godley BF. Oxidative stress-induced mitochondrial DNA damage in human retinal pigment epithelial cells: a possible mechanism for RPE aging and age-related macular degeneration. 40. Exp. Eye Res.76, 397–403 (2003).
   PubMed Web of Science ®Google Scholar
• Beatty S, Koh H, Phil M, Henson D, Boulton M. The role of oxidative stress in the pathogenesis of age-related macular degeneration. Surv. Ophthalmol.45, 115–134 (2000).
   PubMed Web of Science ®Google Scholar
• Donoso LA, Kim D, Frost A, Callahan A, Hageman G. The role of inflammation in the pathogenesis of age-related macular degeneration. Surv. Ophthalmol.51, 137–152 (2006).
   PubMed Web of Science ®Google Scholar
• Macario AJ, Conway de ME. Sick chaperones, cellular stress, and disease. N. Engl. J. Med.353, 1489–1501 (2005).
   PubMed Web of Science ®Google Scholar
• Meriin AB, Sherman MY. Role of molecular chaperones in neurodegenerative disorders. Int. J. Hyperthermia21, 403–419 (2005).
   PubMed Web of Science ®Google Scholar
• Bukau B, Weissman J, Horwich A. Molecular chaperones and protein quality control. Cell125, 443–451 (2006).
   PubMed Web of Science ®Google Scholar
• Ethen CM, Reilly C, Feng X, Olsen TW, Ferrington DA. The proteome of central and peripheral retina with progression of age-related macular degeneration. Invest. Ophthalmol. Vis. Sci.47, 2280–2290 (2006).
   PubMed Web of Science ®Google Scholar
• Ma Y, Hendershot LM. ER chaperone functions during normal and stress conditions. J. Chem. Neuroanat.28, 51–65 (2004).
   PubMed Web of Science ®Google Scholar
• Tuo J, Bojanowski CM, Zhou M et al. Murine ccl2/cx3cr1 deficiency results in retinal lesions mimicking human age-related macular degeneration. Invest. Ophthalmol. Vis. Sci.48, 3827–3836 (2007).
   PubMed Web of Science ®Google Scholar
• Cohen FE, Kelly JW. Therapeutic approaches to protein-misfolding diseases. Nature426, 905–909 (2003).
   PubMed Web of Science ®Google Scholar
• Chaudhuri TK, Paul S. Protein-misfolding diseases and chaperone-based therapeutic approaches. FEBS J.273, 1331–1349 (2006).
   PubMed Web of Science ®Google Scholar
• Bernier V, Lagace M, Bichet DG, Bouvier M. Pharmacological chaperones: potential treatment for conformational diseases. Trends Endocrinol. Metab.15, 222–228 (2004).
   PubMed Web of Science ®Google Scholar
• Papp E, Csermely P. Chemical chaperones: mechanisms of action and potential use. Handb. Exp. Pharmacol.405–416 (2006).
   PubMedGoogle Scholar
• Lai E, Teodoro T, Volchuk A. Endoplasmic reticulum stress: signaling the unfolded protein response. Physiology (Bethesda)22, 193–201 (2007).
   PubMed Web of Science ®Google Scholar
• Kaufman RJ. Orchestrating the unfolded protein response in health and disease. J. Clin. Invest.110, 1389–1398 (2002).
   PubMed Web of Science ®Google Scholar
• Lai JC, Lapolice DJ, Stinnett SS et al. Visual outcomes following macular translocation with 360-degree peripheral retinectomy. Arch. Ophthalmol.120, 1317–1324 (2002).
   PubMedGoogle Scholar
• Badin RA, Lythgoe MF, van der WL, Thomas DL, Gadian DG, Latchman DS. Neuroprotective effects of virally delivered HSPs in experimental stroke. J. Cereb. Blood Flow Metab.26, 371–381 (2006).
   PubMed Web of Science ®Google Scholar
• Wang Y, Loo TW, Bartlett MC, Clarke DM. Additive effect of multiple pharmacological chaperones on maturation of CFTR processing mutants. Biochem. J.406, 257–263 (2007).
   PubMedGoogle Scholar
• Shin SH, Murray GJ, Kluepfel-Stahl S et al. Screening for pharmacological chaperones in Fabry disease. Biochem. Biophys. Res. Commun.359, 168–173 (2007).
   PubMedGoogle Scholar
• Figler RA, Omote H, Nakamoto RK, Al-Shawi MK. Use of chemical chaperones in the yeast Saccharomyces cerevisiae to enhance heterologous membrane protein expression: high-yield expression and purification of human P-glycoprotein. Arch. Biochem. Biophys.376, 34–46 (2000).
   PubMedGoogle Scholar
• Skach WR. Pharmacological chaperoning: two ‘hits’ are better than one. Biochem. J.406, e1-e2 (2007).
   PubMedGoogle Scholar
• Ozcan U, Yilmaz E, Ozcan L et al. Chemical chaperones reduce er stress and restore glucose homeostasis in a mouse model of Type 2 diabetes. Science313, 1137–1140 (2006).
   PubMed Web of Science ®Google Scholar
• de Almeida SF, Picarote G, Fleming JV, Carmo-Fonseca M, Azevedo JE, de SM. Chemical Chaperones Reduce Endoplasmic Reticulum Stress and Prevent Mutant HFE Aggregate Formation. J. Biol. Chem.282, 27905–27912 (2007).
   PubMed Web of Science ®Google Scholar
• Yam GH, Gaplovska-Kysela K, Zuber C, Roth J. Sodium 4-phenylbutyrate acts as a chemical chaperone on misfolded myocilin to rescue cells from endoplasmic reticulum stress and apoptosis. Invest. Ophthalmol. Vis. Sci.48, 1683–1690 (2007).
   PubMed Web of Science ®Google Scholar
• Rodrigues CM, Sola S, Nan Z et al. Tauroursodeoxycholic acid reduces apoptosis and protects against neurological injury after acute hemorrhagic stroke in rats. Proc. Natl Acad. Sci. USA100, 6087–6092 (2003).
   PubMed Web of Science ®Google Scholar
• Boatright JH, Moring AG, McElroy C et al. Tool from ancient pharmacopoeia prevents vision loss. Mol. Vis.12, 1706–1714 (2006).
   PubMedGoogle Scholar
• Leskela TT, Markkanen PM, Pietila EM, Tuusa JT, Petaja-Repo UE. Opioid receptor pharmacological chaperones act by binding and stabilizing newly synthesized receptors in the endoplasmic reticulum. J. Biol. Chem.282, 23171–23183 (2007).
   PubMedGoogle Scholar
• Kuryatov A, Luo J, Cooper J, Lindstrom J. Nicotine acts as a pharmacological chaperone to up-regulate human α4β2 acetylcholine receptors. Mol. Pharmacol.68, 1839–1851 (2005).
   PubMed Web of Science ®Google Scholar
• Robben JH, Deen PM. Pharmacological chaperones in nephrogenic diabetes insipidus: possibilities for clinical application. BioDrugs21, 157–166 (2007).
   PubMedGoogle Scholar
• Shen JK, Dong A, Hackett SF, Bell WR, Green WR, Campochiaro PA. Oxidative damage in age-related macular degeneration. Histol. Histopathol.22, 1301–1308 (2007).
   PubMed Web of Science ®Google Scholar
• Decanini A, Nordgaard CL, Feng X, Ferrington DA, Olsen TW. Changes in select redox proteins of the retinal pigment epithelium in age-related macular degeneration. Am. J. Ophthalmol.143, 607–615 (2007).
   PubMed Web of Science ®Google Scholar
• Suzuki M, Kamei M, Itabe H et al. Oxidized phospholipids in the macula increase with age and in eyes with age-related macular degeneration. Mol. Vis.13, 772–778 (2007).
   PubMed Web of Science ®Google Scholar
• Crabb JW, Miyagi M, Gu X et al. Drusen proteome analysis: an approach to the etiology of age-related macular degeneration. Proc. Natl Acad. Sci. USA99, 14682–14687 (2002).
   PubMed Web of Science ®Google Scholar
• Iadecola C, Zhang F, Niwa K et al. SOD1 rescues cerebral endothelial dysfunction in mice overexpressing amyloid precursor protein. Nat. Neurosci.2, 157–161 (1999).
   PubMedGoogle Scholar
• Age-Related Eye Disease Study Research Group. Risk factors associated with age-related macular degeneration. A case-control study in the age-related eye disease study: age-related eye disease study report number 3. Ophthalmology107, 2224–2232 (2000).
   PubMed Web of Science ®Google Scholar
• Sparrow JR, Boulton M. RPE lipofuscin and its role in retinal pathobiology. Exp. Eye Res.80, 595–606 (2005).
   PubMed Web of Science ®Google Scholar
• Delori FC, Goger DG, Dorey CK. Age-related accumulation and spatial distribution of lipofuscin in RPE of normal subjects. Invest. Ophthalmol. Vis. Sci.42, 1855–1866 (2001).
   PubMed Web of Science ®Google Scholar
• Katz ML, Redmond TM. Effect of Rpe65 knockout on accumulation of lipofuscin fluorophores in the retinal pigment epithelium. Invest. Ophthalmol. Vis. Sci.42, 3023–3030 (2001).
   PubMed Web of Science ®Google Scholar
• Terman A, Gustafsson B, Brunk UT. Autophagy, organelles and ageing. J. Pathol.211, 134–143 (2007).
   PubMed Web of Science ®Google Scholar
• Yang LP, Wu LM, Guo XJ, Tso MO. Activation of endoplasmic reticulum stress in degenerating photoreceptors of the rd1 mouse. Invest. Ophthalmol. Vis. Sci.48, 5191–5198 (2007).
   PubMed Web of Science ®Google Scholar
• Yam GH, Bosshard N, Zuber C, Steinmann B, Roth J. Pharmacological chaperone corrects lysosomal storage in Fabry disease caused by trafficking-incompetent variants. Am. J. Physiol. Cell Physiol.290, C1076–C1082 (2006).
   Google Scholar
• Johnson LV, Leitner WP, Rivest AJ, Staples MK, Radeke MJ, Anderson DH. The Alzheimer’s A β -peptide is deposited at sites of complement activation in pathologic deposits associated with aging and age-related macular degeneration. Proc. Natl Acad. Sci. USA99(18), 11830–11835, (2002).
   PubMed Web of Science ®Google Scholar
• Luibl V, Isas JM, Kayed R, Glabe CG, Langen R, Chen J. Drusen deposits associated with aging and age-related macular degeneration contain nonfibrillar amyloid oligomers. J. Clin. Invest.116, 378–385 (2006).
   PubMed Web of Science ®Google Scholar
• Yoshida T, Ohno-Matsui K, Ichinose S et al. The potential role of amyloid β in the pathogenesis of age-related macular degeneration. J. Clin. Invest.115, 2793–2800 (2005).
   PubMed Web of Science ®Google Scholar
• Noorwez SM, Kuksa V, Imanishi Y et al. Pharmacological chaperone-mediated in vivo folding and stabilization of the P23H-opsin mutant associated with autosomal dominant retinitis pigmentosa. J. Biol. Chem.278, 14442–14450 (2003).
   PubMed Web of Science ®Google Scholar
• Marmorstein LY, Munier FL, Arsenijevic Y et al. Aberrant accumulation of EFEMP1 underlies drusen formation in Malattia Leventinese and age-related macular degeneration 8. Proc. Natl Acad. Sci. USA99, 13067–13072 (2002).
   PubMedGoogle Scholar
• Schultz DW, Weleber RG, Lawrence G et al. HEMICENTIN-1 (FIBULIN-6) and the 1q31 AMD locus in the context of complex disease: review and perspective. Ophthalmic. Genet.26, 101–105 (2005).
   PubMedGoogle Scholar
• Stone EM, Braun TA, Russell SR et al. Missense variations in the fibulin 5 gene and age-related macular degeneration. N. Engl. J. Med.351, 346–353 (2004).
   PubMed Web of Science ®Google Scholar
• Shu X, Tulloch B, Lennon A et al. Disease mechanisms in late-onset retinal macular degeneration associated with mutation in C1QTNF5. Hum. Mol. Genet.15, 1680–1689 (2006).
   PubMedGoogle Scholar
• Karan G, Yang Z, Howes K et al . Loss of ER retention and sequestration of the wild-type ELOVL4 by Stargardt disease dominant negative mutants. Mol. Vis.11, 657–664 (2005).
   PubMed Web of Science ®Google Scholar
• Illing ME, Rajan RS, Bence NF, Kopito RR. A rhodopsin mutant linked to autosomal dominant retinitis pigmentosa is prone to aggregate and interacts with the ubiquitin proteasome system. J. Biol. Chem.277, 34150–34160 (2002).
   PubMed Web of Science ®Google Scholar
• Noorwez SM, Malhotra R, McDowell JH, Smith KA, Krebs MP, Kaushal S. Retinoids assist the cellular folding of the autosomal dominant retinitis pigmentosa opsin mutant P23H. J. Biol. Chem.279, 16278–16284 (2004).
   PubMed Web of Science ®Google Scholar
• Surgucheva I, Ninkina N, Buchman VL, Grasing K, Surguchov A. Protein aggregation in retinal cells and approaches to cell protection. Cell Mol. Neurobiol.25, 1051–1066 (2005).
   PubMedGoogle Scholar
• Zheng W, Padia J, Urban DJ et al. Three classes of glucocerebrosidase inhibitors identified by quantitative high-throughput screening are chaperone leads for Gaucher disease. Proc. Natl Acad. Sci. USA104, 13192–13197 (2007).
   PubMed Web of Science ®Google Scholar
• Tropak MB, Blanchard JE, Withers SG, Brown ED, Mahuran D. High-throughput screening for human lysosomal β-N-acetyl hexosaminidase inhibitors acting as pharmacological chaperones. Chem. Biol.14, 153–164 (2007).
   PubMedGoogle Scholar
• Zhang X, Smith DL, Meriin AB et al. A potent small molecule inhibits polyglutamine aggregation in Huntington's disease neurons and suppresses neurodegeneration in vivo. Proc. Natl Acad. Sci. USA102, 892–897 (2005).
   PubMed Web of Science ®Google Scholar
• Zou Q, Bennion BJ, Daggett V, Murphy KP. The molecular mechanism of stabilization of proteins by TMAO and its ability to counteract the effects of urea. J. Am. Chem. Soc.124, 1192–1202 (2002).
   PubMed Web of Science ®Google Scholar
• Shepshelovich J, Goldstein-Magal L, Globerson A, Yen PM, Rotman-Pikielny P, Hirschberg K. Protein synthesis inhibitors and the chemical chaperone TMAO reverse endoplasmic reticulum perturbation induced by overexpression of the iodide transporter pendrin. J. Cell Sci.118, 1577–1586 (2005).
   PubMedGoogle Scholar
• Tamarappoo BK, Verkman AS. Defective aquaporin-2 trafficking in nephrogenic diabetes insipidus and correction by chemical chaperones. J. Clin. Invest.101, 2257–2267 (1998).
   PubMed Web of Science ®Google Scholar
• Sangiovanni JP, Chew EY, Clemons TE et al. The relationship of dietary carotenoid and vitamin A, E, and C intake with age-related macular degeneration in a case-control study: AREDS Report No. 22. Arch. Ophthalmol.125, 1225–1232 (2007).
   PubMed Web of Science ®Google Scholar
• Formaggio E, Cinque G, Bassi R. Functional architecture of the major light-harvesting complex from higher plants. J. Mol. Biol.314, 1157–1166 (2001).
   PubMed Web of Science ®Google Scholar
• Zhang B, Osborne NN. Oxidative-induced retinal degeneration is attenuated by epigallocatechin gallate. Brain Res.1124, 176–187 (2006).
   PubMed Web of Science ®Google Scholar
• Ehrnhoefer DE, Duennwald M, Markovic P et al. Green tea (-)-epigallocatechin-gallate modulates early events in huntingtin misfolding and reduces toxicity in Huntington's disease models. Hum. Mol. Genet.15, 2743–2751 (2006).
   PubMed Web of Science ®Google Scholar
• Woltjer RL, McMahan W, Milatovic D et al. Effects of chemical chaperones on oxidative stress and detergent-insoluble species formation following conditional expression of amyloid precursor protein carboxy-terminal fragment. Neurobiol. Dis.25, 427–437 (2007).
   PubMed Web of Science ®Google Scholar
• Lim GP, Calon F, Morihara T et al. A diet enriched with the omega-3 fatty acid docosahexaenoic acid reduces amyloid burden in an aged Alzheimer mouse model. J. Neurosci.25, 3032–3040 (2005).
   PubMed Web of Science ®Google Scholar
• Sawkar AR, Cheng WC, Beutler E, Wong CH, Balch WE, Kelly JW. Chemical chaperones increase the cellular activity of N370S β -glucosidase: a therapeutic strategy for Gaucher disease. Proc. Natl Acad. Sci. USA99, 15428–15433 (2002).
   PubMed Web of Science ®Google Scholar
• Okumiya T, Kroos MA, Vliet LV, Takeuchi H, Van der Ploeg AT, Reuser AJ. Chemical chaperones improve transport and enhance stability of mutant α-glucosidases in glycogen storage disease type II. Mol. Genet. Metab.90, 49–57 (2007).
   PubMed Web of Science ®Google Scholar
• Tveten K, Holla OL, Ranheim T, Berge KE, Leren TP, Kulseth MA. 4-Phenylbutyrate restores the functionality of a misfolded mutant low-density lipoprotein receptor. FEBS J274, 1881–1893 (2007).
   PubMedGoogle Scholar
• Yam GH, Zuber C, Roth J. A synthetic chaperone corrects the trafficking defect and disease phenotype in a protein misfolding disorder. FASEB J.19, 12–18 (2005).
   PubMed Web of Science ®Google Scholar
• Maitra R, Hamilton JW. Altered biogenesis of Delta F508-CFTR following treatment with doxorubicin. Cell Physiol. Biochem.20, 465–472 (2007).
   PubMedGoogle Scholar
• Schubert U, Anton LC, Gibbs J, Norbury CC, Yewdell JW, Bennink JR. Rapid degradation of a large fraction of newly synthesized proteins by proteasomes. Nature404, 770–774 (2000).
   PubMed Web of Science ®Google Scholar
• Petaja-Repo UE, Hogue M, Laperriere A, Walker P, Bouvier M. Export from the endoplasmic reticulum represents the limiting step in the maturation and cell surface expression of the human delta opioid receptor. J. Biol. Chem.275, 13727–13736 (2000).
   PubMed Web of Science ®Google Scholar
• Pietila EM, Tuusa JT, Apaja PM et al. Inefficient maturation of the rat luteinizing hormone receptor. A putative way to regulate receptor numbers at the cell surface. J. Biol. Chem.280, 26622–26629 (2005).
   PubMedGoogle Scholar
• Qi X, Hosoi T, Okuma Y, Kaneko M, Nomura Y. Sodium 4-phenylbutyrate protects against cerebral ischemic injury. Mol. Pharmacol.66, 899–908 (2004).
   PubMed Web of Science ®Google Scholar
• Qi X, Okuma Y, Hosoi T, Nomura Y. Edaravone protects against hypoxia/ischemia-induced endoplasmic reticulum dysfunction. J. Pharmacol. Exp. Ther.311, 388–393 (2004).
   PubMed Web of Science ®Google Scholar
• Chang HH, Asano N, Ishii S, Ichikawa Y, Fan JQ. Hydrophilic iminosugar active-site-specific chaperones increase residual glucocerebrosidase activity in fibroblasts from Gaucher patients. FEBS J.273, 4082–4092 (2006).
   PubMed Web of Science ®Google Scholar