Glutathione metabolism and its contribution to antiapoptotic properties of α-crystallins in the retina

Studies on Retinal and Choroidal Disorders

Volumn , Issue , 2012, Pages 181-201

  Sreekumar, Parameswaran G ^a   Hinton, David R ^b   Kannan, Ram ^b  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b DOHENY EYE INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84906797354     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-1-61779-606-7_9     Document Type: Chapter

References (171)

1. Marí M, Morales A, Colell A, García-Ruiz C, Fernández-Checa JC (2009) Mitochondrial glutathione, a key survival antioxidant. Antioxid Redox Signal 11:2685-2700.
2. Ballatori N, Krance SM, Notenboom S, Shi S, Tieu K, Hammond CL (2009) Glutathione dysregulation and the etiology and progression of human diseases. Biol Chem 390:191-214.
3. Moreno MC, Campanelli J, Sande P, Sánez DA, Keller Sarmiento MI, Rosenstein RE (2004) Retinal oxidative stress induced by high intraocular pressure. Free Radic Biol Med 37:803-812.
4. Pau H, Graf P, Sies H (1982) Glutathione content of the lens in various forms of cataract. Graefes Arch Clin Exp Ophthalmol 219:140-142.
5. Pau H, Graf P, Sies H (1990) Glutathione levels in human lens: regional distribution in different forms of cataract. Exp Eye Res 50:17-20.
6. Sternberg P Jr, Davidson PC, Jones DP, Hagen TM, Reed RL, Drews-Botsch C (1993) Protection of retinal pigment epithelium from oxidative injury by glutathione and precursors. Invest Ophthalmol Vis Sci 34:3661-3668.
7. Horwitz J (1992) Alpha-crystallin can function as a molecular chaperone. Proc Natl Acad Sci U S A 89:10449-10453.
8. Klemenz R, Fröhli E, Steiger RH, Schäfer R, Aoyama A (1991) Alpha B-crystallin is a small heat shock protein. Proc Natl Acad Sci U S A 88:3652-3656.
9. Kamradt MC, Chen F, Cryns VL (2001) The small heat shock protein alpha B-crystallin negatively regulates cytochrome c- and caspase-8-dependent activation of caspase-3 by inhibiting its autoproteolytic maturation. J Biol Chem 276:16059-16063.
10. Kamradt MC, Chen F, Sam S, Cryns VL (2002) The small heat shock protein alpha B-crystallin negatively regulates apoptosis during myogenic differentiation by inhibiting caspase-3 activation. J Biol Chem 277:38731-38736.
11. Yaung J, Jin M, Barron E, Spee C, Wawrousek EF, Kannan R, Hinton DR (2007) alpha-Crystallin distribution in retinal pigment epithelium and effect of gene knockouts on sensitivity to oxidative stress. Mol Vis 13:566-577.
12. Sun Y, MacRae TH (2005) Small heat shock proteins: molecular structure and chaperone function. Cell Mol Life Sci 62:2460-2476.
13. Parameswaran S, Spee C, Ryan SJ, Kannan R, Hinton DR (2009) Decreased cellular glutathione (GSH) and increased GSH efflux in (alpha)-crystallin knockout retina. Invest Ophthalmol Vis Sci 50:E-Abstract 1831.
14. De S, Rabin DM, Salero E, Lederman PL, Temple S, Stern JH (2007) Human retinal pigment epithelium cell changes and expression of alphaB-crystallin: a biomarker for retinal pigment epithelium cell change in age-related macular degeneration. Arch Ophthalmol 125:641-645.
15. Masilamoni JG, Vignesh S, Kirubagaran R, Jesudason EP, Jayakumar R (2005) The neuroprotective efficacy of alpha-crystallin against acute inflammation in mice. Brain Res Bull 67:235-241.
16. Ousman SS, Tomooka BH, van Noort JM, Wawrousek EF, O'Connor KC, Hafler DA, Sobel RA, Robinson WH, Steinman L (2007) Protective and therapeutic role for alphaB-crystallin in autoimmune demyelination. Nature 448:474-479.
17. Cooper AJ, Kristal BS (1997) Multiple roles of glutathione in the central nervous system. Biol Chem 378(793-802):20.
18. Jones DP (2008) Radical-free biology of oxidative stress. Am J Physiol Cell Physiol 295:C849-C868.
19. Townsend DM, Tew KD, Tapiero H (2003) The importance of glutathione in human disease. Biomed Pharmacother 57:145-155.
20. Meister A, Anderson ME (1983) Glutathione. Annu Rev Biochem 52:711-760.
21. Dalton TP, Chen Y, Schneider SN, Nebert DW, Shertzer HG (2004) Genetically altered mice to evaluate glutathione homeostasis in health and disease. Free Radic Biol Med 37:1511-1526.
22. Lu SC (2000) Regulation of glutathione synthesis. Curr Top Cell Regul 36:95-116.
23. Dalton TP, Dieter MZ, Yang Y, Shertzer HG, Nebert DW (2000) Knockout of the mouse glutamate cysteine ligase catalytic subunit (Gclc) gene: embryonic lethal when homozygous, and proposed model for moderate glutathione deficiency when heterozygous. Biochem Biophys Res Commun 279:324-329.
24. McConnachie LA, Mohar I, Hudson FN, Ware CB, Ladiges WC, Fernandez C, Chatterton-Kirchmeier S, White CC, Pierce RH, Kavanagh TJ (2007) Glutamate cysteine ligase modifier subunit deficiency and gender as determinants of acetaminophen-induced hepatotoxicity in mice. Toxicol Sci 99:628-636.
25. Njalsson R, Norgren S, Larsson A, Huang CS, Anderson ME, Luo JL (2001) Cooperative binding of gamma-glutamyl substrate to human glutathione synthetase. Biochem Biophys Res Commun 289:80-84.
26. Jaiswal AK (2004) Nrf2 signaling in coordinated activation of antioxidant gene expression. Free Radic Biol Med 36:1199-1207.
27. Jin M, Yaung J, Kannan R, He S, Ryan SJ, Hinton DR (2005) Hepatocyte growth factor protects RPE cells from apoptosis induced by glutathione depletion. Invest Ophthalmol Vis Sci 46:4311-4319.
28. Kannan R, Ouyang B, Wawrousek E, Kaplowitz N, Andley UP (2001) Regulation of GSH in alphaA-expressing human lens epithelial cell lines and in alphaA knockout mouse lenses. Invest Ophthalmol Vis Sci 42:409-416.
29. Lee JM, Johnson JA (2004) An important role of Nrf2-ARE pathway in the cellular defense mechanism. J Biochem Mol Biol 37:139-143.
30. Pallardó FV, Markovic J, García JL, Viña J (2009) Role of nuclear glutathione as a key regulator of cell proliferation. Mol Aspects Med 30:77-85.
31. Hwang C, Sinskey AJ, Lodish HF (1992) Oxidized redox state of glutathione in the endoplasmic reticulum. Science 257:1496-1502.
32. Griffith OW, Meister A (1985) Origin and turnover of mitochondrial glutathione. Proc Natl Acad Sci U S A 82(4668-4672):21.
33. Kaplowitz N, Aw TY, Ookhtens M (1985) The regulation of hepatic glutathione. Annu Rev Pharmacol Toxicol 25:715-744.
34. Ikeda Y, Taniguchi N (2005) Gene expression of gamma-glutamyltranspeptidase. Methods Enzymol 401:408-425.
35. Ballatori N, Hammond CL, Cunningham JB, Krance SM, Marchan R (2005) Molecular mechanisms of reduced glutathione transport: role of the MRP/CFTR/ABCC and OATP/ SLC21A families of membrane proteins. Toxicol Appl Pharmacol 204:238-255.
36. Briz O, Romero MR, Martinez-Becerra P, Macias RI, Perez MJ, Jimenez F, San Martin FG, Marin JJ (2006) OATP8/1B3-mediated cotransport of bile acids and glutathione: an export pathway for organic anions from hepatocytes? J Biol Chem 281:30326-30335.
37. Li L, Lee TK, Meier PJ, Ballatori N (1998) Identification of glutathione as a driving force and leukotriene C4 as a substrate for oatp1, the hepatic sinusoidal organic solute transporter. J Biol Chem 273:16184-16191.
38. Hammond CL, Marchan R, Krance SM, Ballatori N (2007) Glutathione export during apoptosis requires functional multidrug resistance-associated proteins. J Biol Chem 282:14337-14347.
39. Minich T, Riemer J, Schulz JB, Wielinga P, Wijnholds J, Dringen R (2006) The multidrug resistance protein 1 (Mrp1), but not Mrp5, mediates export of glutathione and glutathione disulfide from brain astrocytes. J Neurochem 97:373-384.
40. Kannan R, Sreekumar PG, Ryan SJ, Hinton DR (2009) Role of multidrug resistant protein (MRP1) in oxidant stress-induced glutathione efflux in RPE. Invest Ophthalmol Vis Sci 50:E-Abstract 1830.
41. Chang TS, Cho CS, Park S, Yu S, Kang SW, Rhee SG (2004) Peroxiredoxin III, a mitochondrion- specific peroxidase, regulates apoptotic signaling by mitochondria. J Biol Chem 279:41975-41984.
42. Reed DJ (1990) Glutathione: toxicological implications. Annu Rev Pharmacol Toxicol 30:603-631.
43. Yap LP, Garcia JV, Han D, Cadenas E (2009) The energy-redox axis in aging and age-related neurodegeneration. Adv Drug Deliv Rev 61:1283-1298.
44. Fernández-Checa JC, Kaplowitz N, García-Ruiz C, Colell A (1998) Mitochondrial glutathione:importance and transport. Semin Liver Dis 18:389-401.
45. Fernández-Checa JC, Kaplowitz N, García-Ruiz C, Colell A, Miranda M, Marí M, Ardite E, Morales A (1997) GSH transport in mitochondria: defense against TNF-induced oxidative stress and alcohol-induced defect. Am J Physiol 273(1 Pt 1):G7-G17.
46. Palmieri F (1994) Mitochondrial carrier proteins. FEBS Lett 346:48-54.
47. Han D, Canali R, Rettori D, Kaplowitz N (2003) Effect of glutathione depletion on sites and topology of superoxide and hydrogen peroxide production in mitochondria. Mol Pharmacol 64:1136-1144.
48. Lash LH, Visarius TM, Sall JM, Qian W, Tokarz JJ (1998) Cellular and subcellular heterogeneity of glutathione metabolism and transport in rat kidney cells. Toxicology 130:1-15.
49. Mårtensson J, Jain A, Meister A (1990) Glutathione is required for intestinal function. Proc Natl Acad Sci U S A 87:1715-1719.
50. Cazanave S, Berson A, Haouzi D, Vadrot N, Fau D, Grodet A, Lettéron P, Feldmann G, El-Benna J, Fromenty B, Robin MA, Pessayre D (2007) High hepatic glutathione stores alleviate Fas-induced apoptosis in mice. J Hepatol 46:858-868.
51. Friesen C, Kiess Y, Debatin KM (2004) A critical role of glutathione in determining apoptosis sensitivity and resistance in leukemia cells. Cell Death Differ 11(Suppl 1):S73-S85.
52. Armstrong JS, Steinauer KK, Hornung B, Irish JM, Lecane P, Birrell GW, Peehl DM, Knox SJ (2002) Role of glutathione depletion and reactive oxygen species generation in apoptotic signaling in a human B lymphoma cell line. Cell Death Differ 9:252-263.
53. Will Y, Kaetzel RS, Brown MK, Fraley TS, Reed DJ (2002) In vivo reversal of glutathione deficiency and susceptibility to in vivo dexamethasone-induced apoptosis by N-acetylcysteine and L-2-oxothiazolidine-4-carboxylic acid, but not ascorbic acid, in thymocytes from gammaglutamyltranspeptidase- deficient knockout mice. Arch Biochem Biophys 397:399-406.
54. Garcia-Ruiz C, Fernandez-Checa JC (2006) Mitochondrial glutathione: hepatocellular survival- death switch. J Gastroenterol Hepatol 21(Suppl 3):S3-S6.
55. Lash LH (2006) Mitochondrial glutathione transport: physiological, pathological and toxicological implications. Chem Biol Interact 163:54-67.
56. Marchetti P, Decaudin D, Macho A, Zamzami N, Hirsch T, Susin SA, Kroemer G (1997) Redox regulation of apoptosis: impact of thiol oxidation status on mitochondrial function. Eur J Immunol 27:289-296.
57. Colell A, García-Ruiz C, Miranda M, Ardite E, Marí M, Morales A, Corrales F, Kaplowitz N, Fernández-Checa JC (1998) Selective glutathione depletion of mitochondria by ethanol sensitizes hepatocytes to tumor necrosis factor. Gastroenterology 115:1541-1551.
58. Colell A, Coll O, García-Ruiz C, París R, Tiribelli C, Kaplowitz N, Fernández-Checa JC (2001) Tauroursodeoxycholic acid protects hepatocytes from ethanol-fed rats against tumor necrosis factor-induced cell death by replenishing mitochondrial glutathione. Hepatology 34:964-971.
59. Fernández-Checa JC, García-Ruiz C, Ookhtens M, Kaplowitz N (1991) Impaired uptake of glutathione by hepatic mitochondria from chronic ethanol-fed rats. Tracer kinetic studies in vitro and in vivo and susceptibility to oxidant stress. J Clin Invest 87:397-405.
60. Franco R, Schoneveld OJ, Pappa A, Panayiotidis MI (2007) The central role of glutathione in the pathophysiology of human diseases. Arch Physiol Biochem 113:234-258.
61. Ayer A, Tan SX, Grant CM, Meyer AJ, Dawes IW, Perrone GG (2010) The critical role of glutathione in maintenance of the mitochondrial genome. Free Radic Biol Med 49:1956-1968.
62. Will O, Mahler HC, Arrigo AP, Epe B (1999) Influence of glutathione levels and heat-shock on the steady-state levels of oxidative DNA base modifications in mammalian cells. Carcinogenesis 20:333-337.
63. Pow DV, Crook DK (1995) Immunocytochemical evidence for the presence of high levels of reduced glutathione in radial glial cells and horizontal cells in the rabbit retina. Neurosci Lett 193:25-28.
64. Carter-Dawson L, Shen FF, Harwerth RS, Crawford ML, Smith EL 3rd, Whitetree A (2004) Glutathione content is altered in Müller cells of monkey eyes with experimental glaucoma. Neurosci Lett 364:7-10.
65. Huster D, Hjelle OP, Haug FM, Nagelhus EA, Reichelt W, Ottersen OP (1998) Subcellular compartmentation of glutathione and glutathione precursors. A high resolution immunogold analysis of the outer retina of guinea pig. Anat Embryol (Berl) 198:277-287.
66. Marc RE, Cameron D (2001) A molecular phenotype atlas of the zebrafish retina. J Neurocytol 30:593-654.
67. Schütte M, Werner P (1998) Redistribution of glutathione in the ischemic rat retina. Neurosci Lett 246:53-56.
68. Winkler BS (2008) An hypothesis to account for the renewal of outer segments in rod and cone photoreceptor cells: renewal as a surrogate antioxidant. Invest Ophthalmol Vis Sci 49:3259-3261.
69. Bertram KM, Baglole CJ, Phipps RP, Libby RT (2009) Molecular regulation of cigarette smoke induced-oxidative stress in human retinal pigment epithelial cells: implications for age-related macular degeneration. Am J Physiol Cell Physiol 297:C1200-C1210.
70. Roh YJ, Moon C, Kim SY, Park MH, Bae YC, Chun MH, Moon JI (2007) Glutathione depletion induces differential apoptosis in cells of mouse retina, in vivo. Neurosci Lett 417:266-270.
71. Nordgaard CL, Karunadharma PP, Feng X, Olsen TW, Ferrington DA (2008) Mitochondrial proteomics of the retinal pigment epithelium at progressive stages of age-related macular degeneration. Invest Ophthalmol Vis Sci 49:2848-2855.
72. Liang FQ, Godley BF (2003) Oxidative stress-induced mitochondrial DNA damage in human retinal pigment epithelial cells: a possible mechanism for RPE aging and age-related macular degeneration. Exp Eye Res 76:397-403.
73. Wang AL, Lukas TJ, Yuan M, Neufeld AH (2008) Increased mitochondrial DNA damage and down-regulation of DNA repair enzymes in aged rodent retinal pigment epithelium and choroid. Mol Vis 14:644-651.
74. He Y, Ge J, Tombran-Tink J (2008) Mitochondrial defects and dysfunction in calcium regulation in glaucomatous trabecular meshwork cells. Invest Ophthalmol Vis Sci 49:4912-4922.
75. Bhat SP (2003) Crystallins, genes and cataract. Prog Drug Res 60:205-262.
76. Sreekumar PG, Kannan R, Hinton DR (2009) There are three major families of crystallins:misnaming of alphaB crystallin. Acta Physiol (Oxf) 195:503.
77. Horwitz J (2003) Alpha-crystallin. Exp Eye Res 76:145-153.
78. Andley UP (2007) Crystallins in the eye: function and pathology. Prog Retin Eye Res 26:78-98.
79. de Jong WW, Caspers GJ, Leunissen JA (1998) Genealogy of the alpha-crystallin-small heatshock protein superfamily. Int J Biol Macromol 22:151-162.
80. Ingolia TD, Craig EA (1982) Four small Drosophila heat shock proteins are related to each other and to mammalian alpha-crystallin. Proc Natl Acad Sci U S A 79:2360-2364.
81. Bhat SP, Nagineni CN (1989) alpha B subunit of lens-specific protein alpha-crystallin is present in other ocular and non-ocular tissues. Biochem Biophys Res Commun 158:319-325.
82. Dubin RA, Wawrousek EF, Piatigorsky J (1989) Expression of the murine alpha B-crystallin gene is not restricted to the lens. Mol Cell Biol 9:1083-1091.
83. Kato K, Shinohara H, Kurobe N, Goto S, Inaguma Y, Ohshima K (1991) Immunoreactive alpha A crystallin in rat non-lenticular tissues detected with a sensitive immunoassay method. Biochim Biophys Acta 1080:173-180.
84. Sax CM, Piatigorsky J (1994) Expression of the alpha-crystallin/small heat-shock protein/ molecular chaperone genes in the lens and other tissues. Adv Enzymol Relat Areas Mol Biol 69:155-201.
85. Srinivasan AN, Nagineni CN, Bhat SP (1992) alpha A-crystallin is expressed in non-ocular tissues. J Biol Chem 267:23337-23341.
86. Xi J, Farjo R, Yoshida S, Kern TS, Swaroop A, Andley UP (2003) A comprehensive analysis of the expression of crystallins in mouse retina. Mol Vis 9(410-419):28.
87. van Rijk AF, Bloemendal H (2000) Alpha-B-crystallin in neuropathology. Ophthalmologica 214:7-12.
88. Brady JP, Garland DL, Green DE, Tamm ER, Giblin FJ, Wawrousek EF (2001) AlphaBcrystallin in lens development and muscle integrity: a gene knockout approach. Invest Ophthalmol Vis Sci 42:2924-2934.
89. Arai H, Atomi Y (1997) Chaperone activity of alpha B-crystallin suppresses tubulin aggregation through complex formation. Cell Struct Funct 22:539-544.
90. Longoni S, James P, Chiesi M (1990) Cardiac alpha-crystallin I. Isolation and identification. I. Isolation and identification. Mol Cell Biochem 99:113-120.
91. Gangalum RK, Schibler MJ, Bhat SP (2004) Small heat shock protein alphaB-crystallin is part of cell cycle-dependent Golgi reorganization. J Biol Chem 279:43374-43377.
92. Nakata K, Crabb JW, Hollyfield JG (2005) Crystallin distribution in Bruch's membranechoroid complex from AMD and age-matched donor eyes. Exp Eye Res 80:821-826.
93. Yuan X, Gu X, Crabb JS, Yue X, Shadrach K, Hollyfield JG, Crabb JW (2010) Quantitative proteomics: comparison of the macular Bruch's membrane/choroid complex from agerelated macular degeneration and normal eyes. Mol Cell Proteomics 9:1031-1046.
94. Hauck SM, Schoeffmann S, Deeg CA, Gloeckner CJ, Swiatek-de Lange M, Ueffing M (2005) Proteomic analysis of the porcine interphotoreceptor matrix. Proteomics 5:3623-3636.
95. Steiner-Champliaud MF, Sahel J, Hicks D (2006) Retinoschisin forms a mutli-molecular matrix and cytoplasmic proteins: interactions with beta2 laminin and alphaB-crystallin. Mol Vis 12:892-901.
96. Arrigo AP, Simon S (2010) Expression and functions of heat shock proteins in the normal and pathological mammalian eye. Curr Mol Med 10:776-793.
97. Litt M, Kramer P, LaMorticella DM, Murphey W, Lovrien EW, Weleber RG (1998) Autosomal dominant congenital cataract associated with a missense mutation in the human alpha crystallin gene CRYAA. Hum Mol Genet 7:471-474.
98. Koteiche HA, Mchaourab HS (2006) Mechanism of a hereditary cataract phenotype. Mutations in alphaA-crystallin activate substrate binding. J Biol Chem 281, 14273-14279.
99. Kumar LV, Ramakrishna T, Rao CM (1999) Structural and functional consequences of the mutation of a conserved arginine residue in alphaA and alphaB crystallins. J Biol Chem 274:24137-24141.
100. Brown Z, Ponce A, Lampi K, Hancock L, Takemoto L (2007) Differential binding of mutant (R116C) and wildtype alphaA crystallin to actin. Curr Eye Res 32:1051-1054.
101. Graw J (2009) Genetics of crystallins: cataract and beyond. Exp Eye Res 88:173-189.
102. Reilich P, Schoser B, Schramm N, Krause S, Schessl J, Kress W, Müller-Höcker J, Walter MC, Lochmuller H (2010) The p.G154S mutation of the alpha-B crystallin gene (CRYAB) causes late-onset distal myopathy. Neuromuscul Disord 20:255-259.
103. Maloyan A, Sanbe A, Osinska H, Westfall M, Robinson D, Imahashi K, Murphy E, Robbins J (2005) Mitochondrial dysfunction and apoptosis underlie the pathogenic 24 process in alpha-B-crystallin desmin-related cardiomyopathy. Circulation 112:3451-3461.
104. Pilotto A, Marziliano N, Pasotti M, Grasso M, Costante AM, Arbustini E (2006) alphaBcrystallin mutation in dilated cardiomyopathies: low prevalence in a consecutive series of 200 unrelated probands. Biochem Biophys Res Commun 346:1115-1117.
105. Chen Q, Ma J, Yan M, Mothobi ME, Liu Y, Zheng F (2009) A novel mutation in CRYAB associated with autosomal dominant congenital nuclear cataract in a Chinese family. Mol Vis 15:1359-1365.
106. Brady JP, Garland D, Duglas-Tabor Y, Robison WG Jr, Groome A, Wawrousek EF (1997) Targeted disruption of the mouse alpha A-crystallin gene induces cataract and cytoplasmic inclusion bodies containing the small heat shock protein alpha B-crystallin. Proc Natl Acad Sci U S A 94:884-889.
107. Boyle DL, Takemoto L, Brady JP, Wawrousek EF (2003) Morphological characterization of the alpha A- and alpha B-crystallin double knockout mouse lens. BMC Ophthalmol 3:3.
108. Morozov V, Wawrousek EF (2006) Caspase-dependent secondary lens fiber cell disintegration in alphaA-/alphaB-crystallin double-knockout mice. Development 133:813-821.
109. Arrigo AP, Simon S, Gibert B, Kretz-Remy C, Nivon M, Czekalla A, Guillet D, Moulin M, Diaz-Latoud C, Vicart P (2007) Hsp27 (HspB1) and alphaB-crystallin (HspB5) as therapeutic targets. FEBS Lett 581:3665-3674.
110. Hogan JM, Pitteri SJ, McLuckey SA (2003) Phosphorylation site identification via ion trap tandem mass spectrometry of whole protein and peptide ions: bovine alpha-crystallin A chain. Anal Chem 75:6509-6916.
111. Schaefer H, Marcus K, Sickmann A, Herrmann M, Klose J, Meyer HE (2003) Identification of phosphorylation and acetylation sites in alphaA-crystallin of the eye lens (mus musculus) after two-dimensional gel electrophoresis. Anal Bioanal Chem 376:966-972.
112. van den IJssel PR, Overkamp P, Knauf U, Gaestel M, de Jong WW (1994) Alpha A-crystallin confers cellular thermoresistance. FEBS Lett 355:54-56.
113. Mehlen P, Schulze-Osthoff K, Arrigo AP (1996) Small stress proteins as novel regulators of apoptosis. Heat shock protein 27 blocks Fas/APO-1- and staurosporine-induced cell death. J Biol Chem 271:16510-16514.
114. Merck KB, Groenen PJ, Voorter CE, de Haard-Hoekman WA, Horwitz J, Bloemendal H, de Jong WW (1993) Structural and functional similarities of bovine alpha-crystallin and mouse small heat-shock protein. A family of chaperones. J Biol Chem 268:1046-1052.
115. Nicholl ID, Quinlan RA (1994) Chaperone activity of alpha-crystallins modulates intermediate filament assembly. EMBO J 13(945-953):25.
116. Stege GJ, Renkawek K, Overkamp PS, Verschuure P, van Rijk AF, Reijnen-Aalbers A, Boelens WC, Bosman GJ, de Jong WW (1999) The molecular chaperone alphaB-27 crystallin enhances amyloid beta neurotoxicity. Biochem Biophys Res Commun 262:152-156.
117. Narberhaus F (2002) Alpha-crystallin-type heat shock proteins: socializing minichaperones in the context of a multichaperone network. Microbiol Mol Biol Rev 66:64-93.
118. Sreekumar PG, Kannan R, Kitamura M, Spee C, Barron E, Ryan SJ, Hinton DR (2010) a Bcrystallin is apically secreted within exosomes by polarized human retinal pigment epithelium and provides neuroprotection to adjacent cells. PLoS One 5:e12578.
119. Yaung J, Kannan R, Wawrousek EF, Spee C, Sreekumar PG, Hinton DR (2008) Exacerbation of retinal degeneration in the absence of alpha crystallins in an in vivo model of chemically induced hypoxia. Exp Eye Res 86:355-365.
120. Kase S, He S, Sonoda S, Kitamura M, Spee C, Wawrousek E, Ryan SJ, Kannan R, Hinton DR (2010) alphaB-crystallin regulation of angiogenesis by modulation of VEGF. Blood 115:3398-3406.
121. Kerr BA, Byzova TV (2010) alphaB-crystallin: a novel VEGF chaperone. Blood 115:3181-3183.
122. Mehlen P, Kretz-Remy C, Préville X, Arrigo AP (1996) Human hsp27, Drosophila hsp27 and human alphaB-crystallin expression-mediated increase in glutathione is essential for the protective activity of these proteins against TNFalpha-induced cell death. EMBO J 15:2695-2706.
123. Cherian M, Smith JB, Jiang XY, Abraham EC (1997) Influence of protein-glutathione mixed disulfide on the chaperone-like function of alpha-crystallin. J Biol Chem 272:29099-29103.
124. Pal J, Bera S, Ghosh SK (1998) The effect of glutathione upon chaperone activity of alphacrystallin is probably mediated through target modulation. Ophthalmic Res 30:271-279.
125. Cherian M, Abraham EC (1995) Diabetes affects a -crystallin chaperone function. Biochem Biophys Res Commun 212:184-189.
126. Kumar PA, Suryanarayana P, Reddy PY, Reddy GB (2005) Modulation of alpha-crystallin chaperone activity in diabetic rat lens by curcumin. Mol Vis 11:561-568.
127. Thampi P, Zarina S, Abraham EC (2002) alpha-Crystallin chaperone function in diabetic rat and human lenses. Mol Cell Biochem 229:113-118.
128. Baek SH, Min JN, Park EM, Han MY, Lee YS, Lee YJ, Park YM (2000) Role of small heat shock protein HSP25 in radioresistance and glutathione-redox cycle. J Cell Physiol 183:100-107.
129. Yan LJ, Christians ES, Liu L, Xiao X, Sohal RS, Benjamin IJ (2002) Mouse heat shock transcription factor 1 deficiency alters cardiac redox homeostasis and increases mitochondrial oxidative damage. EMBO J 21:5164-5172.
130. Rajasekaran NS, Connell P, Christians ES, Yan LJ, Taylor RP, Orosz A, Zhang XQ, Stevenson TJ, Peshock RM, Leopold JA, Barry WH, Loscalzo J, Odelberg SJ, Benjamin IJ (2007) Human alpha B-crystallin mutation causes oxido-reductive stress and protein aggregation cardiomyopathy in mice. Cell 130:427-439.
131. Bhattacharyya J, Padmanabha Udupa EG, Wang J, Sharma KK (2006) Mini-alphaBcrystallin:a functional element of alphaB-crystallin with chaperone-like activity. Biochemistry 45:3069-3076.
132. Kannan R, Sreekumar PG, Kannan N, Ryan SJ, Kompella UB, Sharma K, Hinton DR (2010) Alpha crystallin derived peptide chaperone protects human RPE cells from oxidative injury. Invest Ophthalmol Vis Sci 51:E-Abstract 1441.
133. Santhoshkumar P, Sharma KK (2004) Inhibition of amyloid fibrillogenesis and toxicity by a peptide chaperone. Mol Cell Biochem 267:147-155.
134. Gu M, Owen AD, Toffa SE, Cooper JM, Dexter DT, Jenner P, Marsden CD, Schapira AH (1998) Mitochondrial function, GSH and iron in neurodegeneration and Lewy body diseases. J Neurol Sci 158:24-29.
135. Liu H, Wang H, Shenvi S, Hagen TM, Liu RM (2004) Glutathione metabolism during aging and in Alzheimer disease. Ann N Y Acad Sci 1019:346-349.
136. Gironi M, Bianchi A, Russo A, Alberoni M, Ceresa L, Angelini A, Cursano C, Mariani E, Nemni R, Kullmann C, Farina E, Martinelli Boneschi F (2011) Oxidative imbalance in different neurodegenerative diseases with memory impairment. Neurodegener Dis 8(3):129-37.
137. Sian J, Dexter DT, Lees AJ, Daniel S, Jenner P, Marsden CD (1994) Glutathione-related enzymes in brain in Parkinson's disease. Ann Neurol 36:356-361.
138. Baillet A, Chanteperdrix V, Trocmé C, Casez P, Garrel C, Besson G (2010) The role of oxidative stress in amyotrophic lateral sclerosis and Parkinson's disease. Neurochem Res 35:1530-1537.
139. Jiang H, Talaska AE, Schacht J, Sha SH (2007) Oxidative imbalance in the aging inner ear. Neurobiol Aging 28(1605-1612):22.
140. Estrela JM, Ortega A, Obrador E (2006) Glutathione in cancer biology and therapy. Crit Rev Clin Lab Sci 43:143-181.
141. Ortega A, Carretero J, Obrador E, Estrela JM (2008) Tumoricidal activity of endotheliumderived NO and the survival of metastatic cells with high GSH and Bcl-2 levels. Nitric Oxide 19:107-114.
142. Leopold JA, Loscalzo J (2005) Oxidative enzymopathies and vascular disease. Arterioscler Thromb Vasc Biol 25:1332-1340.
143. Li S, Zheng MQ, Rozanski GJ (2009) Glutathione homeostasis in ventricular myocytes from rat hearts with chronic myocardial infarction. Exp Physiol 94:815-824.
144. Kobayashi T, Watanabe Y, Saito Y, Fujioka D, Nakamura T, Obata JE, Kitta Y, Yano T, Kawabata K, Watanabe K, Mishina H, Ito S, Kugiyama K (2010) Mice lacking the glutamate- cysteine ligase modifier subunit are susceptible to myocardial ischaemia-reperfusion injury. Cardiovasc Res 85:785-795.
145. Malhotra D, Thimmulappa R, Navas-Acien A, Sandford A, Elliott M, Singh A, Chen L, Zhuang X, Hogg J, Pare P, Tuder RM, Biswal S (2008) Decline in NRF2-regulated antioxidants in chronic obstructive pulmonary disease lungs due to loss of its positive regulator, DJ-1. Am J Respir Crit Care Med 178:592-604.
146. van der Toorn M, Smit-de Vries MP, Slebos DJ, de Bruin HG, Abello N, van Oosterhout AJ, Bischoff R, Kauffman HF (2007) Cigarette smoke irreversibly modifies glutathione in airway epithelial cells. Am J Physiol Lung Cell Mol Physiol 293:L1156-L1162.
147. Roum JH, Buhl R, McElvaney NG, Borok Z, Crystal RG (1993) Systemic deficiency of glutathione in cystic fibrosis. J Appl Physiol 75:2419-2424.
148. Hassan MQ, Hadi RA, Al-Rawi ZS, Padron VA, Stohs SJ (2001) The glutathione defense system in the pathogenesis of rheumatoid arthritis. J Appl Toxicol 21:69-73.
149. Staro A, Makosa G, Koter-Michalak M (2010 Nov 17) Oxidative stress in erythrocytes from patients with rheumatoid arthritis. Rheumatol Int. [Epub ahead of print].
150. Sido B, Hack V, Hochlehnert A, Lipps H, Herfarth C, Dröge W (1998) Impairment of intestinal glutathione synthesis in patients with inflammatory bowel disease. Gut 42:485-492.
151. Biagioni C, Favilli F, Catarzi S, Marcucci T, Fazi M, Tonelli F, Vincenzini MT, Iantomasi T (2006) Redox state and O2*- production in neutrophils of Crohn's disease patients. Exp Biol Med (Maywood) 231:186-195.
152. Zargari M, Allameh A, Sanati MH, Tiraihi T, Lavasani S, Emadyan O (2007) Relationship between the clinical scoring and demyelination in central nervous system with total antioxidant capacity of plasma during experimental autoimmune encephalomyelitis development in mice. Neurosci Lett 412:24-28.
153. Choi IY, Lee SP, Denney D, Lynch S (2011) Lower levels of glutathione in the brains of secondary progressive multiple sclerosis patients measured by 1H magnetic resonance chemical shift imaging at 3 T. Mult Scler 17(3):289-96.
154. Kökçam I, Nazirolu M (1999) Antioxidants and lipid peroxidation status in the blood of patients with psoriasis. Clin Chim Acta 289:23-31.
155. Herzenberg LA, De Rosa SC, Dubs JG, Roederer M, Anderson MT, Ela SW, Deresinski SC, Herzenberg LA (1997) Glutathione deficiency is associated with impaired survival in HIV disease. Proc Natl Acad Sci U S A 94:1967-1972.
156. Sharma A, Kharb S, Chugh SN, Kakkar R, Singh GP (2000) Effect of glycemic control and vitamin E supplementation on total glutathione content in non-insulin-dependent diabetes mellitus. Ann Nutr Metab 44:11-13.
157. Maher P, Hanneken A (2005) Flavonoids protect retinal ganglion cells from oxidative stressinduced death. Invest Ophthalmol Vis Sci 46:4796-4803.
158. Coral K, Raman R, Rathi S, Rajesh M, Sulochana KN, Angayarkanni N, Paul PG, Ramakrishnan S (2006) Plasma homocysteine and total thiol content in patients with exudative age-related macular degeneration. Eye (Lond) 20:203-207.
159. Javadzadeh A, Ghorbanihaghjo A, Bahreini E, Rashtchizadeh N, Argani H, Alizadeh S (2010) Plasma oxidized LDL and thiol-containing molecules in patients with exudative agerelated macular degeneration. Mol Vis 16:2578-2584.
160. Iwaki T, Kume-Iwaki A, Liem RK, Goldman JE (1989) Alpha B-crystallin is expressed in non-lenticular tissues and accumulates in Alexander's disease brain. Cell 57:71-78.
161. Renkawek K, de Jong WW, Merck KB, Frenken CW, van Workum FP, Bosman GJ (1992) alpha B-crystallin is present in reactive glia in Creutzfeldt-Jakob disease. Acta Neuropathol 83:324-327.
162. Rekas A, Adda CG, Andrew Aquilina J, Barnham KJ, Sunde M, Galatis D, Williamson NA, Masters CL, Anders RF, Robinson CV, Cappai R, Carver JA (2004) Interaction of 26 the molecular chaperone alphaB-crystallin with alpha-synuclein: effects on amyloid fibril formation and chaperone activity. J Mol Biol 340:1167-1183.
163. Renkawek K, Voorter CE, Bosman GJ, van Workum FP, de Jong WW (1994) Expression of alpha B-crystallin in Alzheimer's disease. Acta Neuropathol 87:155-160.
164. Waudby CA, Knowles TP, Devlin GL, Skepper JN, Ecroyd H, Carver JA, Welland ME, Christodoulou J, Dobson CM, Meehan S (2010) The interaction of alphaB-crystallin with mature alpha-synuclein amyloid fibrils inhibits their elongation. Biophys J 98:843-851.
165. Vicart P, Caron A, Guicheney P, Li Z, Prévost MC, Faure A, Chateau D, Chapon F, Tomé F, Dupret JM, Paulin D, Fardeau M (1998) A missense mutation in the alphaB-crystallin chaperone gene causes a desmin-related myopathy. Nat Genet 20:92-95.
166. Sinclair C, Mirakhur M, Kirk J, Farrell M, McQuaid S (2005) Up-regulation of osteopontin and alphaBeta-crystallin in the normal-appearing white matter of multiple sclerosis: an immunohistochemical study utilizing tissue microarrays. Neuropathol Appl Neurobiol 31:292-303.
167. Rao NA, Saraswathy S, Wu GS, Katselis GS, Wawrousek EF, Bhat S (2008) Elevated retinaspecific expression of the small heat shock protein, alphaA-crystallin, is associated with photoreceptor protection in experimental uveitis. Invest Ophthalmol Vis Sci 49:1161-1171.
168. Kase S, Parikh JG, Rao NA (2009) Expression of alpha-crystallin in retinoblastoma. Arch Ophthalmol 127:187-192.
169. Jones SE, Jomary C, Grist J, Thomas MR, Neal MJ (1998) Expression of alphaB-crystallin in a mouse model of inherited retinal degeneration. Neuroreport 9:4161-4165.
170. Mackay DS, Andley UP, Shiels A (2003) Cell death triggered by a novel mutation in the alphaA-crystallin gene underlies autosomal dominant cataract linked to chromosome 21q. Eur J Hum Genet 11:784-793.
171. Liu M, Ke T, Wang Z, Yang Q, Chang W, Jiang F, Tang Z, Li H, Ren X, Wang X, Wang T, Li Q, Yang J, Liu J, Wang QK (2006) Identification of a CRYAB mutation associated with autosomal dominant posterior polar cataract in a Chinese family. Invest Ophthalmol Vis Sci 47:3461-3466.