Haploinsufficiency of RanBP2 is neuroprotective against light-elicited and age-dependent degeneration of photoreceptor neurons

Cell Death and Differentiation

Volumn 16, Issue 2, 2009, Pages 287-297

  Cho, K In ^a   Yi, H ^a   Yeh, A ^a   Tserentsoodol, N ^a   Cuadrado, L ^a   Searle, K ^a   Hao, Y ^a   Ferreira, P A ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; FATTY ACID; HYDROGEN PEROXIDE; RAN BINDING PROTEIN 2; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG;

AGE; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; AUTOPHAGY; BIOGENESIS; CONTROLLED STUDY; GENOTYPE; HAPLOIDY; HISTOLOGY; IMMUNOBLOTTING; LIGHT EXPOSURE; LIPID DIET; METABOLITE; MITOCHONDRION; MOUSE; NERVE CELL DEGENERATION; NEUROPROTECTION; NICK END LABELING; NONHUMAN; PHOTORECEPTOR; PRIORITY JOURNAL; RETINA; STRESS; WEIGHT GAIN;

AGING; ANIMALS; APOPTOSIS; AUTOPHAGY; DNA TOPOISOMERASES, TYPE II; FATTY ACIDS; HYDROGEN PEROXIDE; LIGHT; MICE; MICE, TRANSGENIC; MOLECULAR CHAPERONES; NUCLEAR PORE COMPLEX PROTEINS; PHOTORECEPTOR CELLS, VERTEBRATE; REACTIVE OXYGEN SPECIES; RETINAL DEGENERATION;

MUS;

EID: 58249095006     PISSN: 13509047     EISSN: 14765403     Source Type: Journal    
DOI: 10.1038/cdd.2008.153     Document Type: Article

References (83)

1. Pacione LR, Szego MJ, Ikeda S, Nishina PM, McInnes RR. Progress toward understanding the genetic and biochemical mechanisms of inherited photoreceptor degenerations. Annu Rev Neurosci 2003; 26: 657-700.
2. Reme CE. The dark side of light: Rhodopsin and the silent death of vision the proctor lecture. Invest Ophthalmol Vis Sci 2005; 46 2671-2682.
3. Danciger M, Lyon J, Worrill D, LaVail MM, Yang H. A strong and highly significant QTL on chromosome 6 that protects the mouse from age-related retinal degeneration. Invest Ophthalmol Vis Sci 2003; 44: 2442-2449.
4. Danciger M, Yang H, Ralston R, Liu Y, Matthes MT, Peirce J et al. Quantitative genetics of age-related retinal degeneration: A second F1 intercross between the A/J and C57BL/6 strains. Mol Vis 2007; 13: 79-85.
5. Hao W, Wenzel A, Obin MS, Chen CK, Brill E, Krasnoperova NV et al. Evidence for two apoptotic pathways in light-induced retinal degeneration. Nat Genet 2002; 32: 254-260.
6. Grimm C, Wenzel A, Williams T, Rol P, Hafezi F, Reme C. Rhodopsin-mediated blue-light damage to the rat retina: Effect of photoreversal of bleaching. Invest Ophthalmol Vis Sci 2001; 42: 497-505.
7. Wenzel A, Reme CE, Williams TP, Hafezi F, Grimm C. The Rpe65 Leu450Met variation increases retinal resistance against light-induced degeneration by slowing rhodopsin regeneration. J Neurosci 2001; 21: 53-58.
8. Woodruff ML, Wang Z, Chung HY, Redmond TM, Fain GL, Lem J. Spontaneous activity of opsin apoprotein is a cause of Leber congenital amaurosis. Nat Genet 2003; 35: 158-164.
9. Grimm C, Wenzel A, Hafezi F, Yu S, Redmond TM, Reme CE. Protection of Rpe65-deficient mice identifies rhodopsin as a mediator of light-induced retinal degeneration. Nat Genet 2000; 25: 63-66.
10. Hollyfield JG, Bonilha VL, Rayborn ME, Yang X, Shadrach KG, Lu L et al. Oxidative damage-induced inflammation initiates age-related macular degeneration. Nat Med 2008; 14: 194-198.
11. Linsenmeier RA. Effects of light and darkness on oxygen distribution and consumption in the cat retina. J Gen Physiol 1986; 88: 521-542.
12. Wright AF, Jacobson SG, Cideciyan AV, Roman AJ, Shu X, Vlachantoni D et al. Lifespan and mitochondrial control of neurodegeneration. Nat Genet 2004; 36: 1153-1158.
13. Imamura Y, Noda S, Hashizume K, Shinoda K, Yamaguchi M, Uchiyama S et al. Drusen, choroidal neovascularization, and retinal pigment epithelium dysfunction in SOD1-deficient mice: A model of age-related macular degeneration. Proc Natl Acad Sci USA 2006; 103: 11282-11287.
14. Grimm C, Wenzel A, Stanescu D, Samardzija M, Hotop S, Groszer M et al Constitutive overexpression of human erythropoietin protects the mouse retina against induced but not inherited retinal degeneration. J Neurosci 2004; 24: 5651-5658.
15. Cideciyan AV, Hood DC, Huang Y, Banin E, Li ZY, Stone EM et al. Disease sequence from mutant rhodopsin allele to rod and cone photoreceptor degeneration in man. Proc Natl Acad Sci USA 1998; 95: 7103-7108.
16. Galy A, Roux MJ, Sahel JA, Leveillard T, Giangrande A. Rhodopsin maturation defects induce photoreceptor death by apoptosis: A fly model for RhodopsinPro23His human retinitis pigmentosa. Hum Mol Genet 2005; 14: 2547-2557.
17. Naash ML, Peachey NS, Li ZY, Gryczan CC, Goto Y, Blanks J et al. Light-induced acceleration of photoreceptor degeneration in transgenic mice expressing mutant rhodopsin. Invest Ophthalmol Vis Sci 1996; 37: 775-782.
18. Organisciak DT, Darrow RM, Barsalou L, Kutty RK, Wiggert B. Susceptibility to retinal light damage in transgenic rats with rhodopsin mutations. Invest Ophthalmol Vis Sci 2003; 44: 486-492.
19. Vaughan DK, Coulibaly SF, Darrow RM, Organisciak DT. A morphometric study of light-induced damage in transgenic rat models of retinitis pigmentosa. Invest Ophthalmol Vis Sci 2003; 44: 848-855.
20. Yokoyama N, Hayashi N, Seki T, Pante N, Ohba T, Nishii K et al. A giant nucleopore protein that binds Ran/TC4. Nature 1995; 376 184-188.
21. Bernad R, van der Velde H, Fornerod M, Pickersgill H. Nup358/RanBP2 attaches to the nuclear pore complex via association with Nup88 and Nup214/CAN and plays a supporting role in CRM1-mediated nuclear protein export. Mol Cell Biol 2004; 24: 2373-2384.
22. Singh BB, Patel HH, Roepman R, Schick D, Ferreira PA. The zinc finger cluster domain of RanBP2 is a specific docking site for the nuclear export factor, exportin-1. J Biol Chem 1999; 274: 37370-37380.
23. Cho KI, Cai Y, Yi H, Yeh A, Aslanukov A, Ferreira PA. Association of the Kinesin-Binding Domain of RanBP2 to KIF5B and KIF5C Determines Mitochondria Localization and Function. Traffic 2007; 8: 1722-1735.
24. Yi H, Friedman J, Ferreira PA. The cyclophilin-like domain of Ran-binding protein-2 modulates selectively the activity of the ubiquitin-proteasome system and protein biogenesis. J Biol Chem 2007; 282: 34770-34778.
25. Ferreira PA, Hom JT, Pak WL. Retina-specifically expressed novel subtypes of bovine cyclophilin. J Biol Chem 1995; 270: 23179-23188.
26. Ferreira PA, Nakayama TA, Pak WL, Travis GH. Cyclophilin-related protein RanBP2 acts as chaperone for red/green opsin. Nature 1996; 383 637-640.
27. Lee GW, Melchior F, Matunis MJ, Mahajan R, Tian Q, Anderson P. Modification of Ran GTPase-activating protein by the small ubiquitin-related modifier SUMO-1 requires Ubc9, an E2-type ubiquitin-conjugating enzyme homologue. J Biol Chem 1998; 273 6503-6507.
28. Mahajan R, Delphin C, Guan T, Gerace L, Melchior F. A small ubiquitin-related polypeptide involved in targeting RanGAP1 to nuclear pore complex protein RanBP2. Cell 1997; 88: 97-107.
29. Mahajan R, Gerace L, Melchior F. Molecular characterization of the SUMO-1 modification of RanGAP1 and its role in nuclear envelope association. J Cell Biol 1998; 140: 259-270.
30. Matunis MJ, Coutavas E, Blobel G. A novel ubiquitin-like modification modulates the partitioning of the Ran-GTPase-activating protein RanGAP1 between the cytosol and the nuclear pore complex. J Cell Biol 1996; 135: 1457-1470.
31. Aslanukov A, Bhowmick R, Guruju M, Oswald J, Raz D, Bush RA et al. RanBP2 Modulates Cox11 and Hexokinase I Activities and Haploinsufficiency of RanBP2 Causes Deficits in Glucose Metabolism. PLoS Genet 2006; 2: E177.
32. Dawlaty MM, Malureanu L, Jeganathan KB, Kao E, Sustmann C, Tahk S et al. Resolution of sister centromeres requires RanBP2-mediated SUMOylation of topoisomerase IIalpha. Cell 2008; 133: 103-115.
33. German DC, Liang CL, Song T, Yazdani U, Xie C, Dietschy JM. Neurodegeneration in the Niemann-Pick C mouse: Glial involvement. Neuroscience 2002; 109: 437-450.
34. Karan G, Lillo C, Yang Z, Cameron DJ, Locke KG, Zhao Y et al. Lipofuscin accumulation, abnormal electrophysiology, and photoreceptor degeneration in mutant ELOVL4 transgenic mice: A model for macular degeneration. Proc Natl Acad Sci USA 2005; 102: 4164-4169.
35. Lakkaraju A, Finnemann SC, Rodriguez-Boulan E. The lipofuscin fluorophore A2E perturbs cholesterol metabolism in retinal pigment epithelial cells. Proc Natl Acad Sci USA 2007; 104: 11026-11031.
36. Patel SC, Suresh S, Kumar U, Hu CY, Cooney A, Blanchette-Mackie EJ et al. Localization of Niemann-Pick C1 protein in astrocytes: implications for neuronal degeneration in Niemann- Pick type C disease. Proc Natl Acad Sci USA 1999; 96: 1657-1662.
37. Phillips SE, Woodruff III EA, Liang P, Patten M, Broadie K. Neuronal loss of Drosophila NPC1a causes cholesterol aggregation and age-progressive neurodegeneration. J Neurosci 2008; 28: 6569-6582.
38. Schmitz G, Muller G. Structure and function of lamellar bodies, lipid-protein complexes involved in storage and secretion of cellular lipids. J Lipid Res 1991; 32: 1539-1570.
39. Anderson RE. Lipids of ocular tissues. IV. A comparison of the phospholipids from the retina of six mammalian species. Exp Eye Res 1970; 10: 339-344.
40. Andrews LD, Cohen AI. Freeze-fracture evidence for the presence of cholesterol in particle-free patches of basal disks and the plasma membrane of retinal rod outer segments of mice and frogs. J Cell Biol 1979; 81: 215-228.
41. O'Brien JS, Sampson EL. Fatty acid and fatty aldehyde composition of the major brain lipids in normal human gray matter, white matter, and myelin. J Lipid Res 1965; 6: 545-551.
42. Albert AD, Boesze-Battaglia K. The role of cholesterol in rod outer segment membranes. Prog Lipid Res 2005; 44: 99-124.
43. Fliesler SJ, Anderson RE. Chemistry and metabolism of lipids in the vertebrate retina. Prog Lipid Res 1983; 22: 79-131.
44. Anderson RE, Maude MB, Alvarez RA, Acland GM, Aguirre GD. Plasma lipid abnormalities in the miniature poodle with progressive rod-cone degeneration. Exp Eye Res 1991; 52: 349-355.
45. Anderson RE, Maude MB, Nilsson SE, Narfstrom K. Plasma lipid abnormalities in the abyssinian cat with a hereditary rod-cone degeneration. Exp Eye Res 1991; 53: 415-417.
46. Connor WE, Weleber RG, DeFrancesco C, Lin DS, Wolf DP. Sperm abnormalities in retinitis pigmentosa. Invest Ophthalmol Vis Sci 1997; 38: 2619-2628.
47. Correa-Cerro LS, Wassif CA, Kratz L, Miller GF, Munasinghe JP, Grinberg A et al. Development and characterization of a hypomorphic Smith-Lemli-Opitz syndrome mouse model and efficacy of simvastatin therapy. Hum Mol Genet 2006; 15: 839-851.
48. Maxfield FR, Tabas I. Role of cholesterol and lipid organization in disease. Nature 2005; 438: 612-621.
49. Vaughan DK, Peachey NS, Richards MJ, Buchan B, Fliesler SJ. Light-induced exacerbation of retinal degeneration in a rat model of Smith-Lemli-Opitz syndrome. Exp Eye Res 2006; 82: 496-504.
50. Bazan NG, Scott BL, Reddy TS, Pelias MZ. Decreased content of docosahexaenoate and arachidonate in plasma phospholipids in Usher's syndrome. Biochem Biophys Res Commun 1986; 141: 600-604.
51. Delton-Vandenbroucke I, Maude MB, Chen H, Aguirre GD, Acland GM, Anderson RE. Effect of diet on the fatty acid and molecular species composition of dog retina phospholipids. Lipids 1998; 33: 1187-1193.
52. Gong J, Rosner B, Rees DG, Berson EL, Weigel-DiFranco CA, Schaefer EJ. Plasma docosahexaenoic acid levels in various genetic forms of retinitis pigmentosa. Invest Ophthalmol Vis Sci 1992; 33: 2596-2602.
53. Hoffman DR, DeMar JC, Heird WC, Birch DG, Anderson RE. Impaired synthesis of DHA in patients with X-linked retinitis pigmentosa. J Lipid Res 2001; 42: 1395-1401.
54. Maude MB, Anderson EO, Anderson RE. Polyunsaturated fatty acids are lower in blood lipids of Usher's type I but not Usher's type II. Invest Ophthalmol Vis Sci 1998; 39: 2164-2166.
55. Simonelli F, Manna C, Romano N, Nunziata G, Voto O, Rinaldi E. Evaluation of fatty acids in membrane phospholipids of erythrocytes in retinitis pigmentosa patients. Ophthalmic Res 1996; 28: 93-98.
56. Richards MJ, Nagel BA, Fliesler SJ. Lipid hydroperoxide formation in the retina: Correlation with retinal degeneration and light damage in a rat model of Smith-Lemli-Opitz syndrome. Exp Eye Res 2006; 82: 538-541.
57. Artwohl M, Roden M, Waldhausl W, Freudenthaler A, Baumgartner-Parzer SM. Free fatty acids trigger apoptosis and inhibit cell cycle progression in human vascular endothelial cells. Faseb J 2004; 18: 146-148.
58. Shimabukuro M, Zhou YT, Levi M, Unger RH. Fatty acid-induced beta cell apoptosis: A link between obesity and diabetes. Proc Natl Acad Sci USA 1998; 95: 2498-2502.
59. Leung HT, Tseng-Crank J, Kim E, Mahapatra C, Shino S, Zhou Y et al DAG lipase activity is necessary for TRP channel regulation in Drosophila photoreceptors. Neuron 2008; 58: 884-896.
60. Das UN. Essential fatty acids, lipid peroxidation and apoptosis. Prostaglandins Leukot Essent Fatty Acids 1999; 61: 157-163.
61. Johnson RA, Hamilton JA, Worgall TS, Deckelbaum RJ. Free fatty acids modulate intermembrane trafficking of cholesterol by increasing lipid mobilities: Novel 13C NMR analyses of free cholesterol partitioning. Biochemistry 2003; 42: 1637-1645.
62. Aikens J, Dix TA. Perhydroxyl radical (HOO.) initiated lipid peroxidation. The role of fatty acid hydroperoxides. J Biol Chem 1991; 266: 15091-15098.
63. Spiteller G. Are changes of the cell membrane structure causally involved in the aging process? Ann N Y Acad Sci 2002; 959: 30-44.
64. Chandra J, Samali A, Orrenius S. Triggering and modulation of apoptosis by oxidative stress. Free Radic Biol Med 2000; 29: 323-333.
65. Kim JS, He L, Lemasters JJ. Mitochondrial permeability transition: A common pathway to necrosis and apoptosis. Biochem Biophys Res Commun 2003; 304: 463-470.
66. Greenberg ME, Li XM, Gugiu BG, Gu X, Qin J, Salomon RG et al. The lipid whisker model of the structure of oxidized cell membranes. J Biol Chem 2008; 283: 2385-2396.
67. Organisciak DT, Darrow RM, Jiang YL, Blanks JC. Retinal light damage in rats with altered levels of rod outer segment docosahexaenoate. Invest Ophthalmol Vis Sci 1996; 37: 2243-2257.
68. Bloomquist BT, Shortridge RD, Schneuwly S, Perdew M, Montell C, Steller H et al. Isolation of a putative phospholipase C gene of Drosophila, norpA, and its role in phototransduction. Cell 1988; 54: 723-733.
69. Ferreira PA, Pak WL. Bovine phospholipase C highly homologous to the norpA protein of Drosophila is expressed specifically in cones. J Biol Chem 1994; 269: 3129-3131.
70. Ferreira PA, Shortridge RD, Pak WL. Distinctive subtypes of bovine phospholipase C that have preferential expression in the retina and high homology to the norpA gene product of Drosophila. Proc Natl Acad Sci USA 1993; 90: 6042-6046.
71. Ghalayini A, Anderson RE. Phosphatidylinositol 4,5-bisphosphate: light-mediated breakdown in the vertebrate retina. Biochem Biophys Res Commun 1984; 124: 503-506.
72. Ghalayini AJ, Tarver AP, Mackin WM, Koutz CA, Anderson RE. Identification and immunolocalization of phospholipase C in bovine rod outer segments. J Neurochem 1991; 57: 1405-1412.
73. Choe HG, Ghalayini AJ, Anderson RE. Phosphoinositide metabolism in frog rod outer segments. Exp Eye Res 1990; 51: 167-176.
74. Hayashi F, Amakawa T. Light-mediated breakdown of phosphatidylinositol-4,5-bisphosphate in isolated rod outer segments of frog photoreceptor. Biochem Biophys Res Commun 1985; 128: 954-959.
75. Hayashi F, Sumi M, Amakawa T. Phosphatidylinositol stimulates phosphorylation of protein components I and II in rod outer segments of frog photoreceptors. Biochem Biophys Res Commun 1987; 148: 54-60.
76. Millar FA, Fisher SC, Muir CA, Edwards E, Hawthorne JN. Polyphosphoinositide hydrolysis in response to light stimulation of rat and chick retina and retinal rod outer segments. Biochim Biophys Acta 1988; 970: 205-211.
77. Gehm BD, Mc Connell DG. Phosphatidylinositol-4,5-bisphosphate phospholipase C in bovine rod outer segments. Biochemistry 1990; 29: 5447-5452.
78. Gehm BD, Pinke RM, Laquerre S, Chafouleas JG, Schultz DA, Pepperl DJ et al. Activation of bovine rod outer segment phosphatidylinositol-4,5-bisphosphate phospholipase C by calmodulin antagonists does not depend on calmodulin. Biochemistry 1991; 30: 11302-11306.
79. Peng YW, Rhee SG, Yu WP, Ho YK, Schoen T, Chader GJ et al. Identification of components of a phosphoinositide signaling pathway in retinal rod outer segments. Proc Natl Acad Sci USA 1997; 94: 1995-2000.
80. Neilson DE, Eiben RM, Waniewski S, Hoppel CL, Varnes ME, Bangert BA et al. Autosomal dominant acute necrotizing encephalopathy. Neurology 2003; 61: 226-230.
81. Neilson DE, Feiler HS, Wilhelmsen KC, Lynn A, Eiben RM, Kerr DS et al Autosomal dominant acute necrotizing encephalopathy maps to 2q12.1-2q13. Ann Neurol 2004; 55: 291-294.
82. Krebber H, Bastians H, Hoheisel J, Lichter P, Ponstingl H, Joos S. Localization of the gene encoding the Ran-binding protein RanBP2 to human chromosome 2q11-q13 by fluorescence in situ hybridization. Genomics 1997; 43: 247-248.
83. Ferreira PA. Characterization of RanBP2-associated molecular components in neuroretina. Methods enzymol 2000; 315: 455-468.