Looking chloride channels straight in the eye: Bestrophins, lipofuscinosis, and retinal degeneration

Physiology

Volumn 20, Issue 5, 2005, Pages 292-302

  Hartzell, Criss ^a   Qu, Zhiqiang ^a   Putzier, Ilva ^a   Artinian, Liana ^a   Chien, Li Ting ^a   Cui, Yuanyuan ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 26844540936     PISSN: 15489213     EISSN: None     Source Type: Journal    
DOI: 10.1152/physiol.00021.2005     Document Type: Review

References (96)

1. Al Awqati Q. Proton-translocating ATPases. Annu Rev Cell Biol 2: 179-199, 1986.
2. 2+ in murine neuroblastoma cells studied with fluorescent probes. J Gen Physiol 112: 145-160, 1998.
3. Anderson DH, Talaga KC, Rivest AJ, Barron E, Hageman GS, and Johnson LV. Characterization of beta amyloid assemblies in drusen: the deposits associated with aging and age-related macular degeneration. Exp Eye Res 78: 243-256, 2004.
4. Bakall B, Marmorstein LY, Hoppe G, Peachey NS, Wadelius C, and Marmorstein AD. Expression and localization of bestrophin during normal mouse development. Invest Ophthalmol Vis Sci 44: 3622-3628, 2003.
5. Besharse JC and Defoe D. The role of retinal pigment epithelium in photoreceptor membrane turnover. In: The Retinal Pigment Epithelium, edited by Marmor MF and Wolfensberger TJ. New York: Oxford University Press, 1998, p. 152-172.
6. -transport mechanisms in bovine pigment epithelium that can modulate subretinal space volume and composition. J Physiol 475: 401-417, 1994.
7. Bok D. New insights and new approaches toward the study of age-related macular degeneration. Proc Natl Acad Sci USA 99: 14619-14621, 2002.
8. - channel disruption. EMBO J 20: 1289-1299, 2001.
9. Botchkin LM and Matthews G. Chloride current activated by swelling in retinal pigment epithelium cells. Am J Physiol Cell Physiol 265: C1037-C1045, 1993.
10. Caldwell GM, Kakuk LE, Griesinger IB, Simpson SA, Nowak NJ, Small KW, Maumenee IH, Rosenfeld PJ, Sieving PA, Shows TB, and Ayyagari R. Bestrophin gene mutations in patients with Best vitelliform macular dystrophy. Genomics 58: 98-101, 1999.
11. Clapham DE. The list of potential volume-sensitive chloride currents continues to swell (and shrink). J Gen Physiol 111: 623-624, 1998.
12. Cooper JD. Progress towards understanding the neurobiology of Batten disease or neuronal ceroid lipofuscinosis. Curr Opin Neurol 16: 121-128, 2003.
13. Crabb JW, Miyagi M, Gu X, Shadrach K, West KA, Sakaguchi H, Kamei M, Hasan A, Yan L, Rayborn ME, Salomon RG, and Hollyfield JG. Drusen proteome analysis: an approach to the etiology of age-related macular degeneration. Proc Natl Acad Sci USA 99: 14682-14687, 2002.
14. Davis-Kaplan SR, Askwith CC, Bengtzen AC, Radisky D, and Kaplan J. Chloride is an allosteric effector of copper assembly for the yeast multicopper oxidase Fet3p: an unexpected role for intracellular chloride channels. Proc Natl Acad Sci USA 95: 13641-13645, 1998.
15. Dawson G and Cho S. Batten's disease: clues to neuronal protein catabolism in lysosomes. J Neurosci Res 60: 133-140, 2000.
16. Dmitriev AV, Govardovskii VI, Schwahn HN, and Steinberg RH. Light-induced changes of extracellular ions and volume in the isolated chick retina-pigment epithelium preparation. Vis Neurosci 16: 1157-1167, 1999.
17. Edwards AO, Ritter R III, Abel KJ, Manning A, Panhuysen C, and Farrer LA. Complement factor H polymorphism and age-related macular degeneration. Science 308: 421-424, 2005.
18. Eldred GE. Lipofuscin fluorophore inhibits lysosomal protein degradation and may cause early stages of macular degeneration. Gerontology 41: 15-28, 1995.
19. Eldred GE and Lasky MR. Retinal age pigments generated by self-assembling lysosomotropic detergents. Nature 361: 724-726, 1993.
20. Faundez V and Hartzell HC. Intracellular chloride channels: determinants of function in the endosomal pathway. Science STKE 2004: re8, 2004.
21. Finnemann SC, Leung LW, and Rodriguez-Boulan E. The lipofuscin component A2E selectively inhibits phagolysosomal degradation of photoreceptor phospholipid by the retinal pigment epithelium. Proc Natl Acad Sci USA 99: 3842-3847, 2002.
22. Fischmeister R and Hartzell C. Volume-sensitivity of the bestrophin family of chloride channels. J Physiol 562: 477-491, 2004.
23. - conductance in toad retinal pigment epithelium. Am J Physiol Cell Physiol 262: C374-C383, 1992.
24. Gallemore RP, Hughes BA, and Miller SS. Retinal pigment epithelial transport mechanisms and their contributions to the electroretinogram. Prog Retinal Eye Res 16: 509-566, 1997.
25. Gass JDM. Stereoscopic Atlas of Macular Diseases: Diagnosis and Treatment. St. Louis, MO: C. V. Mosby, 1987.
26. Gibson A, Lewis AP, Affleck K, Meldrum E, and Thompson N. hCLCA1 and mCLCA3 are secreted non-integral membrane proteins and therefore are not ion channels. J Biol Chem 280: 27205-27212, 2005.
27. Goebel HH and Wisniewski KE. Current state of clinical and morphological features in human NCL. Brain Pathol 14: 61-69, 2004.
28. Guharay F and Sachs F. Stretch-activated single ion channel currents in tissue-cultured embryonic chick skeletal muscle. J Physiol 352: 685-701, 1984.
29. Hageman GS, Luthert PJ, Victor Chong NH, Johnson LV, Anderson DH, and Mullins RF. An integrated hypothesis that considers drusen as biomarkers of immune-mediated processes at the RPE-Bruch's membrane interface in aging and age-related macular degeneration. Prog Retinal Eye Res 20: 705-732, 2001.
30. Hageman GS, Anderson DH, Johnson LV, Hancox LS, Taiber AJ, Hardisty LI, Hageman JL, Stockman HA, Borchardt JD, Gehrs KM, Smith RJH, Silvestri G, Russell SR, Klaver CCW, Barbazetto I, Chang S, Yannuzzi LA, Barile GR, Merriam JC, Smith RT, Olsh AK, Bergeron J, Zernant J, Merriam JE, Gold B, Dean M, and Allikmets R. A common haplotype in the complement regulatory gene factor H (HF1/CFH) predisposes individuals to age-related macular degeneration. Proc Natl Acad Sci USA 102: 7227-7232, 2005.
31. Haines JL, Hauser MA, Schmidt S, Scott WK, Olson LM, Gallins P, Spencer KL, Kwan SY, Noureddine M, Gilbert JR, Schnetz-Boutaud N, Agarwal A, Postel EA, and Pericak-Vance MA. Complement factor H variant increases the risk of age-related macular degeneration. Science 308: 419-421, 2005.
32. Hartzell HC, Putzier I, and Arreola J. Calcium-activated chloride channels. Annu Rev Physiol 67: 715-758, 2005.
33. Hartzell HC and Qu Z. Chloride currents in acutely isolated Xenopus retinal pigment epithelial cells. J Physiol 549: 453-469, 2003.
34. Huang B and Karwoski CJ. Light-evoked expansion of subretinal space volume in the retina of the frog. J Neurosci 12: 4243-4252, 1992.
35. Jentsch TJ, Stein V, Weinreich F, and Zdebik AA. Molecular structure and physiological function of chloride channels. Physiol Rev 82: 503-568, 2002.
36. Karlin A and Akabas MH. Substituted-cysteine accessibility method. Methods Enyzmol 293: 123-145, 1998.
37. Kaspar D, Planells-Cases R, Fuhrmann JC, Scheel O, Zeitz O, Ruether K, Poet M, Steinfield R, Schweizer M, Kornak U, and Jentsch JT. Loss of the chloride channel ClC-7 leads to lysosomal storage disease and neurodegeneration. EMBO J 24: 1879-1091, 2005.
38. Kennedy BG. Volume regulation in cultured cells derived from human retinal pigment epithelium. Am J Physiol Cell Physiol 266: C676-C683, 1994.
39. Kornak U, Kasper D, Bosl MR, Kaiser E, Schweizer M, Schulz A, Friedrich W, Delling G, and Jentsch TJ. Loss of the ClC-7 chloride channel leads to the osteoporosis in mice and men. Cell 104: 205-215, 2001.
40. Kramer F, Stohr H, and Weber BH. Cloning and characterization of the murine Vmd2 RFP-TM gene family. Cytogenetics Genome Res 105: 107-114, 2004.
41. Linsenmeier RA and Steinberg RH. Origin and sensitivity of the light peak in the intact cat eye. J Physiol 331: 653-673, 1982.
42. + "leak." J Biol Chem 266: 24540-24548, 1991.
43. Ma D, Zerangue N, Raab-Graham K, Fried SR, Jan YN, and Jan LY. Diverse trafficking patterns due to multiple traffic motifs in G protein-activated inwardly rectifying potassium channels from brain and heart. Neuron 33: 715-729, 2002.
44. Mannerstrom M, Maenpaa H, Toimela T, Salminen L, and Tahti H. The phagocytosis of rod outer segments is inhibited by selected drugs in retinal pigment epithelial cell cultures. Pharmacol Toxicol 88: 27-33, 2001.
45. Marmorstein AD, Marmorstein LY, Sakaguchi H, and Hollyfield JG. Spectral profiling of autofluorescence associated with lipofuscin, Bruch's membrane, and sub-RPE deposits in normal and AMD eyes. Invest Ophthalmol Vis Sci 43: 2435-2441, 2002.
46. Marmorstein AD, Mormorstein LY, Rayborn M, Wang X, Hollyfield JG, and Petrukhin K. Bestrophin, the product of the Best vitelliform macular dystrophy gene (VMD2), localizes to the basolateral membrane of the retinal pigment epithelium. Proc Natl Acad Sci USA 97: 12758-12763, 2000.
47. Marmorstein AD, Stanton JB, Yocom J, Bakall B, Schiavone MT, Wadelius C, Marmorstein LY, and Peachey NS. A model of best vitelliform macular dystrophy in rats. Invest Ophthalmol Vis Sci 45: 3733-3739, 2004.
48. Marquardt A, Stohr H, Passmore LA, Kramer F, Rivera A, and Weber BH. Mutations in a novel gene, VMD2, encoding a protein of unknown properties cause juvenile-onset vitelliform macular dystrophy (Best's disease). Hum Mol Genet 7: 1517-1525, 1998.
49. Matsumoto B, Defoe DM, and Besharse JC. Membrane turnover in rod photoreceptors: ensheathment and phagocytosis of outer segment distal tips by pseudopodia of the retinal pigment epithelium. Proc R Soc Lond B Biol Sci 230: 339-354, 1987.
50. Mellman I. The importance of being acid: the role of acidification in intracellular membrane traffic. J Exp Biol 172: 39-45, 1992.
51. 2+ signaling and calcium binding chaperones of the endoplasmic reticulum. Cell Calcium 32: 269-278, 2002.
52. Mitchison HM, Lim MJ, and Cooper JD. Selectivity and types of cell death in the neuronal ceroid lipofuscinoses. Brain Pathol 14: 86-96, 2004.
53. Musarella MA. Molecular genetics of macular degeneration. Doc Ophthalmol 102: 165-177, 2001.
54. Nguyen-Legros J and Hicks D. Renewal of photoreceptor outer segments and their phagocytosis by the retinal pigment epithelium. Int Rev Cytol 196: 245-313, 2000.
55. Nilius B, Eggermont J, Voets T, Buyse G, Manolopoulos V, and Droogmans G. Properties of volume-regulated anion channels in mammalian cells. Prog Biophys Mol Biol 68: 69-119, 1997.
56. O'Gorman S, Flaherty WA, Fishman GA, and Berson EL. Histopathologic findings in Best's vitelliform macular dystrophy. Arch Ophthalmol 106: 1261-1268, 1988.
57. Penfold PL, Madigan MC, Gillies MC, and Provis JM. Immunological and aetiological aspects of macular degeneration. Prog Retinal Eye Res 20: 385-414, 2001.
58. Petrukhin K, Koisti MJ, Bakall B, Li W, Xie G, Marknell T, Sandgren O, Forsman K, Holmgren G, Andreasson S, Vujic M, Bergen AAB, McGarty-Dugan V, Figueroa D, Austin CP, Metzker ML, Caskey CT, and Wadelius C. Identification of the gene responsible for Best macular dystrophy. Nat Genet 19: 241-247, 1998.
59. Picollo A and Pusch M. Chloride/proton antiporter activity of mammalian ClC proteins ClC-4 and ClC-5. Nature 436: 420-423, 2005.
60. 2+ uptake by the smooth muscle sarcoplasmic reticulum. Biophys J 75: 1759-1766, 1998.
61. 2+-activated chloride channels go molecular. J Gen Physiol 123: 323-325, 2004.
62. - channel: identification of a residue important in anion binding and conduction. J Gen Physiol 123: 327-340, 2004.
63. Qu Z, Wei RW, Mann W, and Hartzell HC. Two bestrophins cloned from Xenopus laevis oocytes express Ca-activated Cl currents. J Biol Chem 278: 49563-49572, 2003.
64. Qu Z and Hartzell HC. Determinants of anion permeation in the second transmembrane domain of the mouse bestrophin-2 chloride channel. J Gen Physiol 124: 371-382, 2004.
65. Quinn RH, Quong JN, and Miller SS. Adrenergic receptor activated ion transport in human fetal retinal pigment epithelium. Invest Ophthalmol Vis Sci 42: 255-264, 2001.
66. Renner AB, Tillack H, Kraus H, Kramer F, Mohr N, Weber BH, Foerster MH, and Kellner U. Late onset is common in best macular dystrophy associated with VMD2 gene mutations. Ophthalmology 112: 586-592, 2005.
67. in and KCl-coupled fluid absorption in bovine RPE. Invest Ophthalmol Vis Sci 42: 1921-1929, 2001.
68. Scheel O, Zdebik A, Lourdel S, and Jentsch TJ. Voltage-dependent electrogenic chloride/proteon excahnge by endosomal ClC proteins. Nature 436: 424-427, 2005.
69. Schutt F, Ueberle B, Schnolzer M, Holz FG, and Kopitz J. Proteome analysis of lipofuscin in human retinal pigment epithelial cells. FEBS Lett 528: 217-221, 2002.
70. Shamsi FA and Boulton M. Inhibition of RPE lysosomal and antioxidant activity by the age pigment lipofuscin. Invest Ophthalmol Vis Sci 42: 3041-3046, 2001.
71. Shroyer NF, Lewis RA, and Lupski JR. Analysis of the ABCR (ABCA4) gene in 4-aminoquinoline retinopathy: is retinal toxicity by chloroquine and hydroxychloroquine related to Stargardt disease? Am J Ophthalmol 131: 761-766, 2001.
72. Sparrow JR and Cai B. Blue light-induced apoptosis of A2E-containing RPE: involvement of caspase-3 and protection by Bcl-2. Invest Ophthalmol Vis Sci 42: 1356-1362, 2001.
73. Stobrawa SM, Breiderhoff T, Takamori S, Engel D, Schweizer M, Zdebik AA, Bosl MR, Ruether K, Jahn H, Draguhn A, Jahn R, and Jentsch TJ. Disruption of ClC-3, a chloride channel expressed on synaptic vesicles, leads to a loss of the hippocampus. Neuron 29: 185-196, 2001.
74. Stohr H, Marquardt A, Nanda I, Schmid M, and Weber BH. Three novel human VMD2-like genes are members of the evolutionary highly conserved RFP-TM family. Eur J Hum Genet 10: 281-284, 2002.
75. Stone EM, Sheffield VC, and Hageman GS. Molecular genetics of age-related macular degeneration. Hum Mol Genet 10: 2285-2292, 2001.
76. Strauss O. The retinal pigment epithelium in visual function. Physiol Rev 85: 845-881, 2005.
77. Sun H, Tsunenari T, Yau KW, and Nathans J. The vitelliform macular dystrophy protein defines a new family of chloride channels. Proc Natl Acad Sci USA 99: 4008-4013, 2002.
78. Sundelin SP and Terman A. Different effects of chloroquine and hydroxychloroquine on lysosomal function in cultured retinal pigment epithelial cells. APMIS 110: 481-489, 2002.
79. Toimela T, Salminen L, and Tahti H. Effects of tamoxifen, toremifene and chloroquine on the lysosomal enzymes in cultured retinal pigment epithelial cells. Pharmacol Toxicol 83: 246-251, 1998.
80. Tsuboi S and Pederson JE. Volume transport across the isolated retinal pigment epithelium of cynomolgus monkey eyes. Invest Ophthalmol Vis Sci 29: 1652-1655, 1988.
81. Tsukamoto Y. Pigment epithelial ensheathment and phagocytosis of rod tips in the retina of Rana catesbeiana. J Morphol 188: 303-313, 1986.
82. Tsunenari T, Sun H, Williams J, Cahill H, Smallwood P, Yau KW, and Nathans J. Structure-function analysis of the bestrophin family of anion channels. J Biol Chem 278: 41114-41125, 2003.
83. 2+ homeostasis and neuronal death. J Cell Mol Med 7: 351-361, 2003.
84. Wajima R, Chater SB, Katsumi O, Mehta MC, and Hirose T. Correlating visual acuity and electrooculogram recordings in Best's Disease. Ophthalmologe 207: 174-181, 1993.
85. Warskulat U, Zhang F, and Haussinger D. Modulation of phagocytosis by anisoosmolarity and betaine in rat liver macrophages (Kupffer cells) and RAW 264.7 mouse macrophages. FEBS Lett 391: 287-292, 1996.
86. Weingeist TA, Kobrin JL, and Watzke RC. Histopathology of Best's macular dystrophy. Arch Ophthalmol 100: 1108-1114, 1982.
87. Weleber RG. Fast and slow oscillations of the electro-oculogram in Best's macular dystrophy and retinitis pigmentosa. Arch Ophthalmol 107: 530-537, 1989.
88. Weng TX, Godley BF, Jin GF, Mangini NJ, Kennedy BG, Yu ASL, and Wills NK. Oxidant and antioxidant modulation of chloride channels expressed in human retinal pigment epithelium. Am J Physiol Cell Physiol 283: C839-C849, 2002.
89. Wettstein M, Peters-Regehr T, Kubitz R, Fischer R, Holneicher C, Monnighoff I, and Haussinger D. Release of osmolytes induced by phagocytosis and hormones in rat liver. Am J Physiol Gastrointest Liver Physiol 278: G227-G233, 2000.
90. White K, Marquardt A, and Weber BHF. VMD2 mutations in vitelliform macular dystrophy (Best disease) and other maculopathies. Hum Mutat 15: 301-308, 2000.
91. White SH and Wimley WC. Membrane protein folding and stability: physical principles. Annu Rev Biophys Biomol Struct 28: 319-365, 1999.
92. Wills NK, Weng T, Mo L, Hellmich HL, Yu A, Wang T, Buchheit S, and Godley BF. Chloride channel expression in cultured human fetal RPE cells: response to oxidative stress. Invest Ophthalmol Vis Sci 41: 4247-4255, 2000.
93. Wu J, Peachey NS, and Marmorstein AD. Light-evoked responses of the mouse retinal pigment epithelium. J Neurophysiol 91: 1134-1142, 2004.
94. Yardley J, Leroy BP, Hart-Holden N, Lafaut BA, Loeys B, Messiaen LM, Perveen R, Reddy MA, Bhattacharya SS, Traboulsi E, Baralle D, De Laey JJ, Puech B, Kestelyn P, Moore AT, Manson FD, and Black GC. Mutations of VMD2 splicing regulators cause nanophthalmos and autosomal dominant vitreoretinochoroidopathy (ADVIRC). Invest Ophthalmol Vis Sci 45: 3683-3689, 2004.
95. Yoshikawa M, Uchida S, Ezaki J, Rai T, Hayama A, Kobayashi K, Kida Y, Noda M, Koike M, Uchiyama Y, Marumo F, Kominami E, and Sasaki S. CLC-3 deficiency leads to phenotypes similar to human neuronal ceroid lipofuscinosis. Genes Cells 7: 597-605, 2002.
96. Young RW. Pathophysiology of age-related macular degeneration. Surv Ophthalmol 31: 291-306, 1987.