Elimination of the ρ1 Subunit Abolishes GABAC Receptor Expression and Alters Visual Processing in the Mouse Retina

Journal of Neuroscience

Volumn 22, Issue 10, 2002, Pages 4163-4174

  McCall, Maureen A ^a,b   Lukasiewicz, Peter D ^c   Gregg, Ronald G ^a,b   Peachey, Neal S ^d,e,f  

^a UNIVERSITY OF LOUISVILLE   (United States)

^b University of Louisville School of Medicine   (United States)

^c WASHINGTON UNIVERSITY   (United States)

^d LOUIS STOKES CLEVELAND VA MEDICAL CENTER   (United States)

^e LERNER RESEARCH INSTITUTE   (United States)

^f CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Chloride channel; Electroretinogram; Inhibition; Ionotropic receptor; IPSC; Knock out; Rod bipolar cell; TPMPA; Whole cell patch clamp

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID C RECEPTOR; RECEPTOR SUBUNIT; 4 AMINOBUTYRIC ACID RECEPTOR; 4 AMINOBUTYRIC ACID RECEPTOR BLOCKING AGENT; GABA-C RECEPTOR; PROTEIN SUBUNIT;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EMBRYO; GENE TARGETING; KNOCKOUT MOUSE; MOUSE; NERVE ENDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RETINA; RETINA AMACRINE CELL; RETINA BIPOLAR GANGLION CELL; SIGNAL TRANSDUCTION; VISUAL NERVOUS SYSTEM; ANIMAL; C57BL MOUSE; CYTOLOGY; DARK ADAPTATION; DRUG EFFECT; ELECTRORETINOGRAPHY; GENE DELETION; GENETIC RECOMBINATION; GENETICS; IN VITRO STUDY; METABOLISM; METHODOLOGY; MOUSE MUTANT; NERVE CELL; NERVE CELL INHIBITION; PATCH CLAMP; PHOTOSTIMULATION; PHYSIOLOGY; RETINA ROD; STEM CELL; STIMULATION; SYNAPTOSOME; VISION;

ANIMALS; DARK ADAPTATION; ELECTRORETINOGRAPHY; GABA ANTAGONISTS; GAMMA-AMINOBUTYRIC ACID; GENE TARGETING; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEURAL INHIBITION; NEURONS; PATCH-CLAMP TECHNIQUES; PHOTIC STIMULATION; PRESYNAPTIC TERMINALS; PROTEIN SUBUNITS; RECEPTORS, GABA; RECOMBINATION, GENETIC; RETINA; RODS (RETINA); SEQUENCE DELETION; STEM CELLS; STIMULATION, CHEMICAL; VISION;

EID: 0037095773     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.22-10-04163.2002     Document Type: Article

References (95)

1. Arnarsson A, Eysteinsson T (1997) The role of GABA in modulating the Xenopus electroretinogram. Vis Neurosci 14:1143-1152.
2. Barthel L, Raymond PA (1990) Improved method for obtaining 3-micron cryosections for immunocytochemistry. J Histochem Cytochem 38:1383-1388.
3. Bloomfield SA, Xin D (2000) Surround inhibition of mammalian AII amacrine cells is generated in the proximal retina. J Physiol (Lond) 523:771-783.
4. Boue-Grabot E, Roudbaraki M, Bascles L, Tramu G, Bloch B, Garret M (1998) Expression of GABA receptor rho subunits in rat brain. J Neurochem 70:899-907.
5. Cook PB, McReynolds JS (1998a) Lateral inhibition in the inner retina is important for spatial tuning of ganglion cells. Nat Neurosci 1:714-719.
6. Cook PB, McReynolds JS (1998b) Modulation of sustained and transient lateral inhibitory mechanisms in the mudpuppy retina during light adaptation. J Neurophysiol 79:197-204.
7. Cook PB, Lukasiewicz PD, McReynolds JS (2000) GABA(C) receptors control adaptive changes in a glycinergic inhibitory pathway in salamander retina. J Neurosci 20:806-812.
8. Cutting GR, Curristin S, Zoghbi H, O'Hara B, Seldin MF, Uhl GR. (1992) Identification of a putative gamma-aminobutyric acid (GABA) receptor subunit rho2 cDNA and colocalization of the genes encoding rho2 (GABRR2) and rho1 (GABRR1) to human chromosome 6q14-q21 and mouse chromosome 4. Genomics 12:801-806.
9. Dick E, Miller RF (1985) Extracellular K+ activity changes related to electroretinogram components. I. Amphibian (I-type) retinas. J Gen Physiol 85:885-909.
10. Dong CJ, Werblin FS (1998) Temporal contrast enhancement via GABAC feedback at bipolar terminals in the tiger salamander retina. J Neurophysiol 79:2171-2180.
11. Du JL, Yang XL (2000) Subcellular localization and complements of GABA(A) and GABA(C) receptors on bullfrog retinal bipolar cells. J Neurophysiol 84:666-676.
12. Enz R (2001) GABA(C) receptors: a molecular view. J Biol Chem 382:1111-1122.
13. Enz R, Cutting GR (1999a) GABAC receptor rho subunits are heterogeneously expressed in the human CNS and form. Eur J Neurosci 11:41-50.
14. Enz R, Cutting GR (1999b) Identification of 70 amino acids important for GABA(C) receptor rho1 subunit assembly. Brain Res 846:177-185.
15. Enz R, Brandstatter JH, Hartveit E, Wassle H, Bormann J (1995) Expression of GABA receptor p1 and p2 subunits in the retina and brain of the rat. Eur J Neurosci 7:1495-1501.
16. Enz R, Brandstatter JH, Wassle H, Bormann J (1996) Immunocytochemical localization of the GABAc receptor rho subunits in the mammalian retina. J Neurosci 16:4479-4490.
17. Euler T, Masland RH (2000) Light-evoked responses of bipolar cells in a mammalian retina. J Neurophysiol 83:1817-1829.
18. Euler T, Wassle H (1995) Immunocytochemical identification of cone bipolar cells in the rat retina. J Comp Neurol 361:461-478.
19. Euler T, Wassle H (1998) Different contributions of GABAA and GABAc receptors to rod and cone bipolar cells in a rat retinal slice preparation. J Neurophysiol 79:1384-1395.
20. Feigenspan A, Bormann J (1998) GABA-gated Cl- channels in the rat retina. Prog Retin Eye Res 17:99-126.
21. Feigenspan A, Wassle H, Bormann J (1993) Pharmacology of GABA receptor Cl- channels in rat retinal bipolar cells. Nature 361:159-162.
22. Fletcher EL, Wassle H (1999) Indoleamine-accumulating amacrine cells are presynaptic to rod bipolar cells through GABA(C) receptors. J Comp Neurol 413:155-167.
23. Fletcher EL, Koulen P, Wassle H (1998) GABAA and GABAC receptors on mammalian rod bipolar cells. J Comp Neurol 396:351-365.
24. Flores-Herr N, Protti DA, Wassle H (2001) Synaptic currents generating the inhibitory surround of ganglion cells in the mammalian retina. J Neurosci 21:4852-4863.
25. A-receptor subtypes demonstrated in mouse hippocampal and olfactory neurons in vivo. Neurosci Lett 249:99-102.
26. Garrett KM, Haque D, Berry D, Niekrasz I, Gan J, Rotter A, Seale TW (1997) The GABAA receptor alpha 6 subunit gene (Gabra6) is tightly linked to the alpha 1-gamma 2 subunit cluster on mouse chromosome 11. Brain Res Mol Brain Res 45:133-137.
27. Green DG, Kapousta-Bruneau NV (1999) A dissection of the electroretinogram from the isolated rat retina with microelectrodes and drugs. Vis Neurosci 16:727-741.
28. Greka A, Lipton SA, Zhang D (2000) Expression of GABAC receptor rho1 and rho2 subunits during development of the mouse retina. Eur J Neurosci 12:3575-3582.
29. Hackam AS, Wang TL, Guggino WB, Cutting GR (1998) Sequences in the amino termini of GABA rho and GABA(A) subunits specify their selective interaction in vitro. J Neurochem 70:40-46.
30. Hartveit E (1999) Reciprocal synaptic interactions between rod bipolar cells and amacrine cells in the rat retina. J Neurophysiol 81:2923-2936.
31. Haverkamp S, Wassle H (2000) Immunocytochemical analysis of the mouse retina. J Comp Neurol 424:1-23.
32. Hood DC, Birch DG (1996) Assessing abnormal rod photoreceptor activity with the a-wave of the electroretinogram: applications and methods. Doc Ophthalmol 92:253-267.
33. Jiang M, Gold MS, Boulay G, Spicher K, Peyton M, Brabet P, Srinivasan Y, Rudolph U, Ellison G, Birnbaumer L (1998) Multiple neurological abnormalities in mice deficient in the G protein Go. Proc Natl Acad Sci USA 95:3269-3274.
34. Johnston GA (1994) GABAC receptors. Prog Brain Res 100:61-65.
35. Kapousta-Bruneau NV (2000) Opposite effects of GABA(A) and GABA(C) receptor antagonists on the b-wave of ERG recorded from the isolated rat retina. Vision Res 40:1653-1665.
36. Kogan SC, Doherty M, Gitschier J (1987) An improved method for prenatal diagnosis of genetic diseases by analysis of amplified DNA sequences. Application to hemophilia A. N Engl J Med 317:985-990.
37. Kolb H, Nelson R (1981) Amacrine cells of the cat retina. Vision Res 21:1625-1633.
38. Kolb H, Nelson R (1983) Rod pathways in the retina of the cat. Vision Res 23:301-312.
39. Koulen P, Brandstatter JH, Enz R, Bormann J, Wassle H (1998) Synaptic clustering of GABA(C) receptor rho-subunits in the rat retina. Eur J Neurosci 10:115-127.
40. Koulen P, Brandstatter JH, Kroger S, Enz R, Bormann J, Wassle H (1997) Immunocytochemical localization of the GABA(C) receptor rho subunits in the cat, goldfish, and chicken retina. J Comp Neurol 380:520-532.
41. Lamb TD (1996) Gain and kinetics of activation in the G-protein cascade of phototransduction. Proc Natl Acad Sci USA 93:566-570.
42. Lukasiewicz PD (1996) GABAC receptors in the vertebrate retina. Mol Neurobiol 12:181-194.
43. Lukasiewicz PD, Roeder RC (1995) Evidence for glycine modulation of excitatory synaptic inputs to retinal ganglion cells. J Neurosci 15:4592-4601.
44. Lukasiewicz P, Shields CR (1998) A diversity of GABA receptors in the retina. Cell Dev Biol 9:293-299.
45. Lukasiewicz PD, Werblin FS (1990) The spatial distribution of excitatory and inhibitory inputs to ganglion cell dendrites in the tiger salamander retina. JNSCI 10:210-221.
46. Lukasiewicz PD, Werblin FS (1994) A novel GABA receptor modulates synaptic transmission from bipolar to ganglion and amacrine cells in the tiger salamander retina. J Neurosci 14:1213-1223.
47. Lukasiewicz PD, Wong RO (1997) GABAC receptors on ferret retinal bipolar cells: a diversity of subtypes in mammals? Vis Neurosci 14:989-994.
48. Lukasiewicz PD, Maple BR, Werblin FS (1994) A novel GABA receptor on bipolar cell terminals in the tiger salamander retina. J Neurosci 14:1202-1212.
49. Masu M, Iwakabe H, Tagawa Y, Miyoshi T, Yamashita J, Fukuda Y, Sasaki H, Hiroi K, Nakamura Y, Shigemoto R, Takada M, Nakamura K, Nakao K, Katsuki M, Nakanishi S. (1995) Specific deficit of the ON response in visual transmission by targeted disruption of the mGluR6 gene. Cell 80:757-765.
50. McCall MA, Gregg RG, Behringer RR, Brenner M, Delaney CL, Galbreath EJ, Zhang CL, Pearce RA, Chiu SY, Messing A (1996a) Targeted deletion in astrocyte intermediate filament (GFAP) alters neuronal physiology. Proc Natl Acad Sci USA 93:6361-6366.
51. McCall MA, Gregg RG, Merriman K, Goto Y, Peachey NS, Stanford LR (1996b) Morphological and physiological consequences of the selective elimination of rod photoreceptors in transgenic mice. Exp Eye Res 63:35-50.
52. McGillem GS, Rotolo TC, Dacheux RF (2000) GABA responses of rod bipolar cells in rabbit retinal slices. Vis Neurosci 17:381-389.
53. Moss SJ, Smart TG (2001) Constructing inhibitory synapses. Nat Rev Neurosci 2:240-250.
54. Naarendorp F, Sieving PA (1991) The scotopic threshold response of the cat ERG is suppressed selectively by GABA and glycine. Vision Res 31:1-15.
55. Nusser Z, Kay LM, Laurent G, Homanics GE, Mody I (2001) Disruption of GABA(A) receptors on GABAergic interneurons leads to increased oscillatory power in the olfactory bulb network. J Neurophysiol 86:2823-2833.
56. Pan ZH, Lipton SA (1995) Multiple GABA receptor subtypes mediate inhibition of calcium influx at rat retinal bipolar cell terminals. J Neurosci 15:2668-2679.
57. Pan ZH, Zhang D, Zhang X, Lipton SA (2000) Evidence for coassembly of mutant GABAC rho1 with GABAA gamma2S, glycine alpha1 and glycine alpha2 receptor subunits in vitro. Eur J Neurosci 12:3137-3145.
58. Pardue MT, McCall MA, LaVail MM, Gregg RG, Peachey NS (1998) A naturally occurring mouse model of X-linked congenital stationary night blindness. Invest Ophthalmol Vis Sci 39:2443-2449.
59. Pattnaik B, Jellali A, Sahel J, Dreyfus H, Picaud S (2000) GABAC receptors are localized with microtubule-associated protein 1B in mammalian cone photoreceptors. J Neurosci 20:6789-6796.
60. Peachey NS, Roveri L, Messing A, McCall MA (1997) Functional consequences of oncogene-induced horizontal cell degeneration in the retinas of transgenic mice. Vis Neurosci 14:627-632.
61. Persohn E, Malherbe P, Richards JG (1992) Comparative molecular neuroanatomy of cloned GABAA receptor subunits in the rat CNS. J Comp Neurol 326:193-216.
62. Picaud S, Pattnaik B, Hicks D, Forster V, Fontaine V, Sahel J, Dreyfus H (1998) GABAA and GABAC receptors in adult porcine cones: evidence from a photoreceptor-glia co-culture model. J Physiol (Lond) 513:33-42.
63. Qian H, Ripps H (1999) Response kinetics and pharmacological properties of heteromeric receptors formed by coassembly of GABA rho- and gamma 2-subunits. Proc R Soc Lond B Biol Sci 266:2419-2425.
64. Ragozzino D, Woodward RM, Murata Y, Eusebi F, Overman LE, Miledi R (1996) Design and in vitro pharmacology of a selective gamma-aminobutyric acidC receptor antagonist. Mol Pharmacol 50:1024-1030.
65. Redburn DA (1992) Development of GABAergic neurons in the mammalian retina. Prog Brain Res 90:133-147.
66. Robson JG, Frishman LJ (1995) Response linearity and dynamics of the cat retina: the bipolar cell component of the dark-adapted ERG. Vis Neurosci 12:837-850.
67. Robson JG, Frishman LJ (1998) Dissecting the dark-adapted electroretinogram. Doc Ophthalmol 95:187-215.
68. Rohrer B, Korenbrot JI, LaVail MM, Reichardt LF, Xu B (1999) Role of neurotrophin receptor TrkB in the maturation of rod photoreceptors and establishment of synaptic transmission to the inner retina. J Neurosci 19:8919-8930.
69. Roska B, Nemeth E, Werblin FS (1998) Response to change is facilitated by a three-neuron disinhibitory pathway in the tiger salamander retina. J Neurosci 18:3451-3459.
70. Rozzo A, Ballerini L, Nistri A (1999) Antagonism by (1,2,5,6-tetrahydropyridine-4-yl) methylphosphinic acid of synaptic transmission in the neonatal rat spinal cord in vitro: an electrophysiological studv. Neuroscience 90:1085-1092.
71. Shields CR, Tran MN, Wong RO, Lukasiewicz PD (2000) Distinct ionotropic GABA receptors mediate presynaptic and postsynaptic inhibition in retinal bipolar cells. J Neurosci 20:2673-2682.
72. Shimada S, Cutting G, Uhl GR. (1992) gamma-Aminobutyric acid A or C receptor? Gamma-aminobutyric acid rho 1 receptor RNA induces bicuculline-, barbiturate-, and benzodiazepine-insensitive gamma-aminobutyric acid responses in Xenopus oocytes. Mol Pharmacol 41:683-687.
73. Shingai R, Yanagi K, Fukushima T, Sakata K, Ogurusu T (1996) Functional expression of GABA rho 3 receptors in Xenopus oocytes. Neurosci Res 26:387-390.
74. Sivilotti L, Nistri A (1991) GABA receptor mechanisms in the central nervous system. Prog Neurobiol 36:35-92.
75. Thibos LN, Werblin FS (1978) The properties of surround antagonism elicited by spinning windmill patterns in the mudpuppy retina. J Physiol (Lond) 278:101-116.
76. Uusi-Oukari M, Heikkila J, Sinkkonen ST, Makela R, Hauer B, Homanics GE, Sieghart W, Wisden W, Korpi ER (2000) Long-range interactions in neuronal gene expression: evidence from gene targeting in the GABA(A) receptor beta2-alpha6-alpha1-gamma2 subunit gene cluster. Mol Cell Neurosci 16:34-41.
77. Verweij J, Kamermans M, Spekreijse H (1996) Horizontal cells feed back to cones by shifting the cone calcium-current activation range. Vision Res 36:3943-3953.
78. Vitanova L, Kupenova P, Haverkamp S, Popova E, Mitova L, Wassle H (2001) Immunocytochemical and electrophysiological characterization of GABA receptors in the frog and turtle retina. Vision Res 41:691-704.
79. Wachtmeister L (1980) Further studies of the chemical sensitivity of the oscillatory potentials of the electroretinogram (ERG) I. Acta Ophthalmol (Copenh) 58:712-725.
80. Wachtmeister L (1998) Oscillatory potentials in the retina: what do they reveal. Prog Retin Eye Res 17:485-521.
81. Wachtmeister L, Dowling JE (1978) The oscillatory potentials of the mudpuppy retina. Invest Ophthalmol Vis Sci 17:1176-1188.
82. Wassle H, Yamashita M, Greferath U, Grunert U, Muller F (1991) The rod bipolar cell of the mammalian retina. Vis Neurosci 7:99-112.
83. Wassle H, Koulen P, Brandstatter JH, Fletcher EL, Becker CM (1998) Glycine and GABA receptors in the mammalian retina. Vision Res 38:1411-1430.
84. Wegelius K, Pasternack M, Hiltunen JO, Rivera C, Kaila K, Saarma M, Reeben M (1998) Distribution of GABA receptor rho subunit transcripts in the rat brain. Eur J Neurosci 10:350-357.
85. Wellis DP, Werblin FS (1995) Dopamine modulates GABAc receptors mediating inhibition of calcium entry into and transmitter release from bipolar cell terminals in tiger salamander retina. J Neurosci 15:4748-4761.
86. Werblin F (1978) Transmission along and between rods in the tiger salamander retina. J Physiol (Lond) 280:449-470.
87. Wisden W, Seeburg PH (1992) GABAA receptor channels: from subunits to functional entities. Curr Opin Neurobiol 2:263-269.
88. Wotring VE, Chang Y, Weiss DS (1999) Permeability and single channel conductance of human homomeric rho1 GABAC receptors. J Physiol (Lond) 521 Pt2:327-336.
89. Wu Y, Cutting GR (2001) Developmentally regulated expression of GABA receptor rho1 and rho2 subunits, L7 and cone-rod homeobox (CRX) genes in mouse retina. Brain Res 912:1-8.
90. Xu X, Quiambao AB, Roveri L, Pardue MT, Marx JL, Rohlich P, Peachey NS, Al Ubaidi MR (2000) Degeneration of cone photoreceptors induced by expression of the Mas1 protooncogene. Exp Neurol 163:207-219.
91. Yang CY, Brecha NC, Tsao E (1997) Immunocytochemical localization of gamma-aminobutyric acid plasma membrane transporters in the tiger salamander retina. J Comp Neurol 389:117-126.
92. Yeh HH, Lee MB, Cheun JE (1990) Properties of GABA-activated whole-cell currents in bipolar cells of the rat retina. Vis Neurosci 4:349-357.
93. Zhang D, Pan ZH, Zhang X, Brideau AD, Lipton SA (1995) Cloning of a gamma-aminobutyric acid type C receptor subunit in rat retina with a methionine residue critical for picrotoxinin channel block. Proc Natl Acad Sci USA 92:11756-11760.
94. Zhang D, Pan ZH, Awobuluyi M, Lipton SA (2001) Structure and function of GABA(C) receptors: a comparison of native versus recombinant receptors. Trends Pharmacol Sci 22:121-132.
95. Zhang J, Jung CS, Slaughter MM (1997) Serial inhibitory synapses in retina. Vis Neurosci 14:553-563.