Skip to main content
Top
Published in: Documenta Ophthalmologica 3/2012

01-12-2012 | Original Research Article

Response properties of slow PIII in the Large vls mutant

Authors: Neal S. Peachey, Gwen M. Sturgill-Short

Published in: Documenta Ophthalmologica | Issue 3/2012

Login to get access

Abstract

Purpose

Mouse mutants for proteins expressed in the dystrophin–glycoprotein complex at the photoreceptor terminal have electroretinogram (ERG) b-waves with a delayed onset and time course. The b-wave is defined by the sum of PII generated by depolarizing bipolar cells and slow PIII generated by Müller glial cells. In this study, we evaluated the hypothesis that the abnormalities observed in one of these mutants, Large vls , are caused by abnormal response properties of slow PIII.

Methods

To isolate slow PIII, we crossed the Large vls mutant to a mouse line (Gpr179 nob5 ) that lacks the ERG b-wave but maintains normal photoreceptor function and in which retinal degeneration does not occur. ERGs were recorded to strobe flash stimuli after overnight dark adaptation.

Results

In comparison with control responses, the a-wave and slow PIII had comparable waveforms but were reduced in amplitude in Large vls mice. The magnitude of this reduction was comparable for these components, and across stimulus luminance. There was no stimulus condition where the amplitude of slow PIII was larger than control.

Conclusions

The data obtained are inconsistent with the idea that the b-wave abnormalities noted in Large vls mutant mice are caused by abnormal response properties of slow PIII.
Literature
1.
go back to reference Penn RD, Hagins WA (1969) Signal transmission along retinal rods and the origin of the electroretinographic a-wave. Nature 223:201–204PubMedCrossRef Penn RD, Hagins WA (1969) Signal transmission along retinal rods and the origin of the electroretinographic a-wave. Nature 223:201–204PubMedCrossRef
2.
go back to reference Granit R (1933) The components of the retinal action potential in mammals and their relation to the discharge in the optic nerve. J Physiol 77:207–239PubMed Granit R (1933) The components of the retinal action potential in mammals and their relation to the discharge in the optic nerve. J Physiol 77:207–239PubMed
3.
go back to reference Kofuji P, Ceelen P, Zahs KR, Surbeck LW, Lester HA, Newman EA (2000) Genetic inactivation of an inwardly rectifying potassium channel (Kir4.1 subunit) in mice: phenotypic impact in retina. J Neurosci 20:5733–5740PubMed Kofuji P, Ceelen P, Zahs KR, Surbeck LW, Lester HA, Newman EA (2000) Genetic inactivation of an inwardly rectifying potassium channel (Kir4.1 subunit) in mice: phenotypic impact in retina. J Neurosci 20:5733–5740PubMed
4.
go back to reference Steinberg RH, Miller S (1973) Aspects of electrolyte transport in frog pigment epithelium. Exp Eye Res 16:365–372PubMedCrossRef Steinberg RH, Miller S (1973) Aspects of electrolyte transport in frog pigment epithelium. Exp Eye Res 16:365–372PubMedCrossRef
5.
go back to reference Oakley B II, Green DG (1976) Correlation of light-induced changes in retinal extracellular potassium concentration with c-wave of the electroretinogram. J Neurophysiol 39:1117–1133PubMed Oakley B II, Green DG (1976) Correlation of light-induced changes in retinal extracellular potassium concentration with c-wave of the electroretinogram. J Neurophysiol 39:1117–1133PubMed
6.
go back to reference Witkovsky P, Dudek FE, Ripps H (1975) Slow PIII component of the carp electroretinogram. J Gen Physiol 65:119–134PubMedCrossRef Witkovsky P, Dudek FE, Ripps H (1975) Slow PIII component of the carp electroretinogram. J Gen Physiol 65:119–134PubMedCrossRef
7.
go back to reference Wu J, Marmorstein AD, Kofuji P, Peachey NS (2004) Contribution of Kir4.1 to the mouse electroretinogram. Mol Vision 10:650–654 Wu J, Marmorstein AD, Kofuji P, Peachey NS (2004) Contribution of Kir4.1 to the mouse electroretinogram. Mol Vision 10:650–654
9.
go back to reference Holzfeind PJ, Grewal PK, Reitsamer HE, Kechvar J, Lassmann H, Hoeger H, Hewitt JE, Bittner RE (2002) Skeletal, cardiac and tongue muscle pathology, defective retinal transmission, and neuronal migration defects in the Large myd mouse defines a natural model for glycosylation-deficient muscle-eye-brain disorders. Hum Mol Genet 11:2673–2687PubMedCrossRef Holzfeind PJ, Grewal PK, Reitsamer HE, Kechvar J, Lassmann H, Hoeger H, Hewitt JE, Bittner RE (2002) Skeletal, cardiac and tongue muscle pathology, defective retinal transmission, and neuronal migration defects in the Large myd mouse defines a natural model for glycosylation-deficient muscle-eye-brain disorders. Hum Mol Genet 11:2673–2687PubMedCrossRef
10.
go back to reference Lee Y, Kameya S, Cox GA, Hsu J, Hicks W, Maddatu TP, Smith RS, Naggert JK, Peachey NS, Nishina PM (2005) Ocular abnormalities in Large myd and Large vls mice, spontaneous models for muscle, eye and brain diseases. Mol Cell Neurosci 30:160–172PubMedCrossRef Lee Y, Kameya S, Cox GA, Hsu J, Hicks W, Maddatu TP, Smith RS, Naggert JK, Peachey NS, Nishina PM (2005) Ocular abnormalities in Large myd and Large vls mice, spontaneous models for muscle, eye and brain diseases. Mol Cell Neurosci 30:160–172PubMedCrossRef
11.
go back to reference Sato S, Omori Y, Katoh K, Kondo M, Kanagawa M, Miyata K, Funabiki K, Koyasu T, Kajimura N, Miyoshi T, Sawai H, Kobayashi K, Tani A, Toda T, Usukura J, Tano Y, Fujikado T, Furukawa T (2008) Pikachurin, a dystroglycan ligand, is essential for photoreceptor ribbon synapse formation. Nat Neurosci 11:923–931PubMedCrossRef Sato S, Omori Y, Katoh K, Kondo M, Kanagawa M, Miyata K, Funabiki K, Koyasu T, Kajimura N, Miyoshi T, Sawai H, Kobayashi K, Tani A, Toda T, Usukura J, Tano Y, Fujikado T, Furukawa T (2008) Pikachurin, a dystroglycan ligand, is essential for photoreceptor ribbon synapse formation. Nat Neurosci 11:923–931PubMedCrossRef
12.
go back to reference Liu J, Ball SL, Yang Y, Mei P, Zhang L, Shi H, Kaminski HJ, Lemmon VP, Hu H (2006) A genetic model for muscle-eye-brain disease in mice lacking protein O-mannose beta1,2-N-acetylglucosaminyltransferase (POMGnT1). Mech Dev 123:228–240PubMedCrossRef Liu J, Ball SL, Yang Y, Mei P, Zhang L, Shi H, Kaminski HJ, Lemmon VP, Hu H (2006) A genetic model for muscle-eye-brain disease in mice lacking protein O-mannose beta1,2-N-acetylglucosaminyltransferase (POMGnT1). Mech Dev 123:228–240PubMedCrossRef
13.
go back to reference Pattnaik BR, Green DG, Pillers D-AM (2009) Aberrant slow wave (Slow PIII) component superimposed on a normal b-wave, accounts for the abnormal electroretinogram in the mdx Cv3 mouse. Invest Ophthalmol Vis Sci 50:E-Abstract 3599 Pattnaik BR, Green DG, Pillers D-AM (2009) Aberrant slow wave (Slow PIII) component superimposed on a normal b-wave, accounts for the abnormal electroretinogram in the mdx Cv3 mouse. Invest Ophthalmol Vis Sci 50:E-Abstract 3599
14.
go back to reference Peachey NS, Ray TA, Florijn R, Rowe LB, Sjoerdsma T, Contreras-Alcantara S, Baba K, Tosini G, Pozdeyev N, Iuvone PM, Bojang P Jr, Pearring JN, Simonsz HJ, van Genderen M, Birch DG, Traboulsi EI, Dorfman A, Lopez I, Ren H, Goldberg AFX, Nishina PM, Lachapelle P, McCall MA, Koenekoop RK, Bergen AAB, Kamermans M, Gregg RG (2012) GPR179 is required for depolarizing bipolar cell function and is mutated in autosomal-recessive complete congenital stationary night blindness. Am J Hum Genet 90:331–339PubMedCrossRef Peachey NS, Ray TA, Florijn R, Rowe LB, Sjoerdsma T, Contreras-Alcantara S, Baba K, Tosini G, Pozdeyev N, Iuvone PM, Bojang P Jr, Pearring JN, Simonsz HJ, van Genderen M, Birch DG, Traboulsi EI, Dorfman A, Lopez I, Ren H, Goldberg AFX, Nishina PM, Lachapelle P, McCall MA, Koenekoop RK, Bergen AAB, Kamermans M, Gregg RG (2012) GPR179 is required for depolarizing bipolar cell function and is mutated in autosomal-recessive complete congenital stationary night blindness. Am J Hum Genet 90:331–339PubMedCrossRef
15.
go back to reference Samuels IS, Sturgill GM, Grossman GH, Rayborn ME, Hollyfield JG, Peachey NS (2010) Light-evoked responses of the retinal pigment epithelium: changes accompanying photoreceptor loss in the mouse. J Neurophysiol 104:391–402PubMedCrossRef Samuels IS, Sturgill GM, Grossman GH, Rayborn ME, Hollyfield JG, Peachey NS (2010) Light-evoked responses of the retinal pigment epithelium: changes accompanying photoreceptor loss in the mouse. J Neurophysiol 104:391–402PubMedCrossRef
16.
go back to reference Hood DC, Birch DG (1992) A computational model of the amplitude and implicit time of the b-wave of the human ERG. Vis Neurosci 8:107–126PubMedCrossRef Hood DC, Birch DG (1992) A computational model of the amplitude and implicit time of the b-wave of the human ERG. Vis Neurosci 8:107–126PubMedCrossRef
17.
go back to reference Robson JG, Frishman LJ (1995) Response linearity and kinetics of the cat electroretinogram: the bipolar cell component of the dark-adapted electroretinogram. Vis Neurosci 12:837–850PubMedCrossRef Robson JG, Frishman LJ (1995) Response linearity and kinetics of the cat electroretinogram: the bipolar cell component of the dark-adapted electroretinogram. Vis Neurosci 12:837–850PubMedCrossRef
18.
go back to reference Goldberg AF (2006) Role of peripherin/rds in vertebrate photoreceptor architecture and inherited retinal degenerations. Int Rev Cytol 253:131–175PubMedCrossRef Goldberg AF (2006) Role of peripherin/rds in vertebrate photoreceptor architecture and inherited retinal degenerations. Int Rev Cytol 253:131–175PubMedCrossRef
19.
go back to reference Cheng T, Peachey NS, Li S, Goto Y, Cao Y, Naash MI (1997) The effect of peripherin/rds haploinsufficiency on rod and cone photoreceptors. J Neurosci 17:8118–8128PubMed Cheng T, Peachey NS, Li S, Goto Y, Cao Y, Naash MI (1997) The effect of peripherin/rds haploinsufficiency on rod and cone photoreceptors. J Neurosci 17:8118–8128PubMed
20.
go back to reference 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 39:2443–2449PubMed 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 39:2443–2449PubMed
21.
go back to reference Gregg RG, Kamermans M, Klooster J, Lukasiewicz PD, Peachey NS, Vessey KA, McCall MA (2007) Nyctalopin expression in retinal bipolar cells restores visual function in a mouse model of complete X-linked congenital stationary night blindness. J Neurophysiol 98:3023–3033PubMedCrossRef Gregg RG, Kamermans M, Klooster J, Lukasiewicz PD, Peachey NS, Vessey KA, McCall MA (2007) Nyctalopin expression in retinal bipolar cells restores visual function in a mouse model of complete X-linked congenital stationary night blindness. J Neurophysiol 98:3023–3033PubMedCrossRef
22.
go back to reference Masu M, Iwakabe H, Tagawa Y, Miyoshi T, Yamashita M, 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 mGIuR6 gene. Cell 80:757–765PubMedCrossRef Masu M, Iwakabe H, Tagawa Y, Miyoshi T, Yamashita M, 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 mGIuR6 gene. Cell 80:757–765PubMedCrossRef
23.
go back to reference Pinto LH, Vitaterna MH, Shimomura K, Siepka SM, Balannik V, McDearmon EL, Omura C, Lumayag S, Invergo BM, Glawe B, Cantrell DR, Inayat S, Olvera MA, Vessey KA, McCall MA, Maddox D, Morgans CW, Young B, Pletcher MT, Mullins RF, Troy JB, Takahashi JS (2007) Generation, identification and functional characterization of the nob4 mutation of Grm6 in the mouse. Vis Neurosci 24:111–123PubMedCrossRef Pinto LH, Vitaterna MH, Shimomura K, Siepka SM, Balannik V, McDearmon EL, Omura C, Lumayag S, Invergo BM, Glawe B, Cantrell DR, Inayat S, Olvera MA, Vessey KA, McCall MA, Maddox D, Morgans CW, Young B, Pletcher MT, Mullins RF, Troy JB, Takahashi JS (2007) Generation, identification and functional characterization of the nob4 mutation of Grm6 in the mouse. Vis Neurosci 24:111–123PubMedCrossRef
24.
go back to reference Maddox DM, Vessey KA, Yarbrough GL, Invergo BM, Cantrell DR, Inayat S, Balannik V, Hicks WL, Hawes NL, Byers S, Smith RS, Hurd R, Howell D, Gregg RG, Chang B, Naggert JK, Troy JB, Pinto LH, Nishina PM, McCall MA (2008) Allelic variance between GRM6 mutants, Grm6 nob3 and Grm6 nob4 results in differences in retinal ganglion cell visual responses. J Physiol 586:4409–4424PubMedCrossRef Maddox DM, Vessey KA, Yarbrough GL, Invergo BM, Cantrell DR, Inayat S, Balannik V, Hicks WL, Hawes NL, Byers S, Smith RS, Hurd R, Howell D, Gregg RG, Chang B, Naggert JK, Troy JB, Pinto LH, Nishina PM, McCall MA (2008) Allelic variance between GRM6 mutants, Grm6 nob3 and Grm6 nob4 results in differences in retinal ganglion cell visual responses. J Physiol 586:4409–4424PubMedCrossRef
25.
go back to reference Morgans CW, Zhang J, Jeffrey BG, Nelson SM, Burke NS, Duvoisin RM, Brown RL (2009) TRPM1 is required for the depolarizing light response in retinal ON-bipolar cells. Proc Natl Acad Sci USA 106:19174–19178PubMedCrossRef Morgans CW, Zhang J, Jeffrey BG, Nelson SM, Burke NS, Duvoisin RM, Brown RL (2009) TRPM1 is required for the depolarizing light response in retinal ON-bipolar cells. Proc Natl Acad Sci USA 106:19174–19178PubMedCrossRef
26.
go back to reference Shen Y, Heimel JA, Kammermans M, Peachey NS, Gregg RG, Nawy S (2009) A transient receptor potential-like channel mediates synaptic transmission in rod bipolar cells. J Neurosci 29:6088–6093PubMedCrossRef Shen Y, Heimel JA, Kammermans M, Peachey NS, Gregg RG, Nawy S (2009) A transient receptor potential-like channel mediates synaptic transmission in rod bipolar cells. J Neurosci 29:6088–6093PubMedCrossRef
27.
go back to reference Koike C, Obara T, Uriu Y, Numata T, Sanuki R, Miyata K, Koyasu T, Ueno S, Funabiki K, Tani A, Ueda H, Kondo M, Mori Y, Tachibana M, Furukawa T (2010) TRPM1 is a component of the retinal ON bipolar cell transduction channel in the mGluR6 cascade. Proc Natl Acad Sci USA 107:332–337PubMedCrossRef Koike C, Obara T, Uriu Y, Numata T, Sanuki R, Miyata K, Koyasu T, Ueno S, Funabiki K, Tani A, Ueda H, Kondo M, Mori Y, Tachibana M, Furukawa T (2010) TRPM1 is a component of the retinal ON bipolar cell transduction channel in the mGluR6 cascade. Proc Natl Acad Sci USA 107:332–337PubMedCrossRef
28.
go back to reference Peachey NS, McCall MA, Nobles RD, Hirschtritt ME, Pearring JN, Bojang P, Shen Y, Nawy SA, Nishina PM, Gregg RG (2011) Trpm1 point mutation underlies retinal dysfunction in the Mtvr27 mouse model of complete congenital stationary night blindness. Invest Ophthalmol Vis Sci 51:E-Abstract 4124 Peachey NS, McCall MA, Nobles RD, Hirschtritt ME, Pearring JN, Bojang P, Shen Y, Nawy SA, Nishina PM, Gregg RG (2011) Trpm1 point mutation underlies retinal dysfunction in the Mtvr27 mouse model of complete congenital stationary night blindness. Invest Ophthalmol Vis Sci 51:E-Abstract 4124
29.
go back to reference Omori Y, Araki F, Chaya T, Kajimura N, Irie S, Terada K, Muranishi Y, Tsujii T, Ueno S, Koyasu T, Tamaki Y, Kondo M, Amano S, Furukawa T (2012) Presynaptic dystroglycan-pikachurin complex regulates the proper synaptic connection between retinal photoreceptor and bipolar cells. J Neurosci 32:6126–6137PubMedCrossRef Omori Y, Araki F, Chaya T, Kajimura N, Irie S, Terada K, Muranishi Y, Tsujii T, Ueno S, Koyasu T, Tamaki Y, Kondo M, Amano S, Furukawa T (2012) Presynaptic dystroglycan-pikachurin complex regulates the proper synaptic connection between retinal photoreceptor and bipolar cells. J Neurosci 32:6126–6137PubMedCrossRef
Metadata
Title
Response properties of slow PIII in the Large vls mutant
Authors
Neal S. Peachey
Gwen M. Sturgill-Short
Publication date
01-12-2012
Publisher
Springer-Verlag
Published in
Documenta Ophthalmologica / Issue 3/2012
Print ISSN: 0012-4486
Electronic ISSN: 1573-2622
DOI
https://doi.org/10.1007/s10633-012-9347-9

Other articles of this Issue 3/2012

Documenta Ophthalmologica 3/2012 Go to the issue