Distinct synaptic localization patterns of brefeldin A-resistant guanine nucleotide exchange factors BRAG2 and BRAG3 in the mouse retina

Journal of Comparative Neurology

Volumn 521, Issue 4, 2013, Pages 860-876

  Sakagami, Hiroyuki ^a   Katsumata, Osamu ^a   Hara, Yoshinobu ^a   Tamaki, Hideaki ^a   Watanabe, Masahiko ^b   Harvey, Robert J ^c   Fukaya, Masahiro ^a  

^a KITASATO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b HOKKAIDO UNIVERSITY   (Japan)

^c UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

ADP ribosylation factor; Dystrophin; Guanine nucleotide exchange factor; Photoreceptor; Retina

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; AMPA RECEPTOR; BETA DYSTROGLYCAN; BREFELDIN A RESISTANT GUANINE NUCLEOTIDE EXCHANGE FACTOR 2; BREFELDIN A RESISTANT GUANINE NUCLEOTIDE EXCHANGE FACTOR 3; DYSTROPHIN; GEPHYRIN; GLYCINE RECEPTOR; GUANINE NUCLEOTIDE EXCHANGE FACTOR; POSTSYNAPTIC DENSITY PROTEIN 95; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; FEMALE; GUINEA PIG; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; NERVE ENDING; NONHUMAN; PHOTORECEPTOR; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RETINA; RETINA CONE; RETINA INNER PLEXIFORM LAYER; RETINA ROD; SYNAPSE;

ANIMALS; BLOTTING, WESTERN; FEMALE; GUANINE NUCLEOTIDE EXCHANGE FACTORS; IMMUNOHISTOCHEMISTRY; MALE; MICE; MICE, INBRED C57BL; MICROSCOPY, IMMUNOELECTRON; RETINA; SYNAPSES;

EID: 84872731382     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.23206     Document Type: Article

References (82)

1. Blank M, Koulen P, Blake DJ, Kröger S. 1999. Dystrophin and beta-dystroglycan in photoreceptor terminals from normal and mdx3Cv mouse retinae. Eur J Neurosci 11: 2121-2133.
2. A-receptors at GABAergic synaptic contacts demonstrated by triple immunofluorescence staining. Brain Res 642: 59-69.
3. Brandon C, Lam DM. 1983. The ultrastructure of rat rod synaptic terminals: effects of dark-adaptation. J Comp Neurol 217: 167-175.
4. Brändstatter JH, Koulen P, Kuhn R, van der Putten H, Wässle H. 1996. Compartmental localization of a metabotropic glutamate receptor (mGluR7): two different active sites at a retinal synapse. J Neurosci 16: 4749-4756.
5. Brändstatter JH, Koulen P, Wässle H. 1997. Selective synaptic distribution of kainate receptor subunits in the two plexiform layers of the rat retina. J Neurosci 17: 9298-9307.
6. Brenman JE, Chao DS, Xia H, Aldape K, Bredt DS. 1995. Nitric oxide synthase complexed with dystrophin and absent from skeletal muscle sarcolemma in Duchenne muscular dystrophy. Cell 82: 743-752.
7. Campbell KP. 1995. Three muscular dystrophies: loss of cytoskeleton-extracellular matrix linkage. Cell 80: 675-679.
8. Casanova JE. 2007. Regulation of Arf activation: the Sec7 family of guanine nucleotide exchange factors. Traffic 8: 1476-1485.
9. Cibis GW, Fitzgerald KM, Harris DJ, Rothberg PG, Rupani M. 1993. The effects of dystrophin gene mutations on the ERG in mice and humans. Invest Ophthalmol Vis Sci 34: 3646-3652.
10. Cohn RD, Campbell KP. 2000. Molecular basis of muscular dystrophies. Muscle Nerve 23: 1456-1471.
11. Cox R, Mason-Gamer RJ, Jackson CL, Segev N. 2004. Phylogenetic analysis of Sec7-domain-containing Arf nucleotide exchangers. Mol Biol Cell 15: 1487-1505.
12. D'Souza-Schorey C, Chavrier P. 2006. ARF proteins: roles in membrane traffic and beyond. Nat Rev Mol Cell Biol 7: 347-358.
13. Dalloz C, Sarig R, Fort P, Yaffe D, Bordais A, Pannicke T, Grosche J, Mornet D, Reichenbach A, Sahel J, Nudel U, Rendon A. 2003. Targeted inactivation of dystrophin gene product Dp71: phenotypic impact in mouse retina. Hum Mol Genet 12: 1543-1554.
14. De Becker I, Riddell DC, Dooley JM, Tremblay F. 1994. Correlation between electroretinogram findings and molecular analysis in the Duchenne muscular dystrophy phenotype. Br J Ophthalmol 78: 719-722.
15. Dunphy JL, Moravec R, Ly K, Lasell TK, Melancon P, Casanova JE. 2006. The Arf6 GEF GEP100/BRAG2 regulates cell adhesion by controlling endocytosis of beta1 integrins. Curr Biol 16: 315-320.
16. Fischer F, Kneussel M, Tintrup H, Haverkamp S, Rauen T, Betz H, Wässle H. 2000. Reduced synaptic clustering of GABA and glycine receptors in the retina of the gephyrin null mutant mouse. J Comp Neurol 427: 634-648.
17. Fitzgerald KM, Cibis GW, Giambrone SA, Harris DJ. 1994. Retinal signal transmission in Duchenne muscular dystrophy: evidence for dysfunction in the photoreceptor/depolarizing bipolar cell pathway. J Clin Invest 93: 2425-2430.
18. Fletcher EL, Hack I, Brändstatter JH, Wässle H. 2000. Synaptic localization of NMDA receptor subunits in the rat retina. J Comp Neurol 420: 98-112.
19. Fukaya M, Watanabe M. 2000. Improved immunohistochemical detection of postsynaptically located PSD-95/SAP90 protein family by protease section pretreatment: a study in the adult mouse brain. J Comp Neurol 426: 572-586.
20. Fukaya M, Tsujita M, Yamazaki M, Kushiya E, Abe M, Akashi K, Natsume R, Kano M, Kamiya H, Watanabe M, Sakimura K. 2006. Abundant distribution of TARP γ-8 in synaptic and extrasynaptic surface of hippocampal neurons and its major role in AMPA receptor expression on spines and dendrites. Eur J Neurosci 24: 2177-2190.
21. Fukaya M, Kamata A, Hara Y, Tamaki H, Katsumata O, Ito N, Takeda S, Hata Y, Suzuki T, Watanabe M, Harvey RJ, Sakagami H. 2011. SynArfGEF is a guanine nucleotide exchange factor for Arf6 and localizes preferentially at post-synaptic specializations of inhibitory synapses. J Neurochem 116: 1122-1137.
22. Gerges NZ, Backos DS, Esteban JA. 2004. Local control of AMPA receptor trafficking at the postsynaptic terminal by a small GTPase of the Rab family. J Biol Chem 279: 43870-43878.
23. Ghosh KK, Haverkamp S, Wässle H. 2001. Glutamate receptors in the rod pathway of the mammalian retina. J Neurosci 21: 8636-8647.
24. Gillingham AK, Munro S. 2007. The small G proteins of the Arf family and their regulators. Annu Rev Cell Dev Biol 23: 579-611.
25. Greferath U, Brändstatter JH, Wässle H, Kirsch J, Kuhse J, Grünert U. 1994. Differential expression of glycine receptor subunits in the retina of the rat: a study using immunohistochemistry and in situ hybridization. Vis Neurosci 11: 721-729.
26. A receptor subunits have differential distributions in the rat retina: in situ hybridization and immunohistochemistry. J Comp Neurol 353: 553-571.
27. Grünert U. 2000. Distribution of GABA and glycine receptors on bipolar and ganglion cells in the mammalian retina. Microsc Res Tech 50: 130-140.
28. Grünert U, Wässle H. 1993. Immunocytochemical localization of glycine receptors in the mammalian retina. J Comp Neurol 335: 523-537.
29. Grünert U, Haverkamp S, Fletcher EL, Wässle H. 2002. Synaptic distribution of ionotropic glutamate receptors in the inner plexiform layer of the primate retina. J Comp Neurol 447: 138-151.
30. Hack I, Peichl L, Brändstatter JH. 1999. An alternative pathway for rod signals in the rodent retina: rod photoreceptors, cone bipolar cells, and the localization of glutamate receptors. Proc Natl Acad Sci U S A 96: 14130-14135.
31. Hack I, Koulen P, Peichl L, Brändstatter JH. 2002. Development of glutamatergic synapses in the rat retina: the postnatal expression of ionotropic glutamate receptor subunits. Vis Neurosci 19: 1-13.
32. Hartveit E, Brändstatter JH, Sassoè-Pognetto M, Laurie DJ, Seeburg PH, Wässle H. 1994. Localization and developmental expression of the NMDA receptor subunit NR2A in the mammalian retina. J Comp Neurol 348: 570-582.
33. Haverkamp S, Wässle H. 2000. Immunocytochemical analysis of the mouse retina. J Comp Neurol 424: 1-23.
34. Hondo M, Furutani N, Yamasaki M, Watanabe M, Sakurai T. 2011. Orexin neurons receive glycinergic innervations. PLoS One 6: e25076.
35. Hoon M, Soykan T, Falkenburger B, Hammer M, Patrizi A, Schmidt KF, Sassoè-Pognetto M, Lowel S, Moser T, Taschenberger H, Brose N, Varoqueaux F. 2011. Neuroligin-4 is localized to glycinergic postsynapses and regulates inhibition in the retina. Proc Natl Acad Sci U S A 108: 3053-3058.
36. Ichikawa R, Yamasaki M, Miyazaki T, Konno K, Hashimoto K, Tatsumi H, Inoue Y, Kano M, Watanabe M. 2011. Developmental switching of perisomatic innervation from climbing fibers to basket cell fibers in cerebellar Purkinje cells. J Neurosci 31: 16916-16927.
37. Inaba Y, Tian QB, Okano A, Zhang JP, Sakagami H, Miyazawa S, Li W, Komiyama A, Inokuchi K, Kondo H, Suzuki T. 2004. Brain-specific potential guanine nucleotide exchange factor for Arf, synArfGEF (Po), is localized to postsynaptic density. J Neurochem 89: 1347-1357.
38. Jastrow H, Koulen P, Altrock WD, Kroger S. 2006. Identification of a β-dystroglycan immunoreactive subcompartment in photoreceptor terminals. Invest Ophthalmol Vis Sci 47: 17-24.
39. Jonas P, Bischofberger J, Sandkuhler J. 1998. Corelease of two fast neurotransmitters at a central synapse. Science 281: 419-424.
40. Jordan BA, Fernholz BD, Boussac M, Xu C, Grigorean G, Ziff EB, Neubert TA. 2004. Identification and verification of novel rodent postsynaptic density proteins. Mol Cell Proteomics 3: 857-871.
41. Kameya S, Araki E, Katsuki M, Mizota A, Adachi E, Nakahara K, Nonaka I, Sakuragi S, Takeda S, Nabeshima Y. 1997. Dp260 disrupted mice revealed prolonged implicit time of the b-wave in ERG and loss of accumulation of β-dystroglycan in the outer plexiform layer of the retina. Hum Mol Genet 6: 2195-2203.
42. Katsumata O, Ohara N, Tamaki H, Niimura T, Naganuma H, Watanabe M, Sakagami H. 2009. IQ-ArfGEF/BRAG1 is associated with synaptic ribbons in the mouse retina. Eur J Neurosci 30: 1509-1516.
43. Kins S, Betz H, Kirsch J. 2000. Collybistin, a newly identified brain-specific GEF, induces submembrane clustering of gephyrin. Nat Neurosci 3: 22-29.
44. Koulen P, Malitschek B, Kuhn R, Wässle H, Brändstatter JH. 1996a. Group II and group III metabotropic glutamate receptors in the rat retina: distributions and developmental expression patterns. Eur J Neurosci 8: 2177-2187.
45. A and glycine receptors in the mammalian retina. J Neurosci 16: 2127-2140.
46. Koulen P, Kuhn R, Wässle H, Brändstatter JH. 1997. Group I metabotropic glutamate receptors mGluR1alpha and mGluR5a: localization in both synaptic layers of the rat retina. J Neurosci 17: 2200-2211.
47. Koulen P, Blank M, Kroger S. 1998a. Differential distribution of beta-dystroglycan in rabbit and rat retina. J Neurosci Res 51: 735-747.
48. Koulen P, Fletcher EL, Craven SE, Bredt DS, Wässle H. 1998b. Immunocytochemical localization of the postsynaptic density protein PSD-95 in the mammalian retina. J Neurosci 18: 10136-10149.
49. Koulen P, Garner CC, Wässle H. 1998c. Immunocytochemical localization of the synapse-associated protein SAP102 in the rat retina. J Comp Neurol 397: 326-336.
50. Marc RE, Jones BW. 2002. Molecular phenotyping of retinal ganglion cells. J Neurosci 22: 413-427.
51. Murphy JA, Jensen ON, Walikonis RS. 2006. BRAG1, a Sec7 domain-containing protein, is a component of the postsynaptic density of excitatory synapses. Brain Res 1120: 35-45.
52. Nie Z, Hirsch DS, Randazzo PA. 2003. Arf and its many interactors. Curr Opin Cell Biol 15: 396-404.
53. 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: 6126-6137.
54. Papadopoulos T, Korte M, Eulenburg V, Kubota H, Retiounskaia M, Harvey RJ, Harvey K, O'Sullivan GA, Laube B, Hulsmann S, Geiger JR, Betz H. 2007. Impaired GABAergic transmission and altered hippocampal synaptic plasticity in collybistin-deficient mice. EMBO J 26: 3888-3899.
55. Papadopoulos T, Eulenburg V, Reddy-Alla S, Mansuy IM, Li Y, Betz H. 2008. Collybistin is required for both the formation and maintenance of GABAergic postsynapses in the hippocampus. Mol Cell Neurosci 39: 161-169.
56. Peng YW, Blackstone CD, Huganir RL, Yau KW. 1995. Distribution of glutamate receptor subtypes in the vertebrate retina. Neuroscience 66: 483-497.
57. Peng J, Kim MJ, Cheng D, Duong DM, Gygi SP, Sheng M. 2004. Semiquantitative proteomic analysis of rat forebrain postsynaptic density fractions by mass spectrometry. J Biol Chem 279: 21003-21011.
58. Pillers DA, Bulman DE, Weleber RG, Sigesmund DA, Musarella MA, Powell BR, Murphey WH, Westall C, Panton C, Becker LE, et al. 1993. Dystrophin expression in the human retina is required for normal function as defined by electroretinography. Nat Genet 4: 82-86.
59. Pinto LH, Grünert U, Studholme K, Yazulla S, Kirsch J, Becker CM. 1994. Glycine receptors in the retinas of normal and spastic mutant mice. Invest Ophthalmol Vis Sci 35: 3633-3639.
60. Poulopoulos A, Aramuni G, Meyer G, Soykan T, Hoon M, Papadopoulos T, Zhang M, Paarmann I, Fuchs C, Harvey K, Jedlicka P, Schwarzacher SW, Betz H, Harvey RJ, Brose N, Zhang W, Varoqueaux F. 2009. Neuroligin 2 drives postsynaptic assembly at perisomatic inhibitory synapses through gephyrin and collybistin. Neuron 63: 628-642.
61. Qin P, Pourcho RG. 1996. Distribution of AMPA-selective glutamate receptor subunits in the cat retina. Brain Res 710: 303-307.
62. Qin P, Pourcho RG. 1999a. AMPA-selective glutamate receptor subunits GluR2 and GluR4 in the cat retina: an immunocytochemical study. Vis Neurosci 16: 1105-1114.
63. Qin P, Pourcho RG. 1999b. Localization of AMPA-selective glutamate receptor subunits in the cat retina: a light- and electron-microscopic study. Vis Neurosci 16: 169-177.
64. A receptor clustering. J Biol Chem 285: 29623-29631.
65. Sakagami H, Sanda M, Fukaya M, Miyazaki T, Sukegawa J, Yanagisawa T, Suzuki T, Fukunaga K, Watanabe M, Kondo H. 2008. IQ-ArfGEF/BRAG1 is a guanine nucleotide exchange factor for Arf6 that interacts with PSD-95 at postsynaptic density of excitatory synapses. Neurosci Res 60: 199-212.
66. Sanda M, Kamata A, Katsumata O, Fukunaga K, Watanabe M, Kondo H, Sakagami H. 2009. The postsynaptic density protein, IQ-ArfGEF/BRAG1, can interact with IRSp53 through its proline-rich sequence. Brain Res 1251: 7-15.
67. Sassoè-Pognetto M, Wässle H, Grünert U. 1994. Glycinergic synapses in the rod pathway of the rat retina: cone bipolar cells express the α1 subunit of the glycine receptor. J Neurosci 14: 5131-5146.
68. A-receptor subunits in the rat retina. J Comp Neurol 357: 1-14.
69. 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: 923-931.
70. Schmitt B, Knaus P, Becker CM, Betz H. 1987. The Mr 93, 000 polypeptide of the postsynaptic glycine receptor complex is a peripheral membrane protein. Biochemistry 26: 805-811.
71. Schmitz F, Drenckhahn D. 1997. Localization of dystrophin and beta-dystroglycan in bovine retinal photoreceptor processes extending into the postsynaptic dendritic complex. Histochem Cell Biol 108: 249-255.
72. Scholz R, Berberich S, Rathgeber L, Kolleker A, Kohr G, Kornau HC. 2010. AMPA receptor signaling through BRAG2 and Arf6 critical for long-term synaptic depression. Neuron 66: 768-780.
73. Sigesmund DA, Weleber RG, Pillers DA, Westall CA, Panton CM, Powell BR, Heon E, Murphey WH, Musarella MA, Ray PN. 1994. Characterization of the ocular phenotype of Duchenne and Becker muscular dystrophy. Ophthalmology 101: 856-865.
74. Todd AJ, Watt C, Spike RC, Sieghart W. 1996. Colocalization of GABA, glycine, and their receptors at synapses in the rat spinal cord. J Neurosci 16: 974-982.
75. Ueda H, Baba T, Terada N, Kato Y, Tsukahara S, Ohno S. 1997. Dystrophin in rod spherules; submembranous dense regions facing bipolar cell processes. Histochem Cell Biol 108: 243-248.
76. Ueda H, Gohdo T, Ohno S. 1998. Beta-dystroglycan localization in the photoreceptor and Müller cells in the rat retina revealed by immunoelectron microscopy. J Histochem Cytochem 46: 185-191.
77. Walikonis RS, Jensen ON, Mann M, Provance DW Jr, Mercer JA, Kennedy MB. 2000. Identification of proteins in the postsynaptic density fraction by mass spectrometry. J Neurosci 20: 4069-4080.
78. Wässle H, Yamashita M, Greferath U, Grünert U, Müller F. 1991. The rod bipolar cell of the mammalian retina. Vis Neurosci 7: 99-112.
79. Watanabe M, Fukaya M, Sakimura K, Manabe T, Mishina M, Inoue Y. 1998. Selective scarcity of NMDA receptor channel subunits in the stratum lucidum (mossy fibre-recipient layer) of the mouse hippocampal CA3 subfield. Eur J Neurosci 10: 478-487.
80. Zhang J, Diamond JS. 2006. Distinct perisynaptic and synaptic localization of NMDA and AMPA receptors on ganglion cells in rat retina. J Comp Neurol 498: 810-820.
81. Zhu JJ, Qin Y, Zhao M, Van Aelst L, Malinow R. 2002. Ras and Rap control AMPA receptor trafficking during synaptic plasticity. Cell 110: 443-455.
82. Zhu Y, Pak D, Qin Y, McCormack SG, Kim MJ, Baumgart JP, Velamoor V, Auberson YP, Osten P, van Aelst L, Sheng M, Zhu JJ. 2005. Rap2-JNK removes synaptic AMPA receptors during depotentiation. Neuron 46: 905-916.