Assembly of the outer retina in the absence of GABA synthesis in horizontal cells

Neural Development

Volumn 5, Issue 1, 2010, Pages

  Schubert, Timm ^a,b   Huckfeldt, Rachel M ^a   Parker, Edward ^a   Campbell, John E ^a   Wong, Rachel O L ^a  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; GLUTAMATE DECARBOXYLASE;

ANIMAL; ARTICLE; BIOSYNTHESIS; CELL DIFFERENTIATION; CONGENITAL MALFORMATION; CYTOLOGY; DENDRITE; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MOUSE; MOUSE MUTANT; NERVE TRACT; NEWBORN; PHYSIOLOGY; RETINA; RETINA BIPOLAR GANGLION CELL; RETINA HORIZONTAL NERVE CELL; SYNAPSE; SYNAPTIC TRANSMISSION; TRANSGENIC MOUSE; ULTRASTRUCTURE;

ANIMALS; ANIMALS, NEWBORN; CELL DIFFERENTIATION; DENDRITES; GAMMA-AMINOBUTYRIC ACID; GLUTAMATE DECARBOXYLASE; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; NEURAL PATHWAYS; RETINA; RETINAL BIPOLAR CELLS; RETINAL HORIZONTAL CELLS; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 77953643688     PISSN: None     EISSN: 17498104     Source Type: Journal    
DOI: 10.1186/1749-8104-5-15     Document Type: Article

References (63)

1. Owens DF, Kriegstein AR. Is there more to GABA than synaptic inhibition?. Nat Rev Neurosci 2002, 3:715-727. 10.1038/nrn919, 12209120.
2. Represa A, Ben-Ari Y. Trophic actions of GABA on neuronal development. Trends Neurosci 2005, 28:278-283. 10.1016/j.tins.2005.03.010, 15927682.
3. Bortone D, Polleux F. KCC2 expression promotes the termination of cortical interneuron migration in a voltage-sensitive calcium-dependent manner. Neuron 2009, 62:53-71. 10.1016/j.neuron.2009.01.034, 19376067.
4. Shen W, Da Silva JS, He H, Cline HT. Type A GABA-receptor-dependent synaptic transmission sculpts dendritic arbor structure in Xenopus tadpoles in vivo. J Neurosci 2009, 29:5032-5043. 10.1523/JNEUROSCI.5331-08.2009, 2706946, 19369572.
5. Chattopadhyaya B, Di Cristo G, Wu CZ, Knott G, Kuhlman S, Fu Y, Palmiter RD, Huang ZJ. GAD67-mediated GABA synthesis and signaling regulate inhibitory synaptic innervation in the visual cortex. Neuron 2007, 54:889-903. 10.1016/j.neuron.2007.05.015, 2077924, 17582330.
6. Kanold PO, Kim YA, GrandPre T, Shatz CJ. Co-regulation of ocular dominance plasticity and NMDA receptor subunit expression in glutamic acid decarboxylase-65 knock-out mice. J Physiol 2009, 587:2857-2867. 10.1113/jphysiol.2009.171215, 2718245, 19406876.
7. Hartveit E. Reciprocal synaptic interactions between rod bipolar cells and amacrine cells in the rat retina. J Neurophysiol 1999, 81:2923-2936.
8. Haverkamp S, Grünert U, Wässle H. The cone pedicle, a complex synapse in the retina. Neuron 2000, 27:85-95. 10.1016/S0896-6273(00)00011-8, 10939333.
9. Pan F, Massey SC. Rod and cone input to horizontal cells in the rabbit retina. J Comp Neurol 2007, 500:815-831. 10.1002/cne.21127, 17177254.
10. Kamermans M, Fahrenfort I, Schultz K, Janssen-Bienhold U, Sjoerdsma T, Weiler R. Hemichannel-mediated inhibition in the outer retina. Science 2001, 292:1178-1180. 10.1126/science.1060101, 11349152.
11. Hirasawa H, Kaneko A. pH changes in the invaginating synaptic cleft mediate feedback from horizontal cells to cone photoreceptors by modulating Ca2+ channels. J Gen Physiol 2003, 122:657-671. 10.1085/jgp.200308863, 2229595, 14610018.
12. Hughes TE, Grunert U, Karten HJ. GABAA receptors in the retina of the cat: an immunohistochemical study of wholemounts, sections, and dissociated cells. Vis Neurosci 1991, 6:229-238. 10.1017/S0952523800006246, 1647196.
13. Vardi N, Masarachia P, Sterling P. Immunoreactivity to GABAA receptor in the outer plexiform layer of the cat retina. J Comp Neurol 1992, 320:394-397. 10.1002/cne.903200310, 1377202.
14. Wässle H. Parallel processing in the mammalian retina. Nat Rev Neurosci 2004, 5:747-757. 10.1038/nrn1497, 15378035.
15. Mosinger JL, Yazulla S, Studholme KM. GABA-like immunoreactivity in the vertebrate retina: a species comparison. Exp Eye Res 1986, 42:631-644. 10.1016/0014-4835(86)90052-7, 3487464.
16. Grünert U, Wässle H. GABA-like immunoreactivity in the macaque monkey retina: a light and electron microscopic study. J Comp Neurol 1990, 297:509-524. 10.1002/cne.902970405, 2384611.
17. Osborne NN, Patel S, Beaton DW, Neuhoff V. GABA neurones in retinas of different species and their postnatal development in situ and in culture in the rabbit retina. Cell Tissue Res 1986, 243:117-123. 10.1007/BF00221859, 3510739.
18. Schnitzer J, Rusoff AC. Horizontal cells of the mouse retina contain glutamic acid decarboxylase-like immunoreactivity during early developmental stages. J Neurosci 1984, 4:2948-2955.
19. Messersmith EK, Redburn DA. gamma-Aminobutyric acid immunoreactivity in multiple cell types of the developing rabbit retina. Vis Neurosci 1992, 8:201-211. 10.1017/S0952523800002856, 1547159.
20. Pow DV, Crook DK, Wong RO. Early appearance and transient expression of putative amino acid neurotransmitters and related molecules in the developing rabbit retina: an immunocytochemical study. Vis Neurosci 1994, 11:1115-1134. 10.1017/S0952523800006933, 7841121.
21. Yamasaki EN, Barbosa VD, De Mello FG, Hokoc JN. GABAergic system in the developing mammalian retina: dual sources of GABA at early stages of postnatal development. Int J Dev Neurosci 1999, 17:201-213. 10.1016/S0736-5748(99)00002-7, 10452364.
22. Haverkamp S, Wässle H. Immunocytochemical analysis of the mouse retina. J Comp Neurol 2000, 424:1-23. 10.1002/1096-9861(20000814)424:1<1::AID-CNE1>3.0.CO;2-V, 10888735.
23. Dkhissi O, Julien JF, Wasowicz M, Dalil-Thiney N, Nguyen-Legros J, Versaux-Botteri C. Differential expression of GAD(65) and GAD(67) during the development of the rat retina. Brain Res 2001, 919:242-249. 10.1016/S0006-8993(01)03022-0, 11701136.
24. Cueva JG, Haverkamp S, Reimer RJ, Edwards R, Wässle H, Brecha NC. Vesicular gamma-aminobutyric acid transporter expression in amacrine and horizontal cells. J Comp Neurol 2002, 445:227-237. 10.1002/cne.10166, 11920703.
25. Jellali A, Stussi-Garaud C, Gasnier B, Rendon A, Sahel JA, Dreyfus H, Picaud S. Cellular localization of the vesicular inhibitory amino acid transporter in the mouse and human retina. J Comp Neurol 2002, 449:76-87. 10.1002/cne.10272, 12115694.
26. Johnson J, Tian N, Caywood MS, Reimer RJ, Edwards RH, Copenhagen DR. Vesicular neurotransmitter transporter expression in developing postnatal rodent retina: GABA and glycine precede glutamate. J Neurosci 2003, 23:518-529.
27. Mitchell CK, Huang B, Redburn-Johnson DA. GABA(A) receptor immunoreactivity is transiently expressed in the developing outer retina. Vis Neurosci 1999, 16:1083-1088. 10.1017/S0952523899166082, 10614588.
28. Huang BO, Redburn DA. GABA-induced increases in [Ca2+]i in retinal neurons of postnatal rabbits. Vis Neurosci 1996, 13:441-447. 10.1017/S0952523800008117, 8782371.
29. Huang B, Mitchell CK, Redburn-Johnson DA. GABA and GABA(A) receptor antagonists alter developing cone photoreceptor development in neonatal rabbit retina. Vis Neurosci 2000, 17:925-935. 10.1017/S0952523800176126, 11193109.
30. Feigenspan A, Weiler R. Electrophysiological properties of mouse horizontal cell GABAA receptors. J Neurophysiol 2004, 92:2789-2801. 10.1152/jn.00284.2004, 15240758.
31. Vardi N, Sterling P. Subcellular localization of GABAA receptor on bipolar cells in macaque and human retina. Vision Res 1994, 34:1235-1246. 10.1016/0042-6989(94)90198-8, 8023433.
32. Greferath U, Grünert U, Müller F, Wässle H. Localization of GABAA receptors in the rabbit retina. Cell Tissue Res 1994, 276:295-307.
33. Chattopadhyaya B, Di Cristo G, Higashiyama H, Knott GW, Kuhlman SJ, Welker E, Huang ZJ. Experience and activity-dependent maturation of perisomatic GABAergic innervation in primary visual cortex during a postnatal critical period. J Neurosci 2004, 24:9598-9611. 10.1523/JNEUROSCI.1851-04.2004, 15509747.
34. Huckfeldt RM, Schubert T, Morgan JL, Godinho L, Di Cristo G, Huang ZJ, Wong RO. Transient neurites of retinal horizontal cells exhibit columnar tiling via homotypic interactions. Nat Neurosci 2009, 12:35-43. 10.1038/nn.2236, 2743396, 19060895.
35. Bu DF, Erlander MG, Hitz BC, Tillakaratne NJ, Kaufman DL, Wagner-McPherson CB, Evans GA, Tobin AJ. Two human glutamate decarboxylases, 65-kDa GAD and 67-kDa GAD, are each encoded by a single gene. Proc Natl Acad Sci USA 1992, 89:2115-2119. 10.1073/pnas.89.6.2115, 48607, 1549570.
36. Asada H, Kawamura Y, Maruyama K, Kume H, Ding RG, Kanbara N, Kuzume H, Sanbo M, Yagi T, Obata K. Cleft palate and decreased brain gamma-aminobutyric acid in mice lacking the 67-kDa isoform of glutamic acid decarboxylase. Proc Natl Acad Sci USA 1997, 94:6496-6499. 10.1073/pnas.94.12.6496, 21078, 9177246.
37. Condie BG, Bain G, Gottlieb DI, Capecchi MR. Cleft palate in mice with a targeted mutation in the gamma-aminobutyric acid-producing enzyme glutamic acid decarboxylase 67. Proc Natl Acad Sci USA 1994, 94:11451-11455.
38. Marquardt T, Ashery-Padan R, Andrejewski N, Scardigli R, Guillemot F, Gruss P. Pax6 is required for the multipotent state of retinal progenitor cells. Cell 2001, 105:43-55. 10.1016/S0092-8674(01)00295-1, 11301001.
39. Young RW. Cell proliferation during postnatal development of the retina in the mouse. Brain Res 1985, 353:229-239.
40. Sherry DM, Wang MM, Bates J, Frishman LJ. Expression of vesicular glutamate transporter 1 in the mouse retina reveals temporal ordering in development of rod vs. cone and ON vs. OFF circuits. J Comp Neurol 2003, 465:480-498. 10.1002/cne.10838, 12975811.
41. Messersmith EK, Redburn DA. Kainic acid lesioning alters development of the outer plexiform layer in neonatal rabbit retina. Int J Dev Neurosci 1990, 8:447-461. 10.1016/0736-5748(90)90077-F, 2251935.
42. Rodieck RW. The density recovery profile: a method for the analysis of points in the plane applicable to retinal studies. Vis Neurosci 1991, 6:95-111. 10.1017/S095252380001049X, 2049333.
43. Raviola E, Gilula NB. Intramembrane organization of specialized contacts in the outer plexiform layer of the retina. A freeze-fracture study in monkeys and rabbits. J Cell Biol 1975, 65:192-222. 10.1083/jcb.65.1.192, 2111162, 1127010.
44. Manent JB, Demarque M, Jorquera I, Pellegrino C, Ben-Ari Y, Aniksztejn L, Represa A. A noncanonical release of GABA and glutamate modulates neuronal migration. J Neurosci 2005, 25:4755-4765. 10.1523/JNEUROSCI.0553-05.2005, 15888651.
45. Heng JI, Moonen G, Nguyen L. Neurotransmitters regulate cell migration in the telencephalon. Eur J Neurosci 2007, 26:537-546. 10.1111/j.1460-9568.2007.05694.x, 17686035.
46. Vu TQ, Payne JA, Copenhagen DR. Localization and developmental expression patterns of the neuronal K-Cl cotransporter (KCC2) in the rat retina. J Neurosci 2000, 20:1414-1423.
47. Messersmith EK, Redburn DA. The role of GABA during development of the outer retina in the rabbit. Neurochem Res 1993, 18:463-470. 10.1007/BF00967250, 8474569.
48. Spoerri PE. Neurotrophic effects of GABA in cultures of embryonic chick brain and retina. Synapse 1988, 2:11-22. 10.1002/syn.890020104, 3420527.
49. Barbin G, Pollard H, Gairasa JL, Ben-Ari Y. Involvement of GABAA receptors in the outgrowth of cultured hippocampal neurons. Neurosci Lett 1993, 152:150-154. 10.1016/0304-3940(93)90505-F, 8390627.
50. Borodinsky LN, O'Leary D, Neale JH, Vicini S, Coso OA, Fiszman ML. GABA-induced neurite outgrowth of cerebellar granule cells is mediated by GABA(A) receptor activation, calcium influx and CaMKII and erk1/2 pathways. J Neurochem 2003, 84:1411-1420. 10.1046/j.1471-4159.2003.01638.x, 12614341.
51. Ji F, Obata K. Development of the GABA system in organotypic culture of hippocampal and cerebellar slices from a 67-kDa isoform of glutamic acid decarboxylase (GAD67)-deficient mice. Neurosci Res 1999, 33:233-237. 10.1016/S0168-0102(99)00005-X, 10211768.
52. Ji F, Kanbara N, Obata K. GABA and histogenesis in fetal and neonatal mouse brain lacking both the isoforms of glutamic acid decarboxylase. Neurosci Res 1999, 33:187-194. 10.1016/S0168-0102(99)00011-5, 10211762.
53. May CA, Nakamura K, Fujiyama F, Komatsu Y, Yanagawa Y. Homozygous GAD65 and heterozygous GAD67 knock-out mice reveal normal retinal development and maintenance despite reduced amounts of GABA. Acta Neuropathol (Berl) 2007, 113:101-103.
54. Lewis CA, Ahmed Z, Faber DS. A characterization of glycinergic receptors present in cultured rat medullary neurons. J Neurophysiol 1991, 66:1291-1303.
55. O'Byrne MB, Tipton KF. Taurine-induced attenuation of MPP+ neurotoxicity in vitro a possible role for the GABA(A) subclass of GABA receptors. J Neurochem 2000, 74:2087-2093. 10.1046/j.1471-4159.2000.0742087.x, 10800953.
56. Lake N. Taurine and GABA in the rat retina during postnatal development. Vis Neurosci 1994, 11:253-260. 10.1017/S0952523800001619, 8003452.
57. Young TL, Cepko CL. A role for ligand-gated ion channels in rod photoreceptor development. Neuron 2004, 41:867-879. 10.1016/S0896-6273(04)00141-2, 15046720.
58. Fritschy JM, Panzanelli P, Kralic JE, Vogt KE, Sassoè-Pognetto M. Differential dependence of axo-dendritic and axo-somatic GABAergic synapses on GABAA receptors containing the alpha1 subunit in Purkinje cells. J Neurosci 2006, 26:3245-3255. 10.1523/JNEUROSCI.5118-05.2006, 16554475.
59. Dedek K, Breuninger T, de Sevilla Müller LP, Maxeiner S, Schultz K, Janssen-Bienhold U, Willecke K, Euler T, Weiler R. A novel type of interplexiform amacrine cell in the mouse retina. Eur J Neurosci 2009, 30:217-228. 10.1111/j.1460-9568.2009.06808.x, 19614986.
60. Zhu X, Li A, Brown B, Weiss ER, Osawa S, Craft CM. Mouse cone arrestin expression pattern: light induced translocation in cone photoreceptors. Mol Vis 2002, 8:462-471.
61. Nikonov SS, Brown BM, Davis JA, Zuniga FI, Bragin A, Pugh EN, Craft CM. Mouse cones require an arrestin for normal inactivation of phototransduction. Neuron 2008, 59:462-474. 10.1016/j.neuron.2008.06.011, 2610856, 18701071.
62. Reese BE, Raven MA, Stagg SB. Afferents and homotypic neighbors regulate horizontal cell morphology, connectivity, and retinal coverage. J Neurosci 2005, 25:2167-2175. 10.1523/JNEUROSCI.4876-04.2005, 15745942.
63. Stacy RC, Demas J, Burgess RW, Sanes JR, Wong RO. Disruption and recovery of patterned retinal activity in the absence of acetylcholine. J Neurosci 2005, 25:9347-9357. 10.1523/JNEUROSCI.1800-05.2005, 16221843.