Vesicular glutamate transporter 1 is required for photoreceptor synaptic signaling but not for intrinsic visual functions

Journal of Neuroscience

Volumn 27, Issue 27, 2007, Pages 7245-7255

  Johnson, Juliette ^a   Fremeau Jr , Robert T ^a   Duncan, Jacque L ^a   Rentería, René C ^a   Yang, Haidong ^a   Hua, Zhaolin ^a   Liu, Xiaorong ^a   LaVail, Matthew M ^a   Edwards, Robert H ^a   Copenhagen, David R ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

ERG; Immunohistochemistry; Multielectrode array; Photoentrainment; Pupillary light response; VEP

Indexed keywords

MELANOPSIN; VESICULAR GLUTAMATE TRANSPORTER 1; VESICULAR GLUTAMATE TRANSPORTER 2;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; MOUSE; NEUROTRANSMISSION; NONHUMAN; PHOTOREACTIVITY; PHOTORECEPTOR; PHOTOSENSITIVITY; PRIORITY JOURNAL; PUPIL REFLEX; RAT; RETINA CONE; RETINA GANGLION CELL; RETINA NERVE CELL; RETINA ROD; SIGNAL TRANSDUCTION; SYNAPSE VESICLE; VISION;

ANIMALS; EVOKED POTENTIALS, VISUAL; MICE; MICE, KNOCKOUT; PHOTIC STIMULATION; PHOTORECEPTORS; PROTEIN ISOFORMS; RATS; RATS, LONG-EVANS; RETINAL GANGLION CELLS; SIGNAL TRANSDUCTION; SYNAPSES; VESICULAR GLUTAMATE TRANSPORT PROTEIN 1; VISION;

EID: 34447126865     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0815-07.2007     Document Type: Article

References (43)

1. Barth DS, Goldberg N, Brett B, Di S (1995) The spatiotemporal organization of auditory, visual, and auditory-visual evoked potentials in rat cortex. Brain Res 678:177-190.
2. Bellocchio EE, Hu H, Pohorille A, Chan J, Pickel VM, Edwards RH (1998) The localization of the brain-specific inorganic phosphate transporter suggests a specific presynaptic role in glutamatergic transmission. J Neurosci 18:8648-8659.
3. Bellocchio EE, Reimer RJ, Fremeau Jr RT, Edwards RH (2000) Uptake of glutamate into synaptic vesicles by an inorganic phosphate transporter. Science 289:957-960.
4. Berson DM, Dunn FA, Takao M (2002) Phototransduction by retinal ganglion cells that set the circadian clock. Science 295:1070-1073.
5. Chang B, Heckenlively JR, Bayley PR, Brecha NC, Davisson MT, Hawes NL, Hirano AA, Hurd RE, Ikeda A, Johnson BA, McCall MA, Morgans CW, Nusinowitz S, Peachey NS, Rice DS, Vessey KA, Gregg RG. (2006) The nob2 mouse, a null mutation in Cacna1f: anatomical and functional abnormalities in the outer retina and their consequences on ganglion cell visual responses. Vis Neurosci 23:11-24.
6. Copenhagen DR, Jahr CE (1989) Release of endogenous excitatory amino acids from turtle photoreceptors. Nature 341:536-539.
7. Copenhagen DR, Hemila S, Reuter T (1990) Signal transmission through the dark-adapted retina of the toad (Bufo marinus). Gain, convergence, and signal/noise. J Gen Physiol 95:717-732.
8. Dick O, tom Dieck S, Altrock WD, Ammermuller J, Weiler R, Garner CC, Gundelfinger ED, Brandstatter JH (2003) The presynaptic active zone protein bassoon is essential for photoreceptor ribbon synapse formation in the retina. Neuron 37:775-786.
9. Duncan JL, LaVail MM, Yasumura D, Matthes MT, Yang H, Trautmann N, Chappelow AV, Feng W, Earp HS, Matsushima GK, Vollrath D (2003) An RCS-like retinal dystrophy phenotype in mer knockout mice. Invest Ophthalmol Vis Sci 44:826-838.
10. Duncan JL, Yang H, Doan T, Silverstein RS, Murphy GJ, Nune G, Liu X, Copenhagen D, Tempel BL, Rieke F, Krizaj D (2006) Scotopic visual signaling in the mouse retina is modulated by high-affinity plasma membrane calcium extrusion. J Neurosci 26:7201-7211.
11. Fisher LJ (1979) Development of synaptic arrays in the inner plexiform layer of neonatal mouse retina. J Comp Neurol 187:359-372.
12. Freedman MS, Lucas RJ, Soni B, von Schantz M, Munoz M, David-Gray Z, Foster R (1999) Regulation of mammalian circadian behavior by non-rod, non-cone, ocular photoreceptors. Science 284:502-504.
13. Fremeau Jr RT, Troyer MD, Pahner I, Nygaard GO, Tran CH, Reimer RJ, Bellocchio EE, Fortin D, Storm-Mathisen J, Edwards RH (2001) The expression of vesicular glutamate transporters defines two classes of excitatory synapse. Neuron 31:247-260.
14. Fremeau Jr RT, Voglmaier S, Seal RP, Edwards RH (2004a) VGLUTs define subsets of excitatory neurons and suggest novel roles for glutamate. Trends Neurosci 27:98-103.
15. Fremeau Jr RT, Kam K, Qureshi T, Johnson J, Copenhagen DR, Storm-Mathisen J, Chaudhry FA, Nicoll RA, Edwards RH (2004b) Vesicular glutamate transporters 1 and 2 target to functionally distinct synaptic release sites. Science 304:1815-1819.
16. Fujiyama F, Hioki H, Tomioka R, Taki K, Tamamaki N, Nomura S, Okamoto K, Kaneko T (2003) Changes of immunocytochemical localization of vesicular glutamate transporters in the rat visual system after the retinofugal denervation. J Comp Neurol 465:234-249.
17. Fyk-Kolodziej B, Dzhagaryan A, Qin P, Pourcho RG (2004) Localization of three vesicular glutamate transporters in the cat retina. J Comp Neurol 475:518-530.
18. Haeseleer F, Imanishi Y, Maeda T, Possin DE, Maeda A, Lee A, Rieke F, Palczewski K (2004) Free in PMC Essential role of Ca2+-binding protein 4, a Cav1.4 channel regulator, in photoreceptor synaptic function. Nat Neurosci 7:1079-1087.
19. Hannibal J, Fahrenkrug J (2004) Melanopsin containing retinal ganglion cells are light responsive from birth. NeuroReport 15:2317-2320.
20. Hao H, Rivkees SA (1999) The biological clock of very premature primate infants is responsive to light. Proc Natl Acad Sci USA 96:2426-2429.
21. Hattar S, Liao HW, Takao M, Berson DM, Yau KW (2002) Melanopsin- containing retinal ganglion cells: architecture, projections, and intrinsic photosensitivity. Science 295:1065-1070.
22. Haverkamp S, Wässle H (2004) Characterization of an amacrine cell type of the mammalian retina immunoreactive for vesicular glutamate transporter 3. J Comp Neurol 468:251-263.
23. Johnson J, Tian N, Caywood MS, Reimer RJ, Edwards RH, Copenhagen DR (2003) Vesicular neurotransmitter transporter expression in developing postnatal rodent retina: GABA and glycine precede glutamate. J Neurosci 23:518-529.
24. Johnson J, Sherry DM, Liu X, Fremeau Jr RT, Seal RP, Edwards RH, Copenhagen DR (2004) Vesicular glutamate transporter 3 expression identifies glutamatergic amacrine cells in the rodent retina. J Comp Neurol 477:386-398.
25. Kang Derwent JJ, Linsenmeier RA (2001) Intraretinal analysis of the a-wave of the electroretinogram (ERG) in dark-adapted intact cat retina. Vis Neurosci 18:353-363.
26. Land PW, Kyonka E, Shamalla-Hannah L (2004) Vesicular glutamate transporters in the lateral geniculate nucleus: expression of VGLUT2 by retinal terminals. Brain Res 996:251-254.
27. Lin W, McKinney K, Liu L, Lakhlani S, Jennes L (2003) Distribution of vesicular glutamate transporter-2 messenger ribonucleic Acid and protein in the septum-hypothalamus of the rat. Endocrinology 144:662-670.
28. Liu X, Green CB (2002) Circadian regulation of nocturnin transcription by phosphorylated CREB in Xenopus retinal photoreceptor cells. Mol Cell Biol 22:7501-7511.
29. Lucas RJ, Douglas RH, Foster RG (2001) Characterization of an ocular photopigment capable of driving pupillary constriction in mice. Nat Neurosci 4:621-626.
30. Peachey NS, Goto Y, al-Ubaidi MR, Naash MI (1993) Properties of the mouse cone-mediated electroretinogram during light adaptation Neurosci Lett 162:9-11.
31. 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.
32. Ralph RJ, Caine SB (2005) Dopamine D1 and D2 agonist effects on prepulse inhibition and locomotion: comparison of Sprague-Dawley rats to Swiss-Webster, 129X1/SvJ, C57BL/6J, and DBA/2J mice. J Pharmacol Exp Ther 312:733-741.
33. Rentería RC, Tian N, Cang J, Nakanishi S, Stryker MP, Copenhagen DR (2006) Intrinsic ON responses of the retinal OFF pathway are suppressed by the ON pathway. J Neurosci 26:11857-11869.
34. Robson JG, Frishman LJ (1995) Response linearity and kinetics of the cat retina: the bipolar cell component of the dark-adapted electroretinogram. Vis Neurosci 12:837-850.
35. Schwartz EA (1986) Synaptic transmission in amphibian retinae during conditions unfavourable for calcium entry into presynaptic terminals. J Physiol (Lond) 376:411-428.
36. Sekaran S, Lupi D, Jones SL, Sheely CJ, Hattar S, Yau KW, Lucas RJ, Foster RG, Hankins MW (2005) Melanopsin-dependent photoreception provides earliest light detection in the mammalian retina. Curr Biol 15:1099-1107.
37. Sherry DM, Wang MM, Bates J, Frishman LJ (2003) 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 465:480-498.
38. Takamori S, Rhee JS, Rosenmund C, Jahn R (2000) Identification of a vesicular glutamate transporter that defines a glutamatergic phenotype in neurons. Nature 407:189-194.
39. Tian N, Copenhagen DR (2003) Visual stimulation is required for refinement of ON and OFF pathways in postnatal retina. Neuron 39:85-96.
40. Tu DC, Zhang D, Demas J, Slutsky EB, Provencio I, Holy TE, Van Gelder RN (2005) Physiologic diversity and development of intrinsically photosensitive retinal ganglion cells. Neuron 48:987-999.
41. Van Gelder RN (2003) Making (a) sense of non-visual ocular photoreception. Trends Neurosci 26:458-461.
42. Wässle H, Regus-Leidig H, Haverkamp S (2006) Expression of the vesicular glutamate transporter vGluT2 in a subset of cones of the mouse retina. J Comp Neurol 496:544-555.
43. Ziegler DR, Cullinan WE, Herman JP (2002) Distribution of vesicular glutamate transporter mRNA in rat hypothalamus. J Comp Neurol 448:217-229.