Kainate receptor subunit diversity underlying response diversity in retinal Off bipolar cells

Journal of Physiology

Volumn 592, Issue 7, 2014, Pages 1457-1477

  Lindstrom, Sarah H ^a   Ryan, David G ^a   Shi, Jun ^a   Devries, Steven H ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPA RECEPTOR; GLUTAMIC ACID; KAINATE RECEPTOR SUBUNIT 1; KAINATE RECEPTOR SUBUNIT 2; KAINATE RECEPTOR SUBUNIT 3; KAINATE RECEPTOR SUBUNIT 5; KAINIC ACID RECEPTOR; NEUROPILIN AND TOLLOID LIKE PROTEIN 1; NEUROPILIN AND TOLLOID LIKE PROTEIN 2; UNCLASSIFIED DRUG; GLUK1 KAINATE RECEPTOR; GLUK3 KAINATE RECEPTOR; PROTEIN SUBUNIT;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EXCITATORY POSTSYNAPTIC POTENTIAL; ICTIDOMYS TRIDECIMLINEATUS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; NEUROTRANSMITTER RELEASE; NONHUMAN; PRIORITY JOURNAL; RETINA BIPOLAR GANGLION CELL; SCIURIDAE; SYNAPTIC TRANSMISSION; ANIMAL; DRUG EFFECTS; GENETICS; METABOLISM; PROTEIN SUBUNIT; RETINA CONE; TIME;

ANIMALS; EXCITATORY POSTSYNAPTIC POTENTIALS; GLUTAMIC ACID; PROTEIN SUBUNITS; RECEPTORS, KAINIC ACID; RETINAL BIPOLAR CELLS; RETINAL CONE PHOTORECEPTOR CELLS; SCIURIDAE; SYNAPTIC TRANSMISSION; TIME FACTORS;

EID: 84897062589     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2013.265033     Document Type: Article

References (71)

1. Alt A, Weiss B, Ogden AM, Knauss JL, Oler J, Ho K, Large TH & Bleakman D (2004). Pharmacological characterization of glutamatergic agonists and antagonists at recombinant human homomeric and heteromeric kainate receptors in vitro. Neuropharmacology 46, 793-806.
2. 3H]UBP310. Molecular Pharmacology 78, 1036-1045.
3. Barberis A, Sachidhanandam S & Mulle C (2008). GluR6/KA2 kainate receptors mediate slow-deactivating currents. J Neurosci 28, 6402-6406.
4. Bowie D & Mayer ML. (1995). Inward rectification of both AMPA and kainate subtype glutamate receptors generated by polyamine-mediated ion channel block. Neuron 15, 453-462.
5. Buldyrev I, Puthussery T & Taylor WR (2012). Synaptic pathways that shape the excitatory drive in an OFF retinal ganglion cell. J Neurophysiol 107, 1795-1807.
6. Burmeister M, Novak J, Liang MY, Basu S, Ploder L, Hawes NL, Vidgen D, Hoover F, Goldman D, Kalnins VI, Roderick TH, Taylor BA, Hankin MH & McInnes RR (1996). Ocular retardation mouse caused by Chx10 homeobox null allele: impaired retinal progenitor proliferation and bipolar cell differentiation. Nature Genetics 12, 376-384.
7. Burnashev N, Monyer H, Seeburg PH & Sakmann B (1992). Divalent ion permeability of AMPA receptor channels is dominated by the edited form of a single subunit. Neuron 8, 189-198.
8. Castillo PE, Malenka RC & Nicoll RA (1997). Kainate receptors mediate a slow postsynaptic current in hippocampal CA3 neurons. Nature 388, 182-186.
9. Chavez AE, Singer JH & Diamond JS (2006). Fast neurotransmitter release triggered by Ca influx through AMPA-type glutamate receptors. Nature 443, 705-708.
10. Chow RL, Volgyi B, Szilard RK, Ng D, McKerlie C, Bloomfield SA, Birch DG & McInnes RR (2004). Control of late off-centre cone bipolar cell differentiation and visual signalling by the homeobox gene Vsx1. Proc Nat Acad Sci U S A 101, 1754-1759.
11. Contractor A, Swanson GT, Sailer A, O'Gorman S & Heinemann SF (2000). Identification of the kainate receptor subunits underlying modulation of excitatory synaptic transmission in the CA3 region of the hippocampus. J Neurosci 20, 8269-8278.
12. Copits BA, Robbins JS, Frausto S & Swanson GT (2011). Synaptic targeting and functional modulation of GluK1 kainate receptors by the auxiliary neuropilin and tolloid-like (NETO) proteins. J Neurosci 31, 7334-7340.
13. Copits BA & Swanson GT (2012). Dancing partners at the synapse: auxiliary subunits that shape kainate receptor function. Nat Rev Neurosci 13, 675-686.
14. Cossart R, Epsztein J, Tyzio R, Becq H, Hirsch J, Ben-Ari Y & Crepel V (2002). Quantal release of glutamate generates pure kainate and mixed AMPA/kainate EPSCs in hippocampal neurons. Neuron 35, 147-159.
15. Coussen F (2009). Molecular determinants of kainate receptor trafficking. Neuroscience 158, 25-35.
16. Cui C & Mayer ML (1999). Heteromeric kainate receptors formed by the coassembly of GluR5, GluR6, and GluR7. J Neurosci 19, 8281-8291.
17. de Melo J, Qiu X, Du G, Cristante L & Eisenstat DD (2003). Dlx1, Dlx2, Pax6, Brn3b, and Chx10 homeobox gene expression defines the retinal ganglion and inner nuclear layers of the developing and adult mouse retina. J Comp Neurol 461, 187-204.
18. DeVries SH (2000). Bipolar cells use kainate and AMPA receptors to filter visual information into separate channels. Neuron 28, 847-856.
19. DeVries SH (2014). Cone bipolar cells: ON and OFF pathways in the outer retina. In The New Visual Neurosciences, ed. Werner JS & Chalupa LM, pp. 53-62. MIT Press, Cambridge, MA, USA.
20. DeVries SH, Li W & Saszik S (2006). Parallel processing in two transmitter microenvironments at the cone photoreceptor synapse. Neuron 50, 735-748.
21. DeVries SH & Schwartz EA (1999). Kainate receptors mediate synaptic transmission between cones and 'Off' bipolar cells in a mammalian retina. Nature 397, 157-160.
22. Fernandes HB, Catches JS, Petralia RS, Copits BA, Xu J, Russell TA, Swanson GT & Contractor A (2009). High-affinity kainate receptor subunits are necessary for ionotropic but not metabotropic signalling. Neuron 63, 818-829.
23. Fisher JL & Mott DD (2011). Distinct functional roles of subunits within the heteromeric kainate receptor. J Neurosci 31, 17113-17122.
24. Fisher JL & Mott DD (2013). Modulation of homomeric and heteromeric kainate receptors by the auxiliary subunit Neto1. J Physiol 591, 4711-4724.
25. Frerking M & Ohliger-Frerking P (2002). AMPA receptors and kainate receptors encode different features of afferent activity. J Neurosci 22, 7434-7443.
26. Gregor P, O'Hara BF, Yang X & Uhl GR (1993). Expression and novel subunit isoforms of glutamate receptor genes GluR5 and GluR6. Neuroreport 4, 1343-1346.
27. Hamassaki-Britto DE, Hermans-Borgmeyer I, Heinemann S & Hughes TE (1993). Expression of glutamate receptor genes in the mammalian retina: the localization of GluR1 through GluR7 mRNAs. J Neurosci 13, 1888-1898.
28. Haverkamp S, Grünert U & Wässle H (2001). Localization of kainate receptors at the cone pedicles of the primate retina. J Comp Neurol 436, 471-486.
29. Haverkamp S, Haeseleer F & Hendrickson A (2003). A comparison of immunocytochemical markers to identify bipolar cell types in human and monkey retina. Vis Neurosci 20, 589-600.
30. Heckmann M, Bufler J, Franke C & Dudel J (1996). Kinetics of homomeric GluR6 glutamate receptor channels. Biophys J 71, 1743-1750.
31. Huang YH, Dykes-Hoberg M, Tanaka K, Rothstein JD & Bergles DE (2004). Climbing fibre activation of EAAT4 transporters and kainate receptors in cerebellar Purkinje cells. J Neurosci 24, 103-111.
32. Jackman SL, Choi SY, Thoreson WB, Rabl K, Bartoletti TM & Kramer RH (2009). Role of the synaptic ribbon in transmitting the cone light response. Nat Neurosci 12, 303-310.
33. Jakobs TC, Ben Y & Masland RH (2007). Expression of mRNA for glutamate receptor subunits distinguishes the major classes of retinal neurons, but is less specific for individual cell types. Mol Vis 13, 933-948.
34. Kamboj SK, Swanson GT & Cull-Candy SG (1995). Intracellular spermine confers rectification on rat calcium-permeable AMPA and kainate receptors. J Physiol 486, 297-303.
35. Kryger Z, Galli-Resta L, Jacobs GH & Reese BE (1998). The topography of rod and cone photoreceptors in the retina of the ground squirrel. Vis Neurosci 15, 685-691.
36. Lerma J (2003). Roles and rules of kainate receptors in synaptic transmission. Nat Rev Neurosci 4, 481-495.
37. Li W & DeVries SH (2006). Bipolar cell pathways for colour and luminance vision in a dichromatic mammalian retina. Nat Neurosci 9, 669-675.
38. Light AC, Zhu Y, Shi J, Saszik S, Lindstrom S, Davidson L, Li X, Chiodo VA, Hauswirth WW, Li W & DeVries SH (2012). Organizational motifs for ground squirrel cone bipolar cells. J Comp Neurol 520, 2864-2887.
39. Mulle C, Sailer A, Perez-Otano I, Dickinson-Anson H, Castillo PE, Bureau I, Maron C, Gage FH, Mann JR, Bettler B & Heinemann SF (1998). Altered synaptic physiology and reduced susceptibility to kainate-induced seizures in GluR6-deficient mice. Nature 392, 601-605.
40. Pang JJ, Gao F, Barrow A, Jacoby RA & Wu SM (2008). How do tonic glutamatergic synapses evade receptor desensitization? J Physiol 586, 2889-2902.
41. Paternain AV, Herrera MT, Nieto MA & Lerma J (2000). GluR5 and GluR6 kainate receptor subunits coexist in hippocampal neurons and coassemble to form functional receptors. J Neurosci 20, 196-205.
42. Paternain AV, Morales M & Lerma J (1995). Selective antagonism of AMPA receptors unmasks kainate receptor-mediated responses in hippocampal neurons. Neuron 14, 185-189.
43. Perrais D, Coussen F & Mulle C (2009a). Atypical functional properties of GluK3-containing kainate receptors. J Neurosci 29, 15499-15510.
44. Perrais D, Pinheiro PS, Jane DE & Mulle C (2009b). Antagonism of recombinant and native GluK3-containing kainate receptors. Neuropharmacology 56, 131-140.
45. Pinheiro PS, Lanore F, Veran J, Artinian J, Blanchet C, Crepel V, Perrais D & Mulle C (2013). Selective block of postsynaptic kainate receptors reveals their function at hippocampal mossy fibre synapses. Cereb Cortex 23, 323-331.
46. Pinheiro PS, Perrais D, Coussen F, Barhanin J, Bettler B, Mann JR, Malva JO, Heinemann SF & Mulle C (2007). GluR7 is an essential subunit of presynaptic kainate autoreceptors at hippocampal mossy fibre synapses. Proc Nat Acad Sci U S A 104, 12181-12186.
47. Puller C, Ivanova E, Euler T, Haverkamp S & Schubert T (2013). OFF bipolar cells express distinct types of dendritic glutamate receptors in the mouse retina. Neuroscience 243, 136-148.
48. Puller C, Ondreka K & Haverkamp S (2011). Bipolar cells of the ground squirrel retina. J Comp Neurol 519, 759-774.
49. Qin P & Pourcho RG (2001). Immunocytochemical localization of kainate-selective glutamate receptor subunits GluR5, GluR6, and GluR7 in the cat retina. Brain Res 890, 211-221.
50. Rowan S & Cepko CL (2004). Genetic analysis of the homeodomain transcription factor Chx10 in the retina using a novel multifunctional BAC transgenic mouse reporter. Dev Biol 271, 388-402.
51. Schiffer HH, Swanson GT & Heinemann SF (1997). Rat GluR7 and a carboxy-terminal splice variant, GluR7b, are functional kainate receptor subunits with a low sensitivity to glutamate. Neuron 19, 1141-1146.
52. Siegert S, Cabuy E, Scherf BG, Kohler H, Panda S, Le YZ, Fehling HJ, Gaidatzis D, Stadler MB & Roska B (2012). Transcriptional code and disease map for adult retinal cell types. Nat Neurosci 15, 487-495, S481-482.
53. Sommer B, Burnashev N, Verdoorn TA, Keinanen K, Sakmann B & Seeburg PH (1992). A glutamate receptor channel with high affinity for domoate and kainate. EMBO J 11, 1651-1656.
54. Sommer B, Kohler M, Sprengel R & Seeburg PH (1991). RNA editing in brain controls a determinant of ion flow in glutamate-gated channels. Cell 67, 11-19.
55. Sterling P & Matthews G (2005). Structure and function of ribbon synapses. Trends Neurosci 28, 20-29.
56. Stöhr H, Berger C, Frohlich S & Weber BH (2002). A novel gene encoding a putative transmembrane protein with two extracellular CUB domains and a low-density lipoprotein class A module: isolation of alternatively spliced isoforms in retina and brain. Gene 286, 223-231.
57. Straub C, Hunt DL, Yamasaki M, Kim KS, Watanabe M, Castillo PE & Tomita S (2011a). Distinct functions of kainate receptors in the brain are determined by the auxiliary subunit Neto1. Nat Neurosci 14, 866-873.
58. Straub C, Zhang W & Howe JR (2011b). Neto2 modulation of kainate receptors with different subunit compositions. J Neurosci 31, 8078-8082.
59. Swanson GT, Green T, Sakai R, Contractor A, Che W, Kamiya H & Heinemann SF (2002). Differential activation of individual subunits in heteromeric kainate receptors. Neuron 34, 589-598.
60. Swanson GT & Heinemann SF (1998). Heterogeneity of homomeric GluR5 kainate receptor desensitization expressed in HEK293 cells. J Physiol 513, 639-646.
61. Szmajda BA & DeVries SH (2011). Glutamate spillover between mammalian cone photoreceptors. J Neurosci 31, 13431-13441.
62. Tang M, Pelkey KA, Ng D, Ivakine E, McBain CJ, Salter MW & McInnes RR (2011). Neto1 is an auxiliary subunit of native synaptic kainate receptors. J Neurosci 31, 10009-10018.
63. Tomita S & Castillo PE (2012). Neto1 and Neto2: auxiliary subunits that determine key properties of native kainate receptors. J Physiol 590, 2217-2223.
64. Veran J, Kumar J, Pinheiro PS, Athane A, Mayer ML, Perrais D & Mulle C (2012). Zinc potentiates GluK3 glutamate receptor function by stabilizing the ligand binding domain dimer interface. Neuron 76, 565-578.
65. Veruki ML, Mørkve SH & Hartveit E (2006). Activation of a presynaptic glutamate transporter regulates synaptic transmission through electrical signalling. Nat Neurosci 9, 1388-1396.
66. Vignes M & Collingridge GL (1997). The synaptic activation of kainate receptors. Nature 388, 179-182.
67. Wässle H, Puller C, Muller F & Haverkamp S (2009). Cone contacts, mosaics, and territories of bipolar cells in the mouse retina. J Neurosci 29, 106-117.
68. Wersinger E, Schwab Y, Sahel JA, Rendon A, Pow DV, Picaud S & Roux MJ (2006). The glutamate transporter EAAT5 works as a presynaptic receptor in mouse rod bipolar cells. J Physiol 577, 221-234.
69. Wilding TJ & Huettner JE (1995). Differential antagonism of alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid-preferring and kainate-preferring receptors by 2, 3-benzodiazepines. Mol Pharmacol 47, 582-587.
70. Wu LJ, Zhao MG, Toyoda H, Ko SW & Zhuo M (2005). Kainate receptor-mediated synaptic transmission in the adult anterior cingulate cortex. J Neurophysiol 94, 1805-1813.
71. Yan D, Yamasaki M, Straub C, Watanabe M & Tomita S (2013). Homeostatic control of synaptic transmission by distinct glutamate receptors. Neuron 78, 687-699.