CoChat
Sign Up
Cited by 410Neuroscience and Neuropharmacology ResearchReceptor Mechanisms and SignalingNicotinic Acetylcholine Receptors Study

The Expanding Social Network of Ionotropic Glutamate Receptors: TARPs and Other Transmembrane Auxiliary Subunits

Open access
Jackson, Alexander C., Nicoll, Roger A.·2011·Neuron
DOI 10.1016/j.neuron.2011.04.007PMC PMC3119519
Open this paper in CoChat — free accountOpen PDF

Abstract

Ionotropic glutamate receptors (iGluRs) underlie rapid, excitatory synaptic signaling throughout the CNS. After years of intense research, our picture of iGluRs has evolved from them being companionless in the postsynaptic membrane to them being the hub of dynamic supramolecular signaling complexes, interacting with an ever-expanding litany of other proteins that regulate their trafficking, scaffolding, stability, signaling, and turnover. In particular, the discovery that transmembrane AMPA receptor regulatory proteins (TARPs) are AMPA receptor auxiliary subunits that are critical determinants of their trafficking, gating, and pharmacology has changed the way we think about iGluR function. Recently, a number of novel transmembrane proteins have been uncovered that may also serve as iGluR auxiliary proteins. Here we review pivotal developments in our understanding of the role of TARPs in AMPA receptor trafficking and gating, and provide an overview of how newly discovered transmembrane proteins expand our view of iGluR function in the CNS.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1016/j.neuron.2011.04.007

Cites

9 of 9 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Binding of AMPAR/TARPs to PSD-95 is important for synaptic targeting and LTP.

    “Since the binding of AMPAR/TARPs to the PSD protein PSD-95 is known to be important for synaptic targeting and LTP (278, 279)”

    From Synaptic memory and CaMKII (2023) · cites this paper as [279]

    In “The role of TARPs in AMPAR surface trafficking and synaptic targeting” (page not provided), the review says stargazin binds PSD-95 and that this interaction is important for AMPAR synaptic targeting. The same section reports that a phospho-null stargazin construct prevents LTP, but it does not establish that binding to PSD-95 itself is important for LTP. (LLM, conf=0.84)

    Experimental — accuracy not yet measured

  • AMPARs are decorated by auxiliary subunits that control their synthesis, trafficking, and biophysical properties.

    “Evidence has accumulated over the past decade indicating that AMPARs are not stand-alone receptors; rather, they are decorated by numerous types of auxiliary subunits that control the synthesis, trafficking, and biophysical properties of these receptors (278–281).”

    From Synaptic memory and CaMKII (2023) · cites this paper as [279]

    The sections “Transmembrane AMPAR auxiliary subunits beyond TARPs” and “TARPs form an integral component of native AMPAR complexes” describe auxiliary subunits associated with AMPARs that affect trafficking and gating. “TARPs and AMPAR biogenesis” reports evidence for a role in biosynthesis and ER export, but says whether TARPs act in earlier steps such as folding and subunit assembly remains undetermined. The claim overstates the evidence by saying auxiliary subunits control AMPAR synthesis. (LLM, conf=0.84)

    Experimental — accuracy not yet measured

  • Delivery of AMPARs to synapses requires binding of TARPs via their PDZ binding motifs to PSD-95.

    “It is now well established that the delivery of AMPARs to synapses requires the binding of TARPs, via their PDZ binding motifs (PBMs), to PSD-95 (278, 279, 286, 289, 294).”

    From Synaptic memory and CaMKII (2023) · cites this paper as [279]

  • Synaptic capture of AMPARs requires the PDZ domain interaction between TARPs and PSD-95.

    “It is also agreed that the synaptic capture of AMPARs requires the PDZ domain interaction between TARPs and PSD-95 (275, 279, 294, 440).”

    From Synaptic memory and CaMKII (2023) · cites this paper as [279]

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 188

  1. Abouda H Hizem Y Gargouri A Depienne C Bouteiller D Riant F Tournier-Lasserve E Gourfinkel-An I LeGuern E Gouider R Familial form of typical childhood absence epilepsy in a consanguineous context Epilepsia 2010 51 1889 1893 20561025
  2. Arbuzova A Schmitz AA Vergères G Cross-talk unfolded: MARCKS proteins Biochem. J 2002 362 1 12 11829734 PMC1222354
  3. Arikkath J Campbell KP Auxiliary subunits: essential components of the voltage-gated calcium channel complex Curr. Opin. Neurobiol 2003 13 298 307 12850214
  4. Armstrong N Sun Y Chen GQ Gouaux E Structure of a glutamate-receptor ligand-binding core in complex with kainate Nature 1998 395 913 917 9804426
  5. Ascher. P Nowak L Quisqualate- and kainate-activated channels in mouse central neurones in culture J. Physiol 1988 399 227 245 2457088 PMC1191661
  6. Bats C Groc L Choquet D The interaction between Stargazin and PSD-95 regulates AMPA receptor surface trafficking Neuron 2007 53 719 734 17329211
  7. Bedoukian MA Weeks AM Partin KM Different domains of the AMPA receptor direct stargazin-mediated trafficking and stargazin-mediated modulation of kinetics J. Biol. Chem 2006 281 23908 23921 16793768
  8. Bedoukian MA Whitesell JD Peterson EJ Clay CM Partin KM The stargazin C terminus encodes an intrinsic and transferable membrane sorting signal J. Biol. Chem 2008 283 1597 1600 17986442
  9. Beenhakker MP Huguenard JR Neurons that fire together also conspire together: is normal sleep circuitry hijacked to generate epilepsy? Neuron 2009 62 612 632 19524522 PMC2748990
  10. Bellamy TC Interactions between Purkinje neurones and Bergmann glia Cerebellum 2006 5 116 126 16818386
  11. Beneyto M Meador-Woodruff JH Lamina-specific abnormalities of AMPA receptor trafficking and signaling molecule transcripts in the prefrontal cortex in schizophrenia Synapse 2006 60 585 598 16983646
  12. Bochet P Audinat E Lambolez B Crépel F Rossier J Iino M Tsuzuki K Ozawa S Subunit composition at the single-cell level explains functional properties of a glutamate-gated channel Neuron 1994 12 383 388 7509161
  13. Boehm J Malinow R AMPA receptor phosphorylation during synaptic plasticity Biochem. Soc. Trans 2005 33 1354 1356 16246117
  14. Bökel C Dass S Wilsch-Bräuninger M Roth S Drosophila Cornichon acts as cargo receptor for ER export of the TGFalpha-like growth factor Gurken Development 2006 133 459 470 16396907
  15. Bork P Beckmann G The CUB domain. A widespread module in developmentally regulated proteins J. Mol. Biol 1993 231 539 545 8510165
  16. Bowie D Mayer ML Inward rectification of both AMPA and kainate subtype glutamate receptors generated by polyamine-mediated ion channel block Neuron 1995 15 453 462 7646897
  17. Bredt DS Nicoll RA AMPA receptor trafficking at excitatory synapses Neuron 2003 40 361 379 14556714
  18. Brockie PJ Maricq AV In a pickle: is cornichon just relish or part of the main dish? Neuron 2010 68 1017 1019 21172604 PMC4076775
  19. Burgess DL Davis CF Gefrides LA Noebels JL Identification of three novel Ca2+ channel gamma subunit genes reveals molecular diversification by tandem and chromosome duplication Genome Res 1999 9 1204 1213 10613843 PMC311002
  20. Burgess DL Gefrides LA Poreman PJ Noebels JL A cluster of three novel Ca2+ channel γ subunit genes on chromasome 19q13.4: evolution and expression profile of the γ subunit gene family Genomics 2001 71 339 350 11170751
  21. Carroll RC Nicoll RA Malenka RC Effects of PKA and PKC on miniature excitatory postsynaptic currents in CA1 pyramidal cells J. Neurophysiol 1998 80 2797 2800 9819284
  22. Castillo PE Malenka RC Nicoll RA Kainate receptors mediate a slow postsynaptic current in hippocampal CA3 neurons Nature 1997 388 182 186 9217159
  23. Castro CP Piscopo D Nakagawa T Derynck R Cornichon regulates transport and secretion of TGFalpha-related proteins in metazoan cells J. Cell Sci 2007 120 2454 2466 17607000
  24. Chen L Bao S Qiao X Thompson RF Impaired cerebellar synapse maturation in waggler, a mutant mouse with a disrupted neuronal calcium channel gamma subunit Proc. Natl. Acad. Sci. U S A 1999 96 12132 12137 10518588 PMC18424
  25. Chen L El-Husseini A Tomita S Bredt DS Nicoll RA Stargazin differentially controls the trafficking of alpha-amino-3-hydroxyl-5-methyl-4-isoxazolepropionate and kainate receptors Mol. Pharmacol 2003 64 703 706 12920207
  26. Chetkovich D Thalamic reticular neurons are unexcited by new stargazer seizure mechanism Epilepsy. Curr 2009 9 59 61 19421384 PMC2673410
  27. Chetkovich DM Chen L Stocker TJ Nicoll RA Bredt DS Phosphorylation of the postsynaptic density-95 (PSD-95)/discs large/zona occludens-1 binding site of stargazin regulates binding to PSD-95 and synaptic targeting of AMPA receptors J. Neurosci 2002 22 5791 5796 12122038 PMC6757934
  28. Cho CH St-Gelais F Zhang W Tomita S Howe JR Two families of TARP isoforms that have distinct effects on the kinetic properties of AMPA receptors and synaptic currents Neuron 2007 55 890 904 17880893
  29. Choi J Ko J Park E Lee JR Yoon J Lim S Kim E Phosphorylation of stargazin by protein kinase A regulates its interaction with PSD-95 J. Biol. Chem 2002 277 12359 12363 11805122
  30. Cokić B Stein V Stargazin modulates AMPA receptor antagonism Neuropharmacol 2008 54 1062 1070 18378265
  31. Coleman SK Möykkynen T Jouppila A Koskelainen S Rivera C Korpi ER Keinänen K Agonist occupancy is essential for forward trafficking of AMPA receptors J. Neurosci 2009 29 303 312 19144831 PMC6664942
  32. Collingridge GL Isaac JT Wang YT Receptor trafficking and synaptic plasticity Nat. Rev. Neurosci 2004 5 952 962 15550950
  33. Colquhoun D Jonas P Sakmann B Action of brief pulses of glutamate on AMPA/kainate receptors in patches from different neurones of rat hippocampal slices J. Physiol 1992 458 261 287 1338788 PMC1175155
  34. Conti F Weinberg RJ Shaping excitation at glutamatergic synapses Trends. Neurosci 1999 22 451 458 10481192
  35. Coombs ID Cull-Candy SG Transmembrane AMPA receptor regulatory proteins and AMPA receptor function in the cerebellum Neurosci 2009 162 656 665 PMC3217091 19185052
  36. Cull-Candy SG Usowicz MM Multiple-conductance channels activated by excitatory amino acids in cerebellar neurons Nature 1987 325 525 528 2433594
  37. Dai S Hall DD Hell JW Supramolecular assemblies and localized regulation of voltage-gated ion channels Physiol. Rev 2009 89 411 452 19342611 PMC2733249
  38. Dakoji S Tomita S Karimzadegan S Nicoll RA Bredt DS Interaction of transmembrane AMPA receptor regulatory proteins with multiple membrane associated guanylate kinases Neuropharmacol 2003 45 849 856 14529722
  39. Derkach VA Oh MC Guire ES Soderling TR Regulatory mechanisms of AMPA receptors in synaptic plasticity Nat. Rev. Neurosci 2007 8 101 113 17237803
  40. Díaz E Ge Y Yang YH Loh KC Serafini TA Okazaki Y Hayashizaki Y Speed TP Ngai J Scheiffele P Molecular analysis of gene expression in the developing pontocerebellar projection system Neuron 2002 36 417 434 12408845
  41. Díaz E SynDIG1 regulation of synaptic AMPA receptor targeting Commun. Integr. Biol 2010a 3 347 349 PMC2928314 20798822
  42. Díaz E Regulation of AMPA receptors by transmembrane accessory proteins Eur. J. Neurosci 2010b 32 261 268 20946114
  43. DiPasquale E Keegan KD Noebels JL Increased excitability and inward rectification in layer V cortical pyramidal neurons in the epileptic mutant mouse Stargazer J. Neurophys 1997 77 621 631 9065835
  44. Dolphin AC Calcium channel diversity: multiple roles of calcium channel subunits Curr. Opin. Neurobiol 2009 19 237 244 19559597
  45. Edmonds B Gibb AJ Colquhoun D Mechanisms of activation of glutamate receptors and the time course of excitatory synaptic currents Ann. Rev. Physiol 1995 57 495 519 7778875
  46. El-Husseini AE Schnell E Dakoji S Sweeney N Zhou Q Prange O Gauthier-Campbell C Aguilera-Moreno A Nicoll RA Bredt DS Synaptic strength regulated by palmitate cycling on PSD-95 Cell 2002 108 849 863 11955437
  47. Elias GM Nicoll RA Synaptic trafficking of glutamate receptors by MAGUK scaffolding proteins Trends Cell Biol 2007 17 343 352 17644382
  48. Everett KV Chioza B Aicardi J Aschauer H Brouwer O Callenbach P Covanis A Dulac O Eeg-Olofsson O Feucht M Friis M Goutieres F Guerrini R Heils A Kjeldsen M Lehesjoki AE Makoff A Nabbout R Olsson I Sander T Sirén A McKeigue P Robinson R Taske N Rees M Gardiner M Linkage and association analysis of CACNG3 in childhood absence epilepsy Eur. J 2007 15 463 472 PMC2556708 17264864
  49. Farrant M Cull-Candy SG Neuroscience. AMPA receptors-another twist? Science 2010 327 1463 1465 20299582
  50. Feng W Zhang M Organization and dynamics of PDZ-domain-related supramodules in the postsynaptic density Nat. Rev. Neurosci 2009 10 87 99 19153575
  51. Ferrario CR Loweth JA Milovanovic M Wang X Wolf ME Distribution of AMPA receptor subunits and TARPs in synaptic and extrasynaptic membranes of the adult rat nucleus accumbens Neurosci. Lett 2010 490 180 184 21182898 PMC3038183
  52. Fukata Y Tzingounis AV Trinidad JC Fukata M Burlingame AL Nicoll RA Bredt DS Molecular constituents of neuronal AMPA receptors J. Cell Biol 2005 169 399 404 15883194 PMC2171936
  53. Fukaya M Yamazaki M Sakimura K Watanabe M Spatial diversity in gene expression for VDCC-gamma subunit family in developing and adult mouse brains Neurosci. Res 2005 53 376 383 16171881
  54. Geiger JR Melcher T Koh DS Sakmann B Seeburg PH Jonas P Monyer H Relative abundance of subunit mRNAs determines gating and Ca2+ permeability of AMPA receptors in principal neurons and interneurons in rat CNS Neuron 1995 15 193 204 7619522
  55. Silberberg G Levit A Collier D St. Clair D Munro J Kerwin RW Tondo L Floris G Breen G Navon R Stargazin involvement with bipolar disorder and response to lithium treatment Pharmacogenet. Genomics 2008 18 403 412 18408563
  56. Greger IH Ziff EB Penn AC Molecular determinants of AMPA receptor subunit assembly Trends Neurosci 2007 30 407 416 17629578
  57. Guzman SJ Jonas P Beyond TARPs: the growing list of auxiliary AMPAR subunits Neuron 2010 66 8 10 20399724
  58. Hall RA Hansen A Andersen PH Soderling TR Surface expression of the AMPA receptor subunits GluR1, GluR2, and GluR4 in stably transfected baby hamster kidney cells J. Neurochem 1997 68 625 630 9003049
  59. Hansel C Linden DJ D'Angelo E Beyond parallel fiber LTD: the diversity of synaptic and non-synaptic plasticity in the cerebellum Nat. Neurosci 2001 4 467 475 11319554
  60. Hashimoto K Fukaya M Qiao X Sakimura K Watanabe M Kano M Impairment of AMPA receptor function in cerebellar granule cells of ataxic mutant mouse stargazer J. Neurosci 1999 19 6027 6036 10407040 PMC6783074
  61. Hayashi Y Shi SH Esteban JA Piccini A Poncer JC Malinow R Driving AMPA receptors into synapses by LTP and CaMKII: requirement for GluR1 and PDZ domain interaction Science 2000 287 2262 2267 10731148
  62. Hollmann M Hartley M Heinemann S Ca2+ permeability of KA-AMPA-gated glutamate receptor channels depends on subunit composition Science 1991 252 851 853 1709304
  63. Hoshino H Uchida T Otsuki T Kawamoto S Okubo K Takeichi M Chisaka O Cornichon-like protein facilitates secretion of HB-EGF and regulates proper development of cranial nerves Mol. Biol. Cell 2007 18 1143 1152 17229890 PMC1839001
  64. Huguenard JR McCormick DA Thalamic synchrony and dynamic regulation of global forebrain oscillations Trends Neurosci 2007 30 350 356 17544519
  65. Hwang SY Oh B Zhang Z Miller W Solter D Knowles BB The mouse cornichon gene family Dev. Genes Evol 1999 209 120 125 10022955
  66. Iino M Goto K Kakegawa W Okado H Sudo M Ishiuchi S Miwa A Takayasu Y Saito I Tsuzuki K Ozawa S Glia-synapse interaction through Ca2+-permeable AMPA receptors in Bergmann glia Science 2001 292 926 929 11340205
  67. Inamura M Itakura M Okamoto H Hoka S Mizoguchi A Fukazawa Y Shigemoto R Yamamori S Takahashi M Differential localization and regulation of stargazin-like protein, gamma-8 and stargazin in the plasma membrane of hippocampal and cortical neurons Neurosci. Res 2006 55 45 53 16516319
  68. Isaac JT Ashby M McBain CJ The role of the GluR2 subunit in AMPA receptor function and synaptic plasticity Neuron 2007 54 859 871 17582328
  69. Jackson AC Nicoll RA Neuroscience: AMPA receptors get 'pickled' Nature 2009 458 585 586 19340072 PMC2716117
  70. Jackson AC Nicoll RA Stargazin (TARP γ-2) is required for compartment- specific AMPA receptor trafficking and synaptic plasticity in cerebellar stellate cells J. Neurosci 2011a 31 3939 3952 21411637 PMC3104604
  71. Jackson AC Milstein AD Soto D Farrant M Cull-Candy SG Nicoll RA Probing TARP modulation of AMPA receptor channel conformation with polyamine toxins J. Neurosci 2011b (In press) PMC3164836 21593335
  72. Jahr CE Stevens CF Glutamate activates multiple single channel conductances in hippocampal neurons Nature 1987 325 522 525 2433593
  73. Jay SD Ellis SB McCue AF Williams ME Vedvick TS Harpold MM Campbell KP Primary structure of the gamma subunit of the DHP-sensitive calcium channel from skeletal muscle Science 1990 248 490 492 2158672
  74. Jin R Banke TG Mayer ML Traynelis SF Gouaux E Structural basis for partial agonist action at ionotropic glutamate receptors Nat. Neurosci 2003 6 803 810 12872125
  75. Jonas P Spruston N Mechanisms shaping glutamate-mediated excitatory postsynaptic currents in the CNS Curr. Opin. Neurobiol 1994 4 366 372 7522678
  76. Jonas P The time course of signaling at central glutamatergic synapses News in Phys. Sci 2000 15 83 89 11390884
  77. Kalashnikova E Lorca RA Kaur I Barisone GA Li B Ishimaru T Trimmer JS Mohapatra DP Díaz E SynDIG1: an activity-regulated, AMPA-receptor-interacting transmembrane protein that regulates excitatory synapse development Neuron 2010 65 80 93 20152115 PMC2822728
  78. Kamboj SK Swanson GT Cull-Candy SG Intracellular spermine confers rectification on rat calcium-permeable AMPA and kainate receptors J. Physiol 1995 486 297 303 7473197 PMC1156521
  79. Kang MG Chen CC Felix R Letts VA Frankel WN Mori Y Campbell KP Biochemical and biophysical evidence for gamma 2 subunit association with neuronal voltage-activated Ca2+ channels J. Biol. Chem 2001 276 32917 32924 11441000
  80. Kang MG Chen CC Wakamori M Hara Y Mori Y Campbell KP A functional AMPA receptor-calcium channel complex in the postsynaptic membrane Proc. Natl. Acad. Sci. USA 2006 103 5561 5566 16567654 PMC1459393
  81. Kato AS Zhou W Milstein AD Knierman MD Siuda ER Dotzlaf JE Yu H Hale JE Nisenbaum ES Nicoll RA Bredt DS New transmembrane AMPA receptor regulatory protein isoform, gamma-7, differentially regulates AMPA receptors J. Neurosci 2007 27 4969 4977 17475805 PMC6672084
  82. Kato AS Siuda ER Nisenbaum ES Bredt DS AMPA receptor subunit-specific regulation by a distinct family of type II TARPs Neuron 2008 59 986 996 18817736
  83. Kato AS Gill MB Yu H Nisenbaum ES Bredt DS TARPs differentially decorate AMPA receptors to specify neuropharmacology Trends Neurosci 2010 33 241 248 20219255
  84. Kerchner GA Nicoll RA Silent synapses and the emergence of a postsynaptic mechanism for LTP Nat. Rev. Neurosci 2008 9 813 825 18854855 PMC2819160
  85. Kessels HW Kopec CD Klein ME Malinow R Roles of stargazin and phosphorylation in the control of AMPA receptor subcellular distribution Nat. Neurosci 2009 12 888 896 19543281 PMC3922706
  86. Kim E Sheng M PDZ domain proteins of synapses Nat. Rev. Neurosci 2004 5 771 781 15378037
  87. Kim KS Yan D Tomita S Assembly and stoichiometry of the AMPA receptor and transmembrane AMPA receptor regulatory protein complex J. Neurosci 2010 30 1064 1072 20089915 PMC2821155
  88. Kinney GA Overstreet LS Slater NT Prolonged physiological entrapment of glutamate in the synaptic cleft of cerebellar unipolar brush cells J. Neurophysiol 1997 78 1320 1333 9310423
  89. Klugbauer N Dai S Specht V Lacinová L Marais E Bohn G Hofmann F A family of gamma-like calcium channel subunits FEBS Lett 2000 470 189 197 10734232
  90. Knight HM Maclean A Irfan M Naeem F Cass S Pickard BS Muir WJ Blackwood DH Ayub M Homozygosity mapping in a family presenting with schizophrenia, epilepsy and hearing impairment Eur. J. Hum. Genet 2008 16 750 758 18322454
  91. Koh DS Burnashev N Jonas P Block of native Ca2+-permeable AMPA receptors in rat brain by intracellular polyamines generates double rectification J. Physiol 1995 486 305 312 7473198 PMC1156522
  92. Körber C Werner M Hoffmann J Sager C Tietze M Schmid SM Kott S Hollmann M Stargazin interaction with alpha-amino-3-hydroxy-5-methyl-4-isoxazole propionate (AMPA) receptors is critically dependent on the amino acid at the narrow constriction of the ion channel J. Biol. Chem 2007a 282 18758 18766 17483093
  93. Körber C Werner M Kott S Ma ZL Hollmann M The transmembrane AMPA receptor regulatory protein gamma 4 is a more effective modulator of AMPA receptor function than stargazin (gamma 2) J. Neurosci 2007b 27 8442 8447 PMC6673051 17670991
  94. Kott S Werner M Korber C Hollmann M Electrophysiological properties of AMPA receptors are differentially modulated depending on the associated member of the TARP family J. Neurosci 2007 27 3780 3789 17409242 PMC6672393
  95. Kott S Sager C Tapken D Werner M Hollmann M Comparative analysis of the pharmacology of GluR1 in complex with transmembrane AMPA receptor regulatory proteins gamma2, gamma3, gamma4, and gamma8 Neurosci 2009 158 78 88 18304748
  96. Lee HK Synaptic plasticity and phosphorylation Pharmacol Ther 2006 112 810 832 16904750 PMC2748765
  97. Lee SH Govindaiah G Cox CL Selective excitatory actions of DNQX and CNQX in rat thalamic neurons J. Neurophys 2010 103 1728 1734 PMC2853297 20107128
  98. Letts VA Valenzuela A Kirley JP Sweet HO Davisson MT Frankel WN Genetic and physical maps of the stargazer locus on mouse chromosome 15 Genomics 1997 43 62 68 9226373
  99. Letts VA Felix R Biddlecome GH Arikkath J Mahaffey CL Valenzuela A Bartlett FS 2nd Mori Y Campbell KP Frankel WN The mouse stargazer gene encodes a neuronal Ca2+-channel gamma subunit Nat. Genetics 1998 19 340 347 9697694
  100. Letts VA Mahaffey CL Beyer B Frankel WN A targeted mutation in Cacng4 exacerbates spike-wave seizures in stargazer (Cacng2) mice Proc. Natl. Acad. Sci. USA 2005 102 2123 2128 15677329 PMC548574
  101. Letts VA Stargazer-a mouse to seize! Epilepsy Curr 2005 5 161 165 16175212 PMC1201632
  102. Liu YL Fann CS Liu CM Chen WJ Wu JY Hung SI Chen CH Jou YS Liu SK Hwang TJ Hsieh MH Chang CC Yang WC Lin JJ Chou FH Faraone SV Tsuang MT Hwu HG RASD2, MYH9, and CACNG2 genes at chromosome 22q12 associated with the subgroup of schizophrenia with non-deficit in sustained attention and executive function Biol. Psychiatry 2008 64 789 796 18571626
  103. Maccaferri G Dingledine R Complex effects of CNQX on CA1 interneurons of the developing rat hippocampus Neuropharmacol 2002 43 523 529 12367599
  104. Malenka RC Bear MF LTP and LTD: an embarrassment of riches Neuron 2004 44 5 21 15450156
  105. Mayer ML Glutamate receptor ion channels Curr. Opin. Neurobiol 2005 15 282 288 15919192
  106. McBain CJ Dingledine R Heterogeneity of synaptic glutamate receptors on CA3 stratum radiatum interneurones of rat hippocampus J. Physiol 1993 462 373 392 8101227 PMC1175306
  107. Menuz K Stroud RM Nicoll RA Hays FA TARP auxiliary subunits switch AMPA receptor antagonists into partial agonists Science 2007 318 815 817 17975069
  108. Menuz K Nicoll RA Loss of inhibitory neuron AMPA receptors contributes to ataxia and epilepsy in stargazer mice J. Neurosci 2008 28 10599 10603 18923036 PMC3164835
  109. Menuz K O'Brien JL Karmizadegan S Bredt DS Nicoll RA TARP redundancy is critical for maintaining AMPA receptor function J. Neurosci 2008 28 8740 8746 18753375 PMC3159041
  110. Menuz K Kerchner GA O'Brien JL Nicoll RA Critical role for TARPs in early development despite broad functional redundancy Neuropharmacol 2009 56 22 29 PMC3111090 18634809
  111. Merrill MA Chen Y Strack S Hell JW Activity-driven postsynaptic translocation of CaMKII Trends Pharmacol. Sci 2005 26 645 653 16253351
  112. Milstein AD Zhou W Karimzadegan S Bredt DS Nicoll RA TARP subtypes differentially and dose-dependently control synaptic AMPA receptor gating Neuron 2007 55 905 918 17880894 PMC3167227
  113. Milstein AD Nicoll RA Regulation of AMPA receptor gating and pharmacology by TARP auxiliary subunits Trends in Pharmacol. Sci 2008 29 333 339 18514334 PMC2819157
  114. Milstein AD Nicoll RA TARP modulation of synaptic AMPA receptor trafficking and gating depends on multiple intracellular domains Proc. Natl. Acad. Sci. USA 2009 27 11348 11351 19549880 PMC2708767
  115. Morimoto-Tomita M Zhang W Straub C Cho CH Kim KS Howe JR Tomita S Autoinactivation of neuronal AMPA receptors via glutamate-regulated TARP interaction Neuron 2009 61 101 112 19146816 PMC2649795
  116. Mosbacher J Schoepfer R Monyer H Burnashev N Seeburg PH Ruppersberg JP A molecular determinant for submillisecond desensitization in glutamate receptors Science 1994 266 1059 1062 7973663
  117. Moss FJ Viard P Davies A Bertaso F Page KM Graham A Cantí C Plumpton M Plumpton C Clare JJ Dolphin AC The novel product of a five-exon stargazin-related gene abolishes Ca(V)2.2 calcium channel expression EMBO J 2002 21 1514 1523 11927536 PMC125363
  118. Nakagawa T Cheng Y Ramm E Sheng M Walz T Structure and different conformational states of native AMPA receptor complexes Nature 2005 433 545 549 15690046
  119. Nakagawa T Cheng Y Sheng M Walz T Three-dimensional structure of an AMPA receptor without associated stargazin/TARP proteins Biol. Chem 2006 387 179 187 16497150
  120. Ng D Pitcher GM Szilard RK Sertie A Kanisek M Clapcote SJ Lipina T Kalia LV Joo D McKerlie C Cortez M Roder JC Salter MW McInnes RR Neto1 is a novel CUB-domain NMDA receptor-interacting protein required for synaptic plasticity and learning PLoS Biol 2009 7 e41 19243221 PMC2652390
  121. Nicoll RA Tomita S Bredt DS Auxiliary subunits assist AMPA-type glutamate receptors Science 2006 311 1253 1256 16513974
  122. Nissenbaum J Devor M Seltzer Z Gebauer M Michaelis M Tal M Dorfman R Abitbul-Yarkoni M Lu Y Elahipanah T delCanho S Minert A Fried K Persson AK Shpigler H Shabo E Yakir B Pisanté A Darvasi A Susceptibility to chronic pain following nerve injury is genetically affected by CACNG2 Genome Res 2010 20 1180 1190 20688780 PMC2928496
  123. Noebels JL Qiao X Bronson RT Spencer C Davisson MT Stargazer: a new neurological mutant on chromosome 15 in the mouse with prolonged cortical seizures Epilepsy Res 1990 7 129 135 2289471
  124. Norton RS Pallaghy PK The cystine knot structure of ion channel toxins and related polypeptides Toxicon 1998 36 1573 1583 9792173
  125. Opazo P Labrecque S Tigaret CM Frouin A Wiseman PW De Koninck P Choquet D CaMKII triggers the diffusional trapping of surface AMPARs through phosphorylation of stargazin Neuron 2010 67 239 252 20670832
  126. Osten P Stern-Bach Y Learning from stargazin: the mouse, the phenotype and the unexpected Curr. Opin. Neurobiol 2006 16 275 280 16678401
  127. Partin KM Patneau DK Mayer ML Cyclothiazide differentially modulates desensitization of alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptor splice variants Mol. Pharmacol 1994 46 129 138 8058047
  128. Patneau DK Mayer ML Kinetic analysis of interactions between kainate and AMPA: evidence for activation of a single receptor in mouse hippocampal neurons Neuron 1991 6 785 798 1673850
  129. Payne HL The role of transmembrane AMPA receptor regulatory proteins (TARPs) in neurotransmission and receptor trafficking Mol. Membr. Biol 2008 25 353 362 18446621
  130. Penn AC Williams SR Greger IH Gating motions underlie AMPA receptor secretion from the endoplasmic reticulum EMBO J 2008 27 3056 3068 18923416 PMC2585171
  131. Pongs O Schwarz JR Ancillary subunits associated with voltage-dependent K+ channels Physiol. Rev 2010 90 755 796 20393197
  132. Powers J Barlowe C Transport of axl2p depends on erv14p, an ER-vesicle protein related to the Drosophila cornichon gene product J. Cell Biol 1998 142 1209 1222 9732282 PMC2149358
  133. Priel A Kolleker A Ayalon G Gillor M Osten P Stern-Bach Y Stargazin reduces desensitization and slows deactivation of the AMPA-type glutamate receptors J. Neurosci 2005 25 2682 2686 15758178 PMC6725153
  134. Raman IM Trussell LO The kinetics of the response to glutamate and kainate in neurons of the avian cochlear nucleus Neuron 1992 9 173 186 1352983
  135. Roth S Neuman-Silberberg FS Barcelo G Schupbach T cornichon and the EGF receptor signaling process are necessary for both anterior-posterior and dorsal-ventral pattern formation in Drosophila Cell 1995 81 967 978 7540118
  136. Rouach N Byrd K Petralia RS Elias GM Adesnik H Tomita S Karimzadegan S Kealey C Bredt DS Nicoll RA TARP gamma-8 controls hippocampal AMPA receptor number, distribution and synaptic plasticity Nat. Neurosci 2005 8 1525 1533 16222232
  137. Rousset M Cens T Restituito S Barrere C Black JL 3rd McEnery MW Charnet P Functional roles of gamma2, gamma3 and gamma4, three new Ca2+ channel subunits, in P/Q-type Ca2+ channel expressed in Xenopus oocytes J. Physiol 2001 532 583 593 11313431 PMC2278567
  138. Sager C Tapken D Kott S Hollmann M Functional modulation of AMPA receptors by transmembrane AMPA receptor regulatory proteins Neurosci 2009a 158 45 54 18304745
  139. Sager C Terhag J Kott S Hollmann M C-terminal domains of transmembrane alpha-amino-3-hydroxy-5-methyl-4-isoxazole propionate (AMPA) receptor regulatory proteins not only facilitate trafficking but are major modulators of AMPA receptor function J. Biol. Chem 2009b 284 32413 32424 19773551 PMC2781656
  140. Sainlos M Tigaret C Poujol C Olivier NB Bard L Breillat C Thiolon K Choquet D Imperiali B Biomimetic divalent ligands for the acute disruption of synaptic AMPAR stabilization Nat. Chem. Biol 2011 7 81 91 21186349
  141. Scannevin RH Huganir RL Postsynaptic organization and regulation of excitatory synapses Nat. Rev. Neurosci 2000 1 133 141 11252776
  142. Schmidt C Klein C Hollmann M Xenopus laevis oocytes endogenously express all subunits of the ionotropic glutamate receptor family J. Mol. Biol 2009 390 182 195 19445955
  143. Schnell E Sizemore M Karimzadegan S Chen L Bredt DS Nicoll RA Direct interactions between PSD-95 and stargazin control synaptic AMPA receptor number Proc. Natl. Acad. Sci. USA 2002 99 13902 13907 12359873 PMC129795
  144. Schwenk J Harmel N Zolles G Bildl W Kulik A Heimrich B Chisaka O Jonas P Schulte U Fakler B Klocker N Functional proteomics identify cornichon proteins as auxiliary subunits of AMPA receptors Science 2009 323 1313 1319 19265014
  145. Selvakumar B Huganir RL Snyder SH S-nitrosylation of stargazin regulates surface expression of AMPA-glutamate neurotransmitter receptors Proc. Natl. Acad. Sci. USA 2009 106 16440 16445 19805317 PMC2752523
  146. Shanks NF Maruo T Farina AN Ellisman MH Nakagawa T Contribution of the global subunit structure and stargazin on the maturation of AMPA receptors J. Neurosci 2010 30 2728 2740 20164357 PMC2842908
  147. Shi Y Lu W Milstein AD Nicoll RA The stoichiometry of AMPA receptors and TARPs varies by neuronal cell type Neuron 2009 62 633 640 19524523 PMC3119531
  148. Shi Y Suh YH Milstein AD Isozaki K Schmid SM Roche KW Nicoll RA Functional comparison of the effects of TARPs and cornichons on AMPA receptor trafficking and gating Proc. Natl. Acad. Sci. USA 2010 107 16315 16319 20805473 PMC2941340
  149. Silver RA Kanichay RT Neuroscience. Refreshing connections Science 2008 320 183 184 18403696
  150. Sobolevsky AI Rosconi MP Gouaux E X-ray structure, symmetry and mechanism of an AMPA-subtype glutamate receptor Nature 2009 462 745 756 19946266 PMC2861655
  151. Song I Huganir RL Regulation of AMPA receptors during synaptic plasticity Trends Neurosci 2002 25 578 588 12392933
  152. Soto D Coombs ID Kelly L Farrant M Cull-Candy SG Stargazin attenuates intracellular polyamine block of calcium-permeable AMPA receptors Nat. Neurosci 2007 10 1260 1267 17873873 PMC2430330
  153. Soto D Coombs ID Renzi M Zonouzi M Farrant M Cull-Candy SG Selective regulation of long-form calcium-permeable AMPA receptors by an atypical TARP, gamma-5 Nat. Neurosci 2009 12 277 285 19234459 PMC2735763
  154. Stein EL Chetkovich DM Regulation of stargazin synaptic trafficking by C-terminal PDZ ligand phosphorylation in bidirectional synaptic plasticity J. Neurochem 2010 113 42 53 19968761 PMC4035483
  155. Sumioka A Yan D Tomita S TARP phosphorylation regulates synaptic AMPA receptors through lipid bilayers Neuron 2010 66 755 767 20547132 PMC2887694
  156. Sun Y Olson R Horning M Armstrong N Mayer M Gouaux E Mechanism of glutamate receptor desensitization Nature 2002 417 245 253 12015593
  157. Suzuki E Kessler M Arai AC The fast kinetics of AMPA GluR3 receptors is selectively modulated by the TARPs gamma 4 and gamma 8 Mol. Cell. Neurosci 2008 38 117 123 18395463
  158. Swanson GT Kamboj SK Cull-Candy SG Single-channel properties of recombinant AMPA receptors depend on RNA editing, splice variation, and subunit composition J. Neurosci 1997 17 58 69 8987736 PMC6793687
  159. Swanson GT Heinemann SF Heterogeneity of homomeric GluR5 kainate receptor desensitization expressed in HEK293 cells J. Physiol 1998 513 639 646 9824706 PMC2231309
  160. Tigaret C Choquet D Neuroscience. More AMPAR garnish Science 2009 323 1295 1296 19265005
  161. Tomita S Chen L Kawasaki Y Petralia RS Wenthold RJ Nicoll RA Bredt DS Functional studies and distribution define a family of transmembrane AMPA receptor regulatory proteins J. Cell Biol 2003 161 805 816 12771129 PMC2199354
  162. Tomita S Fukata M Nicoll RA Bredt DS Dynamic interaction of stargazin-like TARPs with cycling AMPA receptors at synapses Science 2004 303 1508 1511 15001777
  163. Tomita S Stein V Stocker TJ Nicoll RA Bredt DS Bidirectional synaptic plasticity regulated by phosphorylation of stargazin-like TARPs Neuron 2005a 45 269 277 15664178
  164. Tomita S Adesnik H Sekiguchi M Zhang W Wada K Howe JR Nicoll RA Bredt DS Stargazin modulates AMPA receptor gating and trafficking by distinct domains Nature 2005b 435 1052 1058 15858532
  165. Tomita S Shenoy A Fukata Y Nicoll RA Bredt DS Stargazin interacts functionally with the AMPA receptor glutamate-binding module Neuropharmacol 2007a 52 87 91 16919685
  166. Tomita S Byrd RK Rouach N Bellone C Venegas A O'Brien JL Kim KS Olsen O Nicoll RA Bredt DS AMPA receptors and stargazin-like transmembrane AMPA receptor-regulatory proteins mediate hippocampal kainate neurotoxicity Proc. Natl. Acad. Sci. USA 2007b 104 18784 18788 18000041 PMC2141854
  167. Tomita S Regulation of ionotropic glutamate receptors by their auxiliary subunits Physiol 2010 25 41 49 PMC3010179 20134027
  168. Tsui J Malenka RC Substrate localization creates specificity in calcium/calmodulin-dependent protein kinase II signaling at synapses J. Biol. Chem 2006 281 13794 13804 16551613
  169. Turetsky D Garringer E Patneau DK Stargazin modulates native AMPA receptor functional properties by two distinct mechanisms J. Neurosci 2005 25 7438 7448 16093395 PMC6725298
  170. Vacher H Mohapatra DP Trimmer JS Localization and targeting of voltage-dependent ion channels in mammalian central neurons Physiol. Rev 2008 88 1407 1447 18923186 PMC2587220
  171. Vandenberghe W Nicoll RA Bredt DS Stargazin is an AMPA receptor auxiliary subunit Proc. Natl. Acad. Sci. USA 2005a 102 485 490 15630087 PMC544314
  172. Vandenberghe W Nicoll RA Bredt DS Interaction with the unfolded protein response reveals a role for stargazin in biosynthetic AMPA receptor transport J. Neurosci 2005b 25 1095 1102 15689545 PMC6725949
  173. Vitt UA Hsu SY Hsueh AJ Evolution and classification of cystine knot-containing hormones and related extracellular signaling molecules Mol. Endocrinol 2001 15 681 694 11328851
  174. Vlachová V Vyklický L Vyklický L Jr Vyskocil F The action of excitatory amino acids on chick spinal cord neurones in culture J. Physiol 1987 386 425 438 2445965 PMC1192470
  175. Von Engelhardt J Mack V Sprengel R Kavenstock N Li KW Stern-Bach Y Smit AB Seeburg PH Monyer H CKAMP44: a brain-specific protein attenuating short-term synaptic plasticity in the dentate gyrus Science 2010 327 1518 1522 20185686
  176. Walker CS Brockie PJ Madsen DM Francis MM Zheng Y Koduri S Mellem JE Strutz-Seebohm N Maricq AV Reconstitution of invertebrate glutamate receptor function depends on stargazin-like proteins Proc. Natl. Acad. Sci. USA 2006a 103 10781 10786 16818877 PMC1502308
  177. Walker CS Francis MM Brockie PJ Madsen DM Zheng Y Maricq AV Conserved SOL-1 proteins regulate ionotropic glutamate receptor desensitization Proc. Natl. Acad. Sci. USA 2006b 103 10787 10792 16818875 PMC1502309
  178. Wang R Walker CS Brockie PJ Francis MM Mellem JE Madsen DM Maricq AV Evolutionary conserved role for TARPs in the gating of glutamate receptors and tuning of synaptic function Neuron 2008 59 997 1008 18817737 PMC2754846
  179. Wollmuth LP Sobolevsky AI Structure and gating of the glutamate receptor ion channel Trends Neurosci 2004 27 321 328 15165736
  180. Wyllie DJ Traynelis SF Cull-Candy SG Evidence for more than one type of non-NMDA receptor in outside-out patches from cerebellar granule cells of the rat J. Physiol 1993 463 193 226 7504104 PMC1175340
  181. Yamauchi T Molecular constituents and phosphorylation-dependent regulation of the post-synaptic density Mass Spectrom. Rev 2002 21 266 286 12533800
  182. Yamazaki M Ohno-Shosaku T Fukaya M Kano M Watanabe M Sakimura K A novel action of stargazin as an enhancer of AMPA receptor activity Neurosci. Res 2004 50 369 374 15567474
  183. Yamazaki M Fukaya M Hashimoto K Yamasaki M Tsujita M Itakura M Abe M Natsume R Takahashi M Kano M Sakimura K Watanabe M TARPs gamma-2 and gamma-7 are essential for AMPA receptor expression in the cerebellum Eur. J. Neurosci 2010 31 2204 2220 20529126
  184. Zhang W St-Gelais F Grabner CP Trinidad JC Sumioka A Morimoto-Tomita M Kim KS Straub C Burlingame AL Howe JR Tomita S A transmembrane accessory subunit that modulates kainate-type glutamate receptors Neuron 2009 61 385 396 19217376 PMC2803770
  185. Zheng Y Brockie PJ Mellem JE Madsen DM Walker CS Francis MM Maricq AV SOL-1 is an auxiliary subunit that modulates the gating of GLR-1 glutamate receptors in Caenorhabditis elegans Proc. Natl. Acad. Sci. USA 2006 103 1100 1105 16418277 PMC1347967
  186. Zheng Y Mellem JE Brockie PJ Madsen DM Maricq AV SOL-1 is a CUB-domain protein required for GLR-1 glutamate receptor function in C. elegans Nature 2004 427 451 457 14749834
  187. Ziff EB TARPs and the AMPA receptor trafficking paradox Neuron 2007 53 627 633 17329203
  188. Zorumski CF Yang J AMPA, kainate, and quisqualate activate a common receptor-channel complex on embryonic chick motoneurons J. Neurosci 1988 8 4277 4286 2460595 PMC6569484

Cited by

Sorted by citations

Authors
Jackson, A. C., & Nicoll, R. A.
Affiliations
University of California, San Francisco (US)
Corresponding author
  • Jackson, Alexander C.
  • Nicoll, Roger A.
ORCID
Venue
Neuron
Publisher
Elsevier BV
Published
2011-04
Volume
70
Issue
2
Pages
178-199
ISSN
0896-6273 (ISSN-L)
DOI
10.1016/j.neuron.2011.04.007
PMC
PMC3119519
OpenAlex
W2027046812
Cited by
410
References
9
Citations by year
2026: 14 · 2025: 11 · 2024: 13 · 2023: 17 · 2022: 21 · 2021: 31 · 2020: 20 · 2019: 25 · 2018: 29 · 2017: 38 · 2016: 32 · 2015: 26 · 2014: 31 · 2013: 47 · 2012: 39
FWCI
4.03
Type
journal article
Language
en
Open access
Licence
Locations
  • Neuron (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
Funders
National Institute of Mental Health (F32MH081430, R01MH080379)
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Receptor Mechanisms and Signaling
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nicotinic Acetylcholine Receptors Study
Keywords
ionotropic glutamate receptors, TARP, AMPA receptor trafficking, receptor gating, receptor stability, excitatory synaptic transmission
MeSH terms
Animals, Brain, Humans, Models, Molecular, Synaptic Transmission, Nuclear Proteins, Signal Transduction, Protein Subunits, Protein Transport, Receptors, Ionotropic Glutamate

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review