PMCA2 via PSD-95 controls calcium signaling by α7-containing nicotinic acetylcholine receptors on aspiny interneurons

Journal of Neuroscience

Volumn 32, Issue 20, 2012, Pages 6895-6905

  Gómez Varela, David ^a   Schmidt, Manuela ^b   Schoellerman, Jeff ^a   Peters, Eric C ^c   Berg, Darwin K ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

^c GENOMICS INSTITUTE OF THE NOVARTIS RESEARCH FOUNDATION   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BUNGAROTOXIN RECEPTOR; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; IONOTROPIC RECEPTOR; PLASMA MEMBRANE CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE; PLASMA MEMBRANE CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE 2; POSTSYNAPTIC DENSITY PROTEIN 95; QUANTUM DOT; UNCLASSIFIED DRUG; CALCIUM; CALOXIN 3A1; DLGH4 PROTEIN, RAT; MEMBRANE PROTEIN; NICOTINIC RECEPTOR; PEPTIDE; SIGNAL PEPTIDE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CALCIUM CELL LEVEL; CALCIUM SIGNALING; CONTROLLED STUDY; EMBRYO; FEMALE; FUNCTIONAL PROTEOMICS; HIPPOCAMPUS; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; INTERNEURON; MALE; MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; RAT; RNA INTERFERENCE; WESTERN BLOTTING; ANIMAL; DRUG ANTAGONISM; METABOLISM; PHYSIOLOGY; PRIMARY CELL CULTURE; SPRAGUE DAWLEY RAT;

ANIMALS; CALCIUM; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; FEMALE; HIPPOCAMPUS; INTERNEURONS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; MEMBRANE PROTEINS; PEPTIDES; PLASMA MEMBRANE CALCIUM-TRANSPORTING ATPASES; PRIMARY CELL CULTURE; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, NICOTINIC;

EID: 84861142959     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5972-11.2012     Document Type: Article

References (69)

1. Albuquerque EX, Pereira EF, Alkondon M, Rogers SW (2009) Mammalian nicotinic acetylcholine receptors: from structure to function. Physiol Rev 89:73-120.
2. Alkondon M, Albuquerque EX (2001) Nicotinic acetylcholine receptors o7 and a4/32 subtypes differentially control GABAergic input to CA1 neurons in rat hippocampus. J Neurophysiol 86:3043-3055.
3. Aravanis AM, Pyle JL, Tsien RW (2003) Single synaptic vesicles fusing transiently and successively without loss of identity. Nature 423:643-647.
4. Baer K, Bürli T, Huh KH, Wiesner A, Erb-Vogtli S, Gockeritz-Dujmovic D, Moransard M, Nishimune A, Rees MI, Henley JM, Fritschy JM, Fuhrer C (2007) PICK1 interacts with alpha7 neuronal nicotinic acetylcholine receptors and controls their clustering. Mol Cell Neurosci 35:339-355.
5. Bertrand D, Galzi JL, Devillers-Thiery A, Bertrand S, Changeux JP (1993) Mutations at two distinct sites within the channel domain M2 alter calcium permeability of neuronal alpha 7 nicotinic receptor. Proc Natl Acad Sci USA 90:6971-6975.
6. Boczek T, Kozaczuk A, Ferenc B, Kosiorek M, Pikula S, Zylinska L (2012) Gene expression pattern in PC12 cells with reduced PMCA2 or PMCA3 isoform: selective upregulation of calmodulin and neuromodulin. Mol Cell Biochem 360:89-102.
7. Bürli T, Baer K, Ewers H, Sidler C, Fuhrer C, Fritschy JM (2010) Single particle tracking of alpha7 nicotinic AChR in hippocampal neurons reveals regulated confinement at glutamatergic and GABAergic perisynaptic sites. PLoS One 5:e11507.
8. Charrier C, Ehrensperger MV, Dahan M, Levi S, Triller A (2006) Cytoskel-eton regulation of glycine receptor number at synapses and diffusion in the plasma membrane. JNeurosci 26:8502-8511.
9. Conroy WG, Liu Z, Nai Q, Coggan JS, Berg DK (2003) PDZ-containing proteins provide a functional postsynaptic scaffold for nicotinic receptors in neurons. Neuron 38:759-771.
10. Dajas-Bailador F, Wonnacott S (2004) Nicotinic acetylcholine receptors and the regulation of neuronal signalling. TIPS 25:317-324.
11. +-atpase isoforms 2b and 4b interact promiscuously and selectively with members of the membrane-associated guanylate kinase family of PDZ (PSD95/Dlg/ ZO-1) domain-containing proteins. J Biol Chem 276:21594-21600.
12. 2+/calmodulin-kinase II enhances channel conductance of alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionate type glutamate receptors. Proc Natl Acad Sci USA 96:3269-3274.
13. Descarries L, Gisiger V, Steriade M (1997) Diffuse transmission by acetylcholine in the CNS. Prog Neurobiol 53:603-625.
14. Dickinson JA, Hanrott KE, Mok MH, Kew JN, Wonnacott S (2007) Differential coupling of oC7 and nona7 nicotinic acetylcholine receptors to calcium-induced calcium release and voltage-operated calcium channels in PC12 cells. J Neurochem 100:1089-1096.
15. Dingledine R, Borges K, Bowie D, Traynelis SF (1999) The glutamate receptor ion channels. Pharmacol Rev 51:7-61.
16. Ehlers MD, Heine M, Groc L, Lee MC, Choquet D (2007) Diffusional trapping of GluR1 AMPA receptors by input-specific synaptic activity. Neuron 54:447-460.
17. Farías GG, Valles AS, Colombres M, Godoy JA, Toledo EM, Lukas RJ, Bar-rantes FJ, Inestrosa NC (2007) Wnt-7a induces presynaptic colocaliza-tion of alpha 7-nicotinic acetylcholine receptors and adenomatous polyposis coli in hippocampal neurons. J Neurosci 27:5313-5325.
18. 2+ signalling due to activation of alpha 7-containing nicotinic acetylcholine receptors in rat hippocampal neurons. J Physiol 582:597-611.
19. Fernandes CC, Berg DK, Gomez-Varela D (2010) Lateral mobility of nicotinic acetylcholine receptors on neurons is determined by receptor composition, local domain, and cell type. J Neurosci 30:8841-8851.
20. Gardoni F, Polli F, Cattabeni F, Di Luca M (2006) Calcium-calmodulin-dependent protein kinase II phosphorylation modulates PSD-95 binding to NMDA receptors. Eur J Neurosci 24:2694-2704.
21. Garside ML, Turner PR, Austen B, Strehler EE, Beesley PW, Empson RM (2009) Molecular interactions of the plasma membrane calcium ATPase 2 at pre- and postsynaptic sites in rat cerebellum. Neuroscience 162:383-395.
22. Gatto C, Hale CC, Xu W, Milanick MA (1995) Eosin, a potent inhibitor of the plasma membrane Ca pump, does not inhibit the cardiac Na-Ca exchanger. Biochemistry 34:965-972.
23. Goetze B, Grunewald B, Baldassa S, Kiebler M (2004) Chemically controlled formation of a DNA/calcium phosphate coprecipitate: application for transfection of mature hippocampal neurons. J Neurobiol 60:517-525.
24. Goldberg JH, Tamas G, Aronov D, Yuste R (2003) Calcium microdomains in aspiny dendrites. Neuron 40:807-821.
25. Gomez-Varela D, Kohl T, Schmidt M, Rubio ME, Kawabe H, Nehring RB, Schafer S, Stuhmer W, Pardo LA (2010) Characterization of Eag1 channel lateral mobility in rat hippocampal cultures by single-particle-tracking with quantum dots. PLoS One 5:e8858.
26. Govind AP, Walsh H, Green WN (2012) Nicotine-induced upregulation of native neuronal nicotinic receptors is caused by multiple mechanisms. J Neurosci 32:2227-2238.
27. Gray R, Rajan AS, Radcliffe KA, Yakehiro M, Dani JA (1996) Hippocampal synaptic transmission enhanced by low concentrations of nicotine. Nature 383:713-716.
28. Jensen TP, Filoteo AG, Knopfel T, Empson RM (2007) Presynaptic plasma membrane Ca2+ ATPase isoform 2a regulates excitatory synaptic transmission in rat hippocampal CA3. J Physiol 579:85-99.
29. Jones S, Sudweeks S, Yakel JL (1999) Nictinic receptors in the brain: correlating physiology with function. Trends Neurosci 22:555-561.
30. Kabbani N, Woll MP, Levenson R, Lindstrom JM, Changeux JP (2007) Intracellular complexes of the beta2 subunit of the nicotinic acetylcholine receptor in brain identified by proteomics. Proc Natl Acad Sci USA 104:20570-20575.
31. Kaeser PS, Deng L, Wang Y, Dulubova I, Liu X, Rizo J, Südhof TC (2011) RIM proteins tether Ca2+ channels to presynaptic active zones via a direct PDZ-domain interaction. Cell 144:282-295.
32. Kawai H, Zago W, Berg DK (2002) Nicotinic alpha 7 receptor clusters on hippocampal GABAergic neurons: regulation by synaptic activity and neurotrophins. J Neurosci 22:7903-7912.
33. Keller A, Nesvizhskii AI, Kolker E, Aebersold R (2002) Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal Chem 74:5383-5392.
34. + regulation of nicotinic acetylcholine receptor channels in rat hippocampal CA1 neurons. J Neurosci 23:9024-9031.
35. Kozel PJ, Friedman RA, Erway LC, Yamoah EN, Liu LH, Riddle T, Duffy JJ, Doetschman T, Miller ML, Cardell EL, Shull GE (1998) Balance and hearing deficits in mice with a null mutation in the gene encoding plasma membrane Ca2 +-ATPase isoform 2. J Biol Chem 273:18693-18696.
36. Kullmann DM, Lamsa KP (2007) Long-term synaptic plasticity in hippocampal interneurons. Nat Rev Neurosci 8:687-699.
37. Malinow R, Malenka RC (2002) AMPA receptor trafficking and synaptic plasticity. Annu Rev Neurosci 25:103-126.
38. 2+-ATPase in mouse brain. BMC Neurosci 10:112.
39. Mbaya E, Oules B, Caspersen C, Tacine R, Massinet H, Pennuto M, Chretien D, Munnich A, Rotig A, Rizzuto R, Rutter GA, Paterlini-Brechot P, Chami M (2010) Calcium signalling-dependent mitochondrial dysfunction and bioenergetics regulation in respiratory chain Complex II deficiency. Cell Death Differ 17:1855-1866.
40. McCann CM, Tapia JC, Kim H, Coggan JS, Lichtman JW (2008) Rapid and midifiable neurotransmitter receptor dynamics at a neuronal synapse in vivo. Nat Neurosci 11:807-815.
41. McGehee DS, Heath MJ, Gelber S, Devay P, Role LW (1995) Nicotine enhancement of fast excitatory synaptic transmission in CNS by presynaptic receptors. Science 269:1692-1696.
42. Michaelsen K, Lohmann C (2010) Calcium dynamics at developing synapses: mechanisms and functions. Eur J Neurosci 32:218-223.
43. Miwa JM, Freedman R, Lester HA (2011) Neural systems governed by nicotinic acetylcholine receptors: emerging hypotheses. Neuron 70:20-33.
44. Nashmi R, Dickinson ME, McKinney S, Jareb M, Labarca C, Fraser SE, Lester HA (2003) Assembly of a4/32 nicotinic acetylcholine receptors assessed with functional fluorescently labeled subunits: effects of localization, trafficking, and nicotine-induced upregulation in clonal mammalian cells and in cultured midbrain neurons. J Neurosci 23:11554-11567.
45. Neff RA 3rd, Conroy WG, Schoellerman JD, Berg DK (2009) Synchronous and asynchronous transmitter release at nicotinic synapses are differentially regulated by postsynaptic PSD-95 proteins. J Neurosci 29:15770-15779.
46. Nesvizhskii AI, Keller A, Kolker E, Aebersold R (2003) A statistical model for identifying proteins by tandem mass spectrometry. Anal Chem 75:4646-4658.
47. Pande J, Mallhi KK, Grover AK (2005) Role of third extracellular domain of plasma membrane Ca2 + -Mg2 +-ATPase based on the novel inhibitor caloxin 3A1. Cell Calcium 37:245-250.
48. Paulo JA, Brucker WJ, Hawrot E (2009) Proteomic analysis of an alpha7 nicotinic acetylcholine receptor interactome. J Proteome Res 8:1849-1858.
49. Rezvani K, Teng Y, Shim D, De Biasi M (2007) Nicotine regulates multiple synaptic proteins by inhibiting proteasomal activity. J Neurosci 27:10508-10519.
50. Richards CI, Srinivasan R, Xiao C, Mackey ED, Miwa JM, Lester HA (2011) Trafficking of a4* nicotinic receptors revealed by superecliptic phluorin. Effects of a /34 amyotrophic lateral sclerosis-associated mutation and chronic exposure to nicotine. J Biol Chem 286:31241-31249.
51. Rosenberg MM, Yang F, Giovanni M, Mohn JL, Temburni MK, Jacob MH (2008) Adenomatous polyposis coli plays a key role, in vivo, in coordinating assembly of the neuronal nicotinic postsynaptic complex. Mol Cell Neurosci 38:138-152.
52. Rozsa B, Katona G, Kaszas A, Szipocs R, Vizi ES (2008) Dendritic nicotinic receptors modulate backpropagating action potentials and long-term plasticity of interneurons. Eur J Neurosci 27:364-377.
53. Sabio G, Arthur JS, Kuma Y, Peggie M, Carr J, Murray-Tait V, Centeno F, Goedert M, Morrice NA, Cuenda A (2005) p38gamma regulates the localisation of SAP97 in the cytoskeleton by modulating its interaction with GKAP. EMBO J 24:1134-1145.
54. Sage D, Neumann FR, Hediger F, Gasser SM, Unser M (2005) Automatic tracking of individual fluorescence particles: application to the study of chromosome dynamics. IEEE Trans Image Process 14:1372-1383.
55. Schiller J, Schiller Y, Clapham DE (1998) NMDA receptors amplify calcium influx into dendritic spines during associative pre- and postsynaptic activation. Nat Neurosci 1:114-118.
56. Schulte U, Müller CS, Fakler B (2011) Ion channels and their molecular environments-glimpses and insights from functional proteomics. Semin Cell DevBiol 22:132-144.
57. Seguela P, Wadiche J, Dineley-Miller K, Dani JA, Patrick JW (1993) Molecular cloning, functional properties, and distribution of rat brain a7: a nicotinic cation channel highly permeable to calcium. J Neurosci 13:596-604.
58. Sharma G, Vijayaraghavan S (2003) Modulation of presynaptic store calcium induces release of glutamate and postsynaptic firing. Neuron 38:929-939.
59. Strehler EE, Zacharias DA (2001) Role of alternative splicing in generating isoform diversity among plasma membrane calcium pumps. Physiol Rev 81:21-50.
60. Strehler EE, Filoteo AG, Penniston JT, Caride AJ (2007) Plasma-membrane Ca(2 +) pumps: structural diversity as the basis for functional versatility. Biochem Soc Trans 35:919-922.
61. Temburni MK, Rosenberg MM, Pathak N, McConnell R, Jacob MH (2004) Neuronal nicotinic synapse assembly requires the adenomatous polyposis coli tumor suppressor protein. J Neurosci 24:6776-6784.
62. Triller A, Choquet D (2008) New concepts in synaptic biology derived from single-molecule imaging. Neuron 59:359-374.
63. Tsui J, Malenka RC (2006) Substrate localization creates specificity in calcium/calmodulin-dependent protein kinase II signaling at synapses. J Biol Chem 281:13794-13804.
64. Williams BM, Temburni MK, Levey MS, Bertrand S, Bertrand D, Jacob MH (1998) The long internal loop of the a3 subunit targets nAChRs to sub-domains within individual synapses on neurons in vivo. Nat Neurosci 1:557-562.
65. Xu J, Zhu Y, Heinemann SF (2006) Identification of sequence motifs that target neuronal nicotinic receptors to dendrites and axons. J Neurosci 26:9780-9793.
66. Yuste R (2011) Dendritic spines and distributed circuits. Neuron 71:772-781.
67. Yuste R, Majewska A, Cash SS, Denk W (1999) Mechanisms of calcium influx into hippocampal spines: heterogeneity among spines, coincidence detection by NMDA receptors, and optical quantal analysis. J Neurosci 19:1976-1987.
68. Zago WM, Massey KA, Berg DK (2006) Nicotinic activity stabilizes convergence of nicotinic and GABAergic synapses on filopodia of hippocampal interneurons. Mol Cell Neurosci 31:549-559.
69. Zhang D, Hou Q, Wang M, Lin A, Jarzylo L, Navis A, Raissi A, Liu F, Man HY (2009) Na,K-ATPase activity regulates AMPA receptor turnover through proteasome-mediated proteolysis. JNeurosci 29:4498-4511.