NMDA receptors are upregulated and trafficked to the plasma membrane after sigma-1 receptor activation in the rat hippocampus

Journal of Neuroscience

Volumn 34, Issue 34, 2014, Pages 11325-11338

  Pabba, Mohan ^a   Wong, Adrian Y C ^a   Ahlskog, Nina ^a   Hristova, Elitza ^a   Biscaro, Dante ^a   Nassrallah, Wissam ^a   Ngsee, Johnny K ^b   Snyder, Melissa ^a   Beique, Jean Claude ^b   Bergeron, Richard ^a  

^a OTTAWA HOSPITAL RESEARCH INSTITUTE   (Canada)

^b UNIVERSITY OF OTTAWA   (Canada)

Author keywords

NMDA receptor; Protein synthesis; Sigma 1 receptor; Surface biotinylation; Trafficking; Western blot

Indexed keywords

1 PHENYLCYCLOHEXANECARBOXYLIC ACID 2 MORPHOLINOETHYL ESTER; GLUTAMATE RECEPTOR 2; N ALLYLNORMETAZOCINE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N [2 (3,4 DICHLOROPHENYL)ETHYL] 2 DIMETHYLAMINO N METHYLETHYLAMINE; NUCLEOLIN; PENTAZOCINE; POSTSYNAPTIC DENSITY PROTEIN 95; SIGMA 1 OPIATE RECEPTOR; 1-(2-(3,4-DICHLOROPHENYL)ETHYL)-4-METHYLPIPERAZINE; 2-(4-MORPHOLINO)ETHYL-1-PHENYLCYCLOHEXANE-1-CARBOXYLATE; DLGH4 PROTEIN, RAT; ETHYLENEDIAMINE DERIVATIVE; MEMBRANE PROTEIN; MORPHOLINE DERIVATIVE; N-METHYL D-ASPARTATE RECEPTOR SUBTYPE 2A; NR2B NMDA RECEPTOR; PHENAZOCINE; PIPERAZINE DERIVATIVE; SIGMA OPIATE RECEPTOR; SIGMA-1 RECEPTOR; SIGNAL PEPTIDE; SK&F 10047;

ANIMAL TISSUE; ARTICLE; BIOTINYLATION; CELL FRACTIONATION; CELL MEMBRANE; CONTROLLED STUDY; HIPPOCAMPUS; IMMUNOPRECIPITATION; MALE; MEMBRANE CURRENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; RAT; RECEPTOR BINDING; SIGNAL TRANSDUCTION; SYNAPSE; SYNAPTOSOME; UPREGULATION; WESTERN BLOTTING; AGONISTS; ANALOGS AND DERIVATIVES; ANIMAL; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; GENETICS; KNOCKOUT MOUSE; METABOLISM; MOUSE; PHYSIOLOGY; PROTEIN TRANSPORT; SPRAGUE DAWLEY RAT; TIME;

ANIMALS; CELL MEMBRANE; ETHYLENEDIAMINES; HIPPOCAMPUS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; MEMBRANE PROTEINS; MICE; MICE, KNOCKOUT; MORPHOLINES; PENTAZOCINE; PHENAZOCINE; PIPERAZINES; PROTEIN TRANSPORT; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, N-METHYL-D-ASPARTATE; RECEPTORS, SIGMA; SUBCELLULAR FRACTIONS; TIME FACTORS; UP-REGULATION;

EID: 84906227102     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0458-14.2014     Document Type: Article

References (72)

1. Aydar E., Palmer CP, Klyachko VA, Jackson MB (2002) The sigma receptor as a ligand-regulated auxiliary potassium channel subunit. Neuron 34: 399-410. CrossRef Medline
2. Balasuriya D., Stewart AP, Edwardson JM (2013) The sigma-1 receptor interacts directly with GluN1 but not GluN2A in the GluN1/GluN2A NMDA receptor. J Neurosci 33:18219-18224. CrossRef Medline
3. Bergeron R., de Montigny C, Debonnel G (1995) Biphasic effects of sigma ligands on the neuronal response to N-methyl-D-aspartate. Naunyn Schmiedebergs Arch Pharmacol 351:252-260. Medline
4. Bergeron R., de Montigny C, Debonnel G (1996) Potentiation of neuronal NMDAresponse induced by dehydroepiandrosterone and its suppression by progesterone: effects mediated via sigma receptors. J Neurosci 16: 1193-1202. Medline
5. Bergeron R., de Montigny C, Debonnel G (1997) Effect of short-term and long-term treatments with sigma ligands on the N-methyl-D-aspartate response in the CA3 region of the rat dorsal hippocampus. Br J Pharmacol 120:1351-1359. CrossRef Medline
6. Beskid M., Rózycka Z, Taraszewska A (1998) Quinolinic acid and sigma receptor ligand: effect on pyramidal neurons of the CA1 sector of dorsal hippocampus following peripheral administration in rats. Folia Neuropathol 36:94-100. Medline
7. Blackstone C. D, Moss SJ, Martin LJ, Levey AI, Price DL, Huganir RL (1992) Biochemical characterization and localization of a non-N-methyl-Daspartate glutamate receptor in rat brain. J Neurochem 58:1118-1126. CrossRef Medline
8. Crottès D., Martial S, Rapetti-Mauss R, Pisani DF, Loriol C, Pellissier B, Martin P, Chevet E, Borgese F, Soriani O (2011) Sig1R protein regulates hERG channel expression through a post-translational mechanism in leukemic cells. J Biol Chem 286:27947-27958. CrossRef Medline
9. Debonnel G., Bergeron R, de Montigny C (1996a) Potentiation by dehydroepiandrosterone of the neuronal response to N-methyl-D-aspartate in the CA3 region of the rat dorsal hippocampus: an effect mediated via sigma receptors. J Endocrinol [Suppl] 150:S33-S42.
10. Debonnel G., Bergeron R, Monnet FP, De Montigny C (1996b) Differential effects of sigma ligands on the N-methyl-D-aspartate response in the CA1 and CA3 regions of the dorsal hippocampus: effect of mossy fiber lesioning. Neuroscience 71:977-987. CrossRef Medline
11. de Montigny C., Monnet FP, Fournier A, Debonnel G (1992) Sigma ligands and neuropeptide Y selectively potentiate the NMDA response in the rat CA3 dorsal hippocampus: in vivo electrophysiological studies. Clin Neuropharmacol 15 [Suppl 1]:145A-146A.
12. Dennis S. H, Jaafari N, Cimarosti H, Hanley JG, Henley JM, Mellor JR (2011) Oxygen/glucose deprivation induces a reduction in synaptic AMPA receptors on hippocampal CA3 neurons mediated by mGluR1 and adenosine A3 receptors. J Neurosci 31:11941-11952. CrossRef Medline
13. Fischer A., Sananbenesi F, Schrick C, Spiess J, Radulovic J (2004) Distinct roles of hippocampal de novo protein synthesis and actin rearrangement in extinction of contextual fear. J Neurosci 24:1962-1966. CrossRef Medline
14. Fischer von Mollard G, Stahl B, Walch-Solimena C, Takei K, Daniels L, Khoklatchev A., De Camilli P, Südhof TC, Jahn R (1994) Localization of Rab5 to synaptic vesicles identifies endosomal intermediate in synaptic vesicle recycling pathway. Eur J Cell Biol 65:319-326. Medline
15. Fletcher E. J, Church J, Abdel-Hamid K, MacDonald JF (1995) Blockade by sigma site ligands of N-methyl-D-aspartate-evoked responses in rat and mouse cultured hippocampal pyramidal neurones. Br J Pharmacol 116: 2791-2800. CrossRef Medline
16. Forder J. P, TymianskiM (2009) Postsynaptic mechanisms of excitotoxicity: Involvement of postsynaptic density proteins, radicals, and oxidant molecules. Neuroscience 158:293-300. CrossRef Medline
17. Gardner B. M, Pincus D, Gotthardt K, Gallagher CM, Walter P (2013) Endoplasmic reticulum stress sensing in the unfolded protein response. Cold Spring Harb Perspect Biol 5:a013169. CrossRef Medline
18. Guillaud L., Setou M, Hirokawa N (2003) KIF17 dynamics and regulation of NR2B trafficking in hippocampal neurons. J Neurosci 23:131-140. Medline
19. Gundlach A. L, Largent BL, Snyder SH (1986) Autoradiographic localization of sigma receptor binding sites in guinea pig and rat central nervous system with (+)3H-3-(3-hydroxyphenyl)-N-(1-propyl)piperidine. J Neurosci 6:1757-1770. Medline
20. Hallett P. J, Collins TL, Standaert DG, AnthoneW (2008) Biochemical fractionation of brain tissue for studies of receptor distribution and trafficking. Curr Protoc Neurosci Chapter 1:Unit 1.16. CrossRef
21. Hayashi T., Su TP (2003) Intracellular dynamics of sigma-1 receptors (sigma-1 binding sites) in NG108-15 cells. J Pharmacol Exp Ther 306: 726-733. CrossRef Medline
22. Hayashi T., Su TP (2007) Sigma-1 receptor chaperones at the ERmitochondrion interface regulate Ca(2+) signaling and cell survival. Cell 131:596-610. CrossRef Medline
23. Huh K. H, Wenthold RJ (1999) Turnover analysis of glutamate receptors identifies a rapidly degraded pool of the N-methyl-D-aspartate receptor subunit, NR1, in cultured cerebellar granule cells. J Biol Chem 274:151-157. CrossRef Medline
24. Ishima T., Nishimura T, Iyo M, Hashimoto K (2008) Potentiation of nerve growth factor-induced neurite outgrowth in PC12 cells by donepezil: role of sigma-1 receptors and IP3 receptors. Prog Neuropsychopharmacol Biol Psychiatry 32:1656-1659. CrossRef Medline
25. Johannessen M., Ramachandran S, Riemer L, Ramos-Serrano A, Ruoho AE, Jackson M. B (2009) Voltage-gated sodium channel modulation by sigma-receptors in cardiac myocytes and heterologous systems. Am J Physiol Cell Physiol 296:C1049-C1057. CrossRef Medline
26. Karakas E., Furukawa H (2014) Crystal structure of a heterotetrameric NMDA receptor ion channel. Science 344:992-997. CrossRef Medline
27. Kerchner G. A, NicollRA (2008) Silent synapses and the emergence of a postsynaptic mechanism for LTP. Nat Rev Neurosci 9:813-825. CrossRef Medline
28. Kinoshita M., Matsuoka Y, Suzuki T, Mirrielees J, Yang J (2012) Sigma-1 receptor alters the kinetics of Kv1.3 voltage gated potassium channels but not the sensitivity to receptor ligands. Brain Res 1452:1-9. CrossRef Medline
29. Kornau H. C, Schenker LT, Kennedy MB, Seeburg PH (1995) Domain interaction between NMDA receptor subunits and the postsynaptic density protein PSD-95. Science 269:1737-1740. CrossRef Medline
30. Kourrich S., Su TP, Fujimoto M, Bonci A (2012) The sigma-1 receptor: roles in neuronal plasticity and disease. Trends Neurosci 35:762-771. CrossRef Medline
31. Kourrich S., Hayashi T, Chuang JY, Tsai SY, Su TP, Bonci A (2013) Dynamic interaction between sigma-1 receptor and Kv1.2 shapes neuronal and behavioral responses to cocaine. Cell 152:236-247. CrossRef Medline
32. Langa F., Codony X, Tovar V, Lavado A, Giménez E, Cozar P, Cantero M, Dordal A, Hernández E., Pérez R, Monroy X, Zamanillo D, Guitart X, Montoliu L (2003) Generation and phenotypic analysis of sigma receptor type I (sigma 1) knockout mice. Eur J Neurosci 18:2188-2196. CrossRef Medline
33. Lee C. H, Lü W, Michel JC, Goehring A, Du J, Song X, Gouaux E (2014) NMDA receptor structures reveal subunit arrangement and pore architecture. Nature 511:191-197. CrossRef Medline
34. Lupardus P. J, Wilke RA, Aydar E, Palmer CP, Chen Y, Ruoho AE, JacksonMB (2000) Membrane-delimited coupling between sigma receptors and K+ channels in rat neurohypophysial terminals requires neither G-protein nor ATP. J Physiol 526:527-539. CrossRef Medline
35. Martina M., Turcotte ME, Halman S, Bergeron R (2007) The sigma-1 receptor modulates NMDA receptor synaptic transmission and plasticity via SK channels in rat hippocampus. J Physiol 578:143-157. Medline
36. MatsumotoRR (2007) Sigma receptors: historical perspective and background, Chap 1. In: Sigma receptors chemistry, cell biology and clinical implications (Matsumoto RR, Bowen WD, Su TP, eds), pp 125. New York: Springer Science +Business Media.
37. Matsumoto R. R, Bowen WD, Tom MA, Vo VN, Truong DD, De Costa BR (1995) Characterization of two novel sigma receptor ligands: antidystonic effects in rats suggest sigma receptor antagonism. Eur J Pharmacol 280:301-310. CrossRef Medline
38. Maurice T., Su TP (2009) The pharmacology of sigma-1 receptors. Pharmacol Ther 124:195-206. CrossRef Medline
39. McCracken K. A, Bowen WD, de Costa BR, Matsumoto RR (1999) Two novel sigma receptor ligands, BD1047 and LR172, attenuate cocaineinduced toxicity and locomotor activity. Eur J Pharmacol 370:225-232. CrossRef Medline
40. McIlhinney R. A, Molnár E, Atack JR, Whiting PJ (1996) Cell surface expression of the human N-methyl-D-aspartate receptor subunit 1a requires the co-expression of the NR2A subunit in transfected cells. Neuroscience 70:989-997. CrossRef Medline
41. Medzihradsky F., Ahmad K (1971) The uptake of pentazocine into brain. Life Sci I 10:711-720. Medline
42. Miller C. L, Bickford PC, Luntz-Leybman V, Adler LE, Gerhardt GA, Freedman R (1992) Phencyclidine and auditory sensory gating in the hippocampus of the rat. Neuropharmacology 31:1041-1048. CrossRef Medline
43. Monnet F. P, Debonnel G, Junien JL, De Montigny C (1990) N-methyl-Daspartate-induced neuronal activation is selectively modulated by sigma receptors. Eur J Pharmacol 179:441-445. CrossRef Medline
44. Monnet F. P, Debonnel G, Bergeron R, Gronier B, de MontignyC (1994) The effects of sigma ligands and of neuropeptide Y on N-methyl-D-aspartateinduced neuronal activation of CA3 dorsal hippocampus neurones are differentially affected by pertussin toxin. Br J Pharmacol 112:709-715. CrossRef Medline
45. Monnet F. P, de Costa BR, Bowen WD (1996) Differentiation of sigma ligandactivated receptor subtypes that modulate NMDA-evoked [3H]-noradrenaline release in rat hippocampal slices. Br J Pharmacol 119:65-72. CrossRef Medline
46. Morin-Surun M. P, Collin T, Denavit-Saubié M, Baulieu EE, Monnet FP (1999) Intracellular sigma1 receptor modulates phospholipase C and protein kinase C activities in the brainstem. Proc Natl Acad Sci U S A 96:8196-8199. CrossRef Medline
47. Myers A. M, Charifson PS, Owens CE, Kula NS, McPhail AT, Baldessarini RJ, Booth R. G, Wyrick SD (1994) Conformational analysis, pharmacophore identification, and comparative molecular field analysis of ligands for the neuromodulatory sigma 3 receptor. J Med Chem 37:4109-4117. CrossRef Medline
48. Nebl T., Pestonjamasp KN, Leszyk JD, Crowley JL, OhSW, Luna EJ (2002) Proteomic analysis of a detergent-resistant membrane skeleton from neutrophil plasma membranes. J Biol Chem 277:43399-43409. CrossRef Medline
49. Nguyen E. C, McCracken KA, Liu Y, Pouw B, Matsumoto RR (2005) Involvement of sigma (sigma) receptors in the acute actions of methamphetamine: receptor binding and behavioral studies. Neuropharmacology 49:638-645. CrossRef Medline
50. Niethammer M., Kim E, Sheng M (1996) Interaction between the C terminus of NMDA receptor subunits and multiple members of the PSD-95 family of membrane-associated guanylate kinases. J Neurosci 16:2157-2163. Medline
51. Nishimura T., Ishima T, Iyo M, Hashimoto K (2008) Potentiation of nerve growth factor-induced neurite outgrowth by fluvoxamine: role of sigma-1 receptors, IP3 receptors and cellular signaling pathways. PLoS One 3:e2558. CrossRef Medline
52. Pláteník J., Balcar VJ, Yoneda Y, Mioduszewska B, Buchal R, Hynek R, Kilianek L, Kuramoto N, Wilczynski G, Ogita K, Nakamura Y, Kaczmarek L (2005) Apparent presence of Ser133-phosphorylated cyclic AMP response element binding protein (pCREB) in brain mitochondria is due to cross-reactivity of pCREB antibodies with pyruvate dehydrogenase. J Neurochem 95:1446-1460. CrossRef Medline
53. Quirion R., Bowen WD, Itzhak Y, Junien JL, Musacchio JM, Rothman RB, Su TP, Tam SW, Taylor DP (1992) A proposal for the classification of sigma binding sites. Trends Pharmacol Sci 13:85-86. CrossRef Medline
54. Salussolia C. L, Prodromou ML, Borker P, Wollmuth LP (2011) Arrangement of subunits in functional NMDA receptors. J Neurosci 31:11295-11304. CrossRef Medline
55. Sans N., Petralia RS, Wang YX, Blahos J 2nd, Hell JW, Wenthold RJ (2000) A developmental change in NMDA receptor-associated proteins at hippocampal synapses. J Neurosci 20:1260-1271. Medline
56. Sanz-Clemente A., Nicoll RA, Roche KW (2013) Diversity in NMDA receptor composition: many regulators, many consequences. Neuroscientist 19:62-75. CrossRef Medline
57. Sato K., Saito Y, Kawashima S (1995) Identification and characterization of membrane-bound calpains in clathrin-coated vesicles from bovine brain. Eur J Biochem 230:25-31. CrossRef Medline
58. Schneider C. A, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671-675. CrossRef Medline
59. Standley S., Petralia RS, Gravell M, Hamilton R, Wang YX, Schubert M, Wenthold R. J (2012) Trafficking of theNMDAR2Breceptor subunit distal cytoplasmic tail from endoplasmic reticulum to the synapse. PLoS One 7:e39585. CrossRef Medline
60. Steinfels G. F, Alberici GP, Tam SW, Cook L (1988) Biochemical, behavioral, and electrophysiologic actions of the selective sigma receptor ligand (+)-pentazocine. Neuropsychopharmacology 1:321-327. Medline
61. Su T. P, Hayashi T, Maurice T, Buch S, Ruoho AE (2010) The sigma-1 receptor chaperone as an inter-organelle signaling modulator. Trends Pharmacol Sci 31:557-566. CrossRef Medline
62. Suh Y. H, Terashima A, Petralia RS, Wenthold RJ, Isaac JT, Roche KW, Roche PA (2010) A neuronal role for SNAP-23 in postsynaptic glutamate receptor trafficking. Nat Neurosci 13:338-343. CrossRef Medline
63. Taha M. S, Nouri K, Milroy LG, Moll JM, Herrmann C, Brunsveld L, Piekorz RP, Ahmadian MR (2014) Subcellular fractionation and localization studies reveal a direct interaction of the fragile X mental retardation protein (FMRP) with nucleolin. PLoS One 9:e91465. CrossRef Medline
64. Tchedre K. T, Huang RQ, Dibas A, Krishnamoorthy RR, Dillon GH, Yorio T (2008) Sigma-1 receptor regulation of voltage-gated calcium channels involves a direct interaction. Invest Ophthalmol Vis Sci 49:4993-5002. CrossRef Medline
65. Villa A., Sharp AH, Racchetti G, Podini P, Bole DG, Dunn WA, Pozzan T, Snyder S. H, Meldolesi J (1992) The endoplasmic reticulum of purkinje neuron body and dendrites: molecular identity and specializations for Ca2+ transport. Neuroscience 49:467-477. CrossRef Medline
66. Wanisch K., Wotjak CT (2008) Time course and efficiency of protein synthesis inhibition following intracerebral and systemic anisomycin treatment. Neurobiol Learn Mem 90:485-494. CrossRef Medline
67. Zambon A. C, De Costa BR, Kanthasamy AG, Nguyen BQ, Matsumoto RR (1997) Subchronic administration of N-[2-(3,4-dichlorophenyl) ethyl]-N-methyl-2-(dimethylamino) ethylamine (BD1047) alters sigma 1 receptor binding. Eur J Pharmacol 324:39-47. CrossRef Medline
68. Zhang H., Cuevas J (2002) Sigma receptors inhibit high-voltage-activated calcium channels in rat sympathetic and parasympathetic neurons. J Neurophysiol 87:2867-2879. Medline
69. Zhang H., Cuevas J (2005) Sigma receptor activation blocks potassium channels and depresses neuroexcitability in rat intracardiac neurons. J Pharmacol Exp Ther 313:1387-1396. CrossRef Medline
70. Zhang H., Katnik C, Cuevas J (2009) Sigma receptor activation inhibits voltage-gated sodium channels in rat intracardiac ganglion neurons. Int J Physiol Pathophysiol Pharmacol 2:1-11. Medline
71. Zhang X. J, Liu LL, Jiang SX, Zhong YM, Yang XL (2011a) Activation of the sigma receptor 1 suppressesNMDAresponses in rat retinal ganglion cells. Neuroscience 177:12-22. CrossRef Medline
72. Zhang X. J, Liu LL, Wu Y, Jiang SX, Zhong YM, Yang XL (2011b) sigma receptor 1 is preferentially involved in modulation of N-methyl-Daspartate receptor-mediated light-evoked excitatory postsynaptic currents in rat retinal ganglion cells. Neurosignals 19:110-116. CrossRef Medline