The sigma-1 receptor modulates NMDA receptor synaptic transmission and plasticity via SK channels in rat hippocampus

Journal of Physiology

Volumn 578, Issue 1, 2007, Pages 143-157

  Martina, Marzia ^a   Turcotte, Marie Eve B ^a   Halman, Samantha ^a   Bergeron, Richard ^a  

^a OTTAWA HOSPITAL RESEARCH INSTITUTE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ACTIVATED POTASSIUM CHANNEL; CALCIUM ION; LIGAND; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PENTAZOCINE; SIGMA 1 OPIATE RECEPTOR; SMALL CONDUCTANCE CALCIUM ACTIVATED POTASSIUM CHANNEL;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; CALCIUM TRANSPORT; CONTROLLED STUDY; HIPPOCAMPUS POTENTIAL; LONG TERM POTENTIATION; NERVE CELL PLASTICITY; NERVE CONDUCTION; NERVE POTENTIAL; NEUROMODULATION; NONHUMAN; PATCH CLAMP; POSTSYNAPTIC POTENTIAL; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; RECEPTOR BINDING; SYNAPTIC TRANSMISSION; HIPPOCAMPAL CA1 REGION; PROTEIN FUNCTION;

ALGORITHMS; ANIMALS; APAMIN; CALCIUM; CALCIUM SIGNALING; DATA INTERPRETATION, STATISTICAL; ELECTROPHYSIOLOGY; HIPPOCAMPUS; NARCOTIC ANTAGONISTS; NEURONAL PLASTICITY; PATCH-CLAMP TECHNIQUES; PENTAZOCINE; POTASSIUM CHANNELS, CALCIUM-ACTIVATED; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, N-METHYL-D-ASPARTATE; RECEPTORS, SIGMA; SYNAPTIC TRANSMISSION;

EID: 33845773372     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2006.116178     Document Type: Article

References (62)

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.
2. Behnisch T & Reymann KG (1998). Inhibition of apamin-sensitive calcium dependent potassium channels facilitate the induction of long-term potentiation in the CA1 region of rat hippocampus in vitro. Neurosci Lett 253, 91-94.
3. Bergeron R, de Montigny C & Debonnel G (1996). Potentiation of neuronal NMDA response induced by dehydroepiandrosterone and its suppression by progesterone: Effects mediated via sigma receptors. J Neurosci 16, 1193-1202.
4. 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.
5. Bergeron R, Debonnel G & de Montigny C (1993). Modification of the N-methyl-D-aspartate response by antidepressant sigma receptor ligands. Eur J Pharmacol 240, 319-323.
6. Bliss TV & Collingridge GL (1993). A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361, 31-39.
7. Bowen WD (2000). Sigma receptors: Recent advances and new clinical potentials. Pharm Acta Helv 74, 211-218.
8. Chen HX, Otmakhov N & Lisman J (1999). Requirements for LTP induction by pairing in hippocampal CA1 pyramidal cells. J Neurophysiol 82, 526-532.
9. Collingridge GL, Isaac JT & Wang YT (2004). Receptor trafficking and synaptic plasticity. Nat Rev Neurosci 5, 952-962.
10. Cull-Candy SG & Leszkiewicz DN (2004). Role of distinct NMDA receptor subtypes at central synapses. Sci STKE 2004, re16.
11. 2+ dependent afterhyperpolarisation in hippocampal CA3. Neuroscience 102, 297-306.
12. Faber ES, Delaney AJ & Sah P (2005). SK channels regulate excitatory synaptic transmission and plasticity in the lateral amygdala. Nat Neurosci 8, 635-641.
13. Faber ES & Sah P (2002). Physiological role of calcium-activated potassium currents in the rat lateral amygdala. J Neurosci 22, 1618-1628.
14. Ca 2/SK channels, contribute to the somatic medium after-hyperpolarization and excitability control in CA1 hippocampal pyramidal cells. J Physiol 566, 689-715.
15. + channel type 2 (SK2) modulates hippocampal learning, memory, and synaptic plasticity. J Neurosci 26, 1844-1853.
16. Hanner M, Moebius FF, Flandorfer A, Knaus HG, Striessnig J, Kempner E & Glossmann H (1996). Purification, molecular cloning, and expression of the mammalian sigma1-binding site. Proc Natl Acad Sci U S A 93, 8072-8077.
17. 2+ concentration. J Pharmacol Exp Ther 293, 788-798.
18. Hayashi T & Su TP (2004). Sigma-1 receptor ligands: Potential in the treatment of neuropsychiatric disorders. CNS Drugs 18, 269-284.
19. + channels. Neuron 31, 1027-1034.
20. Ishihara K & Sasa M (2002). Modulation of neuronal activities in the central nervous system via sigma receptors (in Japanese). Nihon Shinkei Seishin Yakurigaku Zasshi 22, 23-30.
21. Jbilo O, Vidal H, Paul R, De Nys N, Bensaid M, Silve S et al. (1997). Purification and characterization of the human SR 31747A-binding protein. A nuclear membrane protein related to yeast sterol isomerase. J Biol Chem 272, 27107-27115.
22. Karasawa J, Yamamoto H, Yamamoto T, Sagi N, Horikomi K & Sora I (2002). MS-377, a selective sigma receptor ligand, indirectly blocks the action of PCP in the N-methyl-D-aspartate receptor ion-channel complex in primary cultured rat neuronal cells. Life Sci 70, 1631-1642.
23. Kekuda R, Prasad PD, Fei YJ, Leibach FH & Ganapathy V (1996). Cloning and functional expression of the human type 1 sigma receptor (hSigmaR1). Biochem Biophys Res Commun 229, 553-558.
24. 2+ signals in spines of hippocampal neurons. J Neurosci 20, 1791-1799.
25. Kramar EA, Lin B, Lin C-Y, Arai AC, Gall CM & Lynch G (2004). A novel mechanism for the facilitation of theta-induced long-term potentiation by brain-derived neurotrophic factor. J Neurosci 24, 5151-5161.
26. + channels in rat neurohypophysial terminals requires neither G-protein nor ATP. J Physiol 526, 527-539.
27. McCleskey EW (1994). Calcium channels: Cellular roles and molecular mechanisms. Curr Opin Neurobiol 4, 304-312.
28. Martin WR, Eades CG, Thompson JA, Huppler RE & Gilbert PE (1976). The effects of morphine- and nalorphine-like drugs in the nondependent and morphine-dependent chronic spinal dog. J Pharmacol Exp Ther 197, 517-532.
29. Martina M, Gorfinkel Y, Halman S, Lowe JA, Periyalwar P, Schmidt CJ & Bergeron R (2004). Glycine transporter type 1 blockade changes NMDA receptor-mediated responses and LTP in hippocampal CA1 pyramidal cells by altering extracellular glycine levels. J Physiol 557, 489-500.
30. Moebius FF, Reiter RJ, Hanner M & Glossmann H (1997). High affinity of sigma 1-binding sites for sterol isomerization inhibitors: Evidence for a pharmacological relationship with the yeast sterol C8-C7 isomerase. Br J Pharmacol 121, 1-6.
31. Monnet FP, Debonnel G, Junien JL & de Montigny C (1990). N-methyl-D-aspartate-induced neuronal activation is selectively modulated by sigma receptors. Eur J Pharmacol 179, 441-445.
32. 2+-mediated feedback loop in dendritic spines. Nat Neurosci 8, 642-649.
33. Nicoll RA & Alger BE (1981). Synaptic excitation may activate a calcium-dependent potassium conductance in hippocampal pyramidal cells. Science 212, 957-959.
34. Nowak L, Bregestovski P, Ascher P, Herbet A & Prochiantz A (1984). Magnesium gates glutamate-activated channels in mouse central neurones. Nature 307, 462-465.
35. Oh MM, Kuo AG, Wu WW, Sametsky EA & Disterhoft JF (2003). Watermaze learning enhances excitability of CA1 pyramidal neurons. J Neurophisiol 90, 2171-2179.
36. + current underlying the slow spike frequency adaptation in hippocampal neurons. Neuron 11, 1023-1035.
37. 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.
38. Roman FJ, Pascaud X, Martin B, Vauche D & Junien JL (1990). JO 1784, a potent and selective ligand for rat and mouse brain sigma-sites. J Pharm Pharmacol 42, 439-440.
39. + currents in neurones: Types, physiological roles and modulation. Trends Neurosci 19, 150-154.
40. + channels in rat brain. J Neurosci 22, 9698-9707.
41. Seth P, Fei YJ, Li HW, Huang W, Leibach FH & Ganapathy V (1998). Cloning and functional characterization of a sigma receptor from rat brain. J Neurochem 70, 922-931.
42. Seth P, Leibach FH & Ganapathy V (1997). Cloning and structural analysis of the cDNA and the gene encoding the murine type 1 sigma receptor. Biochem Biophys Res Commun 241, 535-540.
43. + currents generated by NMDA receptor activation in rat hippocampal pyramidal neurons. J Neurophysiol 87, 2983-2989.
44. + channels modulate synaptic plasticity and memory encoding. J Neurosci 22, 10163-10171.
45. Stanley EF (1997). The calcium channel and the organization of the presynaptic transmitter release face. Trends Neurosci 20, 404-409.
46. +)-pentazocine. Neuropsychopharmacology 1, 321-327.
47. Stocca G & Vicini S (1998). Increased contribution of NR2A subunit to synaptic NMDA receptors in developing rat cortical neurons. J Physiol 507, 13-24.
48. + current in hippocampal pyramidal neurons. Proc Natl Acad Sci U S A 96, 4662-4667.
49. Storm JF (1987). Action potential repolarization and a fast after-hyperpolarization in rat hippocampal pyramidal cells. J Physiol 385, 733-759.
50. Storm JF (1989). An after-hyperpolarization of medium duration in rat hippocampal pyramidal cells. J Physiol 409, 171-190.
51. Storm JF (1990). Potassium currents in hippocampal pyramidal cells. Prog Brain Res 83, 161-187.
52. Su TP (1993). Delineating biochemical and functional properties of sigma receptors: Emerging concepts. Crit Rev Neurobiol 7, 187-203.
53. Su TP & Hayashi T (2003). Understanding the molecular mechanism of sigma-1 receptors: Towards a hypothesis that sigma-1 receptors are intracellular amplifiers for signal transduction. Curr Med Chem 10, 2073-2080.
54. Waxman EA & Lynch DR (2005). N-methyl-D-aspartate receptor subtypes: multiple roles in excitotoxicity and neurological disease. Neuroscientist 11, 37-49.
55. Westenbroek RE, Hell JW, Warner C, Dubel SJ, Snutch TP & Catterall WA (1992). Biochemical properties and subcellular distribution of an N-type calcium channel alpha 1 subunit. Neuron 9, 1099-1115.
56. Westenbroek RE, Sakurai T, Elliott EM, Hell JW, Starr TV, Snutch TP & Catterall WA (1995). Immunochemical identification and subcellular distribution of the alpha 1A subunits of brain calcium channels. J Neurosci 15, 6403-6418.
57. + channel modulation in rodent neurohypophysial nerve terminals by sigma receptors and not by dopamine receptors. J Physiol 517, 391-406.
58. Xia XM, Fakler B, Rivard A, Wayman G, Johnson-Pais T, Keen JE et al. (1998). Mechanism of calcium gating in small-conductance calcium-activated potassium channels. Nature 395, 503-507.
59. Yamamoto H, Yamamoto T, Sagi N, Klenerova V, Goji K, Kawai N, Baba A, Takamori E & Moroji T (1995). Sigma ligands indirectly modulate the NMDA receptor-ion channel complex on intact neuronal cells via sigma 1 site. J Neurosci 15, 731-736.
60. Zhang H & Cuevas J (2002). Sigma receptors inhibit high-voltage-activated calcium channels in rat sympathetic and parasympathetic neurons. J Neurophysiol 87, 2867-2879.
61. Zorumski CF, Thio LL, Clark GD & Clifford DB (1989). Calcium influx through N-methyl-D-aspartate channels activates a potassium current in postnatal rat hippocampal neurons. Neurosci Lett 99, 293-299.
62. Zukin SR & Zukin RS (1979). Specific [3H]phencyclidine binding in rat central nervous system. Proc Natl Acad Sci U S A 76, 5372-5376.