The calcium-sensitive Sigma-1 receptor prevents cannabinoids from provoking glutamate NMDA receptor hypofunction: Implications in antinociception and psychotic diseases

International Journal of Neuropsychopharmacology

Volumn 17, Issue 12, 2014, Pages 1943-1955

  Sánchez Blázquez, Pilar ^a   Rodríguez Muñoz, María ^a   Herrero Labrador, Raquel ^a   Burgueño, Javier ^b   Zamanillo, Daniel ^b   Garzón, Javier ^a  

^a INSTITUTO CAJAL   (Spain)

^b Drug Discovery and Preclinical Development   (Spain)

Author keywords

Antinociception; Cannabinoid receptor type 1; HINT1 protein; NMDA receptor hypofunction; Schizophrenia; Sigma 1 receptor

Indexed keywords

1 PHENYLCYCLOHEXANECARBOXYLIC ACID 2 MORPHOLINOETHYL ESTER; 2 [4 METHOXY 3 (2 PHENYLETHOXY)PHENYL] N,N DIPROPYLETHYLAMINE; 4 [ 2 [( 5 METHYL 1 ( 2 NAPHTHALENYL) 1H PYRAZOL 3 YL)OXY]ETHYL]MORPHOLINE; BD 1063; CALCIUM; CANNABINOID; CANNABINOID 1 RECEPTOR; GLUTAMATE RECEPTOR; GLUTAMIC ACID; IFENPRODIL; LIGAND; METHANANDAMIDE; N ALLYLNORMETAZOCINE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT; N [2 (3,4 DICHLOROPHENYL)ETHYL] 2 DIMETHYLAMINO N METHYLETHYLAMINE; OPIATE ANTAGONIST; OPIATE RECEPTOR AFFECTING AGENT; PENTAZOCINE; SIGMA 1 OPIATE RECEPTOR; UNCLASSIFIED DRUG; CNR1 PROTEIN, MOUSE; HINT1 PROTEIN, MOUSE; NERVE PROTEIN; SIGMA OPIATE RECEPTOR;

ANALGESIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANTINOCICEPTION; ARTICLE; BRAIN CELL CULTURE; CONTROLLED STUDY; DRUG ANTAGONISM; DRUG EFFECT; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NEUROPROTECTION; NEUROTRANSMITTER RELEASE; NONHUMAN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PSYCHOSIS; WILD TYPE; ANIMAL; ANTAGONISTS AND INHIBITORS; BRAIN CORTEX; CELL CULTURE; CHO CELL LINE; CRICETULUS; DRUG EFFECTS; KNOCKOUT MOUSE; MALE; METABOLISM; NOCICEPTION; PATHOPHYSIOLOGY; PHYSIOLOGY; SCHIZOPHRENIA;

ANIMALS; CANNABINOIDS; CELLS, CULTURED; CEREBRAL CORTEX; CHO CELLS; CRICETULUS; GLUTAMIC ACID; MALE; MICE, KNOCKOUT; NERVE TISSUE PROTEINS; NOCICEPTION; PSYCHOTIC DISORDERS; RECEPTOR, CANNABINOID, CB1; RECEPTORS, N-METHYL-D-ASPARTATE; RECEPTORS, SIGMA; SCHIZOPHRENIA;

EID: 84910142500     PISSN: 14611457     EISSN: 14695111     Source Type: Journal    
DOI: 10.1017/S1461145714000029     Document Type: Article

References (61)

1. Arseneault L, Cannon M, Witton J, Murray RM (2004) Causal association between cannabis and psychosis: examination of the evidence. Br J Psychiatry 184:110-117.
2. Ashton JC, Milligan ED (2008) Cannabinoids for the treatment of neuropathic pain: clinical evidence. Curr Opin Investig Drugs 9:65-75.
3. Broome MR, Woolley JB, Tabraham P, Johns LC, Bramon E, Murray GK, Pariante C, McGuire PK, Murray RM (2005) What causes the onset of psychosis? Schizophr Res 79:23-34.
4. Cannon M, Clarke MC (2005) Risk for schizophrenia - broadening the concepts, pushing back the boundaries. Schizophr Res 79:5-13.
5. Chen Q, Wang X, O'Neill FA, Walsh D, Kendler KS, Chen X (2008) Is the histidine triad nucleotide-binding protein 1 (HINT1) gene a candidate for schizophrenia? Schizophr Res 106:200-207.
6. Chen Y, Hajipour AR, Sievert MK, Arbabian M, Ruoho AE (2007) Characterization of the cocaine binding site on the sigma-1 receptor. Biochemistry 46:3532-3542.
7. Degenhardt L, Hall W, Lynskey M (2003) Testing hypotheses about the relationship between cannabis use and psycho. Drug Alcohol Depend 71:37-48.
8. Di FM, Iyegbe C, Sallis H, Kolliakou A, Falcone MA, Paparelli A, Sirianni M, La CC, Stilo SA, Marques TR, Handley R, Mondelli V, Dazzan P, Pariante C, David AS, Morgan C, Powell J, Murray RM (2012) Confirmation that the AKT1 (rs2494732) genotype influences the risk of psychosis in cannabis users. Biol Psychiatry 72:811-816.
9. Diaz JL, Cuberes R, Berrocal J, Contijoch M, Christmann U, Fernandez A, Port A, Holenz J, Buschmann H, Laggner C, Serafini MT, Burgueno J, Zamanillo D, Merlos M, Vela JM, Almansa C (2012) Synthesis and biological evaluation of the 1-arylpyrazole class of sigma(1) receptor antagonists: identification of 4-{2-[5-methyl-1-(naphthalen-2-yl)-1H-pyrazol- 3-yloxy]ethyl}morpholine (S1RA, E-52862). J Med Chem 55:8211-8224.
10. Gallagher MJ, Huang H, Pritchett DB, Lynch DR (1996) Interactions between ifenprodil and the NR2B subunit of the N-methyl-D-aspartate receptor. J Biol Chem 271:9603-9611.
11. Garzón J, Rodríguez-Muñoz M, López-Fando A, Sánchez-Blázquez P (2005) Activation of μ-opioid receptors transfers control of Gá subunits to the regulator of G-protein signaling RGS9-2: role in receptor desensitization. J Biol Chem 280:8951-8960.
12. Garzón J, Torre-Madrid E, Rodríguez-Muñoz M, Vicente-Sánchez A, ánchez-Blázquez P (2009) Gz mediates the long-lasting desensitization of brain CB1 receptors and is essential for cross-tolerance with morphine. Mol Pain 5:11.
13. Garzón J, Rodríguez-Muñoz M, Sánchez-Blazquez P (2012) Direct association of Mu-opioid and NMDA glutamate receptors supports their cross-regulation: molecular implications for opioid tolerance. Curr Drug Abuse Rev 5:199-226.
14. Haley TJ, McCormick WG (1957) Pharmacological effects produced by intracerebral injection of drugs in the conscious mouse. Br J Pharmacol Chemother 12:12-15.
15. Hampson RE, Miller F, Palchik G, Deadwyler SA (2011) Cannabinoid receptor activation modifies NMDA receptor mediated release of intracellular calcium: implications for endocannabinoid control of hippocampal neural plasticity. Neuropharmacology 60:944-952.
16. Harrison PJ, Weinberger DR (2005) Schizophrenia genes, gene expression, and neuropathology: on the matter of their convergence. Mol Psychiatry 10:40-68.
17. Hayashi T, Su TP (2007) Sigma-1 receptor chaperones at the ER-mitochondrion interface regulate Ca(2+) signaling and cell survival. Cell 131:596-610.
18. Hayashi T, Tsai SY, Mori T, Fujimoto M, Su TP (2011) Targeting ligand-operated chaperone sigma-1 receptors in the treatment of neuropsychiatric disorders. Expert Opin Ther Targets 15:557-577.
19. Javitt DC (2007) Glutamate and schizophrenia: phencyclidine, N-methyl-D-aspartate receptors, and dopamine-glutamate interactions. Int Rev Neurobiol 78:69-108.
20. Kashiwagi K, Masuko T, Nguyen CD, Kuno T, Tanaka I, Igarashi K, Williams K (2002) Channel blockers acting at N-methyl-D-aspartate receptors: differential effects of mutations in the vestibule and ion channel pore. Mol Pharmacol 61:533-545.
21. Kim FJ, Kovalyshyn I, Burgman M, Neilan C, Chien CC, Pasternak GW (2010) Sigma 1 receptor modulation of G-protein-coupled receptor signaling: potentiation of opioid transduction independent from receptor binding. Mol Pharmacol 77:695-703.
22. Kim SH, Won SJ, Mao XO, Jin K, Greenberg DA (2006) Molecular mechanisms of cannabinoid protection from neuronal excitotoxicity. Mol Pharmacol 69:691-696.
23. Kristiansen LV, Huerta I, Beneyto M, Meador-Woodruff JH (2007) NMDA receptors and schizophrenia. Curr Opin Pharmacol 7:48-55.
24. Kume T, Nishikawa H, Taguchi R, Hashino A, Katsuki H, Kaneko S, Minami M, Satoh M, Akaike A (2002) Antagonism of NMDA receptors by sigma receptor ligands attenuates chemical ischemia-induced neuronal death in vitro. Eur J Pharmacol 455:91-100.
25. Labrie V, Roder JC (2010) The involvement of the NMDA receptor D-serine/glycine site in the pathophysiology and treatment of schizophrenia. Neurosci Biobehav Rev 34:351-372.
26. Langa F, Codony X, Tovar V, Lavado A, Gimenez E, Cozar P, Cantero M, Dordal A, Hernandez E, Perez 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.
27. Laube B, Schemm R, Betz H (2004) Molecular determinants of ligand discrimination in the glutamate-binding pocket of the NMDA receptor. Neuropharmacology 47:994-1007.
28. Li Q, Yan H, Wilson WA, Swartzwelder HS (2010) Modulation of NMDA and AMPA-mediated synaptic transmission by CB1 receptors in frontal cortical pyramidal cells. Brain Res 1342:127-137.
29. Liu Q, Bhat M, Bowen WD, Cheng J (2009) Signaling pathways from cannabinoid receptor-1 activation to inhibition of N-methyl-D-aspartic acid mediated calcium influx and neurotoxicity in dorsal root ganglion neurons. J Pharmacol Exp Ther 331:1062-1070.
30. Lockhart BP, Soulard P, Benicourt C, Privat A, Junien JL (1995) Distinct neuroprotective profiles for sigma ligands against N-methyl-D-aspartate (NMDA), and hypoxia-mediated neurotoxicity in neuronal culture toxicity studies. Brain Res 675:110-120.
31. Marchalant Y, Cerbai F, Brothers HM, Wenk GL (2008) Cannabinoid receptor stimulation is anti-inflammatory and improves memory in old rats. Neurobiol Aging 29:1894-1901.
32. Marsicano G, Goodenough S, Monory K, Hermann H, Eder M, Cannich A, Azad SC, Cascio MG, Gutierrez SO, van der Stelt M, Lopez-Rodriguez ML, Casanova E, Schutz G, Zieglgansberger W, Di Marzo V, Behl C, Lutz B (2003) CB1 cannabinoid receptors and on-demand defense against excitotoxicity. Science 302:84-88.
33. Marx CE, Stevens RD, Shampine LJ, Uzunova V, Trost WT, Butterfield MI, Massing MW, Hamer RM, Morrow AL, Lieberman JA (2006) Neuroactive steroids are altered in schizophrenia and bipolar disorder: relevance to pathophysiology and therapeutics. Neuropsychopharmacology 31:1249-1263.
34. Marx CE, Keefe RS, Buchanan RW, Hamer RM, Kilts JD, Bradford DW, Strauss JL, Naylor JC, Payne VM, Lieberman JA, Savitz AJ, Leimone LA, Dunn L, Porcu P, Morrow AL, Shampine LJ (2009) Proof-of-concept trial with the neurosteroid pregnenolone targeting cognitive and negative symptoms in schizophrenia. Neuropsychopharmacology 34:1885-1903.
35. Moghaddam B, Javitt D (2012) From revolution to evolution: the glutamate hypothesis of schizophrenia and its implication for treatment. Neuropsychopharmacology 37:4-15.
36. Mohn AR, Gainetdinov RR, Caron MG, Koller BH (1999) Mice with reduced NMDA receptor expression display behaviors related to schizophrenia. Cell 98:427-436.
37. Monnet FP, Debonnel G, Junien JL, De MC (1990) N-methyl-D-aspartate-induced neuronal activation is selectively modulated by sigma receptors. Eur J Pharmacol 179:441-445.
38. Mouri A, Noda Y, Enomoto T, Nabeshima T (2007) Phencyclidine animal models of schizophrenia: approaches from abnormality of glutamatergic neurotransmission and neurodevelopment. Neurochem Int 51:173-184.
39. Nishikawa H, Hashino A, Kume T, Katsuki H, Kaneko S, Akaike A (2000) Involvement of direct inhibition of NMDA receptors in the effects of sigma-receptor ligands on glutamate neurotoxicity in vitro. Eur J Pharmacol 404:41-48.
40. Ortega-Roldan JL, Ossa F, Schnell JR (2013) Characterization of the human Sigma-1 receptor chaperone domain structure and BiP interactions. J Biol Chem 288:21448-21457.
41. Pasternak GW, Kolesnikov YA, Babey AM (1995) Perspectives on the N-methyl-D-aspartate/nitric oxide cascade and opioid tolerance. Neuropsychopharmacology 13:309-313.
42. Richardson JD, Aanonsen L, Hargreaves KM (1998) Hypoactivity of the spinal cannabinoid system results in NMDA-dependent hyperalgesia. J Neurosci 18:451-457.
43. Ritsner M, Maayan R, Gibel A, Weizman A (2007) Differences in blood pregnenolone and dehydroepiandrosterone levels between schizophrenia patients and healthy subjects. Eur Neuropsychopharmacol 17:358-365.
44. Ritsner MS (2011) The clinical and therapeutic potentials of dehydroepiandrosterone and pregnenolone in schizophrenia. Neuroscience 191:91-100.
45. Ritsner MS, Gibel A, Shleifer T, Boguslavsky I, Zayed A, Maayan R, Weizman A, Lerner V (2010) Pregnenolone and dehydroepiandrosterone as an adjunctive treatment in schizophrenia and schizoaffective disorder: an 8-week, double-blind, randomized, controlled, 2-center, parallel-group trial. J Clin Psychiatry 71:1351-1362.
46. Robson MJ, Noorbakhsh B, Seminerio MJ, Matsumoto RR (2012) Sigma-1 receptors: potential targets for the treatment of substance abuse. Curr Pharm Des 18:902-919.
47. Rodríguez-Muñoz M, de la Torre-Madrid E, Sánchez-Blázquez P, Garzón J (2007) Morphine induces endocytosis of neuronal μ-opioid receptors through the sustained transfer of Gá subunits to RGSZ2 proteins. Mol Pain 3:19.
48. Rodríguez-Muñoz M, Sánchez-Blázquez P, Vicente-Sánchez A, Bailón C, Martín-Aznar B, Garzón J (2011) The histidine triad nucleotide-binding protein 1 supports mu-opioid receptorglutamate NMDA receptor cross-regulation. Cell Mol Life Sci 68:2933-2949.
49. Rodríguez-Muñoz M, Sánchez-Blázquez P, Vicente-Sánchez A, Berrocoso E, Garzón J (2012) The Mu-Opioid receptor and the NMDA receptor associate in PAG neurons: implications in pain control. Neuropsychopharmacology 37:338-349.
50. Romero L et al. (2012) Pharmacological properties of S1RA, a new sigma-1 receptor antagonist that inhibits neuropathic pain and activity-induced spinal sensitization. Br J Pharmacol 166:2289-2306.
51. Sánchez-Blázquez P, Rodríguez-Muñoz M, Vicente-Sánchez A, Garzón J (2013) Cannabinoid receptors couple to NMDA receptors to reduce the production of NO and the mobilization of zinc induced by glutamate. Antioxid Redox Signal 19:1766-1782.
52. Sánchez-Fernández C, Nieto FR, González-Cano R, Artacho-Cordón A, Romero L, Montilla-García A, Zamanillo D, Baeyens JM, Entrena JM, Cobos EJ (2013) Potentiation of morphine-induced mechanical antinociception by sigma receptor inhibition: role of peripheral sigma receptors. Neuropharmacology 70C:348-358.
53. Shibuya H, Mori H, Toru M (1992) Sigma receptors in schizophrenic cerebral cortices. Neurochem Res 17:983-990.
54. Shimazu S, Katsuki H, Takenaka C, Tomita M, Kume T, Kaneko S, Akaike A (2000) sigma receptor ligands attenuate N-methyl-D-aspartate cytotoxicity in dopaminergic neurons of mesencephalic slice cultures. Eur J Pharmacol 388:139-146.
55. Shirayama Y, Hashimoto K, Suzuki Y, Higuchi T (2002) Correlation of plasma neurosteroid levels to the severity of negative symptoms in male patients with schizophrenia. Schizophr Res 58:69-74.
56. Thorat SN, Bhargava HN (1994) Effects of NMDA receptor blockade and nitric oxide synthase inhibition on the acute and chronic actions of delta 9-tetrahydrocannabinol in mice. Brain Res 667:77-82.
57. Vawter MP, Crook JM, Hyde TM, Kleinman JE, Weinberger DR, Becker KG, Freed WJ (2002) Microarray analysis of gene expression in the prefrontal cortex in schizophrenia: a preliminary study. Schizophr Res 58:11-20.
58. Vawter MP, Shannon WC, Ferran E, Matsumoto M, Overman K, Hyde TM, Weinberger DR, Bunney WE, Kleinman JE (2004) Gene expression of metabolic enzymes and a protease inhibitor in the prefrontal cortex are decreased in schizophrenia. Neurochem Res 29:1245-1255.
59. Vicente-Sánchez A, Sánchez-Blázquez P, Rodríguez-Muñoz M, Garzón J (2013) HINT1 protein cooperates with cannabinoid 1 receptor to negatively regulate glutamate NMDA receptor activity. Mol Brain 6:42.
60. Watanabe Y, Nunokawa A, Kaneko N, Shibuya M, Egawa J, Someya T (2012) Supportive evidence for the association between the Gln2Pro polymorphism in the SIGMAR1 gene and schizophrenia in the Japanese population: a case-control study and an updated meta-analysis. Schizophr Res 141:279-280.
61. Weissman AD, Casanova MF, Kleinman JE, London ED, De Souza EB (1991) Selective loss of cerebral cortical sigma, but not PCP binding sites in schizophrenia. Biol Psychiatry 29:41-54.