The σ1 Receptor Engages the Redox-Regulated HINT1 Protein to Bring Opioid Analgesia Under NMDA Receptor Negative Control

Antioxidants and Redox Signaling

Volumn 22, Issue 10, 2015, Pages 799-818

  Rodríguez Muñoz, María ^a   Sánchez Blázquez, Pilar ^a   Herrero Labrador, Raquel ^a   Martínez Murillo, Ricardo ^a   Merlos, Manuel ^b   Vela, José Miguel ^b   Garzón, Javier ^a  

^a INSTITUTO CAJAL   (Spain)

^b Drug Discovery and Preclinical Development   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

HINT1 PROTEIN; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NITRIC OXIDE SYNTHASE; PROTEIN; PROTEIN KINASE C GAMMA; SIGMA 1 OPIATE RECEPTOR; SUMO 1 PROTEIN; UNCLASSIFIED DRUG; HINT1 PROTEIN, MOUSE; MORPHINE; NARCOTIC ANALGESIC AGENT; NERVE PROTEIN; NITRIC OXIDE; PROTEIN KINASE C; RGS PROTEIN; RGS17 PROTEIN, MOUSE; SIGMA OPIATE RECEPTOR; SIGMA-1 RECEPTOR; ZINC;

ANIMAL EXPERIMENT; ANTINOCICEPTION; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM MEMBRANE; EXTRACELLULAR SPACE; IN VITRO STUDY; MALE; MOUSE; NEGATIVE FEEDBACK; NEUROPATHIC PAIN; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; ZINC METABOLISM; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL MEMBRANE; DRUG EFFECTS; GENETICS; KNOCKOUT MOUSE; METABOLISM; OXIDATION REDUCTION REACTION;

ANIMALIA; MUS;

ANALGESICS, OPIOID; ANIMALS; CELL MEMBRANE; MICE; MICE, KNOCKOUT; MORPHINE; NERVE TISSUE PROTEINS; NITRIC OXIDE; OXIDATION-REDUCTION; PROTEIN KINASE C; RECEPTORS, N-METHYL-D-ASPARTATE; RECEPTORS, SIGMA; RGS PROTEINS; ZINC;

EID: 84924959117     PISSN: 15230864     EISSN: 15577716     Source Type: Journal    
DOI: 10.1089/ars.2014.5993     Document Type: Article

References (70)

1. Abadias M, Escriche M, Vaque A, Sust M, and Encina G. Safety, tolerability and pharmacokinetics of single and multiple doses of a novel sigma-1 receptor antagonist in three randomized phase I studies. Br J Clin Pharmacol 75: 103-117, 2013.
2. Ajit SK, Ramineni S, Edris W, Hunt RA, Hum WT, Hepler JR, and Young KH. RGSZ1 interacts with protein kinase C interacting protein PKCI-1 and modulates mu opioid receptor signaling. Cell Signal 19: 723-730, 2007.
3. Aydar E, Palmer CP, Klyachko VA, and Jackson MB. The sigma receptor as a ligand-regulated auxiliary potassium channel subunit. Neuron 34: 399-410, 2002.
4. Balasuriya D, Stewart AP, and Edwardson JM. The sigma-1 receptor interacts directly with GluN1 but not GluN2A in the GluN1/GluN2A NMDA receptor. J Neurosci 33: 18219-18224, 2013.
5. Chakravarthy B, Morley P, and Whitfield J. Ca2 + -calmodulin and protein kinase Cs: a hypothetical synthesis of their conflicting convergences on shared substrate domains. Trends Neurosci 22: 12-16, 1999.
6. Chen YJ, Oldfield S, Butcher AJ, Tobin AB, Saxena K, Gurevich VV, Benovic JL, Henderson G, and Kelly E. Identification of phosphorylation sites in the COOHterminal tail of the mu-opioid receptor. J Neurochem 124: 189-199, 2013.
7. Chu UB, Ramachandran S, Hajipour AR, and Ruoho AE. Photoaffinity labeling of the sigma-1 receptor with N-[3-(4-nitrophenyl)propyl]-N-dodecylamine: evidence of receptor dimers. Biochemistry 52: 859-868, 2013.
8. Diaz JL, Zamanillo D, Corbera J, Baeyens JM, Maldonado R, Pericas MA, Vela JM, and Torrens A. Selective sigma-1 (σ1) receptor antagonists: emerging target for the treatment of neuropathic pain. Cent Nerv Syst Agents Med Chem 9: 172-183, 2009.
9. Doll C, Konietzko J, Poll F, Koch T, Höllt V, and Schulz S. Agonist-selective patterns of l-opioid receptor phosphorylation revealed by phosphosite-specific antibodies. Br J Pharmacol 164: 298-307, 2011.
10. Doyle T, Bryant L, Muscoli C, Cuzzocrea S, Esposito E, Chen Z, and Salvemini D. Spinal NADPH oxidase is a source of superoxide in the development of morphineinduced hyperalgesia and antinociceptive tolerance. Neurosci Lett 483: 85-89, 2010.
11. Ehlers MD, Zhang S, Bernhadt JP, and Huganir RL. Inactivation of NMDA receptors by direct interaction of calmodulin with the NR1 subunit. Cell 84: 745-755, 1996.
12. Finn AK and Whistler JL. Endocytosis of the mu opioid receptor reduces tolerance and a cellular hallmark of opiate withdrawal. Neuron 32: 829-839, 2001.
13. Garzón J, Rodríguez-Muñoz M, López-Fando A, and Sánchez-Blázquez P. Activation of μ-opioid receptors transfers control of Gα subunits to the regulator of G-protein signaling RGS9-2: role in receptor desensitization. J Biol Chem 280: 8951-8960, 2005.
14. Garzón J, Rodríguez-Muñoz M, and Sánchez-Blazquez P. 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, 2012.
15. Garzón J, Rodríguez-Muñoz M, Vicente-Sánchez A, Bailón C, Martínez-Murillo R, and Sánchez-Blázquez P. RGSZ2 binds to the neural nitric oxide synthase PDZ domain to regulate mu-opioid receptor-mediated potentiation of the N-methyl-D-aspartate receptor-calmodulin-dependent protein kinase II pathway. Antioxid Redox Signal 15: 873-887, 2011.
16. Garzón J, Rodríguez-Muñoz M, Vicente-Sánchez A, García-López MA, Martínez-Murillo R, Fischer T, and Sánchez-Blázquez P. SUMO-SIM Interactions Regulate the Activity of RGSZ2 Proteins. PLoS One 6: e28557, 2011.
17. Garzón J, Torre-Madrid E, Rodríguez-Muñoz M, Vicente-Sánchez A, and Sánchez-Blázquez P. Gz mediates the longlasting desensitization of brain CB1 receptors and is essential for cross-tolerance with morphine. Mol Pain 5: 11, 2009.
18. Gebhart GF and Jones SL. Effects of morphine given in the brain stem on the activity of dorsal horn nociceptive neurons. Prog Brain Res 77: 229-243, 1988.
19. Gibbs TT and Farb DH. Dueling enigmas: neurosteroids and sigma receptors in the limelight. Sci STKE 2000: e1, 2000.
20. Guang W, Wang H, Su T, Weinstein IB, and Wang JB. Role of mPKCI, a novel mu-opioid receptor interactive protein, in receptor desensitization, phosphorylation, and morphineinduced analgesia. Mol Pharmacol 66: 1285-1292, 2004.
21. Hanner M, Moebius FF, Flandorfer A, Knaus HG, Striessnig J, Kempner E, and Glossmann H. Purification, molecular cloning, and expression of the mammalian sigma1-binding site. Proc Natl Acad Sci U S A 93: 8072-8077, 1996.
22. Hayashi T and Su TP. Sigma-1 receptor ligands: potential in the treatment of neuropsychiatric disorders. CNS Drugs 18: 269-284, 2004.
23. Ibi M, Matsuno K, Matsumoto M, Sasaki M, Nakagawa T, Katsuyama M, Iwata K, Zhang J, Kaneko S, and Yabe-Nishimura C. Involvement of NOX1/NADPH oxidase in morphine-induced analgesia and tolerance. J Neurosci 31: 18094-18103, 2011.
24. Kerscher O. SUMO junction-what's your function? New insights through SUMO-interacting motifs. EMBO Rep 8: 550-555, 2007.
25. Kim FJ, Kovalyshyn I, Burgman M, Neilan C, Chien CC, and Pasternak GW. Sigma 1 receptor modulation of G-protein-coupled receptor signaling: potentiation of opioid transduction independent from receptor binding. Mol Pharmacol 77: 695-703, 2010.
26. Kim HW, Kwon YB, Roh DH, Yoon SY, Han HJ, Kim KW, Beitz AJ, and Lee JH. Intrathecal treatment with sigma1 receptor antagonists reduces formalin-induced phosphorylation of NMDA receptor subunit 1 and the second phase of formalin test in mice. Br J Pharmacol 148: 490-498, 2006.
27. Kim HW, Roh DH, Yoon SY, Seo HS, Kwon YB, Han HJ, Kim KW, Beitz AJ, and Lee JH. Activation of the spinal sigma-1 receptor enhances NMDA-induced pain via PKCand PKA-dependent phosphorylation of the NR1 subunit in mice. Br J Pharmacol 154: 1125-1134, 2008.
28. 1) receptor in the mammalian brain and its possible relevance in deficits induced by antagonism of the NMDA receptor complex as revealed using an antisense strategy. J Chem Neuroanat 20: 375-387, 2000.
29. Kitto KF and Fairbanks CA. Supraspinally administered agmatine prevents the development of supraspinal morphine analgesic tolerance. Eur J Pharmacol 536: 133-137, 2006.
30. Kohjitani A, Fuda H, Hanyu O, and Strott CA. Regulation of SULT2B1a (pregnenolone sulfotransferase) expression in rat C6 glioma cells: relevance of AMPA receptormediated NO signaling. Neurosci Lett 430: 75-80, 2008.
31. Kourrich S, Su TP, Fujimoto M, and Bonci A. The sigma-1 receptor: roles in neuronal plasticity and disease. Trends Neurosci 35: 762-771, 2012.
32. 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, and Montoliu L. Generation and phenotypic analysis of sigma receptor type I (sigma 1) knockout mice. Eur J Neurosci 18: 2188-2196, 2003.
33. Laurini E, Da Col, V, Wunsch B, and Pricl S. Analysis of the molecular interactions of the potent analgesic S1RA with the sigma1 receptor. Bioorg Med Chem Lett 23: 2868-2871, 2013.
34. Lima CD, Klein MG, Weinstein IB, and Hendrickson WA. Three-dimensional structure of human protein kinase C interacting protein 1, a member of the HIT family of proteins. Proc Natl Acad Sci U S A 93: 5357-5362, 1996.
35. Martin WR, Eades CG, Thompson JA, Huppler RE, and Gilbert PE. The effects of morphine- and nalorphine-like drugs in the nondependent and morphine-dependent chronic spinal dog. J Pharmacol Exp Ther 197: 517-532, 1976.
36. Martina M, Turcotte ME, Halman S, and Bergeron R. The sigma-1 receptor modulates NMDA receptor synaptic transmission and plasticity via SK channels in rat hippocampus. J Physiol 578: 143-157, 2007.
37. Maurice T. Neurosteroids and sigma1 receptors, biochemical and behavioral relevance. Pharmacopsychiatry 37 Suppl 3: S171-S182, 2004.
38. Maurice T and Su TP. The pharmacology of sigma-1 receptors. Pharmacol Ther 124: 195-206, 2009.
39. Mei J and Pasternak GW. Sigma1 receptor modulation of opioid analgesia in the mouse. J Pharmacol Exp Ther 300: 1070-1074, 2002.
40. Merrill MA, Malik Z, Akyol Z, Bartos JA, Leonard AS, Hudmon A, Shea MA, and Hell JW. Displacement of alpha-actinin from the NMDA receptor NR1 C0 domain By Ca2 + /calmodulin promotes CaMKII binding. Biochemistry 46: 8485-8497, 2007.
41. Monnet FP, Debonnel G, Junien JL, and De MC. N-methyl-D-aspartate-induced neuronal activation is selectively modulated by sigma receptors. Eur J Pharmacol 179: 441-445, 1990.
42. Okamoto T, Schlegel A, Scherer PE, and Lisanti MP. Caveolins, a family of scaffolding proteins for organizing "preassembled signaling complexes" at the plasma membrane. J Biol Chem 273: 5419-5422, 1998.
43. Ortega-Roldan JL, Ossa F, and Schnell JR. Characterization of the human sigma-1 receptor chaperone domain structure and binding immunoglobulin protein (BiP) interactions. J Biol Chem 288: 21448-21457, 2013.
44. Pal A, Chu UB, Ramachandran S, Grawoig D, Guo LW, Hajipour AR, and Ruoho AE. Juxtaposition of the steroid binding domain-like I and II regions constitutes a ligand binding site in the sigma-1 receptor. J Biol Chem 283: 19646-19656, 2008.
45. Pasternak GW, Kolesnikov YA, and Babey AM. Perspectives on the N-methyl-D-aspartate/nitric oxide cascade and opioid tolerance. Neuropsychopharmacology 13: 309-313, 1995.
46. Robson MJ, Noorbakhsh B, Seminerio MJ, and Matsumoto RR. Sigma-1 receptors: potential targets for the treatment of substance abuse. Curr Pharm Des 18: 902-919, 2012.
47. Rodríguez-Muñoz M and Garzón J. Nitric oxide and zincmediated protein assemblies involved in mu opioid receptor signaling. Mol Neurobiol 48: 769-782, 2013.
48. Rodríguez-Muñoz M, Sánchez-Blázquez P, Vicente-Sánchez A, Bailón C, Martín-Aznar B, and Garzón J. The histidine triad nucleotide-binding protein 1 supports muopioid receptor-glutamate NMDA receptor cross-regulation. Cell Mol Life Sci 68: 2933-2949, 2011.
49. Rodríguez-Muñoz M, Sánchez-Blázquez P, Vicente-Sánchez A, Berrocoso E, and Garzón J. The mu-opioid receptor and the nmda receptor associate in PAG neurons: implications in pain control. Neuropsychopharmacology 37: 338-349, 2012.
50. Rodríguez-Muñoz M, Torre-Madrid E, Sánchez-Blázquez P, and Garzón J. NO-released zinc supports the simultaneous binding of Raf-1 and PKCgamma cysteine-rich domains to HINT1 protein at the mu-opioid receptor. Antioxid Redox Signal 14: 2413-2425, 2011.
51. Rodríguez-Muńoz M, Torre-Madrid E, Sánchez-Blázquez P, Wang JB, and Garzón J. NMDAR-nNOS generated zinc recruits PKCgamma to the HINT1-RGS17 complex bound to the C terminus of Mu-opioid receptors. Cell Signal 20: 1855-1864, 2008.
52. Roh DH, Kim HW, Yoon SY, Seo HS, Kwon YB, Kim KW, Han HJ, Beitz AJ, Na HS, and Lee JH. Intrathecal injection of the sigma1 receptor antagonist BD1047 blocks both mechanical allodynia and increases in spinal NR1 expression during the induction phase of rodent neuropathic pain. Anesthesiology 109: 879-889, 2008.
53. Romero L, Zamanillo D, Nadal X, Sanchez-Arroyos R, Rivera-Arconada I, Dordal A, Montero A, Muro A, Bura A, Segales C, Laloya M, Hernandez E, Portillo-Salido E, Escriche M, Codony X, Encina G, Burgueno J, Merlos M, Baeyens JM, Giraldo J, Lopez-Garcia JA, Maldonado R, Plata-Salaman CR, and Vela JM. 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, 2012.
54. Sánchez-Blázquez P, Rodríguez-Muñoz M, Bailón C, and Garzón J. GPCRs promote the release of zinc ions mediated by nNOS/NO and the Redox transducer RGSZ2 protein. Antioxid Redox Signal 17: 1163-1177, 2012.
55. Sánchez-Blázquez P, Rodríguez-Muñoz M, Herrero-Labrador R, Burgueño J, Zamanillo D, and Garzón J. The calcium-sensitive Sigma-1 receptor prevents cannabinoids from provoking glutamate NMDA receptor hypofunction: implications in antinociception and psychotic diseases. Int J Neuropsychopharmacol 17: 1943-1955, 2014.
56. Sánchez-Blázquez P, Rodríguez-Muñoz M, Vicente-Sánchez A, and Garzón J. 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, 2013.
57. Sánchez-Fernández C, Nieto FR, González-Cano R, Artacho-Cordón A, Romero L, Montilla-García A, Zamanillo D, Baeyens JM, Entrena JM, and Cobos EJ. Potentiation of morphine-induced mechanical antinociception by sigma receptor inhibition: role of peripheral sigma receptors. Neuropharmacology 70: 348-358, 2013.
58. Shioda N, Ishikawa K, Tagashira H, Ishizuka T, Yawo H, and Fukunaga K. Expression of a truncated form of the endoplasmic reticulum chaperone protein, sigma1 receptor, promotes mitochondrial energy depletion and apoptosis. J Biol Chem 287: 23318-23331, 2012.
59. Su TP, Hayashi T, Maurice T, Buch S, and Ruoho AE. The sigma-1 receptor chaperone as an inter-organelle signaling modulator. Trends Pharmacol Sci 31: 557-566, 2010.
60. Tingley WG, Ehlers MD, Kameyama K, Doherty C, Ptak JB, Riley CT, and Huganir RL. Characterization of protein kinase A and protein kinase C phosphorylation of the N-methyl-D-aspartate receptor NR1 subunit using phosphorylation site-specific antibodies. J Biol Chem 272: 5157-5166, 1997.
61. Trujillo KA. The neurobiology of opiate tolerance, dependence and sensitization: mechanisms of NMDA receptordependent synaptic plasticity. Neurotox Res 4: 373-391, 2002.
62. Vallee M, Vitiello S, Bellocchio L, Hebert-Chatelain E, Monlezun S, Martin-Garcia E, Kasanetz F, Baillie GL, Panin F, Cathala A, Roullot-Lacarriere V, Fabre S, Hurst DP, Lynch DL, Shore DM, Deroche-Gamonet V, Spampinato U, Revest JM, Maldonado R, Reggio PH, Ross RA, Marsicano G, and Piazza PV. Pregnenolone can protect the brain from cannabis intoxication. Science 343: 94-98, 2014.
63. Vicente-Sánchez A, Sánchez-Blázquez P, Rodríguez-Muñoz M, and Garzón J. HINT1 protein cooperates with cannabinoid 1 receptor to negatively regulate glutamate NMDA receptor activity. Mol Brain 6: 42, 2013.
64. Vidal-Torres A, de la Puente B, Rocasalbas M, Tourino C, Andreea BS, Fernandez-Pastor B, Romero L, Codony X, Zamanillo D, Buschmann H, Merlos M, Manuel BJ, Maldonado R, and Vela JM. Sigma-1 receptor antagonism as opioid adjuvant strategy: Enhancement of opioid antinociception without increasing adverse effects. Eur J Pharmacol 711: 63-72, 2013.
65. Wu FS, Gibbs TT, and Farb DH. Pregnenolone sulfate: a positive allosteric modulator at the N-methyl-D-aspartate receptor. Mol Pharmacol 40: 333-336, 1991.
66. Yaksh TL, Al-Rodhan NR, and Jensen TS. Sites of action of opiates in production of analgesia. Prog Brain Res 77: 371-394, 1988.
67. Yaksh TL, Yeung JC, and Rudy TA. Systematic examination in the rat of brain sites sensitive to the direct application of morphine: observation of differential effects within the periaqueductal gray. Brain Res 114: 83-103, 1976.
68. Yamazaki Y, Ishioka M, Matsubayashi H, Amano T, and Sasa M. Inhibition by sigma receptor ligand, MS-377, of N-methyl-D-aspartate-induced currents in dopamine neurons of the rat ventral tegmental area. Psychopharmacology (Berl) 161: 64-69, 2002.
69. Yoon SY, Roh DH, Seo HS, Kang SY, Moon JY, Song S, Beitz AJ, and Lee JH. An increase in spinal dehydroepiandrosterone sulfate (DHEAS) enhances NMDAinduced pain via phosphorylation of the NR1 subunit in mice: involvement of the sigma-1 receptor. Neuropharmacology 59: 460-467, 2010.
70. Zamanillo D, Romero L, Merlos M, and Vela JM. Sigma 1 receptor: a new therapeutic target for pain. Eur J Pharmacol 716: 78-93, 2013.