Structure of the σ1 receptor and its ligand binding site

Journal of Medicinal Chemistry

Volumn 56, Issue 24, 2013, Pages 9809-9819

  Brune, Stefanie ^a   Pricl, Sabrina ^b   Wünsch, Bernhard ^a  

^a UNIVERSITY OF MÜNSTER   (Germany)

^b UNIVERSITY OF TRIESTE   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ANXIOLYTIC AGENT; BENZOMORPHAN DERIVATIVE; HALOPERIDOL; NARCOTIC ANALGESIC AGENT; OPIATE ANTAGONIST; S1RA; SIGMA OPIATE RECEPTOR; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; AMYOTROPHIC LATERAL SCLEROSIS; BINDING SITE; DEPRESSION; DRUG POTENTIATION; HUMAN; LIGAND BINDING; MEMBRANE STRUCTURE; MOLECULAR MODEL; NEUROPATHIC PAIN; NONHUMAN; PHOTOAFFINITY LABELING; PROTEIN DOMAIN; REVIEW; SCHIZOPHRENIA; SITE DIRECTED MUTAGENESIS; STRUCTURAL HOMOLOGY;

EID: 84891284846     PISSN: 00222623     EISSN: 15204804     Source Type: Journal    
DOI: 10.1021/jm400660u     Document Type: Review

References (84)

1. Gilbert, P. E.; Martin, W. R. The effects of morphine and nalorphine like drugs in the nondependent and morphine dependent chronic spinal dog J. Pharmacol. Exp. Ther. 1976, 197, 517-532
2. Vaupel, D. B. Naltrexone fails to antagonize the σ effects of PCP and SKF 10,047 in the dog Eur. J. Pharmacol. 1983, 92, 269-274
3. Tam, S. W. Naloxone inaccessible σ receptor in rat central nervous system Proc. Natl. Acad. Sci. U. S. A. 1983, 80, 6703-6707
4. Zukin, S. R.; Brady, K. T.; Slifer, B. L.; Balster, R. L. Behavioral and biochemical stereoselectivity of sigma opiate/PCP receptors Brain Res. 1984, 294, 174-177
5. Quirion, R.; Bowen, W. D.; Itzhak, Y.; Junien, J. L.; Musacchio, J. M.; Rothman, R. B.; Su, T. P.; Tam, S. W.; Taylor, D. P. A proposal for the classification of sigma binding sites Trends Pharmacol. Sci. 1992, 13, 85-86
6. Su, T. P. Evidence for sigma opioid receptor: binding of [3H]SKF-10047 to etorphine-inaccessible sites in guinea-pig brain J. Pharmacol. Exp. Ther. 1982, 223, 284-290
7. Tam, S. W.; Cook, L. σ opiates and certain antipsychotic drugs mutually inhibit (+)-[3H]SKF 10,047 and [3H]haloperidol binding in guinea pig brain membranes Proc. Natl. Acad. Sci. U.S.A. 1984, 81, 5618-5621
8. Bowen, W. D.; De Costa, B. R.; Hellewell, S. B.; Walker, J. M.; Rice, K. [3H]-(+)-Pentazocine: a potent and highly selective benzomorphan-based probe for sigma-1 receptors Mol. Neuropharmacol. 1993, 3, 117-126
9. 3H](+)-Pentazocine binding to rat brain σ1 receptors Eur. J. Pharmacol. 1994, 266, 131-138
10. 3H]SKF-10, 047 binding sites (σ sites) exhibit a unique distribution in rat brain subcellular fractions Eur. J. Pharmacol. 1990, 188, 211-218
11. Okuyama, S.; Imagawa, Y.; Ogawa, S. I.; Araki, H.; Ajima, A.; Tnaka, M.; Muramatsu, M.; Nakazato, A.; Yamaguchi, K.; Yoshida, M.; Otomo, S. NE-100, a novel sigma receptor ligand: In vivo tests Life Sci. 1993, 53, PL285-PL290
12. Okuyama, S.; Nakazato, A. NE-100: a novel sigma receptor antagonist CNS Drug Rev. 1996, 2, 226-237
13. Sharkey, J.; Glen, K. A.; Wolfe, S.; Kuhar, M. J. Cocaine binding at σ receptors Eur. J. Pharmacol. 1988, 149, 171-174
14. Moebius, F. F.; Reiter, R. J.; Hanner, M.; Glossmann, H. High affinity of sigma1-binding sites for sterol isomerization inhibitors: evidence for a pharmacological relationship with the yeast sterol C8-C7 isomerase Br. J. Pharmacol. 1997, 121, 1-6
15. Rao, T. S.; Cler, J. A.; Mick, S. J.; Dilworth, V. M.; Contreras, P. C.; Iyengar, S.; Wood, P. L. Neurochemical characterization of dopaminergic effects of opipramol, a potent sigma receptor ligand, in vivo Neuropharmacology 1990, 29, 1191-1197
16. Meunier, J.; Ieni, J.; Maurice, T. The anti-amnesic and neuroprotective effects of donepezil against amyloid beta25-35 peptide-induced toxicity in mice involve an interaction with the sigma1 receptor Br. J. Pharmacol. 2006, 149, 998-1012
17. 3H]3-(-3-hydroxyphenyl)- N -(1-propyl)piperidine Mol. Pharmacol. 1989, 35, 1-5
18. Narita, N.; Hashimoto, K.; Tomitaka, S. I.; Minabe, Y. Interactions of selective serotonin reuptake inhibitors with subtypes of σ receptors in rat brain Eur. J. Pharmacol. 1996, 307, 117-119
19. Su, T. P.; London, E. D.; Jaffe, J. H. Steroid binding at δ receptors suggests a link between endocrine, nervous, and immune systems Science 1988, 239, 219-221
20. Palmer, C. P.; Mahen, R.; Schnell, E.; Djamgoz, M. B. A.; Aydar, E. Sigma-1 receptors bind cholesterol and remodel lipid rafts in breast cancer cell lines Cancer Res. 2007, 67, 11166-11175
21. Fontanilla, D.; Johannessen, M.; Hajipour, A. R.; Cozzi, N. V.; Jackson, M. B.; Ruoho, A. E. The hallucinogen N, N -dimethyltryptamine (DMT) is an endogenous sigma-1 receptor regulator Science 2009, 323, 934-937
22. Mash, D. C.; Zabetian, C. P. Sigma receptors are associated with cortical limbic areas in the primate brain Synapse 1992, 12, 195-205
23. Weissman, A. D.; Su, T. P.; Hedreen, J. C.; London, E. D. Sigma receptors in post-mortem human brains J. Pharmacol. Exp. Ther. 1988, 247, 29-33
24. Mavlyutov, T. A.; Epstein, M. L.; Andersen, K. A.; Ziskind-Conhaim, L.; Ruoho, A. E. The sigma-1 receptor is enriched in postsynaptic sites of C-terminals in mouse motoneurons. An anatomical and behavioral study Neurosci. 2010, 167, 247-255
25. 3H]SK F 10,047 binding sites in rat liver Eur. J. Pharmacol. 1988, 147, 259-264
26. Hellewell, S. B.; Bruce, A.; Feinstein, G.; Orringer, J.; Williams, W.; Bowen, W. D. Rat liver and kidney contain high densities of σ1 and σ2 receptors: characterization by ligand binding and photoaffinity labeling Eur. J. Pharmacol. 1994, 268, 9-18
27. Ela, C.; Barg, J.; Vogel, Z.; Hasin, Y.; Eilam, Y. Sigma receptor ligands modulate contractility, Ca influx and beating rate in cultured cardiac myocytes J. Pharmacol. Exp. Ther. 1994, 269, 1300-1309
28. Ola, M. S.; Moore, P.; El-Sherbeny, A.; Roon, P.; Agarwal, N.; Sarthy, V. P.; Casellas, P.; Ganapathy, V.; Smith, S. B. Expression pattern of sigma receptor 1 mRNA and protein in mammalian retina Mol. Brain Res. 2001, 95, 86-95
29. Wolfe, S. A., Jr.; Culp, S. G.; De Souza, E. B. σ-Receptors in endocrine organs: identification, characterization, and autoradiographic localization in rat pituitary, adrenal, testis, and ovary Endocrinology 1989, 124, 1160-1172
30. Wolfe, S. A., Jr.; Kulsakdinun, C.; Battaglia, G.; Jaffe, J. H.; De Souza, E. B. Initial identification and characterization of sigma receptors on human peripheral blood leukocytes J. Pharmacol. Exp. Ther. 1988, 247, 1114-1119
31. Vilner, B. J.; John, C. S.; Bowen, W. D. Sigma-1 and sigma-2 receptors are expressed in a wide variety of human and rodent tumor cell lines Cancer Res. 1995, 55, 408-413
32. Thomas, G. E.; Szucs, M.; Mamone, J. Y.; Bem, W. T.; Rush, M. D.; Johnson, F. E.; Coscia, C. J. Sigma and opioid receptors in human brain tumors Life Sci. 1990, 46, 1279-1286
33. Bem, W. T.; Thomas, G. E.; Mamone, J. Y.; Homan, S. M.; Levy, B. K.; Johnson, F. E.; Coscia, C. J. Overexpression of σ receptors in nonneural human tumors Cancer Res. 1991, 51, 6558-6562
34. Wang, B.; Rouzier, R.; Albarracin, C. T.; Sahin, A.; Wagner, P.; Yang, Y.; Smith, T. L.; Bernstam, F. M.; Marcelo, A. C.; Hortobagyi, G. N.; Pusztai, L. Expression of sigma 1 receptor in human breast cancer Breast Cancer Res. Treat. 2004, 87, 205-214
35. Aydar, E.; Onganer, P.; Perrett, R.; Djamgoz, M. B.; Palmer, C. P. The expression and functional characterization of sigma (σ) 1 receptors in breast cancer cell lines Cancer Lett. 2006, 242, 245-257
36. Ishiguro, H.; Ohtsuki, T.; Toru, M.; Itokawa, M.; Aoki, J.; Shibuya, H. Association between polymorphisms in the type 1 sigma receptor gene and schizophrenia Neurosci. Lett. 1998, 257, 45-48
37. Ohi, K.; Hashimoto, R.; Yasuda, Y.; Fukumoto, M.; Yamamori, H.; Umeda-Yano, S.; Kamino, K.; Ikezawa, K.; Azechi, M.; Iwase, M.; Kazui, H.; Kasai, K.; Takeda, M. The SIGMAR1 gene is associated with a risk of schizophrenia and activation of the prefrontal cortex Progr. Neuro-Psychopharmacol. Biol. Psychiatry 2011, 35, 1309-1315
38. Sabino, V.; Cottone, P.; Parylak, S. L.; Steardo, L.; Zorrilla, E. P. Sigma-1 receptor knockout mice display a depressive-like phenotype Behav. Brain Res. 2009, 198, 472-476
39. Bergeron, R.; Debonnel, G.; De Montigny, C. Modification of the N -methyl- d -aspartate response by antidepressant sigma receptor ligands Eur. J. Pharmacol. 1993, 240, 319-323
40. Uchida, N.; Ujike, H.; Tanaka, Y.; Sakai, A.; Yamamoto, M.; Fujisawa, Y. A.; Kanzaki, A.; Kuroda, S. A variant of the sigma receptor type 1 gene is a protective factor for Alzheimer's disease Am. J. Geriatr. Psychiatry 2005, 13, 1062-1066
41. Romieu, P.; Martin-Fardon, R.; Maurice, T. Involvement of the sigma1 receptor in the cocaine-induced conditioned place preference NeuroReport 2000, 11, 2885-2888
42. Matsumoto, R. R.; McCracken, K. A.; Pouw, B.; Zhang, Y.; Bowen, W. D. Involvement of sigma receptors in the behavioral effects of cocaine: evidence from novel ligands and antisense oligodeoxynucleotides Neuropharmacology 2002, 42, 1043-1055
43. Chien, C. C.; Pasternak, G. W. Selective antagonism of opioid analgesia by a sigma system J. Pharmacol. Exp. Ther. 1994, 271, 1583-1590
44. Entrena, J. M.; Cobos, E. J.; Nieto, F. R.; Cendan, C. M.; Gris, G.; Del Pozo, E.; Zamanillo, D.; Baeyens, M. Sigma-1 receptors are essential for capsaicin induced mechanical hypersensitivity: studies with selective sigma-1 ligands and sigma-1 knockout mice Pain 2009, 143, 252-261
45. 1 receptor antagonist S1RA is a promising candidate for the treatment of neurogenic pain J. Med. Chem. 2012, 55, 8209-8210
46. Colabufo, N. A.; Berardi, F.; Contino, M.; Niso, M.; Abate, C.; Perrone, R.; Tortorella, V. Antiproliferative and cytotoxic effects of some σ2 agonists and σ1 antagonists in tumour cell lines Naunyn Schmiedeberg's Arch. Pharmacol. 2004, 370, 106-113
47. Diaz, J. L.; Cuberes, R.; Berrocal, J.; Contijoch, M.; Christmann, U.; Fernández, A.; Port, A.; Holenz, J.; Buschmann, H.; Laggner, C.; Serafini, M. T.; Burgeno, J.; Zamanillo, D.; Merlos, M.; Vela, J. M.; Almansa, C. Synthesis and biological evaluation of the 1-arylpyrazole class of sigma-1 receptor antagonists: identification of 4-{2-[5-methyl-1-(naphtalen-2-yl)-1 H -pyrazol-3-yloxy]ethyl}morpholine (S1RA) J. Med. Chem. 2012, 55, 8211-8224
48. 1) ligand ANAVEX2-73, a novel aminotetrahydrofuran derivative J. Psychopharmacol. 2013, 25, 1101-1117
49. Aydar, E.; Palmer, C. P.; Klyachko, V. A.; Jackson, M. B. The sigma receptor as a ligand-regulated auxiliary potassium channel subunit Neuron 2002, 34, 399-410
50. Lupardus, P. J.; Wilke, R. A.; Aydar, E.; Palmer, C. P.; Chen, Y.; Ruoho, A. E.; Jackson, M. B. Membrane-delimited coupling between sigma receptors and K channels in rat neurohypophysial terminals requires neither G-protein nor ATP J. Physiol. (London) 2000, 526, 527-539
51. Morin-Surun, M. P.; Collin, T.; Denavit-Saubie, M.; Baulieu, E. E.; Monnet, F. P. Intracellular σ1 receptor modulates phospholipase C and protein kinase C activities in the brainstem Proc. Natl. Acad. Sci. U.S.A. 1999, 96, 8196-8199
52. Ramamoorthy, J. D.; Ramamoorthy, S.; Mahesh, V. B.; Leibach, F. H.; Ganapathy, V. Cocaine-sensitive σ-receptor and its interaction with steroid hormones in the human placental syncytiotrophoblast and in choriocarcinoma cells Endocrinology 1995, 136, 924-932
53. Hayashi, T.; Su, T. P. Sigma-1 receptor chaperones at the ER- mitochondrion interface regulate Ca2 signaling and cell survival Cell 2007, 131, 596-610
54. Hayashi, T.; Su, T. P. Intracellular dynamics of σ-1 receptors (σ1 binding sites) in NG108-15 cells J. Pharmacol. Exp. Ther. 2003, 306, 726-733
55. Su, T. P.; Hayashi, T.; Maurice, T.; Buch, S.; Ruoho, A. E. The sigma-1 receptor chaperone as an inter-organelle signaling modulator Trends Pharmacol. Sci. 2010, 31, 557-566
56. Hayashi, T.; Su, T. P. σ-1 receptors (σ1 binding sites) form raft-like microdomains and target lipid droplets on the endoplasmic reticulum: roles in endoplasmic reticulum lipid compartmentalization and export J. Pharmacol. Exp. Ther. 2003, 306, 718-725
57. Hayashi, T.; Su, T. P. Regulating ankyrin dynamics: roles of sima-1 receptors Proc. Natl. Acad. Sci. U.S.A. 2001, 98, 491-496
58. Monnet, F. P.; Debonnel, G.; Junien, J.; De Montigny, C. N -Methyl- d -aspartate induced neuronal activation is selectively modulated by σ-receptors Eur. J. Pharmacol. 1990, 179, 441-445
59. Wilke, R. A.; Mehta, R. P.; Lupardus, P. J.; Cben, Y.; Ruoho, A. E.; Jackson, M. B. Sigma receptor photolabeling and sigma receptor-mediated modulation of potassium channels in tumor cells J. Biol. Chem. 1999, 274, 18387-18392
60. Johannessen, M.; Ramachandran, S.; Riemer, L.; Ramos-Serrano, A.; Ruoho, A. E.; Jackson, M. B. Voltage-gated sodium channel modulation by σ-receptors in cardiac myocytes and heterologous systems Am. J. Physiol.: Cell Physiol. 2009, 296, C1049-C1057
61. Zhang, H.; Cuevas, J. Sigma receptors inhibit high-voltage-activated calcium channels in rat sympathetic and parasympathetic neurons J. Neurophysiol. 2002, 87, 2867-2879
62. Hanner, M.; Moebius, F. F.; Flandorfer, A.; Knaus, H. G.; Striessnig, J.; Kempner, E.; Glossmann, H. Purification, molecular cloning, and expression of the mammalian sigma1-binding site Proc. Natl. Acad. Sci. U.S.A. 1996, 93, 8072-8077
63. Kekuda, R.; Prasad, P. D.; Fei, Y. J.; Leibach, F. H.; Ganapathy, V. Cloning and functional expression of the human type 1 sigma receptor (hSigmaR1) Biochem. Biophys. Res. Commun. 1996, 229, 553-558
64. Seth, P.; Fei, Y. J.; Li, H. W.; Huang, W.; Leibach, F. H.; Ganapathy, V. Cloning and functional characterization of a σ receptor from rat brain J. Neurochem. 1998, 70, 922-931
65. Pan, Y. X.; Mei, J.; Xu, J.; Wan, B. L.; Zuckerman, A.; Pasternak, G. W. Cloning and characterization of a mouse σ1 receptor J. Neurochem. 1998, 70, 2279-2285
66. Seth, P.; Leibach, F. H.; Ganapathy, V. Cloning and characterization of the type 1 sigma receptor from rat brain and structural analysis of the murine gene coding for the receptor FASEB J. 1998, 12, A161-A161
67. Mei, J.; Pasternak, G. W. Molecular cloning and pharmacological characterization of the rat sigma1 receptor Biochem. Pharmacol. 2001, 62, 349-355
68. Chen, Y.; Hajipour, A. R.; Sievert, M. K.; Arbabian, M.; Ruoho, A. E. Characterization of the cocaine binding site on the sigma-1 receptor Biochemistry 2007, 46, 3532-3542
69. Prasad, P. D.; Li, H. W.; Fei, Y. J.; Ganapathy, M. E.; Fujita, T.; Plumley, L. H.; Yang-Feng, T. L.; Leibach, F. H.; Ganapathy, V. Exon-intron structure, analysis of promoter region, and chromosomal localization of the human type 1 σ receptor gene J. Neurochem. 1998, 70, 443-451
70. Al-Saif, A.; Al-Mohanna, F.; Bohlega, S. A mutation in sigma-1 receptor causes juvenile amyotrophic lateral sclerosis Ann. Neurol. 2011, 70, 913-919
71. Ganapathy, M. E.; Prasad, P. D.; Huang, W.; Seth, P.; Leibach, F. H.; Ganapathy, V. Molecular and ligand-binding characterization of the σ-receptor in the Jurkat human T lymphocyte cell line J. Pharmacol. Exp. Ther. 1999, 289, 251-260
72. Guitart, X.; Codony, X.; Monroy, X. Sigma receptors: biology and therapeutic potential Psychopharmacology 2004, 174, 301-319
73. Pal, A.; Chu, U. B.; Ramachandran, S.; Grawoig, D.; Guo, L. W.; Hajipour, A. R.; Ruoho, A. E. Juxtaposition of the steroid binding domain-like I and II regions constitutes a ligand binding site in the α-1 receptor J. Biol. Chem. 2008, 283, 19646-19656
74. Fontanilla, D.; Hajipour, A. R.; Pal, A.; Chu, U. B.; Arbabian, M.; Ruoho, A. E. Probing the steroid binding domain-like I (SBDLI) of the sigma-1 receptor binding site using N-substituted photoaffinity labels Biochemistry 2008, 47, 7205-7217
75. Schutze, M. P.; Peterson, P. A.; Jackson, M. R. An N-terminal double-arginine motif maintains type II membrane proteins in the endoplasmic reticulum EMBO J. 1994, 13, 1696-1705
76. Pal, A.; Hajipour, A. R.; Fontanilla, D.; Ramachandran, S.; Chu, U. B.; Mavlyutov, T.; Ruoho, A. E. Identification of regions of the α-1 receptor ligand binding site using a novel photoprobe Mol. Pharmacol. 2007, 72, 921-933
77. Polgar, O.; Robey, R. W.; Morisaki, K.; Dean, M.; Michejda, C.; Sauna, Z. E.; Ambudkar, S. V.; Tarasova, N.; Bates, S. E. Mutational analysis of ABCG2: role of the GXXXG motif Biochemistry 2004, 43, 9448-9456
78. Seth, P.; Ganapathy, M. E.; Conway, S. J.; Bridges, C. D.; Smith, S. B.; Casellas, P.; Ganapathy, V. Expression pattern of the type 1 sigma receptor in the brain and identity of critical anionic amino acid residues in the ligand-binding domain of the receptor Biochim. Biophys. Acta, Mol. Cell Res. 2001, 1540, 59-67
79. Yamamoto, H.; Miura, R.; Yamamoto, T.; Shinohara, K.; Watanabe, M.; Okuyama, S.; Nakazato, A.; Nukada, T. Amino acid residues in the transmembrane domain of the type 1 sigma receptor critical for ligand binding FEBS Lett. 1999, 445, 19-22
80. Wu, Z.; Bowen, W. D. Role of sigma-1 receptor C-terminal segment in inositol 1,4,5-trisphosphate receptor activation: constitutive enhancement of calcium signaling in MCF-7 tumor cells J. Biol. Chem. 2008, 283, 28198-28215
81. 125I)iodoazidococaine, a photoaffinity label for the haloperidol-sensitive sigma receptor Proc. Natl. Acad. Sci. U.S.A. 1992, 89, 1393-1397
82. 1 receptor ACS Med. Chem. Lett. 2011, 2, 834-839
83. Laurini, E.; Marson, D.; Dal Col, V.; Fermeglia, M.; Mamolo, M. G.; Zampieri, D.; Vio, L.; Pricl, S. Another brick in the wall. Validation of the σ1 receptor 3D model by computer-assisted design, synthesis, and activity of new σ1 ligands Mol. Pharmaceutics 2012, 9, 3107-3126
84. Meyer, C.; Schepmann, D.; Yanagisawa, S.; Yamaguchi, J.; Dal Col, V.; Laurini, E.; Itami, K.; Pricl, S.; Wünsch, B. Pd-catalyzed direct C-H bond functionalization of spirocyclic σ1 ligands: generation of a pharmacophore model and analysis of the reverse binding mode by docking into a 3D homology model of the σ1 receptor J. Med. Chem. 2012, 55, 8047-8065