Sigma receptors and their ligands in cancer biology: Overview and new perspectives for cancer therapy

Medicinal Research Reviews

Volumn 32, Issue 2, 2012, Pages 410-427

  Megalizzi, Véronique ^a   Le Mercier, Marie ^b   Decaestecker, Christine ^a,c  

^a Institute of Pharmacy   (Belgium)

^b ERASME HOSPITAL   (Belgium)

^c UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

Author keywords

Cancer; Endoplasmic reticulum stress; Lipid synthesis; Psychotic drug reprofiling; Sigma receptor

Indexed keywords

(3H1) 3 DIOTOLYLGUANIDINE; 4 IBP; CALCIUM; CB 184; CB 64D; CYTOSKELETON PROTEIN; DEXTROMETHORPHAN; DONEPEZIL; HALOPERIDOL; N CYCLOHEXYL N ETHYL 3 (3 CHLORO 4 CYCLOHEXYLPHENYL) 2 PROPENYLAMINE; N,N DIMETHYLTRYPTAMINE; OPIATE ANTAGONIST IPAG; PENTAZOCINE; PLACEBO; PRASTERONE; PREGNENOLONE; PROGESTERONE; RIMCAZOLE; SIGMA 1 OPIATE RECEPTOR; SIGMA 2 OPIATE RECEPTOR; SIGMA RECEPTOR LIGAND; SIRAMESINE; TEMOZOLOMIDE; TRACER; UNCLASSIFIED DRUG;

ANTINEOPLASTIC ACTIVITY; ARTICLE; BREAST CARCINOMA; CANCER CELL; CANCER CHEMOTHERAPY; CANCER TISSUE; CELL ADHESION; COLON CARCINOMA; CYTOSKELETON; DIAGNOSTIC IMAGING; ENDOPLASMIC RETICULUM STRESS; GLIOBLASTOMA; HUMAN; IN VIVO STUDY; ISOTOPE LABELING; KIDNEY CARCINOMA; KIDNEY SARCOMA; LEUKEMIA; LIVER METASTASIS; LUNG CARCINOMA; LUNG NON SMALL CELL CANCER; MELANOMA; NEOPLASM; NEUROBLASTOMA; NONHUMAN; NUCLEOTIDE SEQUENCE; POSITRON EMISSION TOMOGRAPHY; PROSTATE CANCER; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; SINGLE PHOTON EMISSION COMPUTER TOMOGRAPHY;

CALCIUM; CYTOSKELETAL PROTEINS; DRUG DELIVERY SYSTEMS; ENDOPLASMIC RETICULUM STRESS; HUMANS; LIGANDS; MEMBRANE MICRODOMAINS; NEOPLASMS; POSITRON-EMISSION TOMOGRAPHY; RECEPTORS, SIGMA; SIGNAL TRANSDUCTION; TOMOGRAPHY, EMISSION-COMPUTED, SINGLE-PHOTON;

EID: 84857662007     PISSN: 01986325     EISSN: 10981128     Source Type: Journal    
DOI: 10.1002/med.20218     Document Type: Article

References (94)

1. Martin WR, Eades CG, Thompson JA, Huppler RE, Gilbert PE. 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. Quirion R, Bowen WD, Itzhak Y, Junien JL, Musacchio JM, Rothman RB, Su TP, Tam SW, Taylor DP. A proposal for the classification of sigma binding sites. Trends Pharmacol Sci 1992;13:85-86.
3. Bourrie B, Bribes E, Derocq JM, Vidal H, Casellas P. Sigma receptor ligands: Applications in inflammation and oncology. Curr Opin Investig Drugs 2004;5:1158-1163.
4. Bowen WD. Sigma receptors: Recent advances and new clinical potentials. Pharm Acta Helv 2000;74:211-218.
5. Su TP. Delineating biochemical and functional properties of sigma receptors: Emerging concepts. Crit Rev Neurobiol 1993;7:187-203.
6. Walker JM, Hohmann AG, Hemstreet MK. Functional role of sigma receptors in the nervous system. In: Ltd TF, editor. Aspects of synaptic transmission 2: Acetylcholine, sigma receptors, Cck and eicosanoids, neurotoxins. Washington, DC: T.W. Stone; 1993. p 91-112.
7. Volz HP, Stoll KD. Clinical trials with sigma ligands. Pharmacopsychiatry 2004;37:S214-S220.
8. Kunitachi S, Fujita Y, Ishima T, Kohno M, Horio M, Tanibuchi Y, Shirayama Y, Iyo M, Hashimoto K. Phencyclidine-induced cognitive deficits in mice are ameliorated by subsequent subchronic administration of donepezil: Role of sigma-1 receptors. Brain Res 2009;1279:189-196.
9. Maurice T, Su TP. The pharmacology of sigma-1 receptors. Pharmacol Ther 2009;124:195-206.
10. Aydar E, Palmer CP, Djamgoz MB. Sigma receptors and cancer: Possible involvement of ion channels. Cancer Res 2004;64:5029-5035.
11. Palmer CP, Mahen R, Schnell E, Djamgoz MB, Aydar E. Sigma-1 receptors bind cholesterol and remodel lipid rafts in breast cancer cell lines. Cancer Res 2007;67:11166-11175.
12. Meunier J, Maurice T. Beneficial effects of the sigma1 receptor agonists igmesine and dehydroepiandrosterone against learning impairments in rats prenatally exposed to cocaine. Neurotoxicol Teratol 2004;26:783-797.
13. Fontanilla D, Johannessen M, Hajipour AR, Cozzi NV, Jackson MB, Ruoho AE. The hallucinogen N, N-dimethyltryptamine (DMT) is an endogenous sigma-1 receptor regulator. Science 2009;323:934-937.
14. Matsumoto RR. Sigma recptors: Historical perspective and background. In: Matsumoto RR, Bowen WD, Su TP, editors. Sigma receptors: Chemistry, cell biology and clinical implications. New York: Springer; 2007. p 25-69.
15. Guitart X, Codony X, Monroy X. Sigma receptors: Biology and therapeutic potential. Psychopharmacology (Berl) 2004;174:301-319.
16. John CS, Vilner BJ, Geyer BC, Moody T, Bowen WD. Targeting sigma receptor-binding benzamides as in vivo diagnostic and therapeutic agents for human prostate tumors. Cancer Res 1999;59:4578-4583.
17. Spruce BA, Campbell LA, McTavish N, Cooper MA, Appleyard MV, O'Neill M, Howie J, Samson J, Watt S, Murray K, McLean D, Leslie NR, Safrany ST, Ferguson MJ, Peters JA, Prescott AR, Box G, Hayes A, Nutley B, Raynaud F, Downes CP, Lambert JJ, Thompson AM, Eccles S. Small molecule antagonists of the sigma-1 receptor cause selective release of the death program in tumor and self-reliant cells and inhibit tumor growth in vitro and in vivo. Cancer Res 2004;64:4875-4886.
18. Kekuda R, Prasad PD, Fei YJ, Leibach FH, Ganapathy V. Cloning and functional expression of the human type 1 sigma receptor (hSigmaR1). Biochem Biophys Res Commun 1996;229:553-558.
19. Hanner M, Moebius FF, Flandorfer A, Knaus HG, Striessnig J, Kempner E, Glossmann H. Purification, molecular cloning, and expression of the mammalian sigma1-binding site. Proc Natl Acad Sci USA 1996;93:8072-8077.
20. Chang YF, Imam JS, Wilkinson MF. The nonsense-mediated decay RNA surveillance pathway. Annu Rev Biochem 2007;76:51-74.
21. Prasad PD, Li HW, Fei YJ, Ganapathy ME, Fujita T, Plumley LH, Yang-Feng TL, Leibach FH, Ganapathy V. Exon-intron structure, analysis of promoter region, and chromosomal localization of the human type 1 sigma receptor gene. J Neurochem 1998;70:443-451.
22. Ganapathy V, Ganapathy ME, Inoue K. Cloning of sigma-1 receptor and structural analysis of its gene and promoter region. In: Matsumoto RR, Bowen WD, Su TP, editors. Sigma receptors: Chemistry, cell biology and clinical implications. New York: Springer; 2007. p 99-112.
23. Moebius FF, Reiter RJ, Hanner M, Glossmann H. 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 1997;121:1-6.
24. Aydar E, Palmer CP, Klyachko VA, Jackson MB. The sigma receptor as a ligand-regulated auxiliary potassium channel subunit. Neuron 2002;34:399-410.
25. Hellewell SB, Bruce A, Feinstein G, Orringer J, Williams W, Bowen WD. Rat liver and kidney contain high densities of sigma 1 and sigma 2 receptors: Characterization by ligand binding and photoaffinity labeling. Eur J Pharmacol 1994;268:9-18.
26. Wang LM, Wu Q, Mach RH, Wheeler KT, Morton KA. Sigma-2 receptor gene expression involves in tumor cell cycles and cell proliferation. AACR Meet Abstr 2005;2005:1288-1289.
27. Bowen WD, Tolentino PJ, Kirschner BN, Varghese P, de Costa BR, Rice KC. Sigma receptors and signal transduction: Negative modulation of signaling through phosphoinositide-linked receptor systems. NIDA Res Monogr 1993;133:69-93.
28. Matsumoto RR. Sigma recptors: Historical perspective and background. In: Matsumoto RR, Bowen WD, Su TP, editors. Sigma receptors: Chemistry, cell biology and clinical implications. New York: Springer; 2007. p 1-23.
29. Yamamoto H, Yamamoto T, Sagi N, Klenerova V, Goji K, Kawai N, Baba A, Takamori E, Moroji T. Sigma ligands indirectly modulate the NMDA receptor-ion channel complex on intact neuronal cells via sigma 1 site. J Neurosci 1995;15:731-736.
30. Zambon AC, De Costa BR, Kanthasamy AG, Nguyen BQ, Matsumoto RR. Subchronic administration of N-[2-(3, 4-dichlorophenyl) ethyl]-N-methyl-2-(dimethylamino) ethylamine (BD1047) alters sigma 1 receptor binding. Eur J Pharmacol 1997;324:39-47.
31. Zeng C, Vangveravong S, Xu J, Chang KC, Hotchkiss RS, Wheeler KT, Shen D, Zhuang ZP, Kung HF, Mach RH. Subcellular localization of sigma-2 receptors in breast cancer cells using two-photon and confocal microscopy. Cancer Res 2007;67:6708-6716.
32. Thomas GE, Szucs M, Mamone JY, Bem WT, Rush MD, Johnson FE, Coscia CJ. Sigma and opioid receptors in human brain tumors. Life Sci 1990;46:1279-1286.
33. Bem WT, Thomas GE, Mamone JY, Homan SM, Levy BK, Johnson FE, Coscia CJ. Overexpression of sigma receptors in nonneural human tumors. Cancer Res 1991;51:6558-6562.
34. John CS, Bowen WD, Varma VM, McAfee JG, Moody TW. Sigma receptors are expressed in human non-small cell lung carcinoma. Life Sci 1995;56:2385-2392.
35. Vilner BJ, John CS, Bowen WD. 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.
36. Simony-Lafontaine J, Esslimani M, Bribes E, Gourgou S, Lequeux N, Lavail R, Grenier J, Kramar A, Casellas P. Immunocytochemical assessment of sigma-1 receptor and human sterol isomerase in breast cancer and their relationship with a series of prognostic factors. Br J Cancer 2000;82:1958-1966.
37. Wang B, Rouzier R, Albarracin CT, Sahin A, Wagner P, Yang Y, Smith TL, Meric-Bernstam F, Marcelo Aldaz C, Hortobagyi GN, Pusztai L. Expression of sigma 1 receptor in human breast cancer. Breast Cancer Res Treat 2004;87:205-214.
38. Aydar E, Onganer P, Perrett R, Djamgoz MB, Palmer CP. The expression and functional characterization of sigma (sigma) 1 receptors in breast cancer cell lines. Cancer Lett 2006;242:245-257.
39. Megalizzi V, Decaestecker C, Debeir O, Spiegl-Kreinecker S, Berger W, Lefranc F, Kast RE, Kiss R. Screening of anti-glioma effects induced by sigma-1 receptor ligands: Potential new use for old anti-psychiatric medicines. Eur J Cancer 2009;45:2893-2905.
40. Mach RH, Smith CR, al-Nabulsi I, Whirrett BR, Childers SR, Wheeler KT. Sigma 2 receptors as potential biomarkers of proliferation in breast cancer. Cancer Res 1997;57:156-161.
41. Wheeler KT, Wang LM, Wallen CA, Childers SR, Cline JM, Keng PC, Mach RH. Sigma-2 receptors as a biomarker of proliferation in solid tumours. Br J Cancer 2000;82:1223-1232.
42. Colabufo NA, Berardi F, Contino M, Ferorelli S, Niso M, Perrone R, Pagliarulo A, Saponaro P, Pagliarulo V. Correlation between sigma2 receptor protein expression and histopathologic grade in human bladder cancer. Cancer Lett 2006;237:83-88.
43. Kashiwagi H, McDunn JE, Simon PO, Jr., Goedegebuure PS, Xu J, Jones L, Chang K, Johnston F, Trinkaus K, Hotchkiss RS, Mach RH, Hawkins WG. Selective sigma-2 ligands preferentially bind to pancreatic adenocarcinomas: Applications in diagnostic imaging and therapy. Mol Cancer 2007;6:48.
44. Megalizzi V, Mathieu V, Mijatovic T, Gailly P, Debeir O, De Neve N, Van Damme M, Bontempi G, Haibe-Kains B, Decaestecker C, Kondo Y, Kiss R, Lefranc F. 4-IBP, a sigma1 receptor agonist, decreases the migration of human cancer cells, including glioblastoma cells, in vitro and sensitizes them in vitro and in vivo to cytotoxic insults of proapoptotic and proautophagic drugs. Neoplasia 2007;9:358-369.
45. John CS, Vilner BJ, Gulden ME, Efange SM, Langason RB, Moody TW, Bowen WD. Synthesis and pharmacological characterization of 4-[125I]-N-(N-benzylpiperidin-4-yl)-4-iodobenzamide: A high affinity sigma receptor ligand for potential imaging of breast cancer. Cancer Res 1995;55:3022-3027.
46. Choi SR, Yang B, Plossl K, Chumpradit S, Wey SP, Acton PD, Wheeler K, Mach RH, Kung HF. Development of a Tc-99m labeled sigma-2 receptor-specific ligand as a potential breast tumor imaging agent. Nucl Med Biol 2001;28:657-666.
47. Colabufo NA, Abate C, Contino M, Inglese C, Niso M, Berardi F, Perrone R. PB183, a sigma receptor ligand, as a potential PET probe for the imaging of prostate adenocarcinoma. Bioorg Med Chem Lett 2008;18:1990-1993.
48. Everaert H, Flamen P, Franken PR, Verhaeghe W, Bossuyt A. Sigma-receptor imaging by means of I123-IDAB scintigraphy: Clinical application in melanoma and non-small cell lung cancer. Anticancer Res 1997;17:1577-1582.
49. Caveliers V, Everaert H, John CS, Lahoutte T, Bossuyt A. Sigma receptor scintigraphy with N-[2-(1′-piperidinyl)ethyl]-3-(123)I-iodo-4-methoxybenzamide of patients with suspected primary breast cancer: First clinical results. J Nucl Med 2002;43:1647-1649.
50. John CS, Bowen WD, Saga T, Kinuya S, Vilner BJ, Baumgold J, Paik CH, Reba RC, Neumann RD, Varma VM, McAfee JG. A malignant melanoma imaging agent: Synthesis, characterization, in vitro binding and biodistribution of iodine-125-(2-piperidinylaminoethyl)4-iodobenzamide. J Nucl Med 1993;34:2169-2175.
51. Banerjee R, Tyagi P, Li S, Huang L. Anisamide-targeted stealth liposomes: A potent carrier for targeting doxorubicin to human prostate cancer cells. Int J Cancer 2004;112:693-700.
52. Li SD, Huang L. Targeted delivery of antisense oligodeoxynucleotide and small interference RNA into lung cancer cells. Mol Pharm 2006;3:579-588.
53. Li SD, Chono S, Huang L. Efficient oncogene silencing and metastasis inhibition via systemic delivery of siRNA. Mol Ther 2008;16:942-946.
54. Achison M, Boylan MT, Hupp TR, Spruce BA. HIF-1alpha contributes to tumour-selective killing by the sigma receptor antagonist rimcazole. Oncogene 2007;26:1137-1146.
55. Ostenfeld MS, Hoyer-Hansen M, Bastholm L, Fehrenbacher N, Olsen OD, Groth-Pedersen L, Puustinen P, Kirkegaard-Sorensen T, Nylandsted J, Farkas T, Jaattela M. Anti-cancer agent siramesine is a lysosomotropic detergent that induces cytoprotective autophagosome accumulation. Autophagy 2008;4:487-499.
56. Fehrenbacher N, Bastholm L, Kirkegaard-Sorensen T, Rafn B, Bottzauw T, Nielsen C, Weber E, Shirasawa S, Kallunki T, Jaattela M. Sensitization to the lysosomal cell death pathway by oncogene-induced down-regulation of lysosome-associated membrane proteins 1 and 2. Cancer Res 2008;68:6623-6633.
57. Vilner BJ, Bowen WD. Modulation of cellular calcium by sigma-2 receptors: Release from intracellular stores in human SK-N-SH neuroblastoma cells. J Pharmacol Exp Ther 2000;292:900-911.
58. Monnet FP. Sigma-1 receptor as regulator of neuronal intracellular Ca2+: Clinical and therapeutic relevance. Biol Cell 2005;97:873-883.
59. Hayashi T, Su TP. Regulating ankyrin dynamics: Roles of sigma-1 receptors. Proc Natl Acad Sci USA 2001;98:491-496.
60. Siddiqui RA, Harvey KA, Zaloga GP, Stillwell W. Modulation of lipid rafts by omega-3 fatty acids in inflammation and cancer: Implications for use of lipids during nutrition support. Nutr Clin Pract 2007;22:74-88.
61. Yaqoob P. The nutritional significance of lipid rafts. Annu Rev Nutr 2009;29:257-282.
62. Hayashi T, Su TP. Sigma-1 receptor chaperones at the ER-mitochondrion interface regulate Ca(2+) signaling and cell survival. Cell 2007;131:596-610.
63. Gouaze-Andersson V, Cabot MC. Glycosphingolipids and drug resistance. Biochim Biophys Acta 2006;1758:2096-2103.
64. Matsumoto RR, Bowen WD, Su TP. Sigma receptors: Chemistry, cell biology and clinical implications. New York: Springer; 2007. 413p.
65. Crawford KW, Coop A, Bowen WD. sigma(2) Receptors regulate changes in sphingolipid levels in breast tumor cells. Eur J Pharmacol 2002;443:207-209.
66. 2+ concentration of the endoplasmic reticulum is a key determinant of ceramide-induced apoptosis: Significance for the molecular mechanism of Bcl-2 action. EMBO J 2001;20:2690-2701.
67. Szabadkai G, Rizzuto R. Participation of endoplasmic reticulum and mitochondrial calcium handling in apoptosis: More than just neighborhood? FEBS Lett 2004;567:111-115.
68. 2+. J Biol Chem 1997;272:30873-30879.
69. Hendershot LM. The ER function BiP is a master regulator of ER function. Mt Sinai J Med 2004;71:289-297.
70. Cairns RA, Khokha R, Hill RP. Molecular mechanisms of tumor invasion and metastasis: An integrated view. Curr Mol Med 2003;3:659-671.
71. Pawlak G, Helfman DM. Cytoskeletal changes in cell transformation and tumorigenesis. Curr Opin Genet Dev 2001;11:41-47.
72. Su TP, Hayashi T, Vaupel DB. When the endogenous hallucinogenic trace amine N, N-dimethyltryptamine meets the sigma-1 receptor. Sci Signal 2009;2:pe12.
73. 2+ entry. J Biol Chem 2003;278:33492-33500.
74. Zhang B, Zhang Y, Dagher MC, Shacter E. Rho GDP dissociation inhibitor protects cancer cells against drug-induced apoptosis. Cancer Res 2005;65:6054-6062.
75. Ota T, Maeda M, Murakami M, Takegami T, Suto S, Tatsuka M. Activation of Rac1 by Rho-guanine nucleotide dissociation inhibitor-beta with defective isoprenyl-binding pocket. Cell Biol Int 2007;31:92-96.
76. Fewell SW, Travers KJ, Weissman JS, Brodsky JL. The action of molecular chaperones in the early secretory pathway. Annu Rev Genet 2001;35:149-191.
77. Kimata Y, Oikawa D, Shimizu Y, Ishiwata-Kimata Y, Kohno K. A role for BiP as an adjustor for the endoplasmic reticulum stress-sensing protein Ire1. J Cell Biol 2004;167:445-456.
78. Healy SJ, Gorman AM, Mousavi-Shafaei P, Gupta S, Samali A. Targeting the endoplasmic reticulum-stress response as an anticancer strategy. Eur J Pharmacol 2009;625:234-246.
79. Cox JS, Chapman RE, Walter P. The unfolded protein response coordinates the production of endoplasmic reticulum protein and endoplasmic reticulum membrane. Mol Biol Cell 1997;8:1805-1814.
80. Schroder M. Engineering eukaryotic protein factories. Biotechnol Lett 2008;30:187-196.
81. DeBerardinis RJ, Mancuso A, Daikhin E, Nissim I, Yudkoff M, Wehrli S, Thompson CB. Beyond aerobic glycolysis: Transformed cells can engage in glutamine metabolism that exceeds the requirement for protein and nucleotide synthesis. Proc Natl Acad Sci USA 2007;104:19345-19350.
82. Vander Heiden MG, Cantley LC, Thompson CB. Understanding the Warburg effect: The metabolic requirements of cell proliferation. Science 2009;324:1029-1033.
83. Maurice T, Phan VL, Urani A, Kamei H, Noda Y, Nabeshima T. Neuroactive neurosteroids as endogenous effectors for the sigma1 (sigma1) receptor: Pharmacological evidence and therapeutic opportunities. Jpn J Pharmacol 1999;81:125-155.
84. de Costa BR, He XS, Dominguez C, Cutts J, Williams W, Bowen WD. A new approach to the design of sigma-2-selective ligands: Synthesis and evaluation of N-[2-(3, 4-dichlorophenyl)ethyl]-N-methyl-2-(1- pyrrolidinyl)ethylamine-related polyamines at sigma-1 and sigma-2 receptor subtypes. J Med Chem 1994;37:314-321.
85. Mach RH, Dehdashti F, Wheeler KT. PET radiotracers for imaging the proliferative status of solid tumors. PET Clin 2009;4:1-15.
86. Chaki S, Tanaka M, Muramatsu M, Otomo S. NE-100, a novel potent sigma ligand, preferentially binds to sigma 1 binding sites in guinea pig brain. Eur J Pharmacol 1994;251:R1-R2.
87. Xu J, Tu Z, Jones LA, Vangveravong S, Wheeler KT, Mach RH. [3H]N-[4-(3, 4-dihydro-6, 7-dimethoxyisoquinolin-2(1H)-yl)butyl]-2-methoxy-5-methylbenzamide: A novel sigma-2 receptor probe. Eur J Pharmacol 2005;525:8-17.
88. Mach RH, Wheeler KT. Development of molecular probes for imaging sigma-2 receptors in vitro and in vivo. Cent Nerv Syst Agents Med Chem 2009;9:230-245.
89. Cobos EJ, del Pozo E, Baeyens JM. Irreversible blockade of sigma-1 receptors by haloperidol and its metabolites in guinea pig brain and SH-SY5Y human neuroblastoma cells. J Neurochem 2007;102:812-825.
90. Brent PJ. Kappa opioid receptor agonists inhibit sigma-1 (sigma 1) receptor binding in guinea-pig brain, liver and spleen: Autoradiographical evidence. Brain Res 1996;725:155-165.
91. Wilson AA, Dannals RF, Ravert HT, Sonders MS, Weber E, Wagner HN, Jr. Radiosynthesis of sigma receptor ligands for positron emission tomography: 11C- and 18F-labeled guanidines. J Med Chem 1991;34:1867-1870.
92. Maurice T, Meunier J, Feng B, Ieni J, Monaghan DT. Interaction with sigma(1) protein, but not N-methyl-D-aspartate receptor, is involved in the pharmacological activity of donepezil. J Pharmacol Exp Ther 2006;317:606-614.
93. Jbilo O, Vidal H, Paul R, De Nys N, Bensaid M, Silve S, Carayon P, Davi D, Galiegue S, Bourrie B, Guillemot JC, Ferrara P, Loison G, Maffrand JP, Le Fur G, Casellas P. Purification and characterization of the human SR 31747A-binding protein. A nuclear membrane protein related to yeast sterol isomerase. J Biol Chem 1997;272:27107-27115.
94. Shin EJ, Nah SY, Kim WK, Ko KH, Jhoo WK, Lim YK, Cha JY, Chen CF, Kim HC. The dextromethorphan analog dimemorfan attenuates kainate-induced seizures via sigma1 receptor activation: Comparison with the effects of dextromethorphan. Br J Pharmacol 2005;144:908-918.