Afobazole activation of S-1 receptors modulates neuronal responses to amyloid-β25-35

Journal of Pharmacology and Experimental Therapeutics

Volumn 347, Issue 2, 2013, Pages 468-477

  Behensky, Adam A ^a   Yasny, Ilya E ^b   Shuster, Alexander M ^b   Seredenin, Sergei B ^c   Petrov, Andrey V ^b   Cuevas, Javier ^a  

^a UNIVERSITY OF SOUTH FLORIDA   (United States)

^b IBC Generium ^*  (Russian Federation)

^c INSTITUTE OF PHARMACOLOGY   (Russian Federation)

Author keywords

[No Author keywords available]

Indexed keywords

1,3 DI O TOLYLGUANIDINE; AFOBAZOLE; AMYLOID BETA PROTEIN[25-35]; CALCIUM ION; CASPASE 3; CASPASE 3 ANTIBODY; ENZYME ANTIBODY; GUANIDINE DERIVATIVE; N [2 (3,4 DICHLOROPHENYL)ETHYL] 2 DIMETHYLAMINO N METHYLETHYLAMINE; NEUROPROTECTIVE AGENT; NITRIC OXIDE; OPIATE RECEPTOR; PROTEIN BAX; PROTEIN BCL 2; REACTIVE OXYGEN METABOLITE; RIMCAZOLE; THETA 1 OPIATE RECEPTOR; UNCLASSIFIED DRUG; 2-((2-MORPHOLINO)ETHYLTHIO)-5-ETHOXYBENZIMIDAZOLE; AMYLOID BETA PROTEIN; AMYLOID BETA-PROTEIN (25-35); APOPTOSIS REGULATORY PROTEIN; BENZIMIDAZOLE DERIVATIVE; CALCIUM; MORPHOLINE DERIVATIVE; PEPTIDE FRAGMENT; SIGMA OPIATE RECEPTOR; SIGMA-1 RECEPTOR; 2 ((2 MORPHOLINO)ETHYLTHIO) 5 ETHOXYBENZIMIDAZOLE; AMYLOID BETA PROTEIN (25 35); SIGMA 1 OPIATE RECEPTOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN CELL; BRAIN FUNCTION; CALCIUM CELL LEVEL; CELL SURVIVAL; CONCENTRATION RESPONSE; CONTROLLED STUDY; DNA FRAGMENTATION; DOWN REGULATION; DRUG CYTOTOXICITY; EMBRYO; ENZYME ACTIVATION; IC 50; IN VITRO STUDY; NERVE CELL DEGENERATION; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; UPREGULATION; AGONISTS; ALZHEIMER DISEASE; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; CELL CULTURE; CELL MEMBRANE; CULTURE TECHNIQUE; DRUG EFFECTS; FEMALE; IMMUNOHISTOCHEMISTRY; MALE; METABOLISM; NERVE CELL; PATHOLOGY; SPRAGUE DAWLEY RAT; TOXICITY; DRUG ANTAGONISM; DRUG EFFECT; DRUG POTENTIATION;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; APOPTOSIS REGULATORY PROTEINS; BENZIMIDAZOLES; CALCIUM; CELL CULTURE TECHNIQUES; CELL MEMBRANE; CELL SURVIVAL; CELLS, CULTURED; FEMALE; IMMUNOHISTOCHEMISTRY; MALE; MORPHOLINES; NEURONS; NITRIC OXIDE; PEPTIDE FRAGMENTS; RATS; RATS, SPRAGUE-DAWLEY; REACTIVE OXYGEN SPECIES; RECEPTORS, SIGMA;

EID: 84886039708     PISSN: 00223565     EISSN: 15210103     Source Type: Journal    
DOI: 10.1124/jpet.113.208330     Document Type: Article

References (56)

1. Abramov AY, Canevari L, and Duchen MR (2004) Calcium signals induced by amyloid beta peptide and their consequences in neurons and astrocytes in culture. Biochim Biophys Acta 1742:81-87.
2. Allen JW, Eldadah BA, Huang X, Knoblach S.M., and Faden AI (2001) Multiple cas-pases are involved in beta-amyloid-induced neuronal apoptosis. J Neurosci Res 65: 45-53.
3. Antipova TA, Sapozhnikova DS, Stepanichev M.Y., Onufriev MV, Gulyaeva NV, and Seredenin SB (2010) Effects of selective anxiolytic afobazole on active caspase-3. Bull Exp Biol Med 149:201-203.
4. Cho DH, Nakamura T, Fang J., Cieplak P, Godzik A, Gu Z., and Lipton SA (2009) S-nitrosylation of Drp1 mediates beta-amyloid-related mitochondrial fission and neuronal injury. Science 324:102-105.
5. Cuevas J, Behensky A, Deng W., and Katnik C (2011a) Afobazole modulates neuronal response to ischemia and acidosis via activation of sigma-1 receptors. J Pharmacol Exp Ther 339:152-160.
6. Cuevas J, Rodriguez A, Behensky A., and Katnik C (2011b) Afobazole modulates microglial function via activation of both sigma-1 and sigma-2 receptors. J Pharmacol Exp Ther 339:161-172.
7. Ekinci FJ, Linsley MD, and Shea TB (2000) Beta-amyloid-induced calcium influx induces apoptosis in culture by oxidative stress rather than tau phosphorylation. Brain Res Mol Brain Res 76:389-395.
8. Fehér A., Juhász A, László A, Kálmán J, Jr, Pákáski M, Kálmán J, and Janka Z (2012) Association between a variant of the sigma-1 receptor gene and Alzheimer's disease. Neurosci Lett 517:136-139.
9. Ferreiro E, Oliveira CR, and Pereira C (2004) Involvement of endoplasmic reticulum Ca2+ release through ryanodine and inositol 1,4,5-triphosphate receptors in the neurotoxic effects induced by the amyloid-beta peptide. J Neurosci Res 76:872-880.
10. Ferris RM, Tang FL, Chang K.J., and Russell A (1986) Evidence that the potential antipsychotic agent rimcazole (BW 234U) is a specific, competitive antagonist of sigma sites in brain. Life Sci 38:2329-2337.
11. Gamblin TC, Chen F, Zambrano A., Abraha A, Lagalwar S, Guillozet al., Lu M., Fu Y, Garcia-Sierra F, and LaPointe N, et al. (2003) Caspase cleavage of tau: linking amyloid and neurofibrillary tangles in Alzheimer's disease. Proc Natl Acad Sci USA 100:10032-10037.
12. Gaugler J, James B, Johnson T., Scholz K, and Weuve J (2013) Alzheimer's Disease Facts and Figures. Alzheimer's Association. Alzheimers Dement 9:1-71.
13. Gilmore DL, Liu Y, and Matsumoto RR (2004) Review of the pharmacological and clinical profile of rimcazole. CNS Drug Rev 10:1-22.
14. Griesmaier E, Posod A, Gross M., Neubauer V, Wegleiter K, Hermann M., Urbanek M, Keller M, and Kiechl-Kohlendorfer U (2012) Neuroprotective effects of the sigma-1 receptor ligand PRE-084 against excitotoxic perinatal brain injury in newborn mice. Exp Neurol 237:388-395.
15. Herrera Y, Katnik C, Rodriguez J.D., Hall AA, Willing A, Pennypacker KR, and Cuevas J (2008) sigma-1 receptor modulation of acid-sensing ion channel a (ASIC1a) and ASIC1a-induced Ca2+ influx in rat cortical neurons. J Pharmacol Exp Ther 327:491-502.
16. Husbands SM, Izenwasser S, Kopajtic T., Bowen WD, Vilner BJ, Katz JL, and Newman AH (1999) Structure-activity relationships at the monoamine transporters and sigma receptors for a novel series of 9-[3-(cis-3, 5-dimethyl-1- piperazinyl)propyl]carbazole (rimcazole) analogues. J Med Chem 42:4446-4455.
17. Jansen KL, Faull RL, Storey P, and Leslie RA (1993) Loss of sigma binding sites in the CA1 area of the anterior hippocampus in Alzheimer's disease correlates with CA1 pyramidal cell loss. Brain Res 623:299-302.
18. Joseph R and Han E (1992) Amyloid beta-protein fragment 25-35 causes activation of cytoplasmic calcium in neurons. Biochem Biophys Res Commun 184:1441-1447.
19. Kaminsky YG, Marlatt MW, Smith M.A., and Kosenko EA (2010) Subcellular and metabolic examination of amyloid-beta peptides in Alzheimer disease pathogene-sis: evidence for Abeta(25-35). Exp Neurol 221:26-37.
20. Katnik C, Guerrero WR, Pennypacker K.R., Herrera Y., and Cuevas J (2006) Sigma-1 receptor activation prevents intracellular calcium dysregulation in cortical neurons during in vitro ischemia. J Pharmacol Exp Ther 319:1355-1365.
21. Kim ES, Kim RS, Ren R.F., Hawver DB, and Flanders KC (1998) Transforming growth factor-beta inhibits apoptosis induced by beta-amyloid peptide fragment 25-35 in cultured neuronal cells. Brain Res Mol Brain Res 62:122-130.
22. Kourrich S, Su TP, Fujimoto M, and Bonci A (2012) The sigma-1 receptor: roles in neuronal plasticity and disease. Trends Neurosci 35:762-771.
23. 1-42 generation by the aminotetrahydrofuran derivative ANAVEX2-73, a mixed muscarinic and sigma receptor agonist, in a nontransgenic mouse model of Alzheimer's disease. Neuropsychopharmacology 38:1706-1723.
24. Limón I.D., Díaz A, Mendieta L., Chamorro G, Espinosa B, Zenteno E., and Guevara J (2009) Amyloid-beta(25-35) impairs memory and increases NO in the temporal cortex of rats. Neurosci Res 63:129-137.
25. Marín N., Romero B, Bosch-Morell F, Llansola M., Felipo V, Romá J, and Romero FJ (2000) Beta-amyloid-induced activation of caspase-3 in primary cultures of rat neurons. Mech Ageing Dev 119:63-67.
26. Marrazzo A, Caraci F, Salinaro E.T., Su TP, Copani A, and Ronsisvalle G (2005) Neuroprotective effects of sigma-1 receptor agonists against beta-amyloid-induced toxicity. Neuroreport 16:1223-1226.
27. Matsumoto RR, Bowen WD, Tom M.A., Vo VN, Truong DD, and De Costa BR (1995) Characterization of two novel sigma receptor ligands: antidystonic effects in rats suggest sigma receptor antagonism. Eur J Pharmacol 280:301-310.
28. Matsumoto RR, Gilmore DL, Pouw B, Bowen W.D., Williams W., Kausar A, and Coop A (2004) Novel analogs of the sigma receptor ligand BD1008 attenuate cocaine-induced toxicity in mice. Eur J Pharmacol 492:21-26.
29. Mattson MP and Chan SL (2003) Neuronal and glial calcium signaling in Alzheimer's disease. Cell Calcium 34:385-397.
30. Maurice T, Su TP, and Privat A (1998) Sigma1 (sigma 1) receptor agonists and neurosteroids attenuate B25-35-amyloid peptide-induced amnesia in mice through a common mechanism. Neuroscience 83:413-428.
31. Meunier J and Hayashi T (2010) Sigma-1 receptors regulate Bcl-2 expression by reactive oxygen species-dependent transcriptional regulation of nuclear factor kappaB. J Pharmacol Exp Ther 332:388-397.
32. Mishina M, Ohyama M, Ishii K., Kitamura S, Kimura Y, Oda K., Kawamura K, Sasaki T, Kobayashi S, and Katayama Y, et al. (2008) Low density of sigma1 receptors in early Alzheimer's disease. Ann Nucl Med 22:151-156.
33. Molnár Z., Soós K, Lengyel I., Penke B, Szegedi V, and Budai D (2004) Enhancement of NMDA responses by beta-amyloid peptides in the hippocampus in vivo. Neuroreport 15:1649-1652.
34. Mueller BH, 2nd, Park Y, Daudt DR, 3rd, Ma HY, Akopova I, Stankowska DL, Clark AF, and Yorio T (2013) Sigma-1 receptor stimulation attenuates calcium influx through activated L-type Voltage Gated Calcium Channels in purified retinal ganglion cells. Exp Eye Res 107:21-31.
35. Pal A, Fontanilla D, Gopalakrishnan A., Chae YK, Markley JL, and Ruoho AE (2012) The sigma-1 receptor protects against cellular oxidative stress and activates antioxidant response elements. Eur J Pharmacol 682:12-20.
36. Paradis E, Douillard H, Koutroumanis M., Goodyer C, and LeBlanc A (1996) Amyloid beta peptide of Alzheimer's disease downregulates Bcl-2 and upregulates bax expression in human neurons. J Neurosci 16:7533-7539.
37. Parks JK, Smith TS, Trimmer P.A., Bennett JP, Jr, and Parker WD, Jr (2001) Neurotoxic Abeta peptides increase oxidative stress in vivo through NMDA-receptor and nitric-oxide-synthase mechanisms, and inhibit complex IV activity and induce a mitochondrial permeability transition in vitro. J Neurochem 76: 1050-1056.
38. Revett TJ, Baker GB, Jhamandas J, and Kar S (2013) Glutamate system, amyloid β peptides and tau protein: functional interrelationships and relevance to Alzheimer disease pathology. J Psychiatry Neurosci 38:6-23.
39. Rybczynska AA, Dierckx RA, Ishiwata K, Elsinga P.H., and van Waarde A (2008) Cytotoxicity of sigma-receptor ligands is associated with major changes of cellular metabolism and complete occupancy of the sigma-2 subpopulation. J Nucl Med 49: 2049-2056.
40. Schelman WR, Andres RD, Sipe K.J., Kang E., and Weyhenmeyer JA (2004) Glutamate mediates cell death and increases the Bax to Bcl-2 ratio in a differentiated neuronal cell line. Brain Res Mol Brain Res 128:160-169.
41. Schubert D, Behl C, Lesley R., Brack A, Dargusch R, Sagara Y., and Kimura H (1995) Amyloid peptides are toxic via a common oxidative mechanism. Proc Natl Acad Sci USA 92:1989-1993.
42. Selkoe DJ (2001) Alzheimer's disease: genes, proteins, and therapy. Physiol Rev 81: 741-766.
43. Selznick LA, Holtzman DM, Han B.H., Gökden M, Srinivasan A.N., Johnson EM, Jr, and Roth KA (1999) In situ immunodetection of neuronal caspase-3 activation in Alzheimer disease. J Neuropathol Exp Neurol 58:1020-1026.
44. Seredenin SB and Voronin MV (2009) [Neuroreceptor mechanisms of the afobazole effect]. Eksp Klin Farmakol 72:3-11.
45. Silkina IV, Zenina TA, Seredenin S.B., and Mirzoian RS (2006) [Effect of afobazole on the accumulation of free radical oxidation products and the catalase activity in rats with cerebral ischemia]. Eksp Klin Farmakol 69:47-50.
46. Su TP, Hayashi T, Maurice T., Buch S, and Ruoho AE (2010) The sigma-1 receptor chaperone as an inter-organelle signaling modulator. Trends Pharmacol Sci 31: 557-566.
47. Tchedre KT and Yorio T (2008) sigma-1 receptors protect RGC-5 cells from apoptosis by regulating intracellular calcium, Bax levels, and caspase-3 activation. Invest Ophthalmol Vis Sci 49:2577-2588.
48. Tsai SY, Hayashi T, Mori T., and Su TP (2009) Sigma-1 receptor chaperones and diseases. Cent Nerv Syst Agents Med Chem 9:184-189.
49. Uchida N, Ujike H, Tanaka Y., Sakai A, Yamamoto M, Fujisawa Y., Kanzaki A, and Kuroda S (2005) A variant of the sigma receptor type-1 gene is a protective factor for Alzheimer disease. Am J Geriatr Psychiatry 13:1062-1066.
50. Vagnerova K, Hurn PD, Bhardwaj A, and Kirsch JR (2006) Sigma 1 receptor agonists act as neuroprotective drugs through inhibition of inducible nitric oxide synthase. Anesth Analg 103:430-434 table of contents.
51. Varadarajan S, Kanski J, Aksenova M., Lauderback C, and Butterfield DA (2001) Different mechanisms of oxidative stress and neurotoxicity for Alzheimer's A beta (1-42) and A beta(25-35). J Am Chem Soc 123:5625-5631.
52. Yang S, Bhardwaj A, Cheng J., Alkayed NJ, Hurn PD, and Kirsch JR (2007) Sigma receptor agonists provide neuroprotection in vitro by preserving bcl-2. Anesth Analg 104:1179-1184 tables of contents.
53. Yang ZJ, Carter EL, Torbey M.T., Martin LJ, and Koehler RC (2010) Sigma receptor ligand 4-phenyl-1-(4-phenylbutyl)-piperidine modulates neuronal nitric oxide synthase/postsynaptic density-95 coupling mechanisms and protects against neonatal ischemic degeneration of striatal neurons. Exp Neurol 221:166-174.
54. Yao M, Nguyen TV, and Pike CJ (2005) Beta-amyloid-induced neuronal apoptosis involves c-Jun N-terminal kinase-dependent downregulation of Bcl-w. J Neurosci 25:1149-1158.
55. Zenina TA, Gavrish IV, Melkumyan D.S., Seredenina TS, and Seredenin SB (2005) Neuroprotective properties of afobazol in vitro. Bull Exp Biol Med 140: 194-196.
56. Zhang Y, Shi Y, Qiao L., Sun Y, Ding W, Zhang H., Li N, and Chen D (2012) Sigma-1 receptor agonists provide neuroprotection against gp120 via a change in bcl-2 expression in mouse neuronal cultures. Brain Res 1431:13-22.