Stimulation of sigma receptors with afobazole blocks activation of Microglia and reduces toxicity caused by amyloid-β25-35

Journal of Pharmacology and Experimental Therapeutics

Volumn 347, Issue 2, 2013, Pages 458-467

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

^a UNIVERSITY OF SOUTH FLORIDA   (United States)

^b IBC Generium ^*

^c INSTITUTE OF PHARMACOLOGY   (Russian Federation)

Author keywords

[No Author keywords available]

Indexed keywords

AFOBAZOLE; AMYLOID BETA PROTEIN[25-35]; CASPASE 3; DELTA OPIATE RECEPTOR ANTAGONIST; N [2 (3,4 DICHLOROPHENYL)ETHYL] 2 DIMETHYLAMINO N METHYLETHYLAMINE; PROTEIN BAX; RIMCAZOLE; SIGMA OPIATE RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CALCIUM CELL LEVEL; CELL ACTIVATION; CELL DEATH; CELL MIGRATION; CELL PROTECTION; CELL SURVIVAL; CHEMOTAXIS; CONCENTRATION RESPONSE; CONTROLLED STUDY; DOWN REGULATION; DRUG CYTOTOXICITY; DRUG EFFICACY; DRUG MECHANISM; DRUG POTENTIATION; GLIA CELL; MICROGLIA; NONHUMAN; PHARMACOLOGICAL BLOCKING; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT;

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

EID: 84886067734     PISSN: 00223565     EISSN: 15210103     Source Type: Journal    
DOI: 10.1124/jpet.113.208348     Document Type: Article

References (54)

1. Araujo DM and Cotman CW (1992) Beta-amyloid stimulates glial cells in vitro to produce growth factors that accumulate in senile plaques in Alzheimer's disease. Brain Res 569:141-145.
2. Bianca VD, Dusi S, Bianchini E., Dal Prà I, and Rossi F (1999) Beta-amyloid activates the O-2 forming NADPH oxidase in microglia, monocytes, and neutrophils. A possible inflammatory mechanism of neuronal damage in Alzheimer's disease. J Biol Chem 274:15493-15499.
3. Combs CK, Karlo JC, Kao S.C., and Landreth GE (2001) beta-Amyloid stimulation of microglia and monocytes results in TNFalpha-dependent expression of inducible nitric oxide synthase and neuronal apoptosis. J Neurosci 21:1179-1188.
4. Crawford KW and Bowen WD (2002) Sigma-2 receptor agonists activate a novel apoptotic pathway and potentiate antineoplastic drugs in breast tumor cell lines. Cancer Res 62:313-322.
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 and Berg DK (1998) Mammalian nicotinic receptors with alpha7 subunits that slowly desensitize and rapidly recover from alpha-bungarotoxin blockade. J Neurosci 18:10335-10344.
7. 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.
8. Davis JB, McMurray HF, and Schubert D (1992) The amyloid beta-protein of Alzheimer's disease is chemotactic for mononuclear phagocytes. Biochem Biophys Res Commun 189:1096-1100.
9. 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.
10. Garção P, Oliveira CR, and Agostinho P (2006) Comparative study of microglia activation induced by amyloid-beta and prion peptides: role in neurodegeneration. J Neurosci Res 84:182-193.
11. Gilmore DL, Liu Y, and Matsumoto RR (2004) Review of the pharmacological and clinical profile of rimcazole. CNS Drug Rev 10:1-22.
12. Glenner GG and Wong CW (1984) Alzheimer's disease: initial report of the purification and characterization of a novel cerebrovascular amyloid protein. Biochem Biophys Res Commun 120:885-890.
13. Griciuc A, Serrano-Pozo A, Parrado A.R., Lesinski AN, Asselin CN, Mullin K, Hooli B., Choi SH, Hyman BT, and Tanzi RE (2013) Alzheimer's disease risk gene CD33 inhibits microglial uptake of amyloid beta. Neuron 22:631-643.
14. Hall AA, Herrera Y, Ajmo C.T., Jr, Cuevas J, and Pennypacker KR (2009) Sigma receptors suppress multiple aspects of microglial activation. Glia 57:744-754.
15. Hardy J and Allsop D (1991) Amyloid deposition as the central event in the aetiology of Alzheimer's disease. Trends Pharmacol Sci 12:383-388.
16. Hardy J and Selkoe DJ (2002) The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 297:353-356.
17. Herber DL, Mercer M, Roth L.M., Symmonds K., Maloney J, Wilson N, Freeman M.J., Morgan D., and Gordon MN (2007) Microglial activation is required for Abeta clearance after intracranial injection of lipopolysaccharide in APP transgenic mice. J Neuroimmune Pharmacol 2:222-231.
18. 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.
19. Iñiguez M.A., Punzón C, Nieto R., Burgueño J, Vela J.M., and Fresno M (2013) Inhibitory effects of sigma-2 receptor agonists on T lymphocyte activation. Front Pharmacol 4:23 DOI: 10.3389/fphar.2013.00023. eCollection 2013.
20. Jang MH, Jung SB, Lee M.H., Kim CJ, Oh YT, Kang I, Kim J., and Kim EH (2005) Melatonin attenuates amyloid beta25-35-induced apoptosis in mouse microglial BV2 cells. Neurosci Lett 380:26-31.
21. 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.
22. 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.
23. 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.
24. 2 receptor activation. J Neurochem 121:228-238.
25. Korotzer AR, Pike CJ, and Cotman CW (1993) beta-Amyloid peptides induce degeneration of cultured rat microglia. Brain Res 624:121-125.
26. 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.
27. 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.
28. 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.
29. McLarnon JG (2012) Microglial chemotactic signaling factors in Alzheimer's disease. Am J Neurodegener Dis 1:199-204.
30. 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.
31. 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.
32. Naj AC, Jun G, Beecham G.W., Wang LS, Vardarajan BN, Buros J, Gallins P.J., Buxbaum JD, Jarvik GP, and Crane PK, et al. (2011) Common variants at MS4A4/MS4A6E, CD2AP, CD33 and EPHA1 are associated with late-onset Alzheimer's disease. Nat Genet 43:436-441.
33. Orellana JA, Shoji KF, Abudara V, Ezan P., Amigou E, Sáez PJ, Jiang J.X., Naus CC, Sáez JC, and Giaume C (2011) Amyloid β-induced death in neurons involves glial and neuronal hemichannels. J Neurosci 31:4962-4977.
34. 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.
35. Quirion R, Bowen WD, Itzhak Y, Junien J.L., Musacchio JM, Rothman RB, Su TP, Tam S.W., and Taylor DP (1992) A proposal for the classification of sigma binding sites. Trends Pharmacol Sci 13:85-86.
36. 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.
37. Satou T, Cummings BJ, and Cotman CW (1995) Immunoreactivity for Bcl-2 protein within neurons in the Alzheimer's disease brain increases with disease severity. Brain Res 697:35-43.
38. Seredenin SB, Antipova TA, Voronin M.V., Kurchashova SY, and Kuimov AN (2009) Interaction of afobazole with sigma1-receptors. Bull Exp Biol Med 148:42-44.
39. Seth P, Fei YJ, Li H.W., Huang W., Leibach FH, and Ganapathy V (1998) Cloning and functional characterization of a sigma receptor from rat brain. J Neurochem 70: 922-931.
40. Shang YC, Chong ZZ, Wang S, and Maiese K (2012) Prevention of b-amyloid degeneration of microglia by erythropoietin depends on Wnt1, the PI 3-K/mTOR pathway, Bad, and Bcl-xL. Aging (Albany, NY Online) 4:187-201.
41. Solito E and Sastre M (2012) Microglia function in Alzheimer's disease. Front Pharmacol 3:14 DOI: 10.3389/fphar.2012.00014
42. Streit WJ, Braak H, Xue Q.S., and Bechmann I (2009) Dystrophic (senescent) rather than activated microglial cells are associated with tau pathology and likely precede neurodegeneration in Alzheimer's disease. Acta Neuropathol 118:475-485.
43. Su JH, Deng G, and Cotman CW (1997) Bax protein expression is increased in Alzheimer's brain: correlations with DNA damage, Bcl-2 expression, and brain pathology. J Neuropathol Exp Neurol 56:86-93.
44. 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.
45. 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.
46. Vilner BJ and Bowen WD (2000) Modulation of cellular calcium by sigma-2 receptors: release from intracellular stores in human SK-N-SH neuroblastoma cells. J Pharmacol Exp Ther 292:900-911.
47. Walker JM, Bowen WD, Walker F.O., Matsumoto RR, De Costa B, and Rice KC (1990) Sigma receptors: biology and function. Pharmacol Rev 42:355-402.
48. Weldon DT, Rogers SD, Ghilardi J.R., Finke MP, Cleary JP, O'Hare E, Esler WP, Maggio J.E., and Mantyh PW (1998) Fibrillar beta-amyloid induces microglial phagocytosis, expression of inducible nitric oxide synthase, and loss of a select population of neurons in the rat CNS in vivo. J Neurosci 18:2161-2173.
49. Wilcock DM, Munireddy SK, Rosenthal A, Ugen K.E., Gordon MN, and Morgan D (2004) Microglial activation facilitates Abeta plaque removal following intracranial anti-Abeta antibody administration. Neurobiol Dis 15:11-20.
50. Yang F, Sun X, Beech W., Teter B, Wu S, Sigel J., Vinters HV, Frautschy SA, and Cole GM (1998) Antibody to caspase-cleaved actin detects apoptosis in differentiated neuroblastoma and plaque-associated neurons and microglia in Alzheimer's disease. Am J Pathol 152:379-389.
51. Yankner BA (1989) Amyloid and Alzheimer's disease - cause or effect? Neurobiol Aging 10:470-471, discussion 477-478
52. Zhang H, Katnik C, and Cuevas J (2009) Sigma receptor activation inhibits voltagegated sodium channels in rat intracardiac ganglion neurons. Int J Physiol Pathophysiol Pharmacol 2:1-11.
53. Zhang H and Cuevas J (2002) Sigma receptors inhibit high-voltage- activated calcium channels in rat sympathetic and parasympathetic neurons. J Neurophysiol 87: 2867-2879.
54. Zhang H and Cuevas J (2005) sigma Receptor activation blocks potassium channels and depresses neuroexcitability in rat intracardiac neurons. J Pharmacol Exp Ther 313:1387-1396.