γ-Aminobutyric acid type a receptor inhibition triggers a nicotinic neuroprotective mechanism

Journal of Neuroscience Research

Volumn 91, Issue 3, 2013, Pages 416-425

  Ferchmin, P A ^a   Pérez, Dinely ^a   Castro Alvarez, William ^a,b   Penzo, Mario A ^a,c   Maldonado, Héctor M ^a   Eterovic, Vesna A ^a  

^a Universidad Central del Caribe School of Medicine   (Puerto Rico)

^b Bromedicom   (United States)

^c Howard Hughes Medical Institute Cold Spring Harbor Laboratory Cold Spring Harbor   (United States)

Author keywords

Bicuculline; CA1 pyramidal neurons; GABAA receptors; Nicotinic receptors; NMDA toxicity

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 2 [1 (3 AMIDINOTHIOPROPYL) 1H INDOL 3 YL] 3 (1 METHYL 1H INDOL 3 YL)MALEIMIDE; 2 MORPHOLINO 8 PHENYLCHROMONE; 4 AMINOBUTYRIC ACID A RECEPTOR; BICUCULLINE METHIODIDE; BUNGAROTOXIN RECEPTOR; CEMBRATRIENE DIOL; DIHYDRO BETA ERYTHROIDINE; METHYLLYCACONITINE; N METHYL DEXTRO ASPARTIC ACID; NEUROPROTECTIVE AGENT; NICOTINIC RECEPTOR ALPHA4BETA2; UNCLASSIFIED DRUG; VESAMICOL;

ANIMAL TISSUE; ARTICLE; BRAIN FUNCTION; CONTROLLED STUDY; DOSE RESPONSE; ELECTROPHYSIOLOGY; EXCITOTOXICITY; HIPPOCAMPAL CA1 REGION; NEUROPHARMACOLOGY; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; RAT; SPIKE WAVE;

ACTION POTENTIALS; ANIMALS; CA1 REGION, HIPPOCAMPAL; GABA ANTAGONISTS; HUMANS; MALE; NEUROPROTECTIVE AGENTS; NICOTINIC ANTAGONISTS; ORGAN CULTURE TECHNIQUES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, NICOTINIC;

EID: 84872618461     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.23155     Document Type: Article

References (71)

1. Akaike A, Takada-Takatori Y, Kume T, Izumi Y. 2010. Mechanisms of neuroprotective effects of nicotine and acetylcholinesterase inhibitors: role of alpha4 and alpha7 receptors in neuroprotection. J Mol Neurosci 40: 211-216.
2. Albuquerque EX, Alkondon M, Pereira EF, Castro NG, Schrattenholz A, Barbosa CT, Bonfante-Cabarcas R, Aracava Y, Eisenberg HM, Maelicke A. 1997. Properties of neuronal nicotinic acetylcholine receptors: pharmacological characterization and modulation of synaptic function. J Pharmacol Exp Ther 280: 1117-1136.
3. Alessi DR. 1997. The protein kinase C inhibitors Ro 318220 and GF 109203X are equally potent inhibitors of MAPKAP kinase-1beta (Rsk-2) and p70 S6 kinase. FEBS Lett 402: 121-123.
4. Alessi DR, Cuenda A, Cohen P, Dudley DT, Saltiel AR. 1995. PD 098059 is a specific inhibitor of the activation of mitogen-activated protein kinase kinase in vitro and in vivo. J Biol Chem 270: 27489-27494.
5. Alkondon M, Albuquerque EX. 2004. The nicotinic acetylcholine receptor subtypes and their function in the hippocampus and cerebral cortex. Prog Brain Res 145: 109-120.
6. Alkondon M, Braga MF, Pereira EF, Maelicke A, Albuquerque EX. 2000. Alpha7 nicotinic acetylcholine receptors and modulation of gabaergic synaptic transmission in the hippocampus. Eur J Pharmacol 393: 59-67.
7. Andersen P, Bliss TV, Skrede KK. 1971. Unit analysis of hippocampal polulation spikes. Exp Brain Res 13: 208-221.
8. Auld DS, Day JC, Mennicken F, Quirion R. 2000. Pharmacological characterization of endogenous acetylcholine release from primary septal cultures. J Pharmacol Exp Ther 292: 692-697.
9. Auld DS, Mennicken F, Day JC, Quirion R. 2001. Neurotrophins differentially enhance acetylcholine release, acetylcholine content and choline acetyltransferase activity in basal forebrain neurons. J Neurochem 77: 253-262.
10. Buckingham SD, Jones AK, Brown LA, Sattelle DB. 2009. Nicotinic acetylcholine receptor signalling: roles in Alzheimer's disease and amyloid neuroprotection. Pharmacol Rev 61: 39-61.
11. Buhler AV, Dunwiddie TV. 2002. Alpha7 nicotinic acetylcholine receptors on GABAergic interneurons evoke dendritic and somatic inhibition of hippocampal neurons. J Neurophysiol 87: 548-557.
12. Charpantier E, Wiesner A, Huh KH, Ogier R, Hoda JC, Allaman G, Raggenbass M, Feuerbach D, Bertrand D, Fuhrer C. 2005. Alpha7 neuronal nicotinic acetylcholine receptors are negatively regulated by tyrosine phosphorylation and Src-family kinases. J Neurosci 25: 9836-9849.
13. Cobb SR, Bulters DO, Suchak S, Riedel G, Morris RGM, Davies CH. 1999. Activation of nicotinic acetylcholine receptors patterns network activity in the rodent hippocampus. J Physiol 518: 131-140.
14. 2+ dependent mechanism. Neuropharmacology 39: 2799-2807.
15. 3H]methyllycaconitine: a new radioligand for labelling [alpha]7-type neuronal nicotinic acetylcholine receptors. Neuropharmacology 38: 679-690.
16. Davies SP, Reddy H, Caivano M, Cohen P. 2000. Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem J 351: 95-105.
17. DeFazio RA, Raval AP, Lin HW, Dave KR, Della-Morte D, Perez-Pinzon MA. 2009. GABA synapses mediate neuroprotection after ischemic and epsilonPKC preconditioning in rat hippocampal slice cultures. J Cereb Blood Flow Metab 29: 375-384.
18. DeFeudis FV, Balfagon G, De Sagarra MR, Madtes P, Somoza E, Gervas-Camacho J. 1975. Action of N-methyl-bicuculline on the binding of gamma-aminobutyric acid to a synaptosomal fraction of rat cerebral cortex. Exp Neurol 49: 497-505.
19. Demuro A, Palma E, Eusebi F, Miledi R. 2001. Inhibition of nicotinic acetylcholine receptors by bicuculline. Neuropharmacology 41: 854-861.
20. Dziewczapolski G, Glogowski CM, Masliah E, Heinemann SF. 2009. Deletion of the alpha 7 nicotinic acetylcholine receptor gene improves cognitive deficits and synaptic pathology in a mouse model of Alzheimer's disease. J Neurosci 29: 8805-8815.
21. Escubedo E, Camarasa J, Chipana C, Garcia-Rates S, Pubill D. 2009. Involvement of nicotinic receptors in methamphetamine- and MDMA-induced neurotoxicity: pharmacological implications. Int Rev Neurobiol 88: 121-166.
22. Eterovic VA, Perez D, Martins AH, Cuadrado BL, Carrasco M, Ferchmin PA. 2011. A cembranoid protects acute hippocampal slices against paraoxon neurotoxicity. Toxicol In Vitro 25: 1468-1474.
23. Fellous JM, Sejnowski TJ. 2000. Cholinergic induction of oscillations in the hippocampal slice in the slow (0.5-2 Hz), theta (5-12 Hz), and gamma (35-70 Hz) bands. Hippocampus 10: 187-197.
24. Ferchmin PA, Eterovic VA, Rivera EM, Teyler TJ. 1995. Spermine increases paired-pulse facilitation in area CA1 of hippocampus in a calcium-dependent manner. Brain Res 689: 189-196.
25. Ferchmin PA, Perez D, Biello M. 2000. Spermine is neuroprotective against anoxia and N-methyl-D-aspartate in hippocampal slices. Brain Res 859: 273-279.
26. Ferchmin PA, Perez D, Eterovic VA, de Vellis J. 2003. Nicotinic receptors differentially regulate N-methyl-D-aspartate damage in acute hippocampal slices. J Pharmacol Exp Ther 305: 1071-1078.
27. Ferchmin PA, Hao J, Perez D, Penzo M, Maldonado HM, Gonzalez MT, Rodriguez AD, de Vellis J. 2005. Tobacco cembranoids protect the function of acute hippocampal slices against NMDA by a mechanism mediated by alpha4beta2 nicotinic receptors. J Neurosci Res 82: 631-641.
28. Fountain SB, Ting YL, Teyler TJ. 1992. The in vitro hippocampal slice preparation as a screen for neurotoxicity. Toxicol In Vitro 6: 77-87.
29. Frazier CJ, Rollins YD, Breese CR, Leonard S, Freedman R, Dunwiddie TV. 1998. Acetylcholine activates an alpha-bungarotoxin-sensitive nicotinic current in rat hippocampal interneurons, but not pyramidal cells. J Neurosci 18: 1187-1195.
30. Frere RC, Macdonald RL, Young AB. 1982. GABA binding and bicuculline in spinal cord and cortical membranes from adult rat and from mouse neurons in cell culture. Brain Res 244: 145-153.
31. Gahring LC, Meyer EL, Rogers SW. 2003. Nicotine-induced neuroprotection against N-methyl-D-aspartic acid or beta-amyloid peptide occur through independent mechanisms distinguished by pro-inflammatory cytokines. J Neurochem 87: 1125-1136.
32. Giorgetti M, Bacciottini L, Giovannini MG, Colivicchi MA, Goldfarb J, Blandina P. 2000. Local GABAergic modulation of acetylcholine release from the cortex of freely moving rats. Eur J Neurosci 12: 1941-1948.
33. Hu M, Schurdak ME, Puttfarcken PS, El Kouhen R, Gopalakrishnan M, Li J. 2007. High content screen microscopy analysis of A beta 1-42-induced neurite outgrowth reduction in rat primary cortical neurons: neuroprotective effects of alpha 7 neuronal nicotinic acetylcholine receptor ligands. Brain Res 1151: 227-235.
34. Hu M, Waring JF, Gopalakrishnan M, Li J. 2008. Role of GSK-3beta activation and alpha7 nAChRs in Abeta(1-42)-induced tau phosphorylation in PC12 cells. J Neurochem 106: 1371-1377.
35. + current in rat medial preoptic neurons. J Physiol 532: 625-635.
36. + currents. Neurosci Lett 231: 13-16.
37. Kawamata J, Suzuki S, Shimohama S. 2011. Enhancement of nicotinic receptors alleviates cytotoxicity in neurological disease models. Ther Adv Chronic Dis (in press).
38. Khawaled R, Bruening-Wright A, Adelman JP, Maylie J. 1999. Bicuculline block of small-conductance calcium-activated potassium channels. Pflugers Arch 438: 314-321.
39. Khiroug SS, Khiroug L, Yakel JL. 2004. Rat nicotinic acetylcholine receptor alpha2beta2 channels: comparison of functional properties with alpha4beta2 channels in Xenopus oocytes. Neuroscience 124: 817-822.
40. Kihara T, Shimohama S, Sawada H, Honda K, Nakamizo T, Shibasaki H, Kume T, Akaike A. 2001. alpha 7 nicotinic receptor transduces signals to phosphatidylinositol 3-kinase to block A beta-amyloid-induced neurotoxicity. J Biol Chem 276: 13541-13546.
41. Konopacki J, Golebiewski H. 1993. Theta-like activity in hippocampal formation slices: cholinergic-GABAergic interaction. Neuroreport 4: 963-966.
42. Lawrence JJ. 2008. Cholinergic control of GABA release: emerging parallels between neocortex and hippocampus. Trends Neurosci 31: 317-327.
43. Liu Q, Zhang J, Zhu H, Qin C, Chen Q, Zhao B. 2007. Dissecting the signaling pathway of nicotine-mediated neuroprotection in a mouse Alzheimer disease model. FASEB J 21: 61-73.
44. Mabley JG, Pacher P, Szabo C. 2009. Activation of the cholinergic antiinflammatory pathway reduces ricin-induced mortality and organ failure in mice. Mol Med 15: 166-172.
45. Martin SE, de Fiebre NE, de Fiebre CM. 2004. The alpha7 nicotinic acetylcholine receptor-selective antagonist, methyllycaconitine, partially protects against beta-amyloid1-42 toxicity in primary neuron-enriched cultures. Brain Res 1022: 254-256.
46. Martins AH, Alves JM, Perez D, Carrasco M, Torres-Rivera W, Eterovic VA, Ferchmin PA, Ulrich H. 2012. Kinin-B2 receptor mediated neuroprotection after NMDA excitotoxicity is reversed in the presence of kinin-B1 receptor agonists. PLoS ONE 7: e30755.
47. Materi LM, Semba K. 2001. Inhibition of synaptically evoked cortical acetylcholine release by intracortical glutamate: involvement of GABAergic neurons. Eur J Neurosci 14: 38-46.
48. A receptors in hippocampal pyramidal neurons exhibit constitutive GABA-independent gating. Mol Pharmacol 71: 539-548.
49. Monette R, Small DL, Mealing G, Morley P. 1998. A fluorescence confocal assay to assess neuronal viability in brain slices. Brain Res Brain Res Protoc 2: 99-108.
50. Moor E, DeBoer P, Westerink BH. 1998. GABA receptors and benzodiazepine binding sites modulate hippocampal acetylcholine release in vivo. Eur J Pharmacol 359: 119-126.
51. Morishita H, Miwa JM, Heintz N, Hensch TK. 2010. Lynx1, a cholinergic brake, limits plasticity in adult visual cortex. Science 330: 1238-1240.
52. B receptors play a major role in paired-pulse facilitation in area CA1 of the rat hippocampus. Brain Res 531: 55-65.
53. Olney JW, Collins RC, Sloviter RS. 1986. Excitotoxic mechanisms of epileptic brain damage. Adv Neurol 44: 857-877.
54. Pavlov VA, Tracey KJ. 2006. Controlling inflammation: the cholinergic anti-inflammatory pathway. Biochem Soc Trans 34: 1037-1040.
55. Quik M, Wonnacott S. 2011. Alpha6beta2* and alpha4beta2* nicotinic acetylcholine receptors as drug targets for Parkinson's disease. Pharmacol Rev 63: 938-966.
56. Raggenbass M, Bertrand D. 2002. Nicotinic receptors in circuit excitability and epilepsy. J Neurobiol 53: 580-589.
57. Roland JJ, Savage LM. 2009. Blocking GABA-A receptors in the medial septum enhances hippocampal acetylcholine release and behavior in a rat model of diencephalic amnesia. Pharmacol Biochem Behav 92: 480-487.
58. Schurr A, Rigor BM. 1989. Cerebral ischemia revisited: new insights as revealed using in vitro brain slice preparations. Experientia 45: 684-695.
59. Schurr A, Payne RS, Heine MF, Rigor BM. 1995a. Hypoxia, excitotoxicity, and neuroprotection in the hippocampal slice preparation. J Neurosci Methods 59: 129-138.
60. Schurr A, Payne RS, Rigor BM. 1995b. Protection by MK-801 against hypoxia-, excitotoxin-, and depolarization-induced neuronal damage in vitro. Neurochem Int 26: 519-525.
61. Small DL, Monette R, Chakravarthy B, Durkin J, Barbe G, Mealing G, Morley P, Buchan AM. 1996. Mechanisms of 1S, 3R-ACPD-induced neuroprotection in rat hippocampal slices subjected to oxygen and glucose deprivation. Neuropharmacology 35: 1037-1048.
62. A receptors. Acta Neuropathol 105: 197-202.
63. Soriano FX, Papadia S, Hofmann F, Hardingham NR, Bading H, Hardingham GE. 2006. Preconditioning doses of NMDA promote neuroprotection by enhancing neuronal excitability. J Neurosci 26: 4509-4518.
64. Ueda M, Iida Y, Kitamura Y, Kawashima H, Ogawa M, Magata Y, Saji H. 2008. 5-Iodo-A-85380, a specific ligand for alpha 4 beta 2 nicotinic acetylcholine receptors, prevents glutamate neurotoxicity in rat cortical cultured neurons. Brain Res 1199: 46-52.
65. A receptors inhibit acetylcholine release in cat pontine reticular formation: implications for REM sleep regulation. J Neurophysiol 92: 2198-2206.
66. Wang H, Yu M, Ochani M, Amella CA, Tanovic M, Susarla S, Li JH, Yang H, Ulloa L, Al-Abed Y, Czura CJ, Tracey KJ. 2003. Nicotinic acetylcholine receptor alpha7 subunit is an essential regulator of inflammation. Nature 421: 384-388.
67. Wang T, Raley-Susman KM, Wang J, Chambers G, Cottrell JE, Kass IS. 1999. Thiopental attenuates hypoxic changes of electrophysiology, biochemistry, and morphology in rat hippocampal slice CA1 pyramidal cells. Stroke 30: 2400-2407.
68. Wei XW, Yan H, Xu B, Wu YP, Li C, Zhang GY. 2012. Neuroprotection of co-activation of GABA receptors by preventing caspase-3 denitrosylation in KA-induced seizures. Brain Res Bull 88: 617-623.
69. Woodcock TM. 2010. Modulation of the alpha-7 nicotinic acetylcholine receptor following experimental rat brain injury improves cellular and behavioral outcomes. Lexington: University of Kentucky.
70. Xu J, Li C, Yin XH, Zhang GY. 2008. Additive neuroprotection of GABA A and GABA B receptor agonists in cerebral ischemic injury via PI-3K/Akt pathway inhibiting the ASK1-JNK cascade. Neuropharmacology 54: 1029-1040.
71. Zhang ZW, Feltz P. 1991. Bicuculline blocks nicotinic acetylcholine response in isolated intermediate lobe cells of the pig. Br J Pharmacol 102: 19-22.