Galantamine promotes adult hippocampal neurogenesis via M1 muscarinic and α7 nicotinic receptors in mice

International Journal of Neuropsychopharmacology

Volumn 17, Issue 12, 2014, Pages 1957-1968

  Kita, Yuki ^a   Ago, Yukio ^a   Higashino, Kosuke ^a   Asada, Kazuki ^a   Takano, Erika ^a   Takuma, Kazuhiro ^a   Matsuda, Toshio ^a  

^a OSAKA UNIVERSITY   (Japan)

Author keywords

Acetylcholine receptor; Galantamine; Hippocampus; Insulin like growth factor 2 (IGF2); Neurogenesis.

Indexed keywords

BUNGAROTOXIN RECEPTOR; GALANTAMINE; GLIAL FIBRILLARY ACIDIC PROTEIN; IGF2 PROTEIN, MOUSE; MUSCARINIC M1 RECEPTOR; NERVE PROTEIN; NEUN PROTEIN, MOUSE; NEUROPROTECTIVE AGENT; NUCLEAR PROTEIN; RECOMBINANT PROTEIN; SOMATOMEDIN B; SOMATOMEDIN C RECEPTOR;

ANIMAL; ANTAGONISTS AND INHIBITORS; CELL SURVIVAL; DOSE RESPONSE; DRUG EFFECTS; HIPPOCAMPUS; MALE; METABOLISM; MOUSE; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; PHYSIOLOGY;

ALPHA7 NICOTINIC ACETYLCHOLINE RECEPTOR; ANIMALS; CELL SURVIVAL; DOSE-RESPONSE RELATIONSHIP, DRUG; GALANTAMINE; GLIAL FIBRILLARY ACIDIC PROTEIN; HIPPOCAMPUS; INSULIN-LIKE GROWTH FACTOR II; MALE; MICE; NERVE TISSUE PROTEINS; NEUROGENESIS; NEURONS; NEUROPROTECTIVE AGENTS; NUCLEAR PROTEINS; RECEPTOR, IGF TYPE 1; RECEPTOR, MUSCARINIC M1; RECOMBINANT PROTEINS;

EID: 84937511960     PISSN: 14611457     EISSN: 14695111     Source Type: Journal    
DOI: 10.1017/S1461145714000613     Document Type: Article

References (60)

1. Aasebø IE, Blankvoort S, Tashiro A (2011) Critical maturational period of new neurons in adult dentate gyrus for their involvement in memory formation. Eur J Neurosci 33:1094-1100.
2. Agis-Balboa RC, Arcos-Diaz D, Wittnam J, Govindarajan N, Blom K, Burkhardt S, Haladyniak U, Agbemenyah HY, Zovoilis A, Salinas-Riester G, Opitz L, Sananbenesi F, Fischer A (2011) A hippocampal insulin-growth factor 2 pathway regulates the extinction of fear memories. EMBO J 30:4071-4083.
3. Ago Y, Koda K, Takuma K, Matsuda T (2011a) Pharmacological aspects of the acetylcholinesterase inhibitor galantamine. J Pharmacol Sci 116:6-17.
4. Ago Y, Koda K, Ota Y, Kita Y, Fukada A, Takuma K, Matsuda T (2011b) Donepezil, but not galantamine, blocks muscarinic receptor-mediated in vitro and in vivo responses. Synapse 65:1373-1377.
5. Ago Y, Araki R, Tanaka T, Sasaga A, Nishiyama S, Takuma K, Matsuda T (2013) Role of social encounter-induced activation of prefrontal serotonergic systems in the abnormal behaviors of isolation-reared mice. Neuropsychopharmacology 38:1535-1547.
6. Alberini CM, Chen DY (2012) Memory enhancement: consolidation, reconsolidation and insulin-like growth factor 2. Trends Neurosci 35:274-283.
7. Anderson MF, Aberg MA, Nilsson M, Eriksson PS (2002) Insulin-like growth factor-I and neurogenesis in the adult mammalian brain. Dev Brain Res 134:115-122.
8. Berger F, Gage FH, Vijayaraghavan S (1998) Nicotinic receptor-induced apoptotic cell death of hippocampal progenitor cells. J Neurosci 18:6871-6881.
9. Bracko O, Singer T, Aigner S, Knobloch M, Winner B, Ray J, Clemenson GD Jr, Suh H, Couilland-Despres S, Aigner L, Gage FH, Jessberger S (2012) Gene expression profiling of neural stem cells and their neuronal progeny reveals IGF2 as a regulator of adult hippocampal neurogenesis. J Neurosci 32:3376-3387.
10. Cameron HA, McKay RD (2001) Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus. J Comp Neurol 435:406-417.
11. Chen DY, Stern SA, Garcia-Osta A, Saunier-Rebori B, Pollonini G, Bambah-Mukku D, Blitzer RD, Alberini CM (2011) A critical role for IGF-II in memory consolidation and enhancement. Nature 469:491-497.
12. Cooper-Kuhn CM, Winkler J, Kuhn HG (2004) Decreased neurogenesis after cholinergic forebrain lesion in the adult rat. J Neurosci Res 77:155-165.
13. Coronas V, Durand M, Chabot JG, Jourdan F, Quirion R (2000) Acetylcholine induces neuritic outgrowth in rat primary olfactory bulb cultures. Neuroscience 98:213-219.
14. Crews L, Masliah E (2010) Molecular mechanisms of neurodegeneration in Alzheimer's disease. Hum Mol Genet 19(R1):R12-R20.
15. Csernansky JG, Martin M, Shah R, Bertchume A, Colvin J, Dong H (2005) Cholinesterase inhibitors ameliorate behavioral deficits induced by MK-801 in mice. Neuropsychopharmacology 30:2135-2143.
16. Curtis MA, Low VF, Faull RL (2012) Neurogenesis and progenitor cells in the adult human brain: a comparison between hippocampal and subventricular progenitor proliferation. Dev Neurobiol 72:990-1005.
17. 2+ signals and neurotransmitter release. Mol Pharmacol 64:1217-1226.
18. DeCarolis NA, Eisch AJ (2010) Hippocampal neurogenesis as a target for the treatment of mental illness: a critical evaluation. Neuropharmacology 58:884-893.
19. Erb C, Troost J, Kopf S, Schmitt U, Löffelholz K, Soreq H, Klein J (2001) Compensatory mechanisms enhance hippocampal acetylcholine release in transgenic mice expressing human acetylcholinesterase. J Neurochem 77:638-646.
20. Eriksson PS, Perfilieva E, Bjork-Eriksson T, Alborn AM, Nordborg C, Peterson DA, Gage FH (1998) Neurogenesis in the adult human hippocampus. Nat Med 4:1313-1317.
21. Espósito MS, Piatti VC, Laplagne DA, Morgenstern NA, Ferrari CC, Pitossi FJ, Schinder AF (2005) Neuronal differentiation in the adult hippocampus recapitulates embryonic development. J Neurosci 25:10074-10086.
22. Fernandez AM, Torres-Alemán I (2012) The many faces of insulin-like peptide signalling in the brain. Nat Rev Neurosci 13:225-239.
23. Frielingsdorf H, Simpson DR, Thal LJ, Pizzo DP (2007) Nerve growth factor promotes survival of new neurons in the adult hippocampus. Neurobiol Dis 26:47-55.
24. Ge S, Goh EL, Sailor KA, Kitabatake Y, Ming GL, Song H (2006) GABA regulates synaptic integration of newly generated neurons in the adult brain. Nature 439:589-593.
25. Harrist A, Beech RD, King SL, Zanardi A, Cleary MA, Caldarone BJ, Eisch A, Zoli M, Picciotto MR (2004) Alteration of hippocampal cell proliferation in mice lacking the β2 subunit of the neuronal nicotinic acetylcholine receptor. Synapse 54:200-206.
26. Jin K, Xie L, Mao XO, Greenberg DA (2006) Alzheimer's disease drugs promote neurogenesis. Brain Res 1085:183-188.
27. Kaneko N, Okano H, Sawamoto K (2006) Role of the cholinergic system in regulating survival of newborn neurons in the adult mouse dentate gyrus and olfactory bulb. Genes Cells 11:1145-1159.
28. Kita Y, Ago Y, Takano E, Fukada A, Takuma K, Matsuda T (2013) Galantamine increases hippocampal insulin-like growth factor 2 expression via α7 nicotinic acetylcholine receptors in mice. Psychopharmacology 225:543-551.
29. Koda K, Ago Y, Kawasaki T, Hashimoto H, Baba A, Matsuda T (2008) Galantamine and donepezil differently affect isolation rearing-induced deficits of prepulse inhibition in mice. Psychopharmacology 196:293-301.
30. Koda K, Ago Y, Yano K, Nishimura M, Kobayashi H, Fukada A, Takuma K, Matsuda T (2011) Involvement of decreased muscarinic receptor function in prepulse inhibition deficits in mice reared in social isolation. Br J Pharmacol 162:763-772.
31. Kotani S, Yamauchi T, Teramoto T, Ogura H (2006) Pharmacological evidence of cholinergic involvement in adult hippocampal neurogenesis in rats. Neuroscience 142:505-514.
32. Lazarov O, Marr RA (2010) Neurogenesis and Alzheimer's disease: at the crossroads. Exp Neurol 223:267-281.
33. Lee J, Duan W, Mattson MP (2002) Evidence that brain-derived neurotrophic factor is required for basal neurogenesis and mediates, in part, the enhancement of neurogenesis by dietary restriction in the hippocampus of adult mice. J Neurochem 82:1367-1375.
34. Llorens-Martín M, Torres-Alemán I, Trejo JL (2009) Mechanisms mediating brain plasticity: IGF1 and adult hippocampal neurogenesis. Neuroscientist 15:134-148.
35. Ma W, Maric D, Li BS, Hu Q, Andreadis JD, Grant GM, Liu QY, Shaffer KM, Chang YH, Zhang L, Pancrazio JJ, Pant HC, Stenger DA, Barker JL (2000) Acetylcholine stimulates cortical precursor cell proliferation in vitro via muscarinic receptor activation and MAP kinase phosphorylation. Eur J Neurosci 12:1227-1240.
36. Maelicke A, Albuquerque EX (2000) Allosteric modulation of nicotinic acetylcholine receptors as a treatment strategy for Alzheimer's disease. Eur J Pharmacol 393:165-170.
37. Maelicke A, Samochocki M, Jostock R, Fehrenbacher A, Ludwig J, Albuquerque EX, Zerlin M (2001) Allosteric sensitization of nicotinic receptors by galantamine, a new treatment strategy for Alzheimer's disease. Biol Psychiatry 49:279-288.
38. Matsuda T (2013) Neuropharmacological studies on the brain serotonin1A receptor using the selective agonist osemozotan. Biol Pharm Bull 36:1871-1882.
39. Ming GL, Song H (2011) Adult neurogenesis in the mammalian brain: significant answers and significant questions. Neuron 70:687-702.
40. Mohapel P, Leanza G, Kokaia M, Lindvall O (2005) Forebrain acetylcholine regulates adult hippocampal neurogenesis and learning. Neurobiol Aging 26:939-946.
41. Noda Y, Mouri A, Ando Y, Waki Y, Yamada SN, Yoshimi A, Yamada K, Ozaki N, Wang D, Nabeshima T (2010) Galantamine ameliorates the impairment of recognition memory in mice repeatedly treated with methamphetamine: involvement of allosteric potentiation of nicotinic acetylcholine receptors and dopaminergic-ERK1/2 systems. Int J Neuropsychopharmacol 13:1343-1354.
42. Nordberg A, Lundqvist H, Hartvig P, Lilja A, La˚ngström B (1995) Kinetic analysis of regional (S)(-)11C-nicotine binding in normal and Alzheimer brains - in vivo assessment using positron emission tomography. Alzheimer Dis Assoc Disord 9:21-27.
43. Ouchi Y, Banno Y, Shimizu Y, Ando S, Hasegawa H, Adachi K, Iwamoto T (2013) Reduced adult hippocampal neurogenesis and working memory deficits in the Dgcr8-deficient mouse model of 22q11.2 deletion-associated schizophrenia can be rescued by IGF2. J Neurosci 33:9408-9419.
44. Perry E, Martin-Ruiz C, Lee M, Griffiths M, Johnson M, Piggott M, Haroutunian V, Buxbaum JD, Nãsland J, Davis K, Gotti C, Clementi F, Tzartos S, Cohen O, Soreq H, Jaros E, Perry R, Ballard C, McKeith I, Court J (2000) Nicotinic receptor subtypes in human brain ageing. Alzheimer and Lewy body diseases. Eur J Pharmacol 393:215-222.
45. Resende RR, Alves AS, Britto LR, Ulrich H (2008) Role of acetylcholine receptors in proliferation and differentiation of P19 embryonal carcinoma cells. Exp Cell Res 314:1429-1443.
46. Rossi C, Angelucci A, Costantin L, Braschi C, Mazzantini M, Babbini F, Fabbri ME, Tessarollo L, Maffei L, Berardi N, Caleo M (2006) Brain-derived neurotrophic factor (BDNF) is required for the enhancement of hippocampal neurogenesis following environmental enrichment. Eur J Neurosci 24:1850-1856.
47. Samochocki M, Höffle A, Fehrenbacher A, Jostock R, Ludwig J, Christner C, Radina M, Zerlin M, Ullmer C, Pereira EF, Lübbert H, Albuquerque EX, Maelicke A (2003) Galantamine is an allosterically potentiating ligand of neuronal nicotinic but not of muscarinic acetylcholine receptors. J Pharmacol Exp Ther 305:1024-1036.
48. Schänzer A, Wachs FP, Wilhelm D, Acker T, Cooper-Kuhn C, Beck H, Winkler J, Aigner L, Plate KH, Kuhn HG (2004) Direct stimulation of adult neural stem cells in vitro and neurogenesis in vivo by vascular endothelial growth factor. Brain Pathol 14:237-248.
49. Schilström B, Ivanov VB, Wiker C, Svensson TH (2007) Galantamine enhances dopaminergic neurotransmission in vivo via allosteric potentiation of nicotinic acetylcholine receptors. Neuropsychopharmacology 32:43-53.
50. Shruster A, Offen D (2014) Targeting neurogenesis ameliorates danger assessment in a mouse model of Alzheimer's disease. Behav Brain Res 261:193-201.
51. Song G, Ouyang G, Bao S (2005) The activation of Akt/PKB signaling pathway and cell survival. J Cell Mol Med 9:59-71.
52. Tanaka K, Yagi T, Shimakoshi R, Azuma K, Nanba T, Ogo H, Tamura A, Asanuma M (2009) Effects of galantamine on L-NAME-induced behavioral impairment in Y-maze task in mice. Neurosci Lett 462:235-238.
53. Tashiro A, Makino H, Gage FH (2007) Experience-specific functional modification of the dentate gyrus through adult neurogenesis: a critical period during an immature stage. J Neurosci 27:3252-3259.
54. Veyrac A, Gros A, Bruel-Jungerman E, Rochefort C, Kleine Borgmann FB, Jessberger S, Laroche S (2013) Zif268/egr1 gene controls the selection, maturation and functional integration of adult hippocampal newborn neurons by learning. Proc Natl Acad Sci USA 110:7062-7067.
55. Wadenberg ML, Fjällström AK, Federley M, Persson P, Stenqvist P (2011) Effects of adjunct galantamine to risperidone, or haloperidol, in animal models of antipsychotic activity and extrapyramidal side-effect liability: involvement of the cholinergic muscarinic receptor. Int J Neuropsychopharmacol 14:644-654.
56. Wang D, Noda Y, Zhou Y, Mouri A, Mizoguchi H, Nitta A, Chen W, Nabeshima T (2007) The allosteric potentiation of nicotinic acetylcholine receptors by galantamine ameliorates the cognitive dysfunction in beta amyloid 25-35 i.c.v.-injected mice: involvement of dopaminergic systems. Neuropsychopharmacology 32:1261-1271.
57. Wishka DG, Walker DP, Yates KM, Reitz SC, Jia S, Myers JK, Olson KL, Jacobsen EJ, Wolfe ML, Groppi VE, Hanchar AJ, Thornburgh BA, Cortes-Burgos LA, Wong EH, Staton BA, Raub TJ, Higdon NR, Wall TM, Hurst RS, Walters RR et al. (2006) Discovery of N-[(3R)-1-azabicyclo[2.2.2]oct-3-yl]furo [2,3- c]pyridine-5-carboxamide, an agonist of the α7 nicotinic acetylcholine receptor, for the potential treatment of cognitive deficits in schizophrenia: synthesis and structure-activity relationship. J Med Chem 49:4425-4436.
58. Yano K, Koda K, Ago Y, Kobayashi H, Takuma K, Matsuda T (2009) Galantamine improves apomorphine-induced deficits in prepulse inhibition via muscarinic ACh receptors in mice. Br J Pharmacol 156:173-180.
59. Zhao C, Teng EM, Summers RG, Ming GL, Gage FH (2006) Distinct morphological stages of dentate granule neuron maturation in the adult mouse hippocampus. J Neurosci 26:3-11.
60. Zhao C, Deng W, Gage FH (2008) Mechanisms and functional implications of adult neurogenesis. Cell 132:645-660.