Nicotinic acetylcholine receptors mediate donepezil-induced oligodendrocyte differentiation

Journal of Neurochemistry

Volumn 135, Issue 6, 2015, Pages 1086-1098

  Imamura, Osamu ^a   Arai, Masaaki ^a   Dateki, Minori ^a   Ogata, Toru ^b   Uchida, Ryuji ^c   Tomoda, Hiroshi ^c   Takishima, Kunio ^a  

^a NATIONAL DEFENSE MEDICAL COLLEGE   (Japan)

^b NATIONAL REHABILITATION CENTER FOR PERSONS WITH DISABILITIES   (Japan)

^c KITASATO UNIVERSITY   (Japan)

Author keywords

acetylcholinesterase inhibitor; donepezil hydro chloride; gene expression; myelination; oligodendrocytes

Indexed keywords

2',3' CYCLIC NUCLEOTIDE 3' PHOSPHODIESTERASE; DONEPEZIL; MECAMYLAMINE; MESSENGER RNA; MYELIN ASSOCIATED GLYCOPROTEIN; MYELIN BASIC PROTEIN; MYELIN OLIGODENDROCYTE GLYCOPROTEIN; NICOTINIC RECEPTOR; PROTEOLIPID PROTEIN; SCOPOLAMINE; INDAN DERIVATIVE; PIPERIDINE DERIVATIVE;

ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL MATURATION; CELL PROLIFERATION; CELL VIABILITY; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVITY; ENZYME INHIBITION; FEMALE; FETUS; GENE EXPRESSION; IN VITRO STUDY; MOUSE; MYELINATION; NEURAL STEM CELL; NEUROPROTECTION; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; ANIMAL; CELL CULTURE; CENTRAL NERVOUS SYSTEM; CYTOLOGY; DRUG EFFECTS; METABOLISM; MULTIPLE SCLEROSIS; NERVOUS SYSTEM DEVELOPMENT; PHYSIOLOGY; STEM CELL;

ANIMALS; CELL DIFFERENTIATION; CELLS, CULTURED; CENTRAL NERVOUS SYSTEM; FEMALE; GENE EXPRESSION; INDANS; MICE; MULTIPLE SCLEROSIS; MYELIN BASIC PROTEIN; NEUROGENESIS; OLIGODENDROGLIA; PIPERIDINES; RECEPTORS, NICOTINIC; STEM CELLS;

EID: 84955103928     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/jnc.13294     Document Type: Article

References (48)

1. Akaike A., Takada-Takatori Y., Kume T., and, Izumi Y., (2010) Mechanisms of neuroprotective effects of nicotine and acetylcholinesterase inhibitors: role of α4 and α7 receptors in neuroprotection. J. Mol. Neurosci. 40, 211-216.
2. Armstrong R. C., (1998) Isolation and characterization of immature oligodendrocyte lineage cells. Methods 16, 282-292.
3. Bujalka H., Koenning M., Jackson S., et al,. (2013) MYRF is a membrane-associated transcription factor that autoproteolytically cleaves to directly activate myelin genes. PLoS Biol. 11, e1001625.
4. Caillava C., Vandenbosch R., Jablonska B., Deboux C., Spigoni G., Gallo V., Malgrange B., and, Van Evercooren A. B., (2011) J. Cell Biol. 193, 397-407.
5. Chang A., Nishiyama A., Peterson J., Prineas J., and, Trapp B. D., (2000) NG2-positive oligodendrocyte progenitor cells in adult human brain and multiple sclerosis lesions. J. Neurosci. 20, 6404-6412.
6. Chang A., Tourtellotte W. W., Rudick R., and, Trapp B. D., (2002) Premyelinating oligodendrocytes in chronic lesions of multiple sclerosis. N. Engl. J. Med. 346, 165-173.
7. Di Angelantonio S., Bernardi G., and, Mercuri N. B., (2004) Donepezil modulates nicotinic receptors of substantia nigra dopaminergic neurones. Br. J. Pharmacol. 141, 644-652.
8. Emery B., Agalliu D., Cahoy J. D., Watkins T. A., Dugas J. C., Mulinyawe S. B., Ibrahim A., Ligon K. L., Rowitch D. H., and, Barres B. A., (2009) Myelin gene regulatory factor is a critical transcriptional regulator required for CNS myelination. Cell 138, 172-185.
9. Fancy S. P. J., Baranzini S. E., Zhao C., Yuk D. I., Irvine K. A., Kaing S., Sanai N., Franklin R. J. M., and, Rowitch D. H., (2009) Dysregulation of the Wnt pathway inhibits timely myelination and remyelination in the mammalian CNS. Genes Dev. 23, 1571-1585.
10. Goldman S. A., Nedergaard M., and, Windrem M. S., (2012) Glial progenitor cell-based treatment and modeling of neurological disease. Science 338, 491-495.
11. He Y., Dupree J., Wang J., Sandoval J., Li J., Liu H., Shi Y., Nave K. A., and, Casaccia-Bonnefil P., (2007) The transcription factor yin yang 1 is essential for oligodendrocyte progenitor differentiation. Neuron 55, 217-230.
12. Hoshikawa S., Ogata T., Fujiwara S., Nakamura K., and, Tanaka S., (2008) A novel function of RING finger protein 10 in transcriptional regulation of the myelin-associated glycoprotein gene and myelin formation in Schwann cells. PLoS ONE 3, e3464.
13. Howng S. Y. B., Avila R. L., Emery B., et al,. (2010) ZFP191 is required by oligodendrocytes for CNS myelination. Genes Dev. 24, 301-311.
14. Imamura O., Satoh Y., Endo S., and, Takishima K., (2008) Analysis of extracellular signal-regulated kinase 2 function in neural stem/progenitor cells via nervous system-specific gene disruption. Stem Cells 26, 3247-3256.
15. Jiang Y., Yan Z., Chen S., et al,. (2013) The anti-inflammatory effect of donepezil on experimental autoimmune encephalomyelitis in C57 BL/6 mice. Neuropharmacology 73, 415-424.
16. Jin K., Xie L., Mao X. O., and, Greenberg D. A., (2006) Alzheimer's disease drugs promote neurogenesis. Brain Res. 1085, 183-188.
17. Kita Y., Ago Y., Higashino K., Asada K., Takano E., Takuma K., and, Matsuda T., (2014) Galantamine promotes adult hippocampal neurogenesis via M1 muscarinic and α7 nicotinic receptors in mice. Int. J. Neuropsychopharmacol. 17, 1957-1968.
18. Koenning M., Jackson S., Hay C. M., Faux C., Kilpatrick T. J., Willingham M., and, Emery B., (2012) Myelin gene regulatoryfactor is required for maintenance of myelin and mature oligodendrocyte identity in the adult CNS. J. Neurosci. 32, 12528-12542.
19. Kondo T., and, Raff M., (2000) The Id4 HLH protein and the timing of oligodendrocyte differentiation. EMBO J. 19, 1998-2007.
20. Kotani S., Yamauchi T., Teramoto T., and, Ogura H., (2006) Pharmacological evidence of cholinergic involvement in adult hippocampal neurogenesis in rats. Neuroscience 142, 505-514.
21. Kuhlmann T., Miron V., Cuo Q., Wegner C., Antel J., and, Brück W., (2008) Differentiation block of oligodendroglial progenitor cells as a cause for remyelination failure in chronic multiple sclerosis. Brain 131, 1749-1758.
22. Kume T., Sugimoto M., Takada Y., Yamaguchi T., Yonezawa A., Katsuki H., Sugimoto H., and, Akaike A., (2005) Up-regulation of nicotinic acetylcholine receptors by central-type acetylcholinesterase inhibitors in rat cortical neurons. Eur. J. Pharmacol. 527, 77-85.
23. Li H., Lu Y., Smith H. K., and, Richardson W. D., (2007) Olig1 and Sox10 interact synergistically to drive myelin basic protein transcription in oligodendrocytes. J. Neurosci. 27, 14375-14382.
24. Marin-Husstege M., He Y., Li J., Kondo T., Sablitzky F., and, Casaccia-Bonnefil P., (2006) Multiple roles of Id4 in developmental myelination: predicted outcomes and unexpected findings. Glia 54, 285-296.
25. Menn B., Garcia-Verdugo J. M., Yaschine C., Gonzalez-Perez O., Rowitch D., and, Alvarez-Buylla A., (2006) Origin of oligodendrocytes in the subventricular zone of the adult brain. J. Neurosci. 26, 7907-7918.
26. Miller R. H., (2002) Regulation of oligodendrocyte development in the vertebrate CNS. Prog. Neurobiol. 67, 451-467.
27. Noh M.-Y., Koh S.-H., Kim Y., Kim H. Y., Cho G. W., and, Kim S. H., (2009) Neuroprotective effects of donepezil through inhibition of GSK-3 activity in amyloid-beta-induced neuronal cell death. J. Neurochem. 108, 1116-1125.
28. Pfeiffer S. E., Warrington A. E., and, Bansal R., (1993) The oligodendrocyte and its many cellular processes. Trends Cell Biol. 3, 191-197.
29. Pollak Y., Gilboa A., Ben-Menachem O., Ben-Hur T., Soreq H., and, Yirmiya R., (2005) Acetylcholinesterase inhibitors reduce brain and blood interleukin-1beta production. Ann. Neurol. 57, 741-745.
30. Qi Y., Cai J., Wu Y., Wu R., Lee J., Fu H., Rao M., Sussel L., Rubenstein J., and, Qiu M., (2001) Control of oligodendrocyte differentiation by the Nkx2.2 homeodomain transcription factor. Development 128, 2723-2733.
31. Rao R. C., Boyd J., Padmanabhan R., Chenoweth J. G., and, McKay R. D., (2009) Efficient serum-free derivation of oligodendrocyte precursors from neural stem cell-enriched cultures. Stem Cells 27, 116-125.
32. Resende R. R., and, Adhikari A., (2009) Cholinergic receptor pathways involved in apoptosis, cell proliferation and neuronal differentiation. Cell Commun. Signal. 7, 20.
33. Richardson W. D., Kessaris N., and, Pringle N., (2006) Oligodendrocyte wars. Nat. Rev. Neurosci. 7, 11-18.
34. Rogers S. W., Gregori N. Z., Carlson N., Gahring L. C., and, Noble M., (2001) Neuronal nicotinic acetylcholine receptor expression by O2A/oligodendrocyte progenitor cells. Glia 33, 306-313.
35. Shen J. X., and, Yakel J. L., (2012) Functional α7 nicotinic ACh receptors on astrocytes in rat hippocampal CA1 slices. J. Mol. Neurosci. 48, 14-21.
36. Shen H., Kihara T., Hongo H., Wu X., Kem W. R., Shimohama S., Akaike A., Niidome T., and, Sugimoto H., (2010) Neuroprotection by donepezil against glutamate excitotoxicity involves stimulation of α7 nicotinic receptors and internalization of NMDA receptors. Br. J. Pharmacol. 161, 127-139.
37. Sugimoto H., Yamanishi Y., Iimura Y., and, Kawakami Y., (2000) Donepezil hydrochloride (E2020) and other acetylcholinesterase inhibitors. Curr. Med. Chem. 7, 303-339.
38. Takada Y., Yonezawa A., Kume T., Katsuki H., Kaneko S., Sugimoto H., and, Akaike A., (2003) Nicotinic acetylcholine receptor-mediated neuroprotection by donepezil against glutamate neurotoxicity in rat cortical neurons. J. Pharmacol. Exp. Ther. 306, 772-777.
39. Takada-Takatori Y., Kume T., Ohgi Y., Izumi Y., Niidome T., Fujii T., Sugimoto H., and, Akaike A., (2008) Mechanism of neuroprotection by donepezil pretreatment in rat cortical neurons chronically treated with donepezil. J. Neurosci. Res. 86, 3575-3583.
40. Takata K., Kitamura Y., Saeki M., et al,. (2010) Galantamine-induced amyloid-β clearance mediated via stimulation of microglial nicotinic acetylcholine receptors. J. Biol. Chem. 285, 40180-40191.
41. Totoiu M. O., and, Keirstead H. S., (2005) Spinal cord injury is accompanied by chronic progressive demyelination. J. Comp. Neurol. 486, 373-383.
42. Vélez-Fort M., Audinat E., and, Angulo M. C., (2009) Functional α7-containing nicotinic receptors of NG2-expressing cells in the hippocampus. Glia 57, 1104-1114.
43. Wang S.-Z., Dulin J., Wu H., Hurlock E., Lee S.-E., Jansson K., and, Lu Q. R., (2006) An oligodendrocyte-specific zinc-finger transcription regulator cooperates with Olig2 to promote oligodendrocyte differentiation. Development 133, 3389-3398.
44. Wolswijk G., (1998) Chronic stage multiple sclerosis lesions contain a relatively quiescent population of oligodendrocyte precursor cells. J. Neurosci. 18, 601-609.
45. Wolswijk G., (2002) Oligodendrocyte precursor cells in the demyelinated multiple sclerosis spinal cord. Brain 125, 338-349.
46. Wynn Z. J., and, Cummings J. L., (2004) Cholinesterase inhibitor therapies and neuropsychiatric manifestations of Alzheimer's disease. Dement. Geriatr. Cogn. Disord. 17, 100-108.
47. Xin M., Yue T., Ma Z., Wu F., Gow A., and, Lu Q. R., (2005) Myelinogenesis and axonal recognition by oligodendrocytes in brain are uncoupled in Olig1-null mice. J. Neurosci. 25, 1354-1365.
48. Zuchero J. B., and, Barres B. A., (2013) Intrinsic and extrinsic control of oligodendrocyte development. Curr. Opin. Neurobiol. 23, 914-920.