Melatonin attenuates scopolamine-induced memory/synaptic disorder by rescuing EPACs/miR-124/Egr1 pathway

Molecular Neurobiology

Volumn 47, Issue 1, 2013, Pages 373-381

  Wang, Xiong ^a   Wang, Zhi Hao ^a   Wu, Yuan Yuan ^a   Tang, Hui ^a   Tan, Lu ^a   Wang, Xiang ^a   Gao, Xin Ya ^a   Xiong, Yan Si ^a   Liu, Dan ^a,b   Wang, Jian Zhi ^a,b   Zhu, Ling Qiang ^a,b  

^a HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^b BEIJING UNIVERSITY OF POSTS AND TELECOMMUNICATIONS   (China)

Author keywords

Dendritic spine; EPAC; Melatonin; miR 124; Synaptic disorder

Indexed keywords

CAMP REGULATED GUANINE NUCLEOTIDE EXCHANGE FACTOR 1; CYCLIC AMP; EARLY GROWTH RESPONSE FACTOR 1; MELATONIN; MICRORNA 124; SCOPOLAMINE; UNCLASSIFIED DRUG; WATER;

AMNESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AVOIDANCE BEHAVIOR; CONTROLLED STUDY; EPIGENETICS; GOLGI STAIN; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; INHIBITION KINETICS; LONG TERM POTENTIATION; MALE; MAZE TEST; MEMORY DISORDER; NEUROLOGIC DISEASE; NONHUMAN; RAT; REAL TIME POLYMERASE CHAIN REACTION; REVIEW; SIGNAL TRANSDUCTION; SYNAPTIC DISORDER; TASK PERFORMANCE; WESTERN BLOTTING;

EID: 84872501370     PISSN: 08937648     EISSN: 15591182     Source Type: Journal    
DOI: 10.1007/s12035-012-8355-9     Document Type: Review

References (41)

1. Chang CF, Huang HJ, Lee HC, Hung KC, Wu RT, Lin AM (2012) Melatonin attenuates kainic acid-induced neurotoxicity in mouse hippocampus via inhibition of autophagy and alpha-synuclein aggregation. J Pineal Res 52:312-321. doi: 10.1111/j.1600-079X.2011.00945.x
2. Zhu LQ, Wang SH, Ling ZQ, Wang DL, Wang JZ (2004) Effect of inhibiting melatonin biosynthesis on spatial memory retention and tau phosphorylation in rat. J Pineal Res 37:71-77. doi: 10.1111/j.1600-079X.2004.00136.xJPI136 [pii]
3. Zhou JN, Liu RY, Kamphorst W, Hofman MA, Swaab DF (2003) Early neuropathological Alzheimer's changes in aged individuals are accompanied by decreased cerebrospinal fluid melatonin levels. J Pineal Res 35:125-130
4. Ramirez-Rodriguez G, Ortiz-Lopez L, Dominguez-Alonso A, Benitez-King GA, Kempermann G (2010) Chronic treatment with melatonin stimulates dendrite maturation and complexity in adult hippocampal neurogenesis of mice. J Pineal Res 50:29-37. doi: 10.1111/j.1600-079X.2010.00802.x
5. Dominguez-Alonso A, Ramirez-Rodriguez G, Benitez-King G (2012) Melatonin increases dendritogenesis in the hilus of hippocampal organotypic cultures. J Pineal Res 52:427-436. doi: 10.1111/j.1600-079X.2011.00957.x
6. Gonzalez-Burgos I, Letechipia-Vallejo G, Lopez-Loeza E, Morali G, Cervantes M (2007) Long-term study of dendritic spines from hippocampal CA1 pyramidal cells, after neuroprotective melatonin treatment following global cerebral ischemia in rats. Neurosci Lett 423:162-166. doi: 10.1016/j.neulet. 2007.06.050
7. Pascual R, Bustamante C (2010) Melatonin promotes distal dendritic ramifications in layer II/III cortical pyramidal cells of rats exposed to toluene vapors. Brain Res 1355:214-220. doi: 10.1016/j.brainres.2010.07.086
8. Saxena G, Bharti S, Kamat PK, Sharma S, Nath C (2009) Melatonin alleviates memory deficits and neuronal degeneration induced by intracerebroventricular administration of streptozotocin in rats. Pharmacol Biochem Behav 94:397-403. doi: 10.1016/j.pbb.2009.09.022
9. Shen YX, Wei W, Yang J, Liu C, Dong C, Xu SY (2001) Improvement of melatonin to the learning and memory impairment induced by amyloid beta-peptide 25-35 in elder rats. Acta Pharmacol Sin 22:797-803
10. Yang X et al (2010) Melatonin ameliorates Alzheimer-like pathological changes and spatial memory retention impairment induced by calyculin A. J Psychopharmacol 25:1118-1125. doi: 10.1177/0269881110367723
11. Agrawal R, Tyagi E, Shukla R, Nath C (2008) Effect of insulin and melatonin on acetylcholinesterase activity in the brain of amnesic mice. Behav Brain Res 189:381-386. doi: 10.1016/j.bbr.2008.01.015
12. Schratt G (2009) microRNAs at the synapse. Nat Rev Neurosci 10:842-849. doi: 10.1038/nrn2763
13. Lee SE, Kim SJ, Youn JP, Hwang SY, Park CS, Park YS (2011) MicroRNA and gene expression analysis of melatonin-exposed human breast cancer cell lines indicating involvement of the anticancer effect. J Pineal Res 51:345-352. doi: 10.1111/j.1600-079X.2011.00896.x
14. Morris R (1984) Developments of a water-maze procedure for studying spatial learning in the rat. J Neurosci Methods 11:47-60
15. Yin YY et al (2010) Acetyl-l-carnitine attenuates okadaic acid induced tau hyperphosphorylation and spatial memory impairment in rats. J Alzheimers Dis 19:735-746. doi: 10.3233/JAD-2010-1272
16. Zhu LQ et al (2007) Activation of glycogen synthase kinase-3 inhibits long-term potentiation with synapse-associated impairments. J Neurosci 27:12211-12220. doi: 10.1523/JNEUROSCI.3321-07.2007
17. Segal M (2005) Dendritic spines and long-term plasticity. Nat Rev Neurosci 6:277-284. doi: 10.1038/nrn1649
18. Hsieh MT, Hsieh CL, Lin LW, Wu CR, Huang GS (2003) Differential gene expression of scopolamine-treated rat hippocampus-application of cDNA microarray technology. Life Sci 73:1007-1016
19. Roy D, Belsham DD (2002) Melatonin receptor activation regulates GnRH gene expression and secretion in GT1-7 GnRH neurons. Signal transduction mechanisms. J Biol Chem 277:251-258. doi: 10.1074/jbc.M108890200 M108890200 [pii]
20. Yang Y et al (2012) EPAC null mutation impairs learning and social interactions via aberrant regulation of miR-124 and Zif268 translation. Neuron 73:774-788. doi: 10.1016/j.neuron.2012.02.003
21. Verloes R, Scotto AM, Gobert J, Wulfert E (1988) Effects of nootropic drugs in a scopolamine-induced amnesia model in mice. Psychopharmacol (Berl) 95:226-230
22. Brouillette J, Young D, During MJ, Quirion R (2007) Hippocampal gene expression profiling reveals the possible involvement of Homer1 and GABA(B) receptors in scopolamine-induced amnesia. J Neurochem 102:1978-1989. doi: 10.1111/j.1471-4159.2007.04666.x
23. Laurent AC, Breckler M, Berthouze M, Lezoualc'h F (2012) Role of Epac in brain and heart. Biochem Soc Trans 40:51-57. doi: 10.1042/BST20110642
24. Ostroveanu A, van der Zee EA, Eisel UL, Schmidt M, Nijholt IM (2009) Exchange protein activated by cyclic AMP 2 (Epac2) plays a specific and time-limited role in memory retrieval. Hippocampus 20:1018-1026. doi: 10.1002/hipo.20700
25. Ouyang M, Zhang L, Zhu JJ, Schwede F, SA T (2008) Epac signaling is required for hippocampus-dependent memory retrieval. Proc Natl Acad Sci USA 105:11993-11997
26. Ma N, Abel T, Hernandez PJ (2009) Exchange protein activated by cAMP enhances long-term memory formation independent of protein kinase A. Learn Mem 16:367-370. doi: 10.1101/lm.1231009
27. Gelinas JN, Banko JL, Peters MM, Klann E, Weeber EJ, Nguyen PV (2008) Activation of exchange protein activated by cyclic-AMP enhances long-lasting synaptic potentiation in the hippocampus. Learn Mem 15:403-411. doi: 10.1101/lm.830008
28. Ster J et al (2009) Epac mediates PACAP-dependent long-term depression in the hippocampus. J Physiol 587:101-113. doi: 10.1113/jphysiol.2008.157461
29. Gekel I, Neher E (2008) Application of an Epac activator enhances neurotransmitter release at excitatory central synapses. J Neurosci 28:7991-8002. doi: 10.1523/JNEUROSCI.0268-08.2008
30. Woolfrey KM et al (2009) Epac2 induces synapse remodeling and depression and its disease-associated forms alter spines. Nat Neurosci 12:1275-1284. doi: 10.1038/nn.2386
31. Enserink JM et al (2004) The cAMP-Epac-Rap1 pathway regulates cell spreading and cell adhesion to laminin-5 through the alpha3beta1 integrin but not the alpha6beta4 integrin. J Biol Chem 279:44889-44896. doi: 10.1074/jbc.M404599200 M404599200 [pii]
32. Lopez De Jesus M et al (2006) Cyclic AMP-dependent and Epac-mediated activation of R-Ras by G protein-coupled receptors leads to phospholipase D stimulation. J Biol Chem 281:21837-21847. doi: 10.1074/jbc.M604156200
33. Makeyev EV, Zhang J, Carrasco MA, Maniatis T (2007) The MicroRNA miR-124 promotes neuronal differentiation by triggering brain-specific alternative pre-mRNA splicing. Mol Cell 27:435-448. doi: 10.1016/j.molcel.2007.07.015
34. Clokie SJ, Lau P, Kim HH, Coon SL, Klein D (2012) Micro RNAs in the pineal gland: mir-483 regulates melatonin synthesis by targeting arylalkylamine N-acetyltransferase. J Biol Chem. doi: 10.1074/jbc.M112.356733
35. Masilamoni JG et al (2008) The neuroprotective role of melatonin against amyloid beta peptide injected mice. Free Radic Res 42:661-673. doi: 10.1080/10715760802277388
36. Jeong JK, Moon MH, Lee YJ, Seol JW, Park SY (2012) Melatonin-induced autophagy protects against human prion protein-mediated neurotoxicity. J Pineal Res. doi: 10.1111/j.1600-079X.2012.00980.x
37. Lee EJ et al (2005) Melatonin attenuates gray and white matter damage in a mouse model of transient focal cerebral ischemia. J Pineal Res 38:42-52. doi: 10.1111/j.1600-079X.2004.00173.x
38. Asayama K, Yamadera H, Ito T, Suzuki H, Kudo Y, Endo S (2003) Double blind study of melatonin effects on the sleep-wake rhythm, cognitive and non-cognitive functions in Alzheimer type dementia. J Nihon Med Sch 70:334-341
39. Uchida K, Okamoto N, Ohara K, Morita Y (1996) Daily rhythm of serum melatonin in patients with dementia of the degenerate type. Brain Res 717:154-159
40. Crozier RA, Bi C, Han YR, Plummer MR (2008) BDNF modulation of NMDA receptors is activity dependent. J Neurophysiol 100:3264-3274. doi: 10.1152/jn.90418.2008
41. Evans GJ, Cousin MA (2007) Activity-dependent control of slow synaptic vesicle endocytosis by cyclin-dependent kinase 5. J Neurosci 27:401-411. doi: 10.1523/JNEUROSCI.3809-06.2007