Lamotrigine attenuates deficits in synaptic plasticity and accumulation of amyloid plaques in APP/PS1 transgenic mice

Neurobiology of Aging

Volumn 35, Issue 12, 2014, Pages 2713-2725

  Zhang, Mao Ying ^a   Zheng, Chuan Yi ^a   Zou, Ming Ming ^a   Zhu, Jian Wei ^a   Zhang, Yan ^a   Wang, Jing ^a   Liu, Chun Feng ^b   Li, Qi Fa ^c   Xiao, Zhi Cheng ^d   Li, Shao ^c   Ma, Quan Hong ^b   Xu, Ru Xiang ^a  

^a SOUTHERN MEDICAL UNIVERSITY   (China)

^b SOOCHOW UNIVERSITY   (China)

^c DALIAN MEDICAL UNIVERSITY   (China)

^d MONASH UNIVERSITY   (Australia)

Author keywords

Alzheimer's disease; Antiepileptic drug; Hyperexcitability; Lamotrigine; Synaptic plasticity

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; BETA SECRETASE; BRAIN DERIVED NEUROTROPHIC FACTOR; ETIRACETAM; LAMOTRIGINE; NERVE GROWTH FACTOR; PRESENILIN 1; SYNAPTOPHYSIN; ANTICONVULSIVE AGENT; TRIAZINE DERIVATIVE;

AMYLOID PLAQUE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DRUG EFFECT; ELECTROENCEPHALOGRAPHY; HIPPOCAMPUS; IMAGE ANALYSIS; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; LEARNING DISORDER; MEMORY DISORDER; MORRIS WATER MAZE TEST; MOUSE; MUTANT; NERVE CELL; NERVE CELL PLASTICITY; NONHUMAN; NOVEL OBJECT RECOGNITION TEST; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; SPIKE; TRANSGENIC MOUSE; UPREGULATION; ALZHEIMER DISEASE; ANIMAL; BRAIN; C57BL MOUSE; DISEASE MODEL; DOWN REGULATION; DRUG EFFECTS; HUMAN; LEARNING; MEMORY; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; ANTICONVULSANTS; BRAIN; BRAIN-DERIVED NEUROTROPHIC FACTOR; DISEASE MODELS, ANIMAL; DOWN-REGULATION; HUMANS; LEARNING; MEMORY; MICE, INBRED C57BL; MICE, TRANSGENIC; NERVE GROWTH FACTOR; NEURONAL PLASTICITY; PLAQUE, AMYLOID; TRIAZINES; UP-REGULATION;

EID: 84911390394     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2014.06.009     Document Type: Article

References (65)

1. Akiyama H., Barger S., Barnum S., Bradt B., Bauer J., Cole G.M., Cooper N.R., Eikelenboom P., Emmerling M., Fiebich B.L., Finch C.E., Frautschy S., Griffin W.S., Hampel H., Hull M., Landreth G., Lue L., Mrak R., Mackenzie I.R., McGeer P.L., O'Banion M.K., Pachter J., Pasinetti G., Plata-Salaman C., Rogers J., Rydel R., Shen Y., Streit W., Strohmeyer R., Tooyoma I., Van Muiswinkel F.L., Veerhuis R., Walker D., Webster S., Wegrzyniak B., Wenk G., Wyss-Coray T. Inflammation and Alzheimer's disease. Neurobiol. Aging 2000, 21:383-421.
2. Amatniek J.C., Hauser W.A., DelCastillo-Castaneda C., Jacobs D.M., Marder K., Bell K., Albert M., Brandt J., Stern Y. Incidence and predictors of seizures in patients with Alzheimer's disease. Epilepsia 2006, 47:867-872.
3. Arenas E., Persson H. Neurotrophin-3 prevents the death of adult central noradrenergic neurons invivo. Nature 1994, 367:368-371.
4. Arif H., Svoronos A., Resor S.R., Buchsbaum R., Hirsch L.J. The effect of age and comedication on lamotrigine clearance, tolerability, and efficacy. Epilepsia 2011, 52:1905-1913.
5. Bakker A., Krauss G.L., Albert M.S., Speck C.L., Jones L.R., Stark C.E., Yassa M.A., Bassett S.S., Shelton A.L., Gallagher M. Reduction of hippocampal hyperactivity improves cognition in amnestic mild cognitive impairment. Neuron 2012, 74:467-474.
6. Belrose J.C., Masoudi R., Michalski B., Fahnestock M. Increased pro-nerve growth factor and decreased brain-derived neurotrophic factor in non-AD tauopathies. Neurobiol. Aging 2014, 35:926-933.
7. Berardi N., Braschi C., Capsoni S., Cattaneo A., Maffei L. Environmental enrichment delays the onset of memory deficits and reduces neuropathological hallmarks in a mouse model of Alzheimer-like neurodegeneration. J.Alzheimers Dis. 2007, 11:359-370.
8. Blochl A., Thoenen H. Localization of cellular storage compartments and sitesof constitutive and activity-dependent release of nerve growth factor (NGF) in primary cultures of hippocampal neurons. Mol. Cell. Neurosci. 1996, 7:173-190.
9. Brodie M.J., Overstall P.W., Giorgi L. Multicentre, double-blind, randomised comparison between lamotrigine and carbamazepine in elderly patients with newly diagnosed epilepsy. The UK Lamotrigine Elderly Study Group. Epilepsy Res. 1999, 37:81-87.
10. Cabrejo L., Guyant-Marechal L., Laquerriere A., Vercelletto M., De la Fourniere F., Thomas-Anterion C., Verny C., Letournel F., Pasquier F., Vital A., Checler F., Frebourg T., Campion D., Hannequin D. Phenotype associated with APP duplication in five families. Brain 2006, 129:2966-2976.
11. Calhoun M.E., Wiederhold K.H., Abramowski D., Phinney A.L., Probst A., Sturchler-Pierrat C., Staufenbiel M., Sommer B., Jucker M. Neuron loss in APP transgenic mice. Nature 1998, 395:755-756.
12. Capsoni S., Ugolini G., Comparini A., Ruberti F., Berardi N., Cattaneo A. Alzheimer-like neurodegeneration in aged antinerve growth factor transgenic mice. Proc. Natl. Acad. Sci. U.S.A 2000, 97:6826-6831.
13. Capsoni S., Giannotta S., Cattaneo A. Beta-amyloid plaques in a model for sporadic Alzheimer's disease based on transgenic anti-nerve growth factor antibodies. Mol. Cell. Neurosci. 2002, 21:15-28.
14. Capsoni S., Giannotta S., Cattaneo A. Nerve growth factor and galantamine ameliorate early signs of neurodegeneration in anti-nerve growth factor mice. Proc. Natl. Acad. Sci. U.S.A 2002, 99:12432-12437.
15. De Rosa R., Garcia A.A., Braschi C., Capsoni S., Maffei L., Berardi N., Cattaneo A. Intranasal administration of nerve growth factor (NGF) rescues recognition memory deficits in AD11 anti-NGF transgenic mice. Proc. Natl. Acad. Sci. U.S.A 2005, 102:3811-3816.
16. Ding Y., Qiao A., Wang Z., Goodwin J.S., Lee E.S., Block M.L., Allsbrook M., McDonald M.P., Fan G.H. Retinoic acid attenuates beta-amyloid deposition and rescues memory deficits in an Alzheimer's disease transgenic mouse model. J.Neurosci. 2008, 28:11622-11634.
17. D'Souza U.M., Powell-Smith G., Haddley K., Powell T.R., Bubb V.J., Price T., McGuffin P., Quinn J.P., Farmer A.E. Allele-specific expression of the serotonin transporter and its transcription factors following lamotrigine treatment invitro. Am. J. Med. Genet. B Neuropsychiatr. Genet. 2013, 162B:474-483.
18. Figurov A., Pozzo-Miller L.D., Olafsson P., Wang T., Lu B. Regulation of synaptic responses to high-frequency stimulation and LTP by neurotrophins in the hippocampus. Nature 1996, 381:706-709.
19. Garcia-Alloza M., Robbins E.M., Zhang-Nunes S.X., Purcell S.M., Betensky R.A., Raju S., Prada C., Greenberg S.M., Bacskai B.J., Frosch M.P. Characterization of amyloid deposition in the APPswe/PS1dE9 mouse model of Alzheimer disease. Neurobiol. Dis. 2006, 24:516-524.
20. Harris J.A., Devidze N., Verret L., Ho K., Halabisky B., Thwin M.T., Kim D., Hamto P., Lo I., Yu G.Q., Palop J.J., Masliah E., Mucke L. Transsynaptic progression of amyloid-beta-induced neuronal dysfunction within the entorhinal-hippocampal network. Neuron 2010, 68:428-441.
21. Horch H.W., Katz L.C. BDNF release from single cells elicits local dendritic growth in nearby neurons. Nat. Neurosci. 2002, 5:1177-1184.
22. Jardanhazi-Kurutz D., Kummer M.P., Terwel D., Vogel K., Dyrks T., Thiele A., Heneka M.T. Induced LC degeneration in APP/PS1 transgenic mice accelerates early cerebral amyloidosis and cognitive deficits. Neurochem. Int. 2010, 57:375-382.
23. Kamenetz F., Tomita T., Hsieh H., Seabrook G., Borchelt D., Iwatsubo T., Sisodia S., Malinow R. APP processing and synaptic function. Neuron 2003, 37:925-937.
24. Kang H., Schuman E.M. Long-lasting neurotrophin-induced enhancement of synaptic transmission in the adult hippocampus. Science 1995, 267:1658-1662.
25. Leach M.J., Marden C.M., Miller A.A. Pharmacological studies on lamotrigine, a novel potential antiepileptic drug: II. Neurochemical studies on the mechanism of action. Epilepsia 1986, 27:490-497.
26. Lesne S., Gabriel C., Nelson D.A., White E., Mackenzie E.T., Vivien D., Buisson A. Akt-dependent expression of NAIP-1 protects neurons against amyloid-{beta} toxicity. J.Biol. Chem. 2005, 280:24941-24947.
27. Li N., He X., Qi X., Zhang Y., He S. The mood stabilizer lamotrigine produces antidepressant behavioral effects in rats: role of brain-derived neurotrophic factor. J.Psychopharmacol. 2010, 24:1772-1778.
28. Ma Q.H., Futagawa T., Yang W.L., Jiang X.D., Zeng L., Takeda Y., Xu R.X., Bagnard D., Schachner M., Furley A.J., Karagogeos D., Watanabe K., Dawe G.S., Xiao Z.C. ATAG1-APP signalling pathway through Fe65 negatively modulates neurogenesis. Nat. Cell Biol. 2008, 10:283-294.
29. Malik S., Arif H., Hirsch L.J. Lamotrigine and its applications in the treatment of epilepsy and other neurological and psychiatric disorders. Expert Rev. Neurother. 2006, 6:1609-1627.
30. Martin R., Kuzniecky R., Ho S., Hetherington H., Pan J., Sinclair K., Gilliam F., Faught E. Cognitive effects of topiramate, gabapentin, and lamotrigine in healthy young adults. Neurology 1999, 52:321-327.
31. Matrone C., Ciotti M.T., Mercanti D., Marolda R., Calissano P. NGF and BDNF signaling control amyloidogenic route and Abeta production in hippocampal neurons. Proc. Natl. Acad. Sci. U.S.A 2008, 105:13139-13144.
32. Meehan A.L., Yang X., McAdams B.D., Yuan L., Rothman S.M. Anew mechanism for antiepileptic drug action: vesicular entry may mediate the effects of levetiracetam. J.Neurophysiol. 2011, 106:1227-1239.
33. Messenheimer J., Mullens E.L., Giorgi L., Young F. Safety review of adult clinical trial experience with lamotrigine. Drug Saf. 1998, 18:281-296.
34. Minkeviciene R., Rheims S., Dobszay M.B., Zilberter M., Hartikainen J., Fulop L., Penke B., Zilberter Y., Harkany T., Pitkanen A., Tanila H. Amyloid beta-induced neuronal hyperexcitability triggers progressive epilepsy. J.Neurosci. 2009, 29:3453-3462.
35. Morris R. Developments of a water-maze procedure for studying spatial learning in the rat. J.Neurosci. Methods 1984, 11:47-60.
36. Mrak R.E., Griffin W.S. Glia and their cytokines in progression of neurodegeneration. Neurobiol. Aging 2005, 26:349-354.
37. Nagahara A.H., Merrill D.A., Coppola G., Tsukada S., Schroeder B.E., Shaked G.M., Wang L., Blesch A., Kim A., Conner J.M., Rockenstein E., Chao M.V., Koo E.H., Geschwind D., Masliah E., Chiba A.A., Tuszynski M.H. Neuroprotective effects of brain-derived neurotrophic factor in rodent and primate models of Alzheimer's disease. Nat. Med. 2009, 15:331-337.
38. Nagahara A.H., Mateling M., Kovacs I., Wang L., Eggert S., Rockenstein E., Koo E.H., Masliah E., Tuszynski M.H. Early BDNF treatment ameliorates cell loss in the entorhinal cortex of APP transgenic mice. J.Neurosci. 2013, 33:15596-15602.
39. Nitsch R.M., Farber S.A., Growdon J.H., Wurtman R.J. Release of amyloid beta-protein precursor derivatives by electrical depolarization of rat hippocampal slices. Proc. Natl. Acad. Sci. U.S.A 1993, 90:5191-5193.
40. Nunes A.F., Amaral J.D., Lo A.C., Fonseca M.B., Viana R.J., Callaerts-Vegh Z., D'Hooge R., Rodrigues C.M. TUDCA, a bile acid, attenuates amyloid precursor protein processing and amyloid-beta deposition in APP/PS1 mice. Mol. Neurobiol. 2012, 45:440-454.
41. Palop J.J., Mucke L. Epilepsy and cognitive impairments in Alzheimer disease. Arch. Neurol. 2009, 66:435-440.
42. Palop J.J., Chin J., Roberson E.D., Wang J., Thwin M.T., Bien-Ly N., Yoo J., Ho K.O., Yu G.Q., Kreitzer A., Finkbeiner S., Noebels J.L., Mucke L. Aberrant excitatory neuronal activity and compensatory remodeling of inhibitory hippocampal circuits in mouse models of Alzheimer's disease. Neuron 2007, 55:697-711.
43. Rowan A.J., Ramsay R.E., Collins J.F., Pryor F., Boardman K.D., Uthman B.M., Spitz M., Frederick T., Towne A., Carter G.S., Marks W., Felicetta J., Tomyanovich M.L. New onset geriatric epilepsy: a randomized study of gabapentin, lamotrigine, and carbamazepine. Neurology 2005, 64:1868-1873.
44. Ruberti F., Capsoni S., Comparini A., Di Daniel E., Franzot J., Gonfloni S., Rossi G., Berardi N., Cattaneo A. Phenotypic knockout of nerve growth factor in adult transgenic mice reveals severe deficits in basal forebrain cholinergic neurons, cell death in the spleen, and skeletal muscle dystrophy. J.Neurosci. 2000, 20:2589-2601.
45. Rutten B.P., Van der Kolk N.M., Schafer S., van Zandvoort M.A., Bayer T.A., Steinbusch H.W., Schmitz C. Age-related loss of synaptophysin immunoreactive presynaptic boutons within the hippocampus of APP751SL, PS1M146L, and APP751SL/PS1M146L transgenic mice. Am. J. Pathol. 2005, 167:161-173.
46. Sanchez P.E., Zhu L., Verret L., Vossel K.A., Orr A.G., Cirrito J.R., Devidze N., Ho K., Yu G.Q., Palop J.J., Mucke L. Levetiracetam suppresses neuronal network dysfunction and reverses synaptic and cognitive deficits in an Alzheimer's disease model. Proc. Natl. Acad. Sci. U.S.A 2012, 109:E2895-E2903.
47. Schindowski K., Belarbi K., Buee L. Neurotrophic factors in Alzheimer's disease: role of axonal transport. Genes Brain Behav. 2008, 7(Suppl 1):43-56.
48. Schmitz C., Rutten B.P., Pielen A., Schafer S., Wirths O., Tremp G., Czech C., Blanchard V., Multhaup G., Rezaie P., Korr H., Steinbusch H.W., Pradier L., Bayer T.A. Hippocampal neuron loss exceeds amyloid plaque load inatransgenic mouse model of Alzheimer's disease. Am. J. Pathol. 2004, 164:1495-1502.
49. Seo J.G., Lee D.I., Hwang Y.H., Lee H.W., Jung D.K., Suh C.K., Kwon S.H., Park S.P. Comparison of cognitive effects of lamotrigine and oxcarbazepine in epilepsy patients. J.Clin. Neurol. 2007, 3:31-37.
50. Smith D.L., Pozueta J., Gong B., Arancio O., Shelanski M. Reversal of long-term dendritic spine alterations in Alzheimer disease models. Proc. Natl. Acad. Sci. U.S.A 2009, 106:16877-16882.
51. Tanaka J., Horiike Y., Matsuzaki M., Miyazaki T., Ellis-Davies G.C., Kasai H. Protein synthesis and neurotrophin-dependent structural plasticity of single dendritic spines. Science 2008, 319:1683-1687.
52. Tekin S., Aykut-Bingol C., Tanridag T., Aktan S. Antiglutamatergic therapy in Alzheimer's disease-effects of lamotrigine. Short communication. J.Neural Transm. 1998, 105:295-303.
53. Terry R.D., Masliah E., Salmon D.P., Butters N., DeTeresa R., Hill R., Hansen L.A., Katzman R. Physical basis of cognitive alterations in Alzheimer's disease: synapse loss is the major correlate of cognitive impairment. Ann. Neurol. 1991, 30:572-580.
54. Verret L., Mann E.O., Hang G.B., Barth A.M., Cobos I., Ho K., Devidze N., Masliah E., Kreitzer A.C., Mody I., Mucke L., Palop J.J. Inhibitory interneuron deficit links altered network activity and cognitive dysfunction in Alzheimer model. Cell 2012, 149:708-721.
55. Vezzani A., Sperk G., Colmers W.F. Neuropeptide Y: emerging evidence for a functional role in seizure modulation. Trends Neurosci. 1999, 22:25-30.
56. Vogt D.L., Thomas D., Galvan V., Bredesen D.E., Lamb B.T., Pimplikar S.W. Abnormal neuronal networks and seizure susceptibility in mice overexpressing the APP intracellular domain. Neurobiol. Aging 2011, 32:1725-1729.
57. Vossel K.A., Beagle A.J., Rabinovici G.D., Shu H., Lee S.E., Naasan G., Hegde M., Cornes S.B., Henry M.L., Nelson A.B., Seeley W.W., Geschwind M.D., Gorno-Tempini M.L., Shih T., Kirsch H.E., Garcia P.A., Miller B.L., Mucke L. Seizures and epileptiform activity in the early stages of Alzheimer disease. JAMA Neurol. 2013, 70:1158-1166.
58. Wang J.F., Sun X., Chen B., Young L.T. Lamotrigine increases gene expression of GABA-A receptor beta3 subunit in primary cultured rat hippocampus cells. Neuropsychopharmacology 2002, 26:415-421.
59. West M.J., Coleman P.D., Flood D.G., Troncoso J.C. Differences in the pattern of hippocampal neuronal loss in normal ageing and Alzheimer's disease. Lancet 1994, 344:769-772.
60. Williams B., Nelson M., Granholm A.C., Coultrap S., Browning M., Curtis M. Altered NGF response but not release in the aged septo-hippocampal cholinergic system. Exp. Neurol. 2005, 196:30-40.
61. Wyss-Coray T., Mucke L. Inflammation in neurodegenerative disease-a double-edged sword. Neuron 2002, 35:419-432.
62. Xiong Z.G., Chu X.P., MacDonald J.F. Effect of lamotrigine on the Ca(2+)-sensing cation current in cultured hippocampal neurons. J.Neurophysiol. 2001, 86:2520-2526.
63. Zhang R., Xue G., Wang S., Zhang L., Shi C., Xie X. Novel object recognition as a facile behavior test for evaluating drug effects in AbetaPP/PS1 Alzheimer's disease mouse model. J.Alzheimers Dis. 2012, 31:801-812.
64. Zhang R., Miller R.G., Madison C., Jin X., Honrada R., Harris W., Katz J., Forshew D.A., McGrath M.S. Systemic immune system alterations in early stages of Alzheimer's disease. J.Neuroimmunol. 2013, 256:38-42.
65. Ziyatdinova S., Gurevicius K., Kutchiashvili N., Bolkvadze T., Nissinen J., Tanila H., Pitkanen A. Spontaneous epileptiform discharges in a mouse model of Alzheimer's disease are suppressed by antiepileptic drugs that block sodium channels. Epilepsy Res. 2011, 94:75-85.