Lixisenatide rescues spatial memory and synaptic plasticity from amyloid β protein-induced impairments in rats

Neuroscience

Volumn 277, Issue , 2014, Pages 6-13

  Cai, H Y ^a   Holscher C ^b   Yue, X H ^a   Zhang, S X ^a   Wang, X H ^a   Qiao, F ^a   Yang, W ^a   Qi, J S ^a  

^a SHANXI MEDICAL UNIVERSITY   (China)

^b LANCASTER UNIVERSITY   (United Kingdom)

Author keywords

Alzheimer's disease; Amyloid protein; Glycogen synthase kinase 3 ; Lixisenatide; Long term potentiation; Morris water maze

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID BETA-PROTEIN (25-35); GLUCAGON RECEPTOR; GLUCAGON-LIKE PEPTIDE-1 RECEPTOR; GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3 BETA; NEUROPROTECTIVE AGENT; PEPTIDE; PEPTIDE FRAGMENT; ZP10A PEPTIDE; AMYLOID BETA PROTEIN[25-35]; GLYCOGEN SYNTHASE KINASE 3BETA; LIXISENATIDE; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE 3 KINASE; PROTEIN KINASE B; SERINE;

AGONISTS; ALZHEIMER DISEASE; ANIMAL; DISEASE MODEL; DRUG EFFECTS; EXCITATORY POSTSYNAPTIC POTENTIAL; GENETICS; HIPPOCAMPUS; LONG TERM POTENTIATION; MALE; MAZE TEST; MEMORY DISORDERS; METABOLISM; PATHOPHYSIOLOGY; PHOSPHORYLATION; PHYSIOLOGY; RANDOMIZATION; SPATIAL MEMORY; SPRAGUE DAWLEY RAT; ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN ELECTROPHYSIOLOGY; CONTROLLED STUDY; DRUG EFFECT; DRUG MECHANISM; ENZYME ACTIVATION; IN VIVO STUDY; NERVE CELL PLASTICITY; NEUROPROTECTION; NONHUMAN; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; SPATIAL LEARNING;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; DISEASE MODELS, ANIMAL; EXCITATORY POSTSYNAPTIC POTENTIALS; GLYCOGEN SYNTHASE KINASE 3; HIPPOCAMPUS; LONG-TERM POTENTIATION; MALE; MAZE LEARNING; MEMORY DISORDERS; NEUROPROTECTIVE AGENTS; PEPTIDE FRAGMENTS; PEPTIDES; PHOSPHORYLATION; RANDOM ALLOCATION; RATS, SPRAGUE-DAWLEY; RECEPTORS, GLUCAGON; SPATIAL MEMORY;

EID: 84904134776     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2014.02.022     Document Type: Article

References (67)

1. Abbas T., Faivre E., Holscher C. Impairment of synaptic plasticity and memory formation in GLP-1 receptor KO mice: interaction between type 2 diabetes and Alzheimer's disease. Behav Brain Res 2009, 205:265-271.
2. Alvarez G., Munoz-Montano J.R., Satrustegui J., Avila J., Bogonez E., Diaz-Nido J. Regulation of tau phosphorylation and protection against beta-amyloid-induced neurodegeneration by lithium. Possible implications for Alzheimer's disease. Bipolar Disord 2002, 4:153-165.
3. Anderton B.H. Alzheimer's disease: clues from flies and worms. Curr Biol 1999, 9:R106-109.
4. Arnold S.E., Hyman B.T., Flory J., Damasio A.R., Van Hoesen G.W. The topographical and neuroanatomical distribution of neurofibrillary tangles and neuritic plaques in the cerebral cortex of patients with Alzheimer's disease. Cereb Cortex 1991, 1:103-116.
5. Bhat R.V., Budd Haeberlein S.L., Avila J. Glycogen synthase kinase 3: a drug target for CNS therapies. J Neurochem 2004, 89:1313-1317.
6. Bliss T.V., Collingridge G.L. A synaptic model of memory: long-term potentiation in the hippocampus. Nature 1993, 361:31-39.
7. Chang G., Zhang D., Yu H., Zhang P., Wang Y., Zheng A., Qin S. Cardioprotective effects of exenatide against oxidative stress-induced injury. Int J Mol Med 2013, 32:1011-1020.
8. Chen Q.S., Kagan B.L., Hirakura Y., Xie C.W. Impairment of hippocampal long-term potentiation by Alzheimer amyloid beta-peptides. J Neurosci Res 2000, 60:65-72.
9. Craft S. Insulin resistance and Alzheimer's disease pathogenesis: potential mechanisms and implications for treatment. Curr Alzheimer Res 2007, 4:147-152.
10. Deacon C.F., Johnsen A.H., Holst J.J. Degradation of glucagon-like peptide-1 by human plasma in vitro yields an N-terminally truncated peptide that is a major endogenous metabolite in vivo. J Clin Endocrinol Metabol 1995, 80:952-957.
11. Deshpande A., Mina E., Glabe C., Busciglio J. Different conformations of amyloid beta induce neurotoxicity by distinct mechanisms in human cortical neurons. J Neurosci Off J Soc Neurosci 2006, 26:6011-6018.
12. During M.J., Cao L., Zuzga D.S., Francis J.S., Fitzsimons H.L., Jiao X., Bland R.J., Klugmann M., Banks W.A., Drucker D.J., Haile C.N. Glucagon-like peptide-1 receptor is involved in learning and neuroprotection. Nat Med 2003, 9:1173-1179.
13. Eldar-Finkelman H. Glycogen synthase kinase 3: an emerging therapeutic target. Trends Mol Med 2002, 8:126-132.
14. Embi N., Rylatt D.B., Cohen P. Glycogen synthase kinase-3 from rabbit skeletal muscle. Separation from cyclic-AMP-dependent protein kinase and phosphorylase kinase. Eur J Biochem/FEBS 1980, 107:519-527.
15. Gallwitz B. Therapies for the treatment of type 2 diabetes mellitus based on incretin action. Minerva Endocrinol 2006, 31:133-147.
16. Gao C., Holscher C., Liu Y., Li L. GSK3: a key target for the development of novel treatments for type 2 diabetes mellitus and Alzheimer disease. Rev Neurosci 2012, 23:1-11.
17. Gengler S., McClean P.L., McCurtin R., Gault V.A., Holscher C. Val(8)GLP-1 rescues synaptic plasticity and reduces dense core plaques in APP/PS1 mice. Neurobiol Aging 2012, 33:265-276.
18. Hamilton A., Holscher C. Receptors for the incretin glucagon-like peptide-1 are expressed on neurons in the central nervous system. NeuroReport 2009, 20:1161-1166.
19. Hamilton A., Patterson S., Porter D., Gault V.A., Holscher C. Novel GLP-1 mimetics developed to treat type 2 diabetes promote progenitor cell proliferation in the brain. J Neurosci Res 2011, 89:481-489.
20. Hernandez F., Borrell J., Guaza C., Avila J., Lucas J.J. Spatial learning deficit in transgenic mice that conditionally over-express GSK-3beta in the brain but do not form tau filaments. J Neurochem 2002, 83:1529-1533.
21. Holscher C. Development of beta-amyloid-induced neurodegeneration in Alzheimer's disease and novel neuroprotective strategies. Rev Neurosci 2005, 16:181-212.
22. Holscher C., Gengler S., Gault V.A., Harriott P., Mallot H.A. Soluble beta-amyloid[25-35] reversibly impairs hippocampal synaptic plasticity and spatial learning. Eur J Pharmacol 2007, 561:85-90.
23. Horowitz M., Rayner C.K., Jones K.L. Mechanisms and clinical efficacy of lixisenatide for the management of type 2 diabetes. Adv Ther 2013, 30:81-101.
24. Hoyer S. Glucose metabolism and insulin receptor signal transduction in Alzheimer disease. Eur J Pharmacol 2004, 490:115-125.
25. Hunter K., Hölscher C. Drugs developed to treat diabetes, liraglutide and lixisenatide, cross the blood brain barrier and enhance neurogenesis. BMC Neurosci 2012, 13:33.
26. Impey S., Mark M., Villacres E.C., Poser S., Chavkin C., Storm D.R. Induction of CRE-mediated gene expression by stimuli that generate long-lasting LTP in area CA1 of the hippocampus. Neuron 1996, 16:973-982.
27. Kastin A.J., Akerstrom V., Pan W. Interactions of glucagon-like peptide-1 (GLP-1) with the blood-brain barrier. J Mol Neurosci 2002, 18:7-14.
28. Li L., Holscher C. Common pathological processes in Alzheimer disease and type 2 diabetes: a review. Brain Res Rev 2007, 56:384-402.
29. Li S., Hong S., Shepardson N.E., Walsh D.M., Shankar G.M., Selkoe D. Soluble oligomers of amyloid Beta protein facilitate hippocampal long-term depression by disrupting neuronal glutamate uptake. Neuron 2009, 62:788-801.
30. Li S.F., Wu M.N., Wang X.H., Yuan L., Yang D., Qi J.S. Requirement of alpha7 nicotinic acetylcholine receptors for amyloid beta protein-induced depression of hippocampal long-term potentiation in CA1 region of rats in vivo. Synapse 2011, 65:1136-1143.
31. Li Y., Duffy K.B., Ottinger M.A., Ray B., Bailey J.A., Holloway H.W., Tweedie D., Perry T., Mattson M.P., Kapogiannis D., Sambamurti K., Lahiri D.K., Greig N.H. GLP-1 receptor stimulation reduces amyloid-beta peptide accumulation and cytotoxicity in cellular and animal models of Alzheimer's disease. J Alzheimer Dis 2010, 19:1205-1219.
32. Lovshin J.A., Drucker D.J. Incretin-based therapies for type 2 diabetes mellitus. Nat Rev Endocrinol 2009, 5:262-269.
33. Luchsinger J.A., Tang M.X., Shea S., Mayeux R. Hyperinsulinemia and risk of Alzheimer disease. Neurology 2004, 63:1187-1192.
34. Ly P.T., Wu Y., Zou H., Wang R., Zhou W., Kinoshita A., Zhang M., Yang Y., Cai F., Woodgett J., Song W. Inhibition of GSK3beta-mediated BACE1 expression reduces Alzheimer-associated phenotypes. J Clin Investig 2013, 123:224-235.
35. McClean P.L., Parthsarathy V., Faivre E., Hölscher C. The diabetes drug liraglutide prevents degenerative processes in a mouse model of Alzheimer's disease. J Neurosci 2011, 31:6587-6594.
36. Morris R. Developments of a water-maze procedure for studying spatial learning in the rat. J Neurosci Methods 1984, 11:47-60.
37. Nitta A., Fukuta T., Hasegawa T., Nabeshima T. Continuous infusion of beta-amyloid protein into the rat cerebral ventricle induces learning impairment and neuronal and morphological degeneration. Jpn J Pharmacol 1997, 73:51-57.
38. Palop J.J., Mucke L. Amyloid-beta-induced neuronal dysfunction in Alzheimer's disease: from synapses toward neural networks. Nat Neurosci 2010, 13:812-818.
39. Pan Y.F., Chen X.R., Wu M.N., Ma C.G., Qi J.S. Arginine vasopressin prevents against Abeta(25-35)-induced impairment of spatial learning and memory in rats. Horm Behav 2010, 57:448-454.
40. Peineau S., Taghibiglou C., Bradley C., Wong T.P., Liu L., Lu J., Lo E., Wu D., Saule E., Bouschet T., Matthews P., Isaac J.T., Bortolotto Z.A., Wang Y.T., Collingridge G.L. LTP inhibits LTD in the hippocampus via regulation of GSK3beta. Neuron 2007, 53:703-717.
41. Perry T., Holloway H.W., Weerasuriya A., Mouton P.R., Duffy K., Mattison J.A., Greig N.H. Evidence of GLP-1-mediated neuroprotection in an animal model of pyridoxine-induced peripheral sensory neuropathy. Exp Neurol 2007, 203:293-301.
42. Perry T., Lahiri D.K., Chen D., Zhou J., Shaw K.T., Egan J.M., Greig N.H. A novel neurotrophic property of glucagon-like peptide 1: a promoter of nerve growth factor-mediated differentiation in PC12 cells. J Pharmacol Exp Therapeut 2002, 300:958-966.
43. Perry T., Lahiri D.K., Sambamurti K., Chen D., Mattson M.P., Egan J.M., Greig N.H. Glucagon-like peptide-1 decreases endogenous amyloid-beta peptide (Abeta) levels and protects hippocampal neurons from death induced by Abeta and iron. J Neurosci Res 2003, 72:603-612.
44. Prediger R.D., Franco J.L., Pandolfo P., Medeiros R., Duarte F.S., Di Giunta G., Figueiredo C.P., Farina M., Calixto J.B., Takahashi R.N., Dafre A.L. Differential susceptibility following beta-amyloid peptide-(1-40) administration in C57BL/6 and Swiss albino mice: Evidence for a dissociation between cognitive deficits and the glutathione system response. Behav Brain Res 2007, 177:205-213.
45. Qi J.S., Qiao J.T. Amyloid beta-protein fragment 31-35 forms ion channels in membrane patches excised from rat hippocampal neurons. Neuroscience 2001, 105:845-852.
46. + channels by amyloid beta-protein fragment 31-35 in membrane patches excised from hippocampal neurons. Sheng li xue bao: [Acta Physiol Sin] 2001, 53:198-204.
47. Qi J.S., Ye L., Qiao J.T. Amyloid beta-protein fragment 31-35 suppresses delayed rectifying potassium channels in membrane patches excised from hippocampal neurons in rats. Synapse 2004, 51:165-172.
48. Ryu J.K., McLarnon J.G. Minocycline or iNOS inhibition block 3-nitrotyrosine increases and blood-brain barrier leakiness in amyloid beta-peptide-injected rat hippocampus. Exp Neurol 2006, 198:552-557.
49. Ryu J.K., McLarnon J.G. Thalidomide inhibition of perturbed vasculature and glial-derived tumor necrosis factor-alpha in an animal model of inflamed Alzheimer's disease brain. Neurobiol Dis 2008, 29:254-266.
50. Selkoe D.J. Alzheimer's disease: genes, proteins, and therapy. Physiol Rev 2001, 81:741-766.
51. Shankar G.M., Bloodgood B.L., Townsend M., Walsh D.M., Selkoe D.J., Sabatini B.L. Natural oligomers of the Alzheimer amyloid-beta protein induce reversible synapse loss by modulating an NMDA-type glutamate receptor-dependent signaling pathway. J Neurosci Off J Soc Neurosci 2007, 27:2866-2875.
52. Sharma M.K., Jalewa J., Hölscher C. Neuroprotective and anti-apoptotic effects of liraglutide on SH-SY5Y cells exposed to methylglyoxal stress. J Neurochem 2013.
53. Stewart R., Liolitsa D. Type 2 diabetes mellitus, cognitive impairment and dementia. Diabet Med J Brit Diabet Assoc 1999, 16:93-112.
54. Talbot K., Wang H.-Y., Kazi H., Han L.-Y., Bakshi K.P., Stucky A., Fuino R.L., Kawaguchi K.R., Samoyedny A.J., Wilson R.S. Demonstrated brain insulin resistance in Alzheimer's disease patients is associated with IGF-1 resistance, IRS-1 dysregulation, and cognitive decline. J Clin Investig 2012, 122:1316.
55. Terry AV, Jr. (2009) Spatial navigation (water maze) tasks. In: Methods of behavior analysis in neuroscience (Buccafusco JJ, ed). Boca Raton (FL).
56. Thal D.R., Rub U., Orantes M., Braak H. Phases of A beta-deposition in the human brain and its relevance for the development of AD. Neurology 2002, 58:1791-1800.
57. Timmers L., Henriques J.P., de Kleijn D.P., Devries J.H., Kemperman H., Steendijk P., Verlaan C.W., Kerver M., Piek J.J., Doevendans P.A., Pasterkamp G., Hoefer I.E. Exenatide reduces infarct size and improves cardiac function in a porcine model of ischemia and reperfusion injury. J Am Coll Cardiol 2009, 53:501-510.
58. Vella A., Shah P., Reed A.S., Adkins A.S., Basu R., Rizza R.A. Lack of effect of exendin-4 and glucagon-like peptide-1-(7,36)-amide on insulin action in non-diabetic humans. Diabetologia 2002, 45:1410-1415.
59. Wang X.H., Li L., Holscher C., Pan Y.F., Chen X.R., Qi J.S. Val8-glucagon-like peptide-1 protects against Abeta1-40-induced impairment of hippocampal late-phase long-term potentiation and spatial learning in rats. Neuroscience 2010, 170:1239-1248.
60. Werner U., Haschke G., Herling A.W., Kramer W. Pharmacological profile of lixisenatide: a new GLP-1 receptor agonist for the treatment of type 2 diabetes. Regul Pept 2010, 164:58-64.
61. Woodgett J.R. Molecular cloning and expression of glycogen synthase kinase-3/factor A. EMBO J 1990, 9:2431-2438.
62. Yan X.Z., Qiao J.T., Dou Y., Qiao Z.D. Beta-amyloid peptide fragment 31-35 induces apoptosis in cultured cortical neurons. Neuroscience 1999, 92:177-184.
63. Ye C., Walsh D.M., Selkoe D.J., Hartley D.M. Amyloid betaprotein induced electrophysiological changes are dependent on aggregation state: N-methyl-D-aspartate (NMDA) versus non-NMDA receptor/channel activation. Neurosci Lett 2004, 366:320-325.
64. Zetterberg H., Blennow K., Hanse E. Amyloid beta and APP as biomarkers for Alzheimer's disease. Exp Gerontol 2010, 45:23-29.
65. Zhang J.F., Qi J.S., Qiao J.T. Protein kinase C mediates amyloid beta-protein fragment 31-35-induced suppression of hippocampal late-phase long-term potentiation in vivo. Neurobiol Learn Mem 2009, 91:226-234.
66. Zhang J.M., Wu M.N., Qi J.S., Qiao J.T. Amyloid beta-protein fragment 31-35 suppresses long-term potentiation in hippocampal CA1 region of rats in vivo. Synapse 2006, 60:307-313.
67. Zhou X.W., Winblad B., Guan Z., Pei J.J. Interactions between glycogen synthase kinase 3beta, protein kinase B, and protein phosphatase 2A in tau phosphorylation in mouse N2a neuroblastoma cells. J Alzheimer Dis 2009, 17:929-937.