Harpagoside ameliorates the amyloid-β-induced cognitive impairment in rats via up-regulating BDNF expression and MAPK/PI3K pathways

Neuroscience

Volumn 303, Issue , 2015, Pages 103-114

  Li, J ^a   Ding, X ^b   Zhang, R ^a   Jiang, W ^a   Sun, X ^a   Xia, Z ^a   Wang, X ^b   Wu, E ^b   Zhang, Y ^a   Hu, Y ^a  

^a SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b NORTH DAKOTA STATE UNIVERSITY   (United States)

Author keywords

Alzheimer's disease; A ; Brain derived neurotrophic factor (BDNF); Learning and memory deficits; P AKT; P ERK1 2

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID BETA PROTEIN[1-40]; AMYLOID BETA PROTEIN[1-42]; BRAIN DERIVED NEUROTROPHIC FACTOR; CATALPOL; CHOLINE ACETYLTRANSFERASE; HARPAGOSIDE; K 252A; MITOGEN ACTIVATED PROTEIN KINASE; NEUTRALIZING ANTIBODY; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN TYROSINE KINASE INHIBITOR; AMYLOID BETA-PROTEIN (1-41); GLYCOSIDE; NEUROPROTECTIVE AGENT; PEPTIDE FRAGMENT; PYRAN DERIVATIVE;

ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR DISORDER; BRAIN CELL CULTURE; BRAIN CORTEX; CELL VIABILITY; COGNITIVE DEFECT; CONTROLLED STUDY; CULTURE MEDIUM; DRUG STRUCTURE; HIPPOCAMPUS; LEARNING DISORDER; MALE; MEMORY DISORDER; NERVE DEGENERATION; NERVE FIBER GROWTH; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; NOVEL OBJECT RECOGNITION TEST; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RAT MODEL; SIGNAL TRANSDUCTION; SPATIAL LEARNING; SPATIAL MEMORY; UPREGULATION; Y-MAZE TEST; ANIMAL; CHEMICALLY INDUCED; CHOLINERGIC NERVE CELL; COGNITION; DRUG EFFECTS; METABOLISM; NERVE CELL; RECOGNITION; SPRAGUE DAWLEY RAT;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; CEREBRAL CORTEX; CHOLINERGIC NEURONS; COGNITION; GLYCOSIDES; HIPPOCAMPUS; MALE; MAP KINASE SIGNALING SYSTEM; NEURONS; NEUROPROTECTIVE AGENTS; PEPTIDE FRAGMENTS; PYRANS; RATS; RATS, SPRAGUE-DAWLEY; RECOGNITION (PSYCHOLOGY); SPATIAL LEARNING; UP-REGULATION;

EID: 84936882505     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2015.06.042     Document Type: Article

References (52)

1. Abbott J.J., Howlett D.R., Francis P.T., Williams R.J. Abeta(1-42) modulation of Akt phosphorylation via alpha7 nAChR and NMDA receptors. Neurobiol Aging 2008, 29:992-1001.
2. Albert M.S., DeKosky S.T., Dickson D., Dubois B., Feldman H.H., Fox N.C., Gamst A., Holtzman D.M., Jagust W.J., Petersen R.C., Snyder P.J., Carrillo M.C., Thies B., Phelps C.H. The diagnosis of mild cognitive impairment due to Alzheimer's disease: recommendations from the National Institute on Aging-Alzheimer's Association workgroups on diagnostic guidelines for Alzheimer's disease. Alzheimers Dement 2011, 7:270-279.
3. Almeida R.D., Manadas B.J., Melo C.V., Gomes J.R., Mendes C.S., Graos M.M., Carvalho R.F., Carvalho A.P., Duarte C.B. Neuroprotection by BDNF against glutamate-induced apoptotic cell death is mediated by ERK and PI3-kinase pathways. Cell Death Differ 2005, 12:1329-1343.
4. Bekinschtein P., Cammarota M., Katche C., Slipczuk L., Rossato J.I., Goldin A., Izquierdo I., Medina J.H. BDNF is essential to promote persistence of long-term memory storage. Proc Natl Acad Sci U S A 2008, 105:2711-2716.
5. Bevins R.A., Besheer J. Object recognition in rats and mice: a one-trial non-matching-to-sample learning task to study 'recognition memory'. Nat Protoc 2006, 1:1306-1311.
6. Blurton-Jones M., Kitazawa M., Martinez-Coria H., Castello N.A., Muller F.J., Loring J.F., Yamasaki T.R., Poon W.W., Green K.N., LaFerla F.M. Neural stem cells improve cognition via BDNF in a transgenic model of Alzheimer disease. Proc Natl Acad Sci U S A 2009, 106:13594-13599.
7. Brewer G.J., Torricelli J.R., Evege E.K., Price P.J. Optimized survival of hippocampal neurons in B27-supplemented neurobasal, a new serum-free medium combination. J Neurosci Res 1993, 35:567-576.
8. Caccamo A., Maldonado M.A., Bokov A.F., Majumder S., Oddo S. CBP gene transfer increases BDNF levels and ameliorates learning and memory deficits in a mouse model of Alzheimer's disease. Proc Natl Acad Sci U S A 2010, 107:22687-22692.
9. Chacon M.A., Barria M.I., Soto C., Inestrosa N.C. Beta-sheet breaker peptide prevents Abeta-induced spatial memory impairments with partial reduction of amyloid deposits. Mol Psychiatry 2004, 9:953-961.
10. Cheng Y.F., Wang C., Lin H.B., Li Y.F., Huang Y., Xu J.P., Zhang H.T. Inhibition of phosphodiesterase-4 reverses memory deficits produced by Abeta25-35 or Abeta1-40 peptide in rats. Psychopharmacology 2010, 212:181-191.
11. Chiang H.C., Wang L., Xie Z., Yau A., Zhong Y. PI3Kinase signaling is involved in Abeta-induced memory loss in Drosophila. Proc Natl Acad Sci U S A 2010, 107:7060-7065.
12. Christensen R., Marcussen A.B., Wortwein G., Knudsen G.M., Aznar S. Abeta(1-42) injection causes memory impairment, lowered cortical and serum BDNF levels, and decreased hippocampal 5-HT(2A) levels. Exp Neurol 2008, 210:164-171.
13. Connor B., Young D., Yan Q., Faull R.L., Synek B., Dragunow M. Brain-derived neurotrophic factor is reduced in Alzheimer's disease. Brain Res Mol Brain Res 1997, 49:71-81.
14. Dijkhuizen P.A., Ghosh A. BDNF regulates primary dendrite formation in cortical neurons via the PI3-kinase and MAP kinase signaling pathways. J Neurobiol 2005, 62:278-288.
15. Giacobini E., Becker R.E. One hundred years after the discovery of Alzheimer's disease. A turning point for therapy?. J Alzheimers Dis 2007, 12:37-52.
16. Griffin R.J., Moloney A., Kelliher M., Johnston J.A., Ravid R., Dockery P., O'Connor R., O'Neill C. Activation of Akt/PKB, increased phosphorylation of Akt substrates and loss and altered distribution of Akt and PTEN are features of Alzheimer's disease pathology. J Neurochem 2005, 93:105-117.
17. Herrmann N., Chau S.A., Kircanski I., Lanctot K.L. Current and emerging drug treatment options for Alzheimer's disease: a systematic review. Drugs 2011, 71:2031-2065.
18. Hock C., Heese K., Hulette C., Rosenberg C., Otten U. Region-specific neurotrophin imbalances in Alzheimer disease: decreased levels of brain-derived neurotrophic factor and increased levels of nerve growth factor in hippocampus and cortical areas. Arch Neurol 2000, 57:846-851.
19. Hoppe J.B., Coradini K., Frozza R.L., Oliveira C.M., Meneghetti A.B., Bernardi A., Pires E.S., Beck R.C., Salbego C.G. Free and nanoencapsulated curcumin suppress beta-amyloid-induced cognitive impairments in rats: involvement of BDNF and Akt/GSK-3beta signaling pathway. Neurobiol Learn Mem 2013, 106:134-144.
20. Hu Y., Wang Z., Zhang R., Wu P., Xia Z., Orsi A., Rees D. Regulation of M1-receptor mRNA stability by smilagenin and its significance in improving memory of aged rats. Neurobiol Aging 2010, 31:1010-1019.
21. Hu Y., Xia Z., Sun Q., Orsi A., Rees D. A new approach to the pharmacological regulation of memory: Sarsasapogenin improves memory by elevating the low muscarinic acetylcholine receptor density in brains of memory-deficit rat models. Brain Res 2005, 1060:26-39.
22. Iwasaki Y., Negishi T., Inoue M., Tashiro T., Tabira T., Kimura N. Sendai virus vector-mediated brain-derived neurotrophic factor expression ameliorates memory deficits and synaptic degeneration in a transgenic mouse model of Alzheimer's disease. J Neurosci Res 2012, 90:981-989.
23. Jeong E.J., Lee K.Y., Kim S.H., Sung S.H., Kim Y.C. Cognitive-enhancing and antioxidant activities of iridoid glycosides from Scrophularia buergeriana in scopolamine-treated mice. Eur J Pharmacol 2008, 588:78-84.
24. Kim S.R., Koo K.A., Sung S.H., Ma C.J., Yoon J.S., Kim Y.C. Iridoids from Scrophularia buergeriana attenuate glutamate-induced neurotoxicity in rat cortical cultures. J Neurosci Res 2003, 74:948-955.
25. Li J., Wang G., Liu J., Zhou L., Dong M., Wang R., Li X., Lin C., Niu Y. Puerarin attenuates amyloid-beta-induced cognitive impairment through suppression of apoptosis in rat hippocampus in vivo. Eur J Pharmacol 2010, 649:195-201.
26. Li Q., Zhao H.F., Zhang Z.F., Liu Z.G., Pei X.R., Wang J.B., Cai M.Y., Li Y. Long-term administration of green tea catechins prevents age-related spatial learning and memory decline in C57BL/6 J mice by regulating hippocampal cyclic amp-response element binding protein signaling cascade. Neuroscience 2009, 159:1208-1215.
27. Meng C., He Z., Xing D. Low-level laser therapy rescues dendrite atrophy via upregulating BDNF expression: implications for Alzheimer's disease. J Neurosci 2013, 33:13505-13517.
28. Michalski B., Fahnestock M. Pro-brain-derived neurotrophic factor is decreased in parietal cortex in Alzheimer's disease. Brain Res Mol Brain Res 2003, 111:148-154.
29. 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.
30. 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.
31. Paxinos G., Watson C. The rat brain in stereotaxic coordinates 1986, Academic Press, Sydney.
32. Peng S., Garzon D.J., Marchese M., Klein W., Ginsberg S.D., Francis B.M., Mount H.T., Mufson E.J., Salehi A., Fahnestock M. Decreased brain-derived neurotrophic factor depends on amyloid aggregation state in transgenic mouse models of Alzheimer's disease. J Neurosci 2009, 29:9321-9329.
33. Peng S., Wuu J., Mufson E.J., Fahnestock M. Precursor form of brain-derived neurotrophic factor and mature brain-derived neurotrophic factor are decreased in the pre-clinical stages of Alzheimer's disease. J Neurochem 2005, 93:1412-1421.
34. Peng S., Zhang Y., Zhang J., Wang H., Ren B. ERK in learning and memory: a review of recent research. Int J Mol Sci 2010, 11:222-232.
35. Shin M.K., Kim H.G., Baek S.H., Jung W.R., Park D.I., Park J.S., Jo D.G., Kim K.L. Neuropep-1 ameliorates learning and memory deficits in an Alzheimer's disease mouse model, increases brain-derived neurotrophic factor expression in the brain, and causes reduction of amyloid beta plaques. Neurobiol Aging 2014, 35:990-1001.
36. Shin R.W., Ogino K., Kondo A., Saido T.C., Trojanowski J.Q., Kitamoto T., Tateishi J. Amyloid beta-protein (Abeta) 1-40 but not Abeta1-42 contributes to the experimental formation of Alzheimer disease amyloid fibrils in rat brain. J Neurosci 1997, 17:8187-8193.
37. Sipos E., Kurunczi A., Kasza A., Horvath J., Felszeghy K., Laroche S., Toldi J., Parducz A., Penke B., Penke Z. Beta-amyloid pathology in the entorhinal cortex of rats induces memory deficits: implications for Alzheimer's disease. Neuroscience 2007, 147:28-36.
38. Song Y., Cui T., Xie N., Zhang X., Qian Z., Liu J. Protocatechuic acid improves cognitive deficits and attenuates amyloid deposits, inflammatory response in aged AbetaPP/PS1 double transgenic mice. Int Immunopharmacol 2014, 20:276-281.
39. Souza L.C., Filho C.B., Goes A.T., Fabbro L.D., de Gomes M.G., Savegnago L., Oliveira M.S., Jesse C.R. Neuroprotective effect of physical exercise in a mouse model of Alzheimer's disease induced by beta-amyloid(1)(-)(4)(0) peptide. Neurotox Res 2013, 24:148-163.
40. Sultana R., Ravagna A., Mohmmad-Abdul H., Calabrese V., Butterfield D.A. Ferulic acid ethyl ester protects neurons against amyloid beta- peptide(1-42)-induced oxidative stress and neurotoxicity: relationship to antioxidant activity. J Neurochem 2005, 92:749-758.
41. Sun X., Xiong Z., Zhang Y., Meng Y., Xu G., Xia Z., Li J., Zhang R., Ke Z., Hu Y. Harpagoside attenuates MPTP/MPP(+) induced dopaminergic neurodegeneration and movement disorder via elevating glial cell line-derived neurotrophic factor. J Neurochem 2012, 120:1072-1083.
42. Sweatt J.D. Mitogen-activated protein kinases in synaptic plasticity and memory. Curr Opin Neurobiol 2004, 14:311-317.
43. Tang J., Xu H., Fan X., Li D., Rancourt D., Zhou G., Li Z., Yang L. Embryonic stem cell-derived neural precursor cells improve memory dysfunction in Abeta(1-40) injured rats. Neurosci Res 2008, 62:86-96.
44. Tang S.S., Hong H., Chen L., Mei Z.L., Ji M.J., Xiang G.Q., Li N., Ji H. Involvement of cysteinyl leukotriene receptor 1 in Abeta1-42-induced neurotoxicity in vitro and in vivo. Neurobiol Aging 2014, 35:590-599.
45. Tang S.S., Ji M.J., Chen L., Hu M., Long Y., Li Y.Q., Miao M.X., Li J.C., Li N., Ji H., Chen X.J., Hong H. Protective effect of pranlukast on Abeta(1)(-)(4)(2)-induced cognitive deficits associated with downregulation of cysteinyl leukotriene receptor 1. Int J Neuropsychopharmacol 2014, 17:581-592.
46. Wang D., Noda Y., Zhou Y., Mouri A., Mizoguchi H., Nitta A., Chen W., Nabeshima T. 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 2007, 32:1261-1271.
47. Wang Z., Liu Q., Zhang R., Liu S., Xia Z., Hu Y. Catalpol ameliorates beta amyloid-induced degeneration of cholinergic neurons by elevating brain-derived neurotrophic factors. Neuroscience 2009, 163:1363-1372.
48. Wu J., Bie B., Yang H., Xu J.J., Brown D.L., Naguib M. Activation of the CB2 receptor system reverses amyloid-induced memory deficiency. Neurobiol Aging 2013, 34:791-804.
49. Xiang J., Pan J., Chen F., Zheng L., Chen Y., Zhang S., Feng W. L-3-n-butylphthalide improves cognitive impairment of APP/PS1 mice by BDNF/TrkB/PI3K/AKT pathway. Int J Clin Exp Med 2014, 7:1706-1713.
50. Yamada K., Mizuno M., Nabeshima T. Role for brain-derived neurotrophic factor in learning and memory. Life Sci 2002, 70:735-744.
51. Yiannopoulou K.G., Papageorgiou S.G. Current and future treatments for Alzheimer's disease. Ther Adv Neurol Disord 2013, 6:19-33.
52. Zuccato C., Cattaneo E. Brain-derived neurotrophic factor in neurodegenerative diseases. Nat Rev Neurol 2009, 5:311-322.