Leptin and ghrelin prevent hippocampal dysfunction induced by Aβ oligomers

Neuroscience

Volumn 241, Issue , 2013, Pages 41-51

  Martins, I ^a   Gomes, S ^a   Costa, R O ^b   Otvos, L ^d   Oliveira, C R ^b,c   Resende, R ^b   Pereira, C M F ^b,c  

^a UNIVERSITY OF COIMBRA   (Portugal)

^b UNIVERSITY OF COIMBRA   (Portugal)

^c UNIVERSITY OF COIMBRA   (Portugal)

^d Temple University   (United States)

Author keywords

Alzheimer's disease; Amyloid beta oligomers; Ghrelin; Hippocampus; Leptin

Indexed keywords

GHRELIN; GLYCOGEN SYNTHASE KINASE 3BETA; LEPTIN;

ALZHEIMER DISEASE; ANIMAL CELL; ARTICLE; BRAIN DYSFUNCTION; CELL SURVIVAL; CONTROLLED STUDY; DRUG MECHANISM; EMBRYO; ENZYME ACTIVATION; HIPPOCAMPUS; IN VITRO STUDY; MEMBRANE DEPOLARIZATION; MITOCHONDRIAL MEMBRANE POTENTIAL; NERVE CELL CULTURE; NERVE CELL NECROSIS; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; RAT;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; BLOTTING, WESTERN; CELL SURVIVAL; CELLS, CULTURED; GHRELIN; HIPPOCAMPUS; LEPTIN; NEURONS; PEPTIDE FRAGMENTS; PROTEIN MULTIMERIZATION; RATS; RATS, WISTAR;

EID: 84876430099     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2013.02.062     Document Type: Article

References (54)

1. Andrews Z.B., Liu Z.W., Walllingford N., Erion D.M., Borok E., Friedman J.M., Tschöp M.H., Shanabrough M., Cline G., Shulman G.I., Coppola A., Gao X.B., Horvath T.L., Diano S. UCP2 mediates ghrelin's action on NPY/AgRP neurons by lowering free radicals. Nature 2008, 454:846-851.
2. Baldanzi G., Filigheddu N., Cutrupi S., Catapano F., Bonissoni S., Fubini A., Malan D., Baj G., Granata R., Broglio F., Papotti M., Surico N., Bussolino F., Isgaard J., Deghenghi R., Sinigaglia F., Prat M., Muccioli G., Ghigo E., Graziani A. Ghrelin and des-acyl ghrelin inhibit cell death in cardiomyocytes and endothelial cells through ERK1/2 and PI 3-kinase/AKT. J Cell Biol 2002, 159:1029-1037.
3. Chen Y., Cao C.P., Li C.R., Wang W., Zhang D., Han L.L., Zhang X.Q., Kim A., Kim S., Liu G.L. Ghrelin modulates insulin sensitivity and tau phosphorylation in high glucose-induced hippocampal neurons. Biol Pharm Bull 2010, 33:1165-1169.
4. Chung H., Kim E., Lee D.H., Seo S., Ju S., Lee D., Kim H., Park S. Ghrelin inhibits apoptosis in hypothalamic neuronal cells during oxygen-glucose deprivation. Endocrinology 2007, 148:148-159.
5. Chung H., Seo S., Moon M., Park S. Sphatidylinositol-3-kinase/Akt/glycogen synthase kinase-3 beta and ERK1/2 pathways mediate protective effects of acylated and unacylated ghrelin against oxygen-glucose deprivation-induced apoptosis in primary rat cortical neuronal cells. J Endocrinol 2008, 198:511-521.
6. Chung H., Chung H.Y., Bae C.W., Kim C.J., Park S. Ghrelin suppresses tunicamycin- or thapsigargin-triggered endoplasmic reticulum stress-mediated apoptosis in primary cultured rat cortical neuronal cells. Endocr J 2011, 58:409-420.
7. Costa R.O., Lacor P.N., Ferreira I.L., Resende R., Auberson Y.P., Klein W.L., Oliveira C.R., Rego A.C., Pereira C.M. Endoplasmic reticulum stress occurs downstream of GluN2B subunit of N-methyl-d-aspartate receptor in mature hippocampal cultures treated with amyloid-β oligomers. Aging Cell 2012, 11:823-833.
8. Diano S., Farr S.A., Benoit S.C., Ewan C.M., da Silva I., Horvath B., Gaskin S.F., Nonaka N., Jaeger L.B., Banks W.A., Morley J.E., Pinto S., Sherwin R.S., Xu L., Yamada K.A., Sleeman M.W., Tschop M.H., Horvath T.L. Ghrelin controls hippocampal spine synapse density and memory performance. Nat Neurosci 2006, 9:381-388.
9. Dietrich M.O., Horvath T.L. Feeding signals and brain circuitry. Eur J Neurosci 2009, 30:1688-1696.
10. Doherty G.H., Beccano-Kelly D., Yan S.D., Gunn-Moore F.J., Harvey J. Leptin prevents hippocampal synaptic disruption and neuronal cell death induced by amyloid β. Neurobiol Aging 2013, 34:226-237.
11. Ferreira I.L., Bajouco L.M., Mota S.I., Auberson Y.P., Oliveira C.R., Rego A.C. Amyloid beta peptide 1-42 disturbs intracellular calcium homeostasis through activation of GluN2B-containing N-methyl-d-aspartate receptors in cortical cultures. Cell Calcium 2012, 51:95-106.
12. Ferreiro E., Baldeiras I., Ferreira I.L., Costa R.O., Rego A.C., Pereira C.F., Oliveira C.R. Mitochondrial- and endoplasmic reticulum-associated oxidative stress in Alzheimer's disease: from pathogenesis to biomarkers. Int J Cell Biol 2012, 2012:735206.
13. Ferrini F., Salio C., Lossi L., Merighi A. Ghrelin in central neurons. Curr Neuropharmacol 2009, 7:37-49.
14. Fewlass D.C., Noboa K., Pi-Sunyer F.X., Jonhston J.M., Yan S.D., Tezapsidis N. Obesity-related leptin regulates Alzheimerǐs Aβ. FASEB J 2004, 18:1870-1878.
15. Gahete M.D., Rubio A., Córdoba-Chacón J., Gracia-Navarro F., Kineman R.D., Avila J., Luque R.M., Castaño J.P. Expression of the ghrelin and neurotensin systems is altered in the temporal lobe of Alzheimer's disease patients. J Alzheimers Dis 2010, 22:819-828.
16. Garza J.C., Guo M., Zhang W., Lu X.Y. Leptin increases adult hippocampal neurogenesis in vivo and in vitro. J Biol Chem 2008, 283:18238-18247.
17. Greco S.J., Sarkar S., Johnston J.M., Zhu X., Su B., Smith M.A., Tezapsidis N. Leptin reduces Alzheimer's disease-related tau phosphorylation in neuronal cells. Biochem Biophys Res Commun 2008, 376:536-541.
18. Greco S.J., Sarkar S., Casadesus G., Zhu X., Smith M.A., Ashford J.W., Johnston J.M., Tezapsidis N. Leptin inhibits glycogen synthase kinase-3beta to prevent tau phosphorylation in neuronal cells. Neurosci Lett 2009, 455:191-194.
19. Greco S.J., Sarkar S., Johnston J.M., Tezapsidis N. Leptin reduces Alzheimerǐs disease-related tau phosphorylation and amyloid through AMPK in neuronal cells. Biochem Biophys Res Commun 2009, 380:98-104.
20. Greco S.J., Bryan K.J., Sarkar S., Zhu X., Smith M.A., Ashford J.W., Johnston J.M., Tezapsidis N., Casadesus G. Leptin reduces pathology and improves memory in a transgenic mouse model of Alzheimer's disease. J Alzheimers Dis 2010, 19:1155-1167.
21. Guo Z., Jiang H., Xu X., Duan W., Mattson M.P. Leptin-mediated cell survival signaling in hippocampal neurons mediated by JAK STAT3 and mitochondrial stabilization. J Biol Chem 2008, 283:1754-1763.
22. Hardy J., Selkoe D.J. The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 2002, 297:353-356.
23. Harvey J. Leptin: the missing link in Alzheimer disease?. Clin Chem 2010, 56:696-697.
24. Ho P.W., Liu H., Ho J.W., Zhang W., Chu A.C., Kwok K.H., Ge X., Chan K., Ramdsen D.B., Ho S. Mitochondrial uncoupling protein-2 (UCP2) mediates leptin protection against MPP+ toxicity in neuronal cells. Neurotox Res 2010, 17:332-343.
25. Isidori A.M., Strollo F., More M., Caprio M., Aversa A., Moretti C., Frajese G., Riondino G., Fabbri A. Leptin and aging: correlation with endocrine changes in male and female healhty adult populations of different body weights. J Clin Endocrinol Metab 2000, 85:1954-1962.
26. Kim M.S., Yoon C.Y., Jang P.G., Park Y.J., Shin C.S., Park H.S., Ryu J.W., Pak Y.K., Park J.Y., Lee K.U., Kim S.Y., Lee H.K., Kim Y.B., Park K.S. The mitogenic and antiapoptotic actions of ghrelin in 3T3-L1 adipocytes. Mol Endocrinol 2004, 18:2291-2301.
27. Kojima M., Kangawa K. Drug insight: the functions of ghrelin and its potential as a multitherapeutic hormone. Nat Clin Pract Endocrinol Metab 2006, 2:80-88.
28. Lee J., Lim E., Kim Y., Li E., Park S. Ghrelin attenuates kainic acid-induced neuronal cell death in the mouse hippocampus. J Endocrinol 2010, 205:263-270.
29. Lieb W., Beiser A.S., Vasan R.S., Tan Z.S., Au R., Harris T.B., Roubenoff R., Auerbach S., DeCarli C., Wolf P.A., Seshadri S. Association of plasma leptin levels with incident Alzheimer disease and MRI measures of brain aging. JAMA 2009, 302:2565-2572.
30. Lim E., Lee S., Li E., Kim Y., Park S. Ghrelin protects spinal cord motoneurons against chronic glutamate-induced excitotoxicity via ERK1/2 and phosphatidylinositol-3-kinase/Akt/glycogen synthase kinase-3β pathways. Exp Neurol 2011, 230:114-122.
31. Liu Y., Chen L., Xu X., Vicaut E., Sercombe R. Both ischemic preconditioning and ghrelin administration protect hippocampus from ischemia/reperfusion and upregulate uncoupling protein-2. BMC Physiol 2009, 22:17.
32. Marwarha G., Dasari B., Prabhakara J.P., Schommer J., Ghribi O. β-Amyloid regulates leptin expression and tau phosphorylation through the mTORC1 signaling pathway. J Neurochem 2010, 115:373-384.
33. McNay E.C. Insulin and ghrelin: peripheral hormones modulating memory and hippocampal function. Curr Opin Pharmacol 2007, 7:628-632.
34. Minciu Macrea M., Misra H., Zagrean L. The neuroprotective effect of intranasally applied leptin against hypoxic neuronal injury. Med Hypotheses 2010, 74:1036-1037.
35. Minokoshi Y., Kim Y.B., Peroni O.D., Fryer L.G., Müller C., Carling D., Kahn B.B. Leptin stimulates fatty-acid oxidation by activating AMP-activated protein kinase. Nature 2002, 415:339-343.
36. Moon M., Kim S., Hwang L., Park S. Ghrelin regulates hippocampal neurogenesis in adult mice. Endocr J 2009, 56:525-531.
37. Moon M., Choi J.G., Nam D.W., Hong H.S., Choi Y.J., Oh M.S., Mook-Jung I. Ghrelin ameliorates cognitive dysfunction and neurodegeneration in intrahippocampal amyloid-β1-42 oligomer-injected mice. J Alzheimers Dis 2011, 23:147-159.
38. Moran T.H., Gao S. Looking for food in all the right places?. Cell Metab. 2006, 3:233-234.
39. Mosmann T. Rapid colorimetric assay for cellular growth and survival. J Immunol Methods 1983, 65:55-63.
40. Oomura Y., Hori N., Shiraishi T., Fukunaga K., Takeda H., Tsuji M., Matsumiya T., Ishibashi M., Aou S., Li X.L., Kohno D., Uramura K., Sougawa H., Yada T., Wayner M.J., Sasaki K. Leptin facilitates learning and memory performance and enhances hippocampal CA1 long-term potentiation and CaMK II phosphorylation in rats. Peptides 2006, 27:2738-2749.
41. Pérez-González R., Antequera D., Vargas T., Spuch C., Bolós M., Carro E. Leptin induces proliferation of neuronal progenitors and neuroprotection in a mouse model of Alzheimer's disease. J Alzheimers Dis 2011, 24:17-25.
42. 2+ homeostasis. Brain Res 2007, 1143:11-21.
43. Resende R., Ferreiro E., Pereira C., Resende de Oliveira C. Neurotoxic effect of oligomeric and fibrillar species of amyloid-beta peptide 1-42: involvement of endoplasmic reticulum calcium release in oligomer-induced cell death. Neuroscience 2008, 155:725-737.
44. Resende R., Ferreiro E., Pereira C., Resende de Oliveira C. ER stress in Aβ-induced GSK-3β activation and tau phosphorylation. J Neurosci Res 2008, 86:2091-2099.
45. Resende R., Oliveira C.R., Pereira C.M.F. Role of glycogen synthase kinase-3β on tau phosphorylation in Alzheimer's disease. Advances in medicine and biology 2010, 197-210. Nova Science Publishers, New York, USA, Chapter 7. L.V. Berhardt (Ed.).
46. Rigamonti A.E., Pincelli A.I., Corra B., Viarengo R., Bonomo S.M., Galimberti D., Scacchi M., Scarpini E., Cavagnini F., Muller E.E. Plasma ghrelin concentration in elderly subjects: comparison with anorexic and obese patients. J Endocrinol 2002, 175:R1-R5.
47. Sakono M., Zako T. Amyloid oligomers: formation and toxicity of Abeta oligomers. FEBS J 2010, 277:1348-1358.
48. Scarpace P.J., Matheny M., Tumer N. Hypothalamic leptin resistance is associated with impaired leptin signal transduction in aged obese rats. Neuroscience 2001, 104:1111-1117.
49. Signore A.P., Zhang F., Weng Z., Gao Y., Chen J. Leptin neuroprotection in the CNS: mechanisms and therapeutic potentials. J Neurochem 2008, 106:1977-1990.
50. Tang B.L. Leptin as a neuroprotective agent. Biochem Biophys Res Commun 2008, 368:181-185.
51. Tezapsidis N., Johnston J.M., Smith M.A., Ashford J.W., Casadesus G., Robakis N.K., Wolozin B., Perry G., Zhu X., Greco S.J., Sarkar S. Leptin: a novel therapeutic strategy for Alzheimer's disease. J Alzheimers Dis 2009, 16:731-740.
52. Valerio A., Ghisi V., Dossena M., Tonello C., Giordano A., Frontini A., Ferrario M., Pizzi M., Spano P., Carruba M.O., Nisoli E. Leptin increases axonal growth cone size in developing mouse cortical neurons by convergent signals inactivating glycogen synthase kinase-3beta. J Biol Chem 2006, 281:12950-12958.
53. Xu Y.P., Zhu J.J., Cheng F., Jiang K.W., Gu W.Z., Shen Z., Wu Y.D., Liang L., Du L.Z. Ghrelin ameliorates hypoxia-induced pulmonary hypertension via phospho-GSK3 β/β-catenin signaling in neonatal rats. J Mol Endocrinol 2011, 47:33-43.
54. Yildiz B.O., Suchard M.A., Wong M.L., McCann S.M., Licinio J. Alteration in the dynamics of circulating ghrelin, adiponectin and leptin in human obesity. Proc Natl Acad Sci U S A 2004, 101:10434-10439.