Differential effects of palmitoylethanolamide against amyloid-β induced toxicity in cortical neuronal and astrocytic primary cultures from wild-type and 3xTg-AD mice

Journal of Alzheimer's Disease

Volumn 46, Issue 2, 2015, Pages 407-421

  Tomasini, Maria Cristina ^a,b   Borelli, Andrea Celeste ^a   Beggiato, Sarah ^a,b   Ferraro, Luca ^a,b   Cassano, Tommaso ^c   Tanganelli, Sergio ^a,b   Antonelli, Tiziana ^a,b  

^a UNIVERSITY OF FERRARA   (Italy)

^b IRET Foundation   (Italy)

^c UNIVERSITY OF FOGGIA   (Italy)

Author keywords

Alzheimer's disease; cell viability; GFAP immunoreactivity; glutamate; MAP2 immunoreactivity

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID BETA PROTEIN[1-42]; GLUTAMIC ACID; MICROTUBULE ASSOCIATED PROTEIN 2; PALMIDROL; ETHANOLAMINE DERIVATIVE; NONSTEROID ANTIINFLAMMATORY AGENT; PALMITIC ACID DERIVATIVE; TAU PROTEIN;

3XTG MOUSE; ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTROCYTE; BRAIN CELL; BRAIN CELL CULTURE; BRAIN CORTEX; CELL VIABILITY; CONTROLLED STUDY; IMMUNOREACTIVITY; MOUSE; NERVE CELL NETWORK; NEUROPROTECTION; NEUROTOXICITY; NEUROTRANSMISSION; NONHUMAN; PRIMARY CULTURE; PRIORITY JOURNAL; PROTEIN EXPRESSION; ANIMAL; BLOOD; CELL CULTURE; CYTOLOGY; DISEASE MODEL; DRUG EFFECTS; METABOLISM; NERVE CELL; TRANSGENIC MOUSE;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; ASTROCYTES; CELLS, CULTURED; CEREBRAL CORTEX; DISEASE MODELS, ANIMAL; ETHANOLAMINES; GLUTAMIC ACID; MICE; MICE, TRANSGENIC; NEURONS; PALMITIC ACIDS; TAU PROTEINS;

EID: 84930422754     PISSN: 13872877     EISSN: 18758908     Source Type: Journal    
DOI: 10.3233/JAD-143039     Document Type: Article

References (83)

1. Fuller S, Steele M, MünchG(2010) Activated astroglia during chronic inflammation in Alzheimer's disease-do they neglect their neurosupportive roles?. Mutat Res 690, 40-49
2. Sun X, Jin L, Ling P (2012) Review of drugs for Alzheimer's disease. Drug Discov Ther 6, 285-290
3. Rubio-Perez JM, Morillas-Ruiz JM (2012) A review. Inflammatory process in Alzheimer's disease, role of cytokines. ScientificWorldJournal 2012, 756357
4. Jung ES, An K, Hong HS, Kim JH, Mook-Jung I (2012) Astrocyte-originated ATP protects A-1-42-induced impairment of synaptic plasticity. J Neurosci 32, 3081-3087
5. Ballard C, Gauthier S, Corbett A, Brayne C, Aarsland D, Jones E (2011) Alzheimer's disease. Lancet 377, 1019-1031
6. Gustaw-Rothenberg K, Lerner A, Bonda DJ, Lee HG, Zhu X, Perry G, Smith MA (2010) Biomarkers in Alzheimer's disease: Past, present and future. Biomark Med 4, 15-26
7. Muirhead KE, Borger E, Aitken L, Conway SJ, Gunn-Moore FJ (2010) The consequences of mitochondrial amyloid betapeptide in Alzheimer's disease. Biochem J 426, 255-270
8. Kofalvi A, Vizi ES, Ledent C, Sperlagh B (2003) Cannabinoids inhibits the release of [3H] glutamate from rodent hippocampal synaptosomes via a novel CB1 receptorindependent action. Eur J Neurosci 18, 1973-1978
9. Rivest S (2006) Cannabinoids in microglia: A new trick for immune surveillance and neuroprotection. Neuron 49, 4-8
10. Li C, Zhao R, Gao K, Wei Z, YinMY, Lau LT, Chui D, Hoi Yu AC (2011) Astrocytes: Implications for neuroinflammatory pathogenesis of Alzheimer's disease. Curr Alzheimer Res 8, 67-80
11. Perry VH, Nicoll JA, Holmes C (2010) Microglia in neurodegenerative disease. Nat Rev Neurol 6, 193-201
12. Sastre M, Walter J, Gentleman SM (2008) Interactions between APP secretases and inflammatory mediators. J Neuroinflammation 5, 25
13. Fernández-Ruiz J, García C, Sagredo O, Gómez-Ruiz M, de Lago E (2010) The endocannabinoid system as a target for the treatment of neuronal damage. Expert Opin Ther Targets 14, 387-340
14. Allaman I, Gavillet M, Bélanger M, Laroche T, Viertl D, Lashuel HA, Magistretti PJ (2010) Amyloid-beta aggregates cause alterations of astrocytic metabolic phenotype: Impact on neuronal viability. J Neurosci 30, 3326-3338
15. Vesce S, Rossi D, Brambilla L, Volterra A (2007) Glutamate release from astrocytes in physiological conditions and in neurodegenerative disorders characterized by neuroinflammation. Int Rev Neurobiol 82, 57-71
16. Bisogno T, Di Marzo V (2008) The role of the endocannabinoid system in Alzheimer's disease: Facts and hypotheses. Curr Pharm Des 14, 2299-3305
17. Pazos MR, Núñez E, Benito C, Tolón RM, Romero J (2004) Role of the endocannabinoid system in Alzheimer's disease: New perspectives. Life Sci 75, 1907-1915
18. Bedse G, Romano A, Lavecchia AM, Cassano T, Gaetani S (2014) The role of endocannabinoid signaling in the molecular mechanisms of neurodegeneration in Alzheimer's disease. J Alzheimers Dis 43, 1115-1136
19. Campillo NE, Páez JA (2009) Cannabinoid system in neurodegeneration: New perspectives in Alzheimer's disease. Mini Rev Med Chem 9, 539-559
20. Ramírez BG, Blázquez C, Gómez del Pulgar T, Guzmán M, de Ceballos ML (2005) Prevention of Alzheimer's disease pathology by cannabinoids: Neuroprotection mediated by blockade of microglial activation. J Neurosci 25, 1904-1913
21. Costa B, Conti S, Giagnoni G, Colleoni M (2002) Therapeutic effect of the endogenous fatty acid amide, palmitoylethanolamide, in rat acute inflammation: Inhibition of nitric oxide and cyclo-oxygenase systems. Br J Pharmacol 137, 413-420
22. Esposito S, Cuzzocrea S (2013) Palmitoylethanolamide in homeostatic and traumatic central nervous system injuries. CNS Neurol Disord Drug Targets 12, 55-61
23. Esposito S, Cuzzocrea S (2013) Palmitoylethanolamide is a new possible pharmacological treatment for the inflammation associated with trauma. Mini Rev Med Chem 13, 237-255
24. Skaper SD, Facci L (2012) Mast cell-glia axis in neuroinflammation and therapeutic potential of the anandamide congener palmitoylethanolamide. Philos Trans R Soc Lond B Biol Sci 367, 3312-3325
25. Moriconi A, Cerbara I, Maccarrone M, Topai A (2010) GPR55: Current knowledge and future perspectives of a purported "Type-3" cannabinoid receptor. Curr Med Chem 17, 1411-1429
26. Lo Verme J, Fu J, Astarita G, La Rana G, Russo R, Calignano A, Piomelli D (2005) The nuclear receptor peroxisome proliferator-Activated receptor-Alpha mediates the anti-inflammatory actions of palmitoylethanolamide. Mol Pharmacol 67, 15-19
27. O'sullivan SE, Kendall DA (2010) Cannabinoid activation of peroxisome proliferator-Activated receptors: Potential for modulation of inflammatory disease. Immunobiology 215, 611-616
28. Re G, Barbero R, Miolo A, Di Marzo V (2007) Palmitoylethanolamide, endocannabinoids and related cannabimimetic compounds in protection against tissue inflammation and pain: Potential use in companion animals. Vet J 173, 21-30
29. Scuderi C, Esposito G, Blasio A, Valenza M, Arietti P, Steardo L Jr, Carnuccio R, De Filippis D, Petrosino S, Iuvone T, Di Marzo V, Steardo L (2011) Palmitoylethanolamide counteracts reactive astrogliosis induced by -Amyloid peptide. J Cell Mol Med 15, 2664-2674
30. Scuderi C, Valenza M, Stecca C, Esposito G, Carratú MR, Steardo L (2012) Palmitoylethanolamide exerts neuroprotective effects in mixed neuroglial cultures and organotypic hippocampal slices via peroxisome proliferator-Activated receptor-. J Neuroinflammation 9, 49
31. Scuderi C, Steardo L (2013) Neuroglial roots of neurodegenerative diseases: Therapeutic potential of palmitoylethanolamide in models of Alzheimer's disease. CNS Neurol Disord Drug Targets 12, 62-69
32. D'Agostino G, Russo R, Avagliano C, Cristiano C, Meli R, Calignano A (2012) Palmitoylethanolamide protects against the amyloid-25-35-induced learning and memory impairment in mice, an experimental model of Alzheimer disease. Neuropsychopharmacology 37, 1784-1792
33. Oddo S, Caccamo A, Shepherd JD, Murphy MP, Golde TE, Kayed R, Metherate R, Mattson MP, Akbari Y, LaFerla FM (2003) Triple-transgenic model of Alzheimer's disease with plaques and tangles: Intracellular Abeta and synaptic dysfunction. Neuron 39, 409-421
34. Vale C, Alonso E, Rubiolo JA, Vieytes MR, LaFerla FM, Giménez-Llort L, BotanaLM(2010) Profile for amyloid-beta and tau expression in primary cortical cultures from 3xTg-AD mice. Cell Mol Neurobiol 30, 577-590
35. Billings LM, Oddo S, Green KN, McGaugh JL, LaFerla FM (2005) Intraneuronal Abeta causes the onset of early Alzheimer's disease-related cognitive deficits in transgenic mice. Neuron 45, 675-688
36. Cassano T, Serviddio G, Gaetani S, Romano A, Dipasquale P, Cianci S, Bellanti F, Laconca L, Romano AD, Padalino I, LaFerla FM, Nicoletti F, Cuomo V, Vendemiale G (2012) Glutamatergic alterations and mitochondrial impairment in a murine model of Alzheimer disease. Neurobiol Aging 33, 1121.e1-e12
37. Oddo S, Caccamo A, Kitazawa M, Tseng BP, LaFerla FM (2003) Amyloid deposition precedes tangle formation in a triple transgenic model of Alzheimer's disease. Neurobiol Aging 24, 1063-1070
38. Antonelli T, Tomasini MC, Fournier J, Mazza R, Tanganelli S, Pirondi S, Fuxe K, Ferraro L (2008) Neurotensin receptor involvement in the rise of extracellular glutamate levels and apoptotic nerve cell death in primary cortical cultures after oxygen and glucose deprivation. Cereb Cortex 18, 1748-1757
39. Repetto G, del Peso A, Zurita JL (2008) Neutral red uptake assay for the estimation of cell viability/cytotoxicity. Nat Protoc 3, 1125-1131
40. Ferraro L, Tomasini MC, Siniscalchi A, Fuxe K, Tanganelli S, Antonelli T (2000) Neurotensin increases endogenous glutamate release in rat cortical slices. Life Sci 66, 927-936
41. Takahashi RH, Capetillo-Zarate E, Lin MT, Milner TA, Gouras GK (2013) Accumulation of intraneuronal -Amyloid 42 peptides is associated with early changes in microtubuleassociated protein 2 in neurites and synapses. PLoS One 8, e51965
42. Alobuia WM, Xia W, Vohra BP (2013) Axon degeneration is key component of neuronal death in amyloid-toxicity. Neurochem Int 63, 782-789
43. Mota SI, Ferreira IL, Pereira C, Oliveira CR, Rego AC (2012) Amyloid-beta peptide 1-42 causes microtubule deregulation through N-methyl-D-Aspartate receptors in mature hippocampal cultures. Curr Alzheimer Res 9, 844-856
44. Zempel H, Thies E, Mandelkow E, Mandelkow EM (2010) Abeta oligomers cause localized Ca(2+) elevation, missorting of endogenous tau into dendrites, tau phosphorylation, and destruction of microtubules and spines. J Neurosci 30, 11938-11950
45. Rönicke R, Mikhaylova M, Rönicke S, Meinhardt J, Schröder UH, Fändrich M, Reiser G, Kreutz MR, Reymann KG (2011) Early neuronal dysfunction by amyloid -oligomers depends on activation of NR2B-containing NMDA receptors. Neurobiol Aging 32, 2219-2228
46. Cuello AC (2006) Intracellular and extracellular Abeta, a tale of two neuropathologies. Brain Pathol 15, 66-71
47. Calkins MJ, Manczak M, Mao P, Shirendeb U, Reddy PH (2011) Impaired mitochondrial biogenesis, defective axonal transport of mitochondria, abnormal mitochondrial dynamics and synaptic degeneration in a mouse model of Alzheimer's disease. Hum Mol Genet 20, 4515-4529
48. Mezler M, Barghorn S, Schoemaker H, Gross G, Nimmrich V (2012) A-Amyloid oligomer directly modulates P/Q-type calcium currents in Xenopus oocytes. Br J Pharmacol 165, 1572-1583
49. Quiroz-Baez R, Flores-Domínguez D, Arias C (2013) Synaptic aging is associated with mitochondrial dysfunction, reduced antioxidant contents and increased vulnerability to amyloid-toxicity. Curr Alzheimer Res 10, 324-331
50. Mota SI, Ferreira IL, Rego AC (2014) Dysfunctional synapse in Alzheimer's disease -A focus on NMDA receptors. Neuropharmacology 76, 16-26
51. Park J, Jang M, Chang S (2013) Deleterious effects of soluble amyloid-oligomers on multiple steps of synaptic vesicle trafficking. Neurobiol Dis 55, 129-139
52. Parodi J, Sepúlveda FJ, Roa J, Opazo C, Inestrosa NC, Aguayo LG(2010) Beta-Amyloid causes depletion of synaptic vesicles leading to neurotransmission failure. J Biol Chem 285, 2506-2514
53. Canas PM, Sim'oes AP, Rodrigues RJ, Cunha RA (2013) Predominant loss of glutamatergic terminal markers in a -Amyloid peptide model of Alzheimer's disease. Neuropharmacology 76, 51-56
54. Ripoli C, Cocco S, Li Puma DD, Piacentini R, Mastrodonato A, Scala F, Puzzo D, D'Ascenzo M, Grassi C (2014) Intracellular accumulation of amyloid-(A-) protein plays a major role in A-induced alterations of glutamatergic synaptic transmission and plasticity. J Neurosci 34, 12893-12903
55. Ferreira IL, Resende R, Ferreiro E, Rego AC, Pereira CF (2010) Multiple defects in energy metabolism in Alzheimer's disease. Curr Drug Targets 11, 1193-1206
56. Reddy PH, Manczak M, Mao P, Calkins MJ, Reddy AP, Shirendeb U (2010) Amyloid-beta and mitochondria in aging and Alzheimer's disease: Implications for synaptic damage and cognitive decline. J Alzheimers Dis 20(Suppl 2), S499-S512
57. Stutzmann GE, Caccamo A, LaFerla FM, Parker I (2004) Dysregulated IP3 signaling in cortical neurons of knock-in mice expressing an Alzheimer's-linked mutation in presenilin1 results in exaggerated Ca2+ signals and altered membrane excitability. J Neurosci 24, 508-513
58. Stutzmann GE, Smith I, Caccamo A, Oddo S, Parker I, Laferla F (2007) Enhanced ryanodine-mediated calcium release in mutant PS1-expressing Alzheimer's mouse models. Ann NY Acad Sci 1097, 265-277
59. Smith IF, Hitt B, Green KN, Oddo S, LaFerla FM (2005) Enhanced caffeine-induced Ca2+ release in the 3xTg-AD mouse model of Alzheimer's disease. J Neurochem 94, 1711-1718
60. Minkeviciene R, Ihalainen J, Malm T, Matilainen O, Keksa-Goldsteine V, Goldsteins G, Iivonen H, Leguit N, Glennon J, Koistinaho J, Banerjee P, Tanila H (2008) Age-related decrease in stimulated glutamate release and vesicular glutamate transporters in APP/PS1 transgenic and wild-type mice. J Neurochem 105, 584-594
61. Hyman BT, Van Hoesen GW, Damasio AR (1987) Alzheimer's disease: Glutamate depletion in the hippocampal perforant pathway zone. Ann Neurol 22, 37-40
62. Lowe SL, Bowen DM, Francis PT, Neary D (1990) Ante mortem cerebral amino acid concentrations indicate selective degeneration of glutamate-enriched neurons in Alzheimer's disease. Neuroscience 38, 571-577
63. Grolla AA, Sim JA, Lim D, Rodriguez JJ, Genazzani AA, Verkhratsky A (2013) Amyloid-And Alzheimer's disease type pathology differentially affects the calcium signalling toolkit in astrocytes from different brain regions. Cell Death Dis 4, e623
64. Lü L, Mak YT, Fang M, Yew DT (2009) The difference in gliosis induced by -Amyloid and Tau treatments in astrocyte cultures derived from senescence accelerated and normal mouse strains. Biogerontology 10, 695-710
65. Verkhratsky A, Olabarria M, Noristani HN, Yeh CY, Rodriguez JJ (2010) Astrocytes in Alzheimer's disease. Neurotherapeutics 7, 399-412
66. Casal C, Serratosa J, Tusell JM (2004) Effects of beta-AP peptides on activation of the transcription factor NF-kappaB and in cell proliferation in glial cell cultures. Neurosci Res 48, 315-323
67. Garwood CJ, Pooler AM, Atherton J, Hanger DP, Noble W (2011) Astrocytes are important mediators of A-induced neurotoxicity and tau phosphorylation in primary culture. Cell Death Dis 2, e167
68. Olabarria M, Noristani HN, Verkhratsky A, Rodríguez JJ (2010) Concomitant astroglial atrophy and astrogliosis in a triple transgenic animal model of Alzheimer's disease. Glia 58, 831-838
69. Yeh CY, Vadhwana B, Verkhratsky A, Rodr'ýguez JJ (2011) Early astrocytic atrophy in the entorhinal cortex of a triple transgenic animal model of Alzheimer's disease. ASN Neuro 3, 271-279
70. Hamilton NB, Attwell D (2010) Do astrocytes really exocytose neurotransmitters?. Nat Rev Neurosci 11, 227-238
71. Orellana JA, Shoji KF, Abudara V, Ezan P, Amigou E, Sáez PJ, Jiang JX, Naus CC, Sáez JC, Giaume C (2011) Amyloid -induced death in neurons involves glial and neuronal hemichannels. J Neurosci 31, 4962-4977
72. Abe K, MisawaM(2003) Amyloid beta protein enhances the clearance of extracellular L-glutamate by cultured rat cortical astrocytes. Neurosci Res 45, 25-31
73. Matos M, Augusto E, Oliveira CR, Agostinho P (2008) Amyloid-beta peptide decreases glutamate uptake in cultured astrocytes: Involvement of oxidative stress and mitogenactivated protein kinase cascade. Neuroscience 156, 898-910
74. Matos M, Augusto E, Machado NJ, dos Santos-Rodrigues A, Cunha RA, Agostinho P (2012) Astrocytic adenosine A2A receptors control the amyloid-peptide-induced decrease of glutamate uptake. J Alzheimers Dis 31, 555-567
75. Scott HL, Tannenberg AE, Dodd PR (1995) Variant forms of neuronal glutamate transporter sites in Alzheimer's disease cerebral cortex. J Neurochem 64, 2193-2202
76. Masliah E, Alford M, DeTeresa R, Mallory M, Hansen L (1996) Deficient glutamate transport is associated with neurodegeneration in Alzheimer's disease. Ann Neurol 40, 759-766
77. Masliah E, Alford M, Mallory M, Rockenstein E, Moechars D, Van Leuven F (2000) Abnormal glutamate transport function in mutant amyloid precursor protein transgenic mice. Exp Neurol 163, 381-387
78. Scott HL, PowDV, Tannenberg AE, Dodd PR (2002) Aberrant expression of the glutamate transporter excitatory amino acid transporter 1 (EAAT1) in Alzheimer's disease. J Neurosci 22, RC206
79. Kulijewicz-Nawrot M, Syková E, Chvátal A, Verkhratsky A, Rodríguez JJ (2013) Astrocytes and glutamate homoeostasis in Alzheimer's disease: A decrease in glutamine synthetase, but not in glutamate transporter-1, in the prefrontal cortex. ASN Neuro 5, 273-282
80. Paterniti I, Impellizzeri D, Crupi R, Morabito R, Campolo M, Esposito E, Cuzzocrea S (2013) Molecular evidence for the involvement of PPAR-d and PPAR-in anti-inflammatory and neuroprotective activities of palmitoylethanolamide after spinal cord trauma. J Neuroinflammation 10, 20
81. Benito C, Nunez E, Tolon RM, Carrier EJ, Rabano A, Hillard CJ, Romero J (2003) Cannabinoid CB2 receptors and fatty acid amide hydrolase are selectively overexpressed in neuritic plaque-Associated glia in Alzheimer's disease brains. J Neurosci 23, 11136-11141
82. Núñez E, Benito C, Tolón RM, Hillard CJ, Griffin WS, Romero J (2008) Glial expression of cannabinoid CB(2) receptors and fatty acid amide hydrolase are beta amyloidlinked events in Down's syndrome. Neuroscience 151, 104-110
83. Alonso E, Vale C, Vieytes MR, Laferla FM, Giménez-Llort L, Botana LM (2011) 13-Desmethyl spirolide-C is neuroprotective and reduces intracellularA-And hyperphosphorylated tau in vitro. Neurochem Int 59, 1056-1065