Lipid-based diets improve muscarinic neurotransmission in the hippocampus of transgenic APPSwe/PS1dE9 mice

Current Alzheimer Research

Volumn 12, Issue 10, 2015, Pages 923-931

  Janíčkova, Helena ^a   Rudajev, Vladimír ^a   Dolejši, Eva ^a   Koivisto, Hennariikka ^b   Jakubík, Jan ^a   Tanilab, Heikki ^c   El Fakahany, Esam E ^d   Doležal, Vladimír ^a  

^a INSTITUTE OF PHYSIOLOGY   (Czech Republic)

^b UNIVERSITY OF EASTERN FINLAND   (Finland)

^c KUOPIO UNIVERSITY HOSPITAL   (Finland)

^d UNIVERSITY OF MINNESOTA   (United States)

Author keywords

G protein activation; Hippocampus; Muscarinic neurotransmission; Nutrition; Omega 3 fatty acids; Stigmasterol

Indexed keywords

ACETYLCHOLINESTERASE; CARBACHOL; CHOLINE ACETYLTRANSFERASE; CHOLINESTERASE; FISH OIL; LIPID; MUSCARINIC RECEPTOR; STIGMASTEROL; AMYLOID PRECURSOR PROTEIN; APP PROTEIN, HUMAN; CASP8 PROTEIN, MOUSE; CASPASE 8; FAT INTAKE; PRESENILIN 1; PSEN1 PROTEIN, HUMAN;

ANIMAL EXPERIMENT; ARTICLE; ATTENUATION; CHOLINERGIC SYNAPSE; CHOLINERGIC TRANSMISSION; CONTROLLED STUDY; DIET SUPPLEMENTATION; ENZYME ACTIVITY; FEMALE; HIPPOCAMPUS; LIPID DIET; MOUSE; NONHUMAN; PRIORITY JOURNAL; RECEPTOR DENSITY; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE; ADMINISTRATION AND DOSAGE; ALZHEIMER DISEASE; ANIMAL; C3H MOUSE; C57BL MOUSE; DIET THERAPY; DISEASE MODEL; FAT INTAKE; GENETICS; HUMAN; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY; SYNAPTIC TRANSMISSION;

ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; CASPASE 8; DIETARY FATS; DISEASE MODELS, ANIMAL; FEMALE; HIPPOCAMPUS; HUMANS; MICE, INBRED C3H; MICE, INBRED C57BL; MICE, TRANSGENIC; PRESENILIN-1; RECEPTORS, MUSCARINIC; SYNAPTIC TRANSMISSION;

EID: 84959563947     PISSN: 15672050     EISSN: 18755828     Source Type: Journal    
DOI: 10.2174/1567205012666151027130350     Document Type: Article

References (69)

1. 1] Kang J, Lemaire HG, Unterbeck A, Salbaum JM, Masters CL, Grzeschik KH, et al. The precursor of Alzheimer's disease amyloid A4 protein resembles a cell-surface receptor. Nature 325: 733-6 (1987)
2. 2] Octave JN, Pierrot N, Ferao Santos S, Nalivaeva NN, Turner AJ. From synaptic spines to nuclear signaling: nuclear and synaptic actions of the amyloid precursor protein. J Neurochem 126: 183-90 (2013)
3. 3] Hardy JA, Higgins GA. Alzheimer's disease: the amyloid cascade hypothesis. Science 256: 184-5 (1992)
4. 4] Selkoe DJ. Alzheimer's disease: genes, proteins, and therapy. Physiol Rev 81: 741-66 (2001)
5. 5] Hardy J, Selkoe DJ. The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 297: 353-6 (2002)
6. 6] Guerreiro RJ, Gustafson DR, Hardy J. The genetic architecture of Alzheimer's disease: beyond APP, PSENs and APOE. Neurobiol Aging 33: 437-56 (2012)
7. 7] Saunders AM, Strittmatter WJ, Schmechel D, George-Hyslop PH, Pericak-Vance MA, Joo SH, et al. Association of apolipoprotein E allele epsilon 4 with late-onset familial and sporadic Alzheimer's disease. Neurology 43: 1467-72 (1993)
8. 8] Corder EH, Saunders AM, Risch NJ, Strittmatter WJ, Schmechel DE, Gaskell PC Jr, et al. Protective effect of apolipoprotein E type 2 allele for late onset Alzheimer disease. Nat Genet 7: 180-4 (1994)
9. 9] Kalmijn S, Launer LJ, Ott A, Witteman JC, Hofman A, Breteler MM. Dietary fat intake and the risk of incident dementia in the Rotterdam Study. Ann Neurol 42: 776-82 (1997)
10. 10] Morris MC, Evans DA, Bienias JL, Tangney CC, Bennett DA, Wilson RS, et al. Consumption of fish and n-3 fatty acids and risk of incident Alzheimer disease. Arch Neurol 60: 940-6 (2003)
11. 11] Morris MC, Evans DA, Tangney CC, Bienias JL, Wilson RS. Fish consumption and cognitive decline with age in a large community study. Arch Neurol 62: 1849-53 (2005)
12. 12] Laitinen MH, Ngandu T, Rovio S, Helkala EL, Uusitalo U, Viitanen M, et al. Fat intake at midlife and risk of dementia and Alzheimer's disease: a population-based study. Dement Geriatr Cogn Disord 22: 99-107 (2006)
13. 13] Schaefer EJ, Bongard V, Beiser AS, Lamon-Fava S, Robins SJ, Au R, et al. Plasma phosphatidylcholine docosahexaenoic acid content and risk of dementia and Alzheimer disease: the Framingham Heart Study. Arch Neurol 63: 1545-50 (2006)
14. 14] Dangour AD, Allen E, Elbourne D, Fletcher A, Richards M, Uauy R. Fish consumption and cognitive function among older people in the UK: baseline data from the OPAL study. J Nutr Health Aging 13: 198-202 (2009)
15. 15] Albanese E, Dangour AD, Uauy R, Acosta D, Guerra M, Guerra SS, et al. Dietary fish and meat intake and dementia in Latin America, China, and India: a 10/66 Dementia Research Group population- based study. Am J Clin Nutr 90: 392-400 (2009)
16. 16] Lopez LB, Kritz-Silverstein D, Barrett CE. High dietary and plasma levels of the omega-3 fatty acid docosahexaenoic acid are associated with decreased dementia risk: the Rancho Bernardo study. J Nutr Health Aging 15: 25-31 (2011)
17. 17] Cole GM, Ma QL, Frautschy SA. Omega-3 fatty acids and dementia. Prostaglandins Leukot Essent Fatty Acids 81: 213-21 (2009)
18. 18] Cottin SC, Sanders TA, Hall WL. The differential effects of EPA and DHA on cardiovascular risk factors. Proc Nutr Soc 70: 215-31 (2011)
19. 19] Jankowsky JL, Fadale DJ, Anderson J, Xu GM, Gonzales V, Jenkins NA, et al. Mutant presenilins specifically elevate the levels of the 42 residue beta-amyloid peptide in vivo: evidence for augmentation of a 42-specific gamma secretase. Hum Mol Genet 13: 159-70 (2004)
20. 20] Savonenko A, Xu GM, Melnikova T, Morton JL, Gonzales V, Wong MP, et al. Episodic-like memory deficits in the APPswe/ PS1dE9 mouse model of Alzheimer's disease: relationships to beta-amyloid deposition and neurotransmitter abnormalities. Neurobiol Dis 18: 602-17 (2005)
21. 21] Minkeviciene R, Ihalainen J, Malm T, Matilainen O, Keksa- Goldsteine V, Goldsteins G, et al. Age-related decrease in stimulated glutamate release and vesicular glutamate transporters in APP/PS1 transgenic and wild-type mice. J Neurochem 105: 584-94 (2008)
22. 22] Sahlin C, Pettersson FE, Nilsson LN, Lannfelt L, Johansson AS. Docosahexaenoic acid stimulates non-amyloidogenic APP processing resulting in reduced Abeta levels in cellular models of Alzheimer's disease. Eur J Neurosci 26: 882-9 (2007)
23. 23] Oksman M, Iivonen H, Hogyes E, Amtul Z, Penke B, Leenders I, et al. Impact of different saturated fatty acid, polyunsaturated fatty acid and cholesterol containing diets on beta-amyloid accumulation in APP/PS1 transgenic mice. Neurobiol Dis 23: 563-72 (2006)
24. 24] Grimm MO, Kuchenbecker J, Grosgen S, Burg VK, Hundsdorfer B, Rothhaar TL, et al. Docosahexaenoic acid reduces amyloid beta production via multiple pleiotropic mechanisms. J Biol Chem 286: 14028-39 (2011)
25. 25] Hooijmans CR, Rutters F, Dederen PJ, Gambarota G, Veltien A, van Groen T, et al. Changes in cerebral blood volume and amyloid pathology in aged Alzheimer APP/PS1 mice on a docosahexaenoic acid (DHA) diet or cholesterol enriched Typical Western Diet (TWD). Neurobiol Dis 28: 16-29 (2007)
26. 26] Zerbi V, Jansen D, Wiesmann M, Fang X, Broersen LM, Veltien A, et al. Multinutrient diets improve cerebral perfusion and neuroprotection in a murine model of Alzheimer's disease. Neurobiol Aging 35: 600-13 (2014)
27. 27] Machova E, Jakubik J, Michal P, Oksman M, Iivonen H, Tanila H, et al. Impairment of muscarinic transmission in transgenic APPswe/ PS1dE9 mice. Neurobiol Aging 29: 368-78 (2008)
28. 28] Machova E, Rudajev V, Smyckova H, Koivisto H, Tanila H, Dolezal V. Functional cholinergic damage develops with amyloid accumulation in young adult APPswe/PS1dE9 transgenic mice. Neurobiol Dis 38: 27-35 (2010)
29. 29] Bartus RT, Dean RL, Beer B, Lippa AS. The cholinergic hypothesis of geriatric memory dysfunction. Science 217: 408-14 (1982)
30. 30] Bartus RT. On neurodegenerative diseases, models, and treatment strategies: lessons learned and lessons forgotten a generation following the cholinergic hypothesis. Exp Neurol 163: 495-529 (2000)
31. 31] Perry EK, Kilford L, Lees AJ, Burn DJ, Perry RH. Increased Alzheimer pathology in Parkinson's disease related to antimuscarinic drugs. Ann Neurol 54: 235-8 (2003)
32. 32] Koivisto H, Grimm MO, Rothhaar TL, Berkecz R, Lutjohann DD, Giniatullina R, et al. Special lipid-based diets alleviate cognitive deficits in the APPswe/PS1dE9 transgenic mouse model of Alzheimer's disease independent of brain amyloid deposition. J Nutr Biochem 25: 157-69 (2014)
33. 33] Reeves PG, Nielsen FH, Fahey GC. AIN-93 purified diets for laboratory rodents: final report of the American Institute of Nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet. J Nutr 123: 1939-51 (1993)
34. 34] Fonnum F. Radiochemical micro assays for the determination of choline acetyltransferase and acetylcholinesterase activities. Biochem J 115: 465-72 (1969)
35. 35] Berrard S, Varoqui H, Cervini R, Israel M, Mallet J, Diebler MF. Coregulation of two embedded gene products, choline acetyltransferase and the vesicular acetylcholine transporter. J Neurochem 65: 939-42 (1995)
36. 36] Bailey JA, Lahiri DK. Chromatographic separation of reaction products from the choline acetyltransferase and carnitine acetyltransferase assay: differential ChAT and CrAT activity in brain extracts from Alzheimer's disease versus controls. J Neurochem 122: 672-80 (2012)
37. 37] Tucek S. The synthesis of acetylcholine in skeletal muscles of the rat. J Physiol 322: 53-69 (1982)
38. 38] Ellman GL, Courtney KD, Andres VJ, Feather-Stone RM. A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7: 88-95 (1961)
39. 39] Rudajev V, Novotny J, Hejnova L, Milligan G, Svoboda P. Dominant portion of thyrotropin-releasing hormone receptor is excluded from lipid domains. Detergent-resistant and detergent-sensitive pools of TRH receptor and Gqalpha/G11alpha protein. J Biochem 138: 111-25 (2005)
40. 40] Peterson GL. A simplification of the protein assay method of Lowry et al. which is more generally applicable. Anal Biochem 83: 346-56 (1977)
41. 41] Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the Folin phenol reagent. J Biol Chem 193: 265-75 (1951)
42. 42] Ivins KJ, Thornton PL, Rohn TT, Cotman CW. Neuronal apoptosis induced by beta-amyloid is mediated by caspase-8. Neurobiol Dis 6: 440-9 (1999)
43. 43] Burguillos MA, Deierborg T, Kavanagh E, Persson A, Hajji N, Garcia-Quintanilla A, et al. Caspase signalling controls microglia activation and neurotoxicity. Nature 472: 319-24 (2011)
44. 44] Hernandez D, Sugaya K, Qu T, McGowan E, Duff K, McKinney M. Survival and plasticity of basal forebrain cholinergic systems in mice transgenic for presenilin-1 and amyloid precursor protein mutant genes. Neuroreport 12: 1377-84 (2001)
45. 45] Luth HJ, Apelt J, Ihunwo AO, Arendt T, Schliebs R. Degeneration of beta-amyloid-associated cholinergic structures in transgenic APP SW mice. Brain Res 977: 16-22 (2003)
46. 46] German DC, Yazdani U, Speciale SG, Pasbakhsh P, Games D, Liang CL. Cholinergic neuropathology in a mouse model of Alzheimer's disease. J Comp Neurol 462: 371-81 (2003)
47. 47] Bellucci A, Luccarini I, Scali C, Prosperi C, Giovannini MG, Pepeu G, et al. Cholinergic dysfunction, neuronal damage and axonal loss in TgCRND8 mice. Neurobiol Dis 23: 260-72 (2006)
48. 48] Perez SE, Dar S, Ikonomovic MD, DeKosky ST, Mufson EJ. Cholinergic forebrain degeneration in the APPswe/PS1DeltaE9 transgenic mouse. Neurobiol Dis 28: 3-15 (2007)
49. 49] Cansev M, van Wijk N, Turkyilmaz M, Orhan F, Sijben JW, Broersen LM. A specific multi-nutrient enriched diet enhances hippocampal cholinergic transmission in aged rats. Neurobiol Aging 36: 344-51 (2015)
50. 50] Vannucchi MG, Casamenti F, Pepeu G. Decrease of acetylcholine release from cortical slices in aged rats: investigations into its reversal by phosphatidylserine. J Neurochem 55: 819-25 (1990)
51. 51] Casamenti F, Scali C, Pepeu G. Phosphatidylserine reverses the age-dependent decrease in cortical acetylcholine release: a microdialysis study. Eur J Pharmacol 194: 11-6 (1991)
52. 52] Kariv-Inbal Z, Yacobson S, Berkecz R, Peter M, Janaky T, Lutjohann D, et al. The isoform-specific pathological effects of apoE4 in vivo are prevented by a fish oil (DHA) diet and are modified by cholesterol. J Alzheimers Dis 28: 667-83 (2012)
53. 53] Jansen D, Zerbi V, Arnoldussen IA, Wiesmann M, Rijpma A, Fang XT, et al. Effects of specific multi-nutrient enriched diets on cerebral metabolism, cognition and neuropathology in AbetaPPswe- PS1dE9 mice. PLoS One 8: e75393 (2013)
54. 54] Jansen D, Zerbi V, Janssen CI, van Rooij D, Zinnhardt B, Dederen PJ, et al. Impact of a multi-nutrient diet on cognition, brain metabolism, hemodynamics, and plasticity in apoE4 carrier and apoE knockout mice. Brain Struct Funct 219: 1841-68 (2014)
55. 55] Weingartner O, Ulrich C, Lutjohann D, Ismail K, Schirmer SH, Vanmierlo T, et al. Differential effects on inhibition of cholesterol absorption by plant stanol and plant sterol esters in apoE-/- mice. Cardiovasc Res 90: 484-92 (2011)
56. 56] Vanmierlo T, Weingartner O, van der Pol S, Husche C, Kerksiek A, Friedrichs S, et al. Dietary intake of plant sterols stably increases plant sterol levels in the murine brain. J Lipid Res 53: 726-35 (2012)
57. 57] Cansev M, Wurtman RJ, Sakamoto T, Ulus IH. Oral administration of circulating precursors for membrane phosphatides can promote the synthesis of new brain synapses. Alzheimers Dement 4: S153-68 (2008)
58. 58] Wurtman RJ. Synapse formation and cognitive brain development: effect of docosahexaenoic acid and other dietary constituents. Metabolism 57 (Suppl 2): S6-10 (2008)
59. 59] van Wijk N, Broersen LM, de Wilde MC, Hageman RJ, Groenendijk M, Sijben JW, et al. Targeting synaptic dysfunction in Alzheimer's disease by administering a specific nutrient combination. J Alzheimers Dis 38: 459-79 (2014)
60. 60] Masliah E, Terry RD, Alford M, DeTeresa R, Hansen LA. Cortical and subcortical patterns of synaptophysin-like immunoreactivity in Alzheimer's disease. Am J Pathol 138: 235-46 (1991)
61. 61] Sze CI, Troncoso JC, Kawas C, Mouton P, Price DL, Martin LJ. Loss of the presynaptic vesicle protein synaptophysin in hippocampus correlates with cognitive decline in Alzheimer disease. J Neuropathol Exp Neurol 56: 933-44 (1997)
62. 62] Zhong N, Scearce-Levie K, Ramaswamy G, Weisgraber KH. Apolipoprotein E4 domain interaction: synaptic and cognitive deficits in mice. Alzheimers Dement 4: 179-92 (2008)
63. 63] Bymaster FP, McKinzie DL, Felder CC, Wess J. Use of M1-M5 muscarinic receptor knockout mice as novel tools to delineate the physiological roles of the muscarinic cholinergic system. Neurochem Res 28: 437-42 (2003)
64. 64] Tzavara ET, Bymaster FP, Felder CC, Wade M, Gomeza J, Wess J, et al. Dysregulated hippocampal acetylcholine neurotransmission and impaired cognition in M2, M4 and M2/M4 muscarinic receptor knockout mice. Mol Psychiatry 8: 673-9 (2003)
65. 65] Dolezal V, Tucek S. The effects of brucine and alcuronium on the inhibition of 3H acetylcholine release from rat striatum by muscarinic receptor agonists. Br J Pharmacol 124: 1213-8 (1998)
66. 66] Zhang W, Basile AS, Gomeza J, Volpicelli LA, Levey AI, Wess J. Characterization of central inhibitory muscarinic autoreceptors by the use of muscarinic acetylcholine receptor knock-out mice. J Neurosci 22: 1709-17 (2002)
67. 67] Janickova H, Rudajev V, Zimcik P, Jakubik J, Tanila H, El- Fakahany EE, et al. Uncoupling of M1 muscarinic receptor/Gprotein interaction by amyloid beta(1-42). Neuropharmacology 67: 272-83 (2013)
68. 68] Savelkoul PJ, Janickova H, Kuipers AA, Hageman RJ, Kamphuis PJ, Dolezal V, et al. A specific multi-nutrient formulation enhances M1 muscarinic acetylcholine receptor responses in vitro. J Neurochem 120: 631-40 (2012)
69. 69] Tsang SW, Lai MK, Kirvell S, Francis PT, Esiri MM, Hope T, et al. Impaired coupling of muscarinic M(1) receptors to G-proteins in the neocortex is associated with severity of dementia in Alzheimer's disease. Neurobiol Aging 27: 1216-23 (2005).