Caffeine consumption prevents memory impairment, neuronal damage, and adenosine A2A receptors upregulation in the hippocampus of a rat model of sporadic dementia

Journal of Alzheimer's Disease

Volumn 34, Issue 2, 2013, Pages 509-518

  Espinosa, Janaína ^a   Rocha, Andreia ^a   Nunes, Fernanda ^a   Costa, Marcelo S ^a   Schein, Vanessa ^a   Kazlauckas, Vanessa ^a   Kalinine, Eduardo ^a   Souza, Diogo O ^a   Cunha, Rodrigo A ^b,c   Porciúncula, Lisiane O ^a  

^a FEDERAL UNIVERSITY OF RIO GRANDE DO SUL   (Brazil)

^b UNIVERSITY OF COIMBRA   (Portugal)

^c UNIVERSITY OF COIMBRA   (Portugal)

Author keywords

Adenosine receptors; Alzheimer's disease; caffeine; memory; streptozotocin

Indexed keywords

ADENOSINE A2A RECEPTOR; CAFFEINE; NEURON SPECIFIC NUCLEAR PROTEIN; STREPTOZOCIN;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DEMENTIA; DRUG MECHANISM; HIPPOCAMPAL CA1 REGION; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MALE; MEMORY DISORDER; NERVE INJURY; NONHUMAN; PRIORITY JOURNAL; RAT; SPORADIC DEMENTIA; UPREGULATION; WESTERN BLOTTING;

EID: 84874311332     PISSN: 13872877     EISSN: 18758908     Source Type: Journal    
DOI: 10.3233/JAD-111982     Document Type: Article

References (68)

1. Ritchie K, Lovestone S (2002) The dementias. Lancet 360, 1759-1766 (Pubitemid 35447916)
2. Blennow K, de Leon MJ, Zetterberg H (2006) Alzheimer's disease. Lancet 368, 387-403 (Pubitemid 44108123)
3. Ashe KH, ZahsKR(2010) Probing the biology of Alzheimer's disease in mice. Neuron 66, 631-645
4. Lannert H, Hoyer S (1998) Intracerebroventricular administration of streptozotocin causes long-term diminutions in learning and memory abilities and in cerebral energy metabolism in adult rats. Behav Neurosci 112, 1199-1208 (Pubitemid 28519002)
5. de la Monte SM, Tong M, Lester-Coll N, Plater M Jr, Wands JR (2006) Therapeutic rescue of neurodegeneration in experimental type 3 diabetes: Relevance to Alzheimer's disease. J Alzheimers Dis 10, 89-109 (Pubitemid 44401370)
6. Salkovic-Petrisic M, Osmanovic J, Grunblatt E, Riederer P, Hoyer S (2009) Modeling sporadic Alzheimer's disease: The insulin resistant brain state generates multiple long-term morphobiological abnormalities including hyperphosphorylated tau protein and amyloid-beta. J Alzheimers Dis 18, 729-750
7. Mayer G, Nitsch R, Hoyer S (1990) Effects of changes in peripheral and cerebral glucose metabolism on locomotor activity, learning and memory in adult male rats. Brain Res 532, 95-100 (Pubitemid 20384645)
8. Duelli R, Schrock H, Kuschinsky W, Hoyer S (1994) Intracerebroventricular injection of streptozotocin induces discrete local changes in cerebral glucose utilization in rats. Int J Dev Neurosci 12, 737-743
9. Heo JH, Lee SR, Lee ST, Lee KM, Oh JH, Jang DP, Chang KT, Cho ZH (2011) Spatial distribution of glucose hypometabolism induced by intracerebroventricularstreptozotocin in monkeys. J Alzheimers Dis 25, 517-523
10. Salkovic-Petrisic M, Osmanovic-Barilar J, Bruckner MK, Hoyer S, Arendt T, Riederer P (2011) Cerebral amyloid angiopathy in streptozotocin rat model of sporadic Alzheimer's disease: A long-term follow up study. J Neural Transm 118, 765-772
11. Grunblatt E, Salkovic-Petrisic M, Osmanovic J, Riederer P, Hoyer S (2007) Brain insulin system dysfunction in streptozotocin intracerebroventricularly treated rats generates hyperphosphorylated tau protein. J Neurochem 101, 757-770 (Pubitemid 46633313)
12. Shoham S, Bejar C, Kovalev E, Weinstock M (2003) Intracerebroventricular injection of streptozotocin causes neurotoxicity to myelin that contributes to spatial memory deficits in rats. Exp Neurol 184, 1043-1052 (Pubitemid 38182835)
13. Shoham S, Bejar C, Kovalev E, Schorer-Apelbaum D, WeinstockM (2007) Ladostigil prevents gliosis, oxidative-nitrative stress and memory deficits induced by intracerebroventricular injection of streptozotocin in rats. Neuropharmacology 52, 836-843 (Pubitemid 46237641)
14. Selkoe DJ (2001) Alzheimer's disease: Genes, proteins, and therapy. Physiol Rev 81, 741-766 (Pubitemid 32267077)
15. Maia L, de Mendonca A (2002) Does caffeine intake protect from Alzheimer's disease? Eur J Neurol 9, 377-382 (Pubitemid 35013893)
16. Ritchie K, Carriere I, de Mendonca A, Portet F, Dartigues JF, Rouaud O, Barberger-Gateau P, Ancelin ML (2007) The neuroprotective effects of caffeine: A prospective population study (the Three City Study). Neurology 69, 536-545 (Pubitemid 47357260)
17. Eskelinen MH, Ngandu T, Tuomilehto J, Soininen H, Kivipelto M (2009) Midlife coffee and tea drinking and the risk of late-life dementia: A population-based CAIDE study. J Alzheimers Dis 16, 85-91
18. Smith AP (2009) Caffeine, cognitive failures and health in a non-working community sample. Hum Psychopharmacol 24, 29-34
19. Santos C, Lunet N, Azevedo A, de Mendonca A, Ritchie K, Barros H (2010) Caffeine intake is associated with a lower risk of cognitive decline: A cohort study from Portugal. J Alzheimers Dis 20(Suppl 1), S175-S185
20. Gelber RP, Petrovitch H, Masaki KH, Ross GW, White LR (2011) Coffee intake in midlife and risk of dementia and its neuropathologic correlates. J Alzheimers Dis 23, 607-615
21. Laitala VS, Kaprio J, Koskenvuo M, Raiha I, Rinne JO, Silventoinen K (2009) Coffee drinking in middle age is not associated with cognitive performance in old age. Am J Clin Nutr 90, 640-646
22. Prediger RD, Batista LC, Takahashi RN (2005) Caffeine reverses age-related deficits in olfactory discrimination and social recognition memory in rats Involvement of adenosine A1 and A2A receptors. Neurobiol Aging 26, 957-964 (Pubitemid 40249499)
23. Costa MS, Botton PH, Mioranzza S, Souza DO, Porciuncula LO (2008) Caffeine prevents age-associated recognition memory decline and changes brain-derived neurotrophic factor and tirosine kinase receptor (TrkB) content in mice. Neuroscience 153, 1071-1078
24. Sallaberry C, Nunes F, Costa MS, Fioreze GT, Ardais AP, Botton PH, Klaudat B, Forte T, Souza DO, Elisabetsky E, Porciuncula LO (2013) Chronic caffeine prevents changes in inhibitory avoidance memory and hippocampal BDNF immunocontent in middle-aged rats. Neuropharmacology 64, 153-159
25. Arendash GW, Schleif W, Rezai-Zadeh K, Jackson EK, Zacharia LC, Cracchiolo JR, Shippy D, Tan J (2006) Caffeine protects Alzheimer's mice against cognitive impairment and reduces brain beta-amyloid production. Neuroscience 142, 941-952 (Pubitemid 44740473)
26. ArendashGW,MoriT, Cao C, MamcarzM,RunfeldtM,Dickson A, Rezai-Zadeh K, Tane J, Citron BA, Lin X, Echeverria V, Potter H (2009) Caffeine reverses cognitive impairment and decreases brain amyloid-beta levels in aged Alzheimer's disease mice. J Alzheimers Dis 17, 661-680
27. Dall'Igna OP, Fett P, GomesMW, Souza DO, Cunha RA, Lara DR (2007) Caffeine and adenosine A(2a) receptor antagonists prevent beta-amyloid (25-35)-induced cognitive deficits in mice. Exp Neurol 203, 241-245 (Pubitemid 44821181)
28. Duarte JM, Carvalho RA, Cunha RA, Gruetter R (2009) Caffeine consumption attenuates neurochemical modifications in the hippocampus of streptozotocin-induced diabetic rats. J Neurochem 111, 368-379
29. Duarte JM, Agostinho PM, Carvalho RA, Cunha RA (2012) Caffeine consumption prevents diabetes-induced memory impairment and synaptotoxicity in the hippocampus of NONcZNO10/ LTJ mice. PLoS One 7, e21899
30. Cognato GP, Agostinho PM, Hockemeyer J, Muller CE, Souza DO, Cunha RA (2010) Caffeine and an adenosine A(2A) receptor antagonist prevent memory impairment and synaptotoxicity in adult rats triggered by a convulsive episode in early life. J Neurochem 112, 453-462
31. Alhaider IA, Aleisa AM, Tran TT, Alzoubi KH, Alkadhi KA (2010) Chronic caffeine treatment prevents sleep deprivation-induced impairment of cognitive function and synaptic plasticity. Sleep 33, 437-444
32. Lieberman HR, Tharion WJ, Shukitt-Hale B, Speckman KL, Tulley R (2002) Effects of caffeine, sleep loss, and stress on cognitive performance and mood during U.S Navy SEAL training. Sea-Air-Land. Psychopharmacology (Berl) 164, 250-261 (Pubitemid 35340991)
33. Alzoubi KH, Abdul-Razzak KK, Khabour OF, Al-Tuweiq GM, Alzubi MA, Alkadhi KA (2013) Caffeine prevents cognitive impairment induced by chronic psychosocial stress and/or high fat-high carbohydrate diet. Behav Brain Res 237, 7-14
34. Fredholm BB, Chen JF, Cunha RA, Svenningsson P,Vaugeois JM (2005) Adenosine and brain function. Int Rev Neurobiol 63, 191-270 (Pubitemid 43631262)
35. Cunha RA (2005) Neuroprotection by adenosine in the brain: From A(1) receptor activation to A (2A) receptor blockade. Purinergic Signal 1, 111-134 (Pubitemid 40466898)
36. Cunha RA, Agostinho PM (2010) Chronic caffeine consumption prevents memory disturbance in different animal models of memory decline. J Alzheimers Dis 20(Suppl 1), S95-s116
37. Costenla AR, Cunha RA, de Mendonca A (2010) Caffeine, adenosine receptors, and synaptic plasticity. J Alzheimers Dis 20(Suppl 1), S25-S34
38. Fredholm BB, Battig K, Holmen J, Nehlig A, Zvartau EE (1999) Actions of caffeine in the brain with special reference to factors that contribute to its widespread use. Pharmacol Rev 51, 83-133 (Pubitemid 29113867)
39. Quarta D, Ferre S, Solinas M, You ZB, Hockemeyer J, Popoli P, Goldberg SR (2004) Opposite modulatory roles for adenosine A1 and A2A receptors on glutamate and dopamine release in the shell of the nucleus accumbens Effects of chronic caffeine exposure. J Neurochem 88, 1151-1158 (Pubitemid 38280682)
40. Bevins RA, Besheer J (2006) Object recognition in rats and mice: A one-trial non-matching-to-sample learning task to study 'recognition memory'. Nat Protoc 1, 1306-1311
41. Santos AR, Duarte CB (2008) Validation of internal control genes for expression studies: Effects of the neurotrophin BDNF on hippocampal neurons. J Neurosci Res 86, 3684-3692
42. Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3, 1101-1108 (Pubitemid 351818697)
43. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: A practical and powerful approach to multiple testing. J Royal Stat Soc Ser B 57, 289-300
44. Gemmell E, Bosomworth H, Allan L, Hall R, Khundakar A, Oakley AE, Deramecourt V, Polvikoski TM, O'Brien JT, Kalaria RN (2012) Hippocampal neuronal atrophy and cognitive function in delayed poststroke and aging-related dementias. Stroke 43, 808-814
45. Cunha GM, Canas PM, Melo CS, Hockemeyer J, Muller CE, Oliveira CR, Cunha RA (2008) Adenosine A2A receptor blockade prevents memory dysfunction caused by betaamyloid peptides but not by scopolamine or MK-801. Exp Neurol 210, 776-781
46. Zhao WQ, Chen H, Quon MJ, Alkon DL (2004) Insulin and the insulin receptor in experimental models of learning and memory. Eur J Pharmacol 490, 71-81 (Pubitemid 38482161)
47. Hoyer S, Lannert H (2007) Long-term abnormalities in brain glucose/energy metabolism after inhibition of the neuronal insulin receptor: Implication of tau-protein. J Neural Transm Suppl 72, 195-202
48. Saxena G, Patro IK, Nath C (2011) ICV STZ induced impairment in memory and neuronal mitochondrial function: A protective role of nicotinic receptor. Behav Brain Res 224, 50-57
49. Park S, Jang JS, Hong SM (2007) Long-term consumption of caffeine improves glucose homeostasis by enhancing insulinotropic action through islet insulin/insulin-like growth factor 1 signaling in diabetic rats. Metabolism 56, 599-607 (Pubitemid 46574722)
50. Egawa T, Tsuda S, Ma X, Hamada T, Hayashi T (2011) Caffeine modulates phosphorylation of insulin receptor substrate-1 and impairs insulin signal transduction in rat skeletal muscle. J Appl Physiol 111, 1629-1636
51. Loopstra-Masters RC, Liese AD, Haffner SM, Wagenknecht LE, Hanley AJ (2011) Associations between the intake of caffeinated and decaffeinated coffee and measures of insulin sensitivity and beta cell function. Diabetologia 54, 320-328
52. Hatonen KA, Virtamo J, Eriksson JG, Sinkko HK, Erlund I, Jousilahti P, Leiviska JM, Valsta LM (2012) Coffee does not modify postprandial glycaemic and insulinaemic responses induced by carbohydrates. Eur J Nutr 51, 801-806
53. Faulhaber-Walter R, JouW, Mizel D, Li L, Zhang J, Kim SM, Huang Y, Chen M, Briggs JP, Gavrilova O, Schnermann JB (2011) Impaired glucose tolerance in the absence of adenosine A1 receptor signaling. Diabetes 60, 2578-2587
54. Johnston-Cox H,Koupenova M,Yang D, Corkey B, Gokce N, Farb MG, LeBrasseur N, Ravid K (2012) The A2b adenosine receptor modulates glucose homeostasis and obesity. PLoS One 7, e40584
55. Salehi A, Parandeh F, Fredholm BB, Grapengiesser E, Hellman B (2009) Absence of adenosine A1 receptors unmasks pulses of insulin release and prolongs those of glucagon and somatostatin. Life Sci 85, 470-476
56. Conde SV, Nunes da Silva T, Gonzalez C, MotaCarmo M, Monteiro EC, Guarino MP (2012) Chronic caffeine intake decreases circulating catecholamines and prevents dietinduced insulin resistance and hypertension in rats. Br J Nutr 107, 86-95
57. Gevaerd MS, Takahashi RN, Silveira R, Da Cunha C (2001) Caffeine reverses the memory disruption induced by intranigral MPTP-injection in rats. Brain Res Bull 55, 101-106 (Pubitemid 32586809)
58. Prediger RD, Pamplona FA, Fernandes D, Takahashi RN (2005) Caffeine improves spatial learning deficits in an animal model of attention deficit hyperactivity disorder (ADHD) -the spontaneously hypertensive rat (SHR). Int J Neuropsychopharmacol 8, 583-594 (Pubitemid 41400889)
59. Pandolfo P, Machado NJ, Kofalvi A, Takahashi RN, Cunha RA (2012) Caffeine regulates frontocorticostriatal dopamine transporter density and improves attention and cognitive deficits in an animal model of attention deficit hyperactivity disorder. Eur Neuropsychopharmacol, doi:10.1016/j.euroneuro.2012. 04.011
60. Botton PH, Costa MS, Ardais AP, Mioranzza S, Souza DO, da Rocha JB, Porciuncula LO (2010) Caffeine prevents disruption of memory consolidation in the inhibitory avoidance and novel object recognition tasks by scopolamine in adult mice. Behav Brain Res 214, 254-259
61. Ferre S (2008) An update on the mechanisms of the psychostimulant effects of caffeine. J Neurochem 105, 1067-1079 (Pubitemid 351590775)
62. Nemeth ZH, Bleich D, Csoka B, Pacher P, Mabley JG, Himer L, Vizi ES, Deitch EA, Szabo C, Cronstein BN, Hasko G (2007) Adenosine receptor activation ameliorates type 1 diabetes. FASEB J 21, 2379-2388 (Pubitemid 47230668)
63. Maeda T, Koos BJ (2009) Adenosine A1 and A2a receptors modulate insulinemia, glycemia, and lactatemia in fetal sheep. Am J Physiol Regul Integr Comp Physiol 296, R693-R701
64. Canas PM, Porciuncula LO, Cunha GM, Silva CG, Machado NJ, Oliveira JM, Oliveira CR, Cunha RA (2009) Adenosine A2A receptor blockade prevents synaptotoxicity and memory dysfunction caused by beta-amyloid peptides via p38 mitogen-activated protein kinase pathway. J Neurosci 29, 14741-14751
65. Duarte JM, Oliveira CR, Ambrosio AF, Cunha RA (2006) Modification of adenosine A1 and A2A receptor density in the hippocampus of streptozotocin- induced diabetic rats. Neurochem Int 48, 144-150 (Pubitemid 41832450)
66. Cunha GM, Canas PM, Oliveira CR, Cunha RA (2006) Increased density and synapto-protective effect of adenosine A2A receptors upon sub-chronic restraint stress. Neuroscience 141, 1775-1781 (Pubitemid 44233132)
67. Albasanz JL, Perez S, Barrachina M, Ferrer I, Martin M (2008) Up-regulation of adenosine receptors in the frontal cortex in Alzheimer's disease. Brain Pathol 18, 211-219 (Pubitemid 351430397)
68. Batalha VL, Pego JM, Fontinha BM, Costenla AR, Valadas JS, Baqi Y, Radjainia H, Muller CE, Sebastiao AM, Lopes LV (2012) Adenosine A(2A) receptor blockade reverts hippocampal stress-induced deficits and restores corticosterone circadian oscillation. Mol Psychiatry, doi: 10.1038/mp.2012.8