Chronic caffeine prevents changes in inhibitory avoidance memory and hippocampal BDNF immunocontent in middle-aged rats

Neuropharmacology

Volumn 64, Issue , 2013, Pages 153-159

  Sallaberry, Cássia ^a   Nunes, Fernanda ^a   Costa, Marcelo S ^a   Fioreze, Gabriela T ^a   Ardais, Ana Paula ^a   Botton, Paulo Henrique S ^a   Klaudat, Bruno ^a   Forte, Thomás ^a   Souza, Diogo O ^a   Elisabetsky, Elaine ^a   Porciúncula, Lisiane O ^a  

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

Author keywords

Aging; BDNF; Caffeine; Memory; TrkB

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; CAFFEINE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN;

AGE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AVOIDANCE BEHAVIOR; CONTROLLED STUDY; FOOD INTAKE; HIPPOCAMPUS; LONG TERM MEMORY; MALE; MEMORY DISORDER; MIDDLE AGED; NONHUMAN; PRIMARY PREVENTION; PRIORITY JOURNAL; RAT; SHORT TERM MEMORY;

AGING; ANIMALS; AVOIDANCE LEARNING; BEHAVIOR, ANIMAL; BRAIN-DERIVED NEUROTROPHIC FACTOR; CAFFEINE; CENTRAL NERVOUS SYSTEM STIMULANTS; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; HIPPOCAMPUS; MALE; MEMORY, LONG-TERM; MEMORY, SHORT-TERM; MILD COGNITIVE IMPAIRMENT; NEURAL INHIBITION; NEURONS; NOOTROPIC AGENTS; PROTEIN PRECURSORS; RATS; RATS, WISTAR; RECEPTOR, TRKB;

EID: 84866378617     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2012.07.010     Document Type: Article

References (83)

1. I.G. Agafonova, N.G. Kolosova, N.P. Mishchenko, E.L. Chaikina, and V.A. Stonik Effect of histochrome on brain vessels and research and exploratory activity of senescence accelerated OXYS rats Bull. Exp. Biol. Med. 143 2007 467 471
2. M. Alonso, M.R. Vianna, A.M. Depino, T. Mello e Souza, P. Pereira, G. Szapiro, H. Viola, F. Pitossi, I. Izquierdo, and J.H. Medina BDNF-triggered events in the rat hippocampus are required for both short- and long-term memory formation Hippocampus 12 2002 551 560
3. M.E. Angelucci, M.A. Vital, C. Cesário, C.R. Zadusky, P.L. Rosalen, and C. Da Cunha The effect of caffeine in animal models of learning and memory Eur. J. Pharmacol. 373 1999 135 140
4. G.W. Arendash, W. Schleif, K. Rezai-Zadeh, E.K. Jackson, L.C. Zacharia, J.R. Cracchiolo, D. Shippy, and J. Tan Caffeine protects Alzheimer's mice against cognitive impairment and reduces brain beta-amyloid production Neuroscience 142 2006 941 952
5. A. Balkowiec, and D.M. Katz Cellular mechanisms regulating activity-dependent release of native brain-derived neurotrophic factor from hippocampal neurons J. Neurosci. 22 2002 10399 10407
6. P. Barnes, and K.L. Thomas Proteolysis of proBDNF is a key regulator in the formation of memory PLoS. ONE 3 2008 e3248
7. P. Bekinschtein, M. Cammarota, L.M. Igaz, L.R. Bevilaqua, I. Izquierdo, and J.H. Medina Persistence of long-term memory storage requires a late protein synthesis- and BDNF-dependent phase in the hippocampus Neuron 53 2007 261 277
8. P. Bekinschtein, M. Cammarota, C. Katche, L. Slipczuk, J.I. Rossato, A. Goldin, I. Izquierdo, and J.H. Medina BDNF is essential to promote persistence of long-term memory storage Proc. Natl. Acad. Sci. U S A 105 2008 2711 2716
9. J.A. Bergado, W. Almaguer, Y. Rojas, V. Capdevila, and J.U. Frey Spatial and emotional memory in aged rats: a behavioral-statistical analysis Neuroscience 172 2011 256 269
10. P.H. Botton, M.S. Costa, A.P. Ardais, S. Mioranzza, D.O. Souza, J.B. da Rocha, and L.O. Porciúncula Caffeine prevents disruption of memory consolidation in the inhibitory avoidance and novel object recognition tasks by scopolamine in adult mice Behav. Brain Res. 214 2010 254 259
11. M. Cammarota, L.R.M. Bevilaqua, J.H. Medina, and I. Izquierdo Studies of short-term avoidance memory F. Bermúdez-Rattoni, Neural Plasticity and Memory: From Genes to Brain Imaging 2007 CRC Press Boca Raton (FL) Chapter 10. Frontiers in neuroscience
12. C. Castellano Effects of caffeine on discrimination learning, consolidation, and learned behavior in mice Psychopharmacology (Berlin) 48 1976 255 260
13. J.F. Chen, and Y. Chern Impacts of methylxanthines and adenosine receptors on neurodegeneration: human and experimental studies Handb Exp. Pharmacol. 200 2011 267 310
14. G. Chen, R. Kolbeck, Y.A. Barde, T. Bonhoeffer, and A. Kossel Relative contribution of endogenous neurotrophins in hippocampal long-term potentiation J. Neurosci. 19 1999 7983 7990
15. J.F. Chen, L. Yu, H.Y. Shen, J.C. He, X. Wang, and R. Zheng What knock-out animals tell us about the effects of caffeine J. Alzheimers Dis. 20 2010 S17 S24
16. L.Y. Chen, C.S. Rex, Y. Sanaiha, G. Lynch, and C.M. Gall Learning induces neurotrophin signaling at hippocampal synapses Proc. Natl. Acad. Sci. U S A 107 2010 7030 7035
17. S. Connolly, and T.J. Kingsbury Caffeine modulates CREB-dependent gene expression in developing cortical neurons Biochem. Biophys. Res. Commun. 397 2010 152 156
18. M.S. Costa, P.H. Botton, S. Mioranzza, D.O. Souza, and L.O. Porciúncula Caffeine prevents age-associated recognition memory decline and changes brain-derived neurotrophic factor and tirosine kinase receptor (TrkB) content in mice Neuroscience 153 2008 1071 1078
19. M.S. Costa, P.H. Botton, S. Mioranzza, A.P. Ardais, J.D. Moreira, D.O. Souza, and L.O. Porciúncula Caffeine improves adult mice performance in the object recognition task and increases BDNF and TrkB independent on phospho-CREB immunocontent in the hippocampus Neurochem. Int. 53 2008 89 94
20. M.S. Costa, A.P. Ardais, G.T. Fioreze, S. Mioranzza, P.H. Botton, L.V. Portela, D.O. Souza, and L.O. Porciúncula Treadmill running frequency on anxiety and hippocampal adenosine receptors density in adult and middle-aged rats Prog. Neuropsychopharmacol. Biol. Psychiatry 36 2012 198 204
21. S.D. Croll, N.Y. Ip, R.M. Lindsay, and S.J. Wiegand Expression of BDNF and trkB as a function of age and cognitive performance Brain Res. 812 1998 200 208
22. T. Crook, R.T. Bartus, S.H. Ferris, P. Whitehouse, G.D. Cohen, and S. Gershon Age-associated memory impairment: proposed diagnostic criteria and measures of clinical change. Report of a National Institute of Mental Health Work Group Dev. Neuropsychol. 2 1986 261 276
23. R.A. Cunha Neuroprotection by adenosine in the brain: from A1 receptor activation to A2A receptor blockade Purinergic Signal. 1 2005 111 134
24. O.P. Dall'Igna, P. Fett, M.W. Gomes, D.O. Souza, R.A. Cunha, and D.R. Lara Caffeine and adenosine A2A receptor antagonists prevent beta amyloid (25 35) induced cognitive deficits in mice Exp. Neurol. 203 2007 241 245
25. O.P. Dall'lgna, L.O. Porciuncula, D.O. Souza, R.A. Cunha, and D.R. Lara Neuroprotection by caffeine and adenosine A(2A) receptor blockade of beta amyloid neurotoxicity Br. J. Pharmacol. 138 2003 1207 1209
26. J.W. Daly Caffeine analogs: biomedical impact Cell. Mol. Life Sci. 64 2007 2153 2169
27. M.J. Diógenes, A.R. Costenla, L.V. Lopes, A. Jerónimo- Santos, V.C. Sousa, B.M. Fontinha, J.A. Ribeiro, and A.M. Sebastião Enhancement of LTP in aged rats is dependent on endogenous BDNF Neuropsychopharmacology 36 2011 1823 1836
28. C.A. Erickson, and C.A. Barnes The neurobiology of memory changes in normal aging Exp. Gerontol. 38 2003 61 69
29. M.H. Eskelinen, T. Ngandu, J. Tuomilehto, H. Soininen, and M. Kivipelto Midlife coffee and tea drinking and the risk of late-life dementia: a population-based CAIDE Study Journal of Alzheimer's Disease 16 2009 85 91
30. A. Figurov, L.D. Pozzo-Miller, P. Olafsson, T. Wang, and B. Lu Regulation of synaptic responses to high-frequency stimulation and LTP by neurotrophins in the hippocampus Nature 381 1996 706 709
31. S. Finkbeiner, S. Tavazoie, A. Maloratsky, K. Jacobs, K. Harris, and M. Greenberg CREB: a major mediator of neuronal neurotrophin responses Neuron 19 1997 1031 1047
32. B.B. Fredholm, K. Battig, J. Holmen, A. Nehlig, and E.E. Zvartau Actions of caffeine in the brain with special reference to factors that contribute to its widespread use Pharmacol. Rev. 51 1999 83 133
33. B.B. Fredholm, R. Cunha, and P. Svenningsson Pharmacology of adenosine A2A receptors and therapeutic applications Curr. Top. Med. Chem. 3 2003 413 426
34. B.B. Fredholm, A.P. IJzerman, K.A. Jacobson, J. Linden, and C.E. Müller International union of basic and clinical pharmacology. LXXXI. Nomenclature and classification of adenosine receptors-an update Pharmacol. Rev. 63 2011 1 34
35. B.B. Fredholm Methylxanthines Handb. Exp. Pharmacol. 200 2011 268 293
36. A. Gärtner, and V. Staiger Neurotrophin secretion from hippocampal neurons evoked by long-term-potentiation-inducing electrical stimulation patterns Proc. Natl. Acad. Sci. U S A 99 2002 6386 6391
37. M.E. Greenberg, B. Xu, B. Lu, and B.L. Hempstead New insights in the biology of BDNF synthesis and release: implications in CNS function J. Neurosci. 29 2009 12764 12767
38. O.B. Halbach Involvement of BDNF in age-dependent alterations in the hippocampus Front. Aging Neurosci. 2 2010 1 11
39. B. Hattiangady, M.S. Rao, G.A. Shetty, and A.K. Shetty Brain-derived neurotrophic factor, phosphorylated cyclic AMP response element binding protein and neuropeptide Y decline as early as middle age in the dentate gyrus and CA1 and CA3 subfields of the hippocampus Exp. Neurol. 195 2005 353 371
40. B.L. Hempstead, D. Martin-Zanca, D.R. Kaplan, L.F. Parada, and M.V. Chao High-affinity NGF binding requires coexpression of the trk proto-oncogene and the low-affinity NGF receptor Nature 350 1991 678 683
41. M.J. Jarvis Does caffeine intake enhance absolute levels of cognitive performance? Psychopharmacology 110 1993 45 52
42. M. Johnson-Kozlow, D. Kritz-Silverstein, E. Barrett-Connor, and D. Morton Coffee consumption and cognitive function among older adults Am. J. Epidemiol. 156 2002 842 850
43. A.B. Jolitha, M.V. Subramanyam, and S. Asha-Devi Age-related responses of the rat cerebral cortex: influence of vitamin E and exercise on the cholinergic system Biogerontology 10 2009 53 63
44. Y. Kaisho, M. Miyamoto, O. Shiho, H. Onoue, Y. Kitamura, and S. Nomura Expression of neurotrophin genes in the brain of senescence-accelerated mouse (SAM) during postnatal development Brain Res. 647 1994 139 144
45. H. Kang, A.A. Welcher, D. Shelton, and E.M. Schuman Neurotrophins and time: different roles for TrkB signaling in hippocampal long-term potentiation Neuron 19 1997 653 664
46. M. Karcz-Kubicha, K. Antoniou, A. Terasmaa, D. Quarta, M. Solinas, Z. Justinova, A. Pezzola, R. Reggio, C.E. Müller, K. Fuxe, S.R. Goldberg, P. Popoli, and S. Ferré Involvement of adenosine A1 and A2A receptors in the motor effects of caffeine after its acute and chronic administration Neuropsychopharmacology 28 2003 1281 1291
47. R. Katoh-Semba, R. Semba, I.K. Takeuchi, and K. Kato Age-related changes in levels of brain-derived neurotrophic factor in selected brain regions of rats, normal mice and senescence-accelerated mice: a comparison to those of nerve growth factor and neurotrophin-3 Neurosci. Res. 31 1998 227 234
48. M. Kivipelto, T. Ngandu, T. Laatikainen, B. Winblad, H. Soininen, and J. Tuomilehto Risk score for the prediction of dementia risk in 20 years among middle aged people: a longitudinal, population-based study Lancet Neurol. 5 2006 735 741
49. S.R. Kopf, A. Melani, F. Pedata, and G. Pepeu Adenosine and memory storage: effect of A(1) and A(2) receptor antagonists Psychopharmacology (Berlin) 146 1999 214 219
50. P.A. Lapchak, D.M. Araujo, K.D. Beck, C.E. Finch, S.A. Johnson, and F. Hefti BDNF and trkB mRNA expression in the hippocampal formation of aging rats Neurobiol. Aging 14 1993 121 126
51. F.S. Lee, and M.V. Chao Activation of Trk neurotrophin receptors in the absence of neurotrophins Proc. Natl. Acad. Sci. U S A 98 2001 3555 3560
52. M.R. Leite, E.A. Wilhelm, C.R. Jesse, R. Brandão, and C.W. Nogueira Protective effect of caffeine and a selective A2A receptor antagonist on impairment of memory and oxidative stress of aged rats Exp. Gerontol. 46 2011 309 315
53. B. Lu, P.T. Pang, and N.H. Woo The yin and yang of neurotrophin action Nat. Rev. Neurosci. 6 2005 603 614
54. L. Maia, and A. de Mendonca Does caffeine intake protect from Alzheimer's disease? Eur. J. Neurol. 9 2002 377 382
55. T. Matsumoto, S. Rauskolb, M. Polack, J. Klose, R. Kolbeck, M. Korte, and Y.A. Barde Biosynthesis and processing of endogenous BDNF: CNS neurons store and secrete BDNF, not pro-BDNF Nat. Neurosci. 11 2008 131 133
56. M. Moretti, A.G. de Souza, G. de Chaves, V.M. de Andrade, P.R. Romao, E.C. Gavioli, and C.R. Boeck Emotional behavior in middle-aged rats: implications for geriatric psychopathologies Physiol. Behav. 102 2011 115 120
57. A.C.J. Nooyens, H.B. Bueno-de-Mesquita, M.P.J. van Boxtel, B.M. van Gelder, H. Verhagen, and W.M.M. Verschuren Fruit and vegetable intake and cognitive decline in middle-aged men and women: the Doetinchem Cohort study Br. J. Nutr. 106 2011 752 761
58. P. Obiang, E. Maubert, I. Bardou, O. Nicole, S. Launay, L. Bezin, D. Vivien, and V. Agin Enriched housing reverses age-associated impairment of cognitive functions and tPA-dependent maturation of BDNF Neurobiol. Learn. Mem. 96 2011 121 129
59. P.T. Pang, H.K. Teng, E. Zaitsev, N.T. Woo, K. Sakata, S. Zhen, K.K. Teng, W.H. Yung, B.L. Hempstead, and B. Lu Cleavage of proBDNF by tPA/plasmin is essential for long-term hippocampal plasticity Science 306 2004 487 491
60. G.S. Pollock, E. Vernon, M.E. Forbes, Q. Yan, Y.T. Ma, T. Hsieh, R. Robichon, D.O. Frost, and J.E. Johnson Effects of early visual experience and diurnal rhythms on BDNF mRNA and protein levels in the visual system, hippocampus, and cerebellum J. Neurosci. 21 2001 3923 3931
61. R.D. Prediger, L.C. Batista, and R.N. Takahashi Caffeine reverses age related deficits in olfactory discrimination and social recognition memory in rats. Involvement of adenosine A1 and A2A receptors Neurobiol. Aging 26 2005 957 964
62. D. Quarta, S. Ferré, M. Solinas, Z.B. You, J. Hockemeyer, P. Popoli, and S.R. Goldberg 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 2004 1151 1158
63. C.S. Rex, E.A. Kramár, L.L. Colgin, B. Lin, C.M. Gall, and G. Lynch Long-term potentiation is impaired in middle-aged rats: regional specificity and reversal by adenosine receptor antagonists J. Neurosci. 25 2005 5956 5966
64. K. Ritchie, I. Carrie're, F. Portet, A. de Mendonca, J.F. Dartigues, O. Rouaud, P. Barberger Gateau, and M.L. Ancelin The neuro protective effects of caffeine: a prospective population study (the Three City Study) Neurology 69 2007 536 545
65. H. Rösch, R. Schweigreiter, T. Bonhoeffer, Y.A. Barde, and M. Korte The neurotrophin receptor p75NTR modulates long-term depression and regulates the expression of AMPA receptor subunits in the hippocampus Proc. Natl. Acad. Sci. U S A 102 2005 7362 7367
66. E.S. Rosenzweig, and C.A. Barnes Impact of aging on hippocampal function: plasticity, network dynamics, and cognition Prog. Neurobiol. 69 2003 143 179
67. J.I. Rossato, L.R. Bevilaqua, I. Izquierdo, J.H. Medina, and M. Cammarota Dopamine controls persistence of long-term memory storage Science 325 2009 1017 1020
68. K.S. Roussinov, and D.I. Yonkov Cholinergic mechanisms in the learning and memory facilitating effect of caffeine Acta Physiol. Pharmacol. Bulg. 2 1976 61 68
69. A.M. Sebastiao, and J.A. Ribeiro Adenosine receptors and the central nervous system Handb. Exp. Pharmacol. 193 2009 471 534
70. G. Segovia, A. Del Arco, M. de Blas, P. Garrido, and F. Mora Effects of an enriched environment on the release of dopamine in the prefrontal cortex produced by stress and on working memory during aging in the awake rat Behav. Brain Res. 187 2007 304 311
71. M. Silhol, V. Bonnichon, F. Rage, and L. Tapia-Arancibia Age-related changes in brain-derived neurotrophic factor and tyrosine kinase receptor isoforms in the hippocampus and hypothalamus in male rats Neuroscience 132 2005 613 624
72. M. Silhol, S. Arancibia, T. Maurice, and L. Tapia-Arancibia Spatial memory training modifies the expression of brain-derived neurotrophic factor tyrosine kinase receptors in young and aged rats Neuroscience 146 2007 962 973
73. M. Silhol, S. Arancibia, D. Perrin, T. Maurice, J. Alliot, and L. Tapia-Arancibia Effect of aging on brain-derived neurotrophic factor, proBDNF, and their receptors in the hippocampus of Lou/C rats Rejuvenation Res. 11 2008 1031 1040
74. N.A. Stefanova, A.Zh. Fursova, and N.G. Kolosova Behavioral effects induced by mitochondria-targeted antioxidant SkQ1 in Wistar and senescence-accelerated OXYS rats J. Alzheimers Dis. 21 2010 479 491
75. T.W. Stone, S. Ceruti, and M.P. Abbracchio Adenosine receptors and neurological disease: neuroprotection and neurodegeneration Handb. Exp. Pharmacol. 193 2009 535 587
76. L. Tapia-Arancibia, E. Aliaga, M. Silhol, and S. Arancibia New insights into brain BDNF function in normal aging and Alzheimer disease Brain Res. Rev. 59 2008 201 220
77. H.K. Teng, K.K. Teng, R. Lee, S. Wright, S. Tevar, R.D. Almeida, P. Kermani, R. Torkin, Z.Y. Chen, and F.S. Lee ProBDNF induces neuronal apoptosis via activation of a receptor complex of p75NTR and sortilin J. Neurosci. 25 2005 5455 5463
78. W.J. Tyler, M. Alonso, C.R. Bramham, and L.D. Pozzo-Miller From acquisition to consolidation: on the role of brain-derived neurotrophic factor signaling in hippocampal-dependent learning Learn. Mem. 9 2002 224 237
79. H. Viola, M. Furman, L.A. Izquierdo, M. Alonso, D.M. Barros, M.M. de Souza, I. Izquierdo, and J.H. Medina Phosphorylated cAMP response element-binding protein as a molecular marker of memory processing in rat hippocampus: effect of novelty J. Neurosci. 20 2000 RC112
80. N.H. Woo, H.K. Teng, C.J. Siao, C. Chiaruttini, P.T. Pang, T.A. Milner, B.L. Hempstead, and B. Lu Activation of p75NTR by proBDNF facilitates hippocampal long-term depression Nat. Neurosci. 8 2005 1069 1077
81. K. Yamada, and T. Nabeshima Brain-derived neurotrophic factor/TrkB signaling in memory processes J. Pharmacol. Sci. 91 2003 267 270
82. J. Yang, C.J. Siao, G. Nagappan, T. Marinic, D. Jing, K. McGrath, Z.Y. Chen, W. Mark, L. Tessarollo, F.S. Lee, B. Lu, and B.L. Hempstead Neuronal release of proBDNF Nat. Neurosci. 12 2009 113 115
83. Y. Zeng, M. Tan, J. Kohyama, M. Sneddon, J.B. Watson, Y.E. Sun, and C.W. Xie Epigenetic enhancement of BDNF signaling rescues synaptic plasticity in aging J. Neurosci. 31 2011 17800 17810