Caffeine neuroprotective effects on 6-OHDA-lesioned rats are mediated by several factors, including pro-inflammatory cytokines and histone deacetylase inhibitions

Behavioural Brain Research

Volumn 264, Issue , 2014, Pages 116-125

  Machado Filho, João Ananias ^a   Correia, Alyne Oliveira ^a   Montenegro, Anyssa Brilhante Aires ^a   Nobre, Maria Elizabeth Pereira ^a   Cerqueira, Gilberto Santos ^b   Neves, Kelly Rose Tavares ^b   Naffah Mazzacoratti, Maria da Graça ^c   Cavalheiro, Esper Abrão ^c   de Castro Brito, Gerly Anne ^b   De Barros Viana, Glauce Socorro ^a,b  

^a Laboratory of Pharmacology and Physiology   (Brazil)

^b FEDERAL UNIVERSITY OF CEARÁ   (Brazil)

^c FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

6 OHDA model; Behavior; Caffeine; Neuroprotection; Parkinson's disease; Pro inflammatory cytokine

Indexed keywords

3,4 DIHYDROXYPHENYLACETIC ACID; CAFFEINE; CYTOKINE; HISTONE DEACETYLASE; INTERLEUKIN 1BETA; TUMOR NECROSIS FACTOR ALPHA; TYROSINE 3 MONOOXYGENASE;

ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL VIABILITY; CIRCLING BEHAVIOR; CONTROLLED STUDY; ENZYME INHIBITION; HIPPOCAMPUS; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; LOCOMOTION; MALE; NERVE CELL; NEUROCHEMISTRY; NEUROPROTECTION; NONHUMAN; OPEN FIELD BEHAVIOR; PARKINSON DISEASE; PRIORITY JOURNAL; RAT;

6-OHDA MODEL; BEHAVIOR; CAFFEINE; NEUROPROTECTION; PARKINSON'S DISEASE; PRO-INFLAMMATORY CYTOKINE;

3,4-DIHYDROXYPHENYLACETIC ACID; ADRENERGIC AGENTS; ANIMALS; APOMORPHINE; BRAIN; CAFFEINE; CYTOKINES; DOPAMINE; DOPAMINE AGONISTS; DOSE-RESPONSE RELATIONSHIP, DRUG; EXPLORATORY BEHAVIOR; HISTONE DEACETYLASES; MALE; MOTOR ACTIVITY; NEUROPROTECTIVE AGENTS; OXIDOPAMINE; PARKINSON DISEASE; RATS; RATS, WISTAR; TYROSINE 3-MONOOXYGENASE;

EID: 84896719369     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2014.01.051     Document Type: Article

References (67)

1. Shapira A.H., Bezard E., Brotchie J., Calon F., Collingridge G.L., Ferger B., et al. Novel pharmacological targets for the treatment of Parkinson's disease. Nature Review Drug Discovery 2006, 5:845-854.
2. Cieslak M., Komoszynski M., Wojtczac A. Adenosine A2A receptors in Parkinson's disease. Purinergic Signalling 2008, 4:305-312.
3. Soriano A., Ventura R., Molero A., Hoen R., Casadó V., Cortés A., et al. Adenosine A2A receptor-antagonist/dopamine D2 receptor-agonist bivalente ligands as pharmacological tools to detect A2A-D2 receptor heteromers. Journal of Medicinal Chemistry 2009, 52:5590-5602.
4. Calon F., Dridi M., Hornykiewicz O., Bedard P.J., Rajput A.H., Paolo T.D. Increased adenosine A2A receptors in the brain of Parkinson's disease patients with dyskinesias. Brain 2004, 127:1075-1084.
5. Ross G.W., Petrovitch H. Current evidence for neuroprotective effects of nicotine and caffeine against Parkinson's disease. Drugs Aging 2001, 18:797-806.
6. Ascherio A., Zhang S.M., Hernan M.A., Kawachi I., Colditz G.A., Speizer F.E., et al. Prospective study of caffeine consumption and risk of Parkinson's disease in men and women. Annals of Neurology 2001, 50:56-63.
7. Costa J., Lunet N., Santos C., Santos J., Vaz-Carneiro A. Caffeine exposure and the risk of Parkinson's disease: a systematic review and meta-analysis of observational studies. Journal of Alzheimer's Disease 2010, 20:S221-S238.
8. Altman R.D., Lang A.E., Postuma R.B. Caffeine in Parkinson's disease: a pilot open-label, dose-escalation study. Movement Disorders 2011, 26:2427-2431.
9. Palacios N., Gao X., McCullough M.L., Schwarzschild M.A., Shah R., Gapstur S., et al. Caffeine and risk of Parkinson's disease in a large cohort of men and women. Movement Disorders 2012, 27:1276-1282.
10. Liu R.M., Guo X., Park Y., Huang X., Sinha R., Freedman N.D., et al. Caffeine intake, smoking, and risk of Parkinson disease in men and women. American Journal of Epidemiology 2012, 175:1200-1207.
11. Andersen L.F., Jacobs D.R., Carlsen M.H., Blomhoff R. Consumption of coffee is associated with reduced risk of death attributed to inflammatory and cardiovascular diseases in the Iowa Women's Health Study 1-4. American Journal of Clinical Nutrition 2006, 83:1039-1046.
12. Kempf K., Herder C., Erlund I., Kolb H., Martin S., Carstensen M., et al. Effects of coffee consumption on subclinical inflammation and other risk factors for type 2 diabetes: a clinical trial. American Journal of Clinical Nutrition 2010, 91:950-957.
13. Przedborski S. Inflammation and Parkinson's disease pathogenesis. Movement Disorders 2010, 25:S55-S57.
14. Beal M.F. Mitochondria, oxidative damage, and inflammation in Parkinson's disease. Annals of the New York Academy of Sciences 2003, 991:120-131.
15. Henchcliffe C., Beal M.F. Mitochondrial biology and oxidative stress in Parkinson's disease pathogenesis. Natural Clinical Practice Neurology 2008, 4:600-609.
16. Taylor J.M., Main B.S., Crack P.J. Neuroinflammation and oxidative stress: co-conspirators in the pathology of Parkinson's disease. Neurochemistry International 2013, 62:803-819.
17. Moreira M.E.C., Pereira R.G.F.A., Dias D.F., Gontijo V.S., Vilela F.C., Moraes G.O.I., et al. Anti-inflammatory effect of aqueous extracts of roasted and green Coffea arabica L. Journal of Functional Foods 2013, 5:466-474.
18. Archer J. Tests for emocionality in rats and mice: a review. Animal Behavior 1973, 21:205-235.
19. Iancu R., Mohapel P., Brundin P., Paul G. Behavioral characterization of a unilateral 6-OHDA-lesion model of Parkinson's disease in mice. Bebavioural Brain Research 2005, 162:1-10.
20. Nicola S.M., Surmeier J., Malenka R.C. Dopaminergic modulation of neuronal excitability in the striatum and nucleus accumbens. Annual Review of Neuroscience 2000, 23:185-215.
21. Weintraub D. Dopamine and impulse control disorders in Parkinson's disease. Annals of Neurology 2008, 2:S93-S100.
22. Fox S.H. Non-dopaminergic treatments for motor control in Parkinson's disease. Drugs 2013, 73:1405-1415.
23. Cunha R.A. Neuroprotection by adenosine in the brain: from A1 receptor activation to A2A receptor blockade. Purinergic Signalling 2005, 1:111-134.
24. Ribeiro J.A., Sebastião A.M. Caffeine and adenosine. Journal of Alzheimers Disease 2010, 20:S3-S15.
25. Hsu C.W., Wang C.S., Chiu T.H. Caffeine and a selective adenosine A2A receptor antagonist induce sensitization and cross-sensitization behavior associated with increased striatal dopamine in mice. Journal of Biomedical Sciences 2010, 17:4. 10.1186/1423-0127-17-4.
26. Yacoubi M., Ledent C., Menard J.-F., Permentier M., Costentin J., Vageois J.-M. The stimulant effects of caffeine on locomotor behavior in mice are mediated through its blockade of adenosine A2A receptors. British Journal of Pharmacology 2000, 129:1465-1473.
27. Marin M.T., Zancheta R., Paro A.H., Possi A.P., Cruz F.C., Planeta C.S. Comparison of caffeine-induced locomotor activity between adolescent and adult rats. European Journal of Pharmacology 2011, 660:363-367.
28. Vickroy T.W., Chang S.K., Chou C.C. Caffeine-induced hyperactivity in the horse: comparisons of drug and metabolite concentrations in blood and cerebrospinal fluid. Journal of Veterinary Pharmacology and Therapeutics 2008, 31:156-166.
29. Xu K., Xu Y.-H., Chen J.-F., Schwarzschild M.A. Neuroprotection by caffeine: time course and role of its metabolites in the MPTP model of Parkinsonson's disease. Neuroscience 2010, 167:475-481.
30. Sonsalla P.K., Wong L.Y., Harris S.L., Richardson J.R., Khobahy I., Li W., et al. Delayed caffeine treatment prevents nigral dopamine neuron loss in a progressive rat model of Parkinson's disease. Experimental Neurology 2012, 234:482-487.
31. Golembiowska K., Wardas J., Noworyta-Sokolowska K., Kaminska K., Gorska A. Effects of adenosine receptor antagonists on the in vivo LPS-induced inflammation model of Parkinson's disease. Neurotoxicology Research 2013, 24:29-40.
32. Solinas M., Ferré S., You Z.-B., Karcz-Kubicha M., Popoli P., Goldberg S.R. Caffeine induces dopamine and glutamate release in the shell of the nucleus accumbens. Journal of Neurosciences 2002, 22:6321-6324.
33. Zhu Y., Zhang J., Zeng Y. Overview of tyrosine hydroxylase in Parkinson's disease. CNS & Neurological Disorders - Drug Targets 2012, 11:350-358.
34. Haavik J., Toska K. Tyrosine hydroxylase and Parkinson's disease. Molecular Neurobiology 1998, 16:285-309.
35. Feve A.P. Current status of tyrosine hydroxylase in management of Parkinson's disease. CNS & Neurological Disorders - Drug Targets 2012, 11:450-455.
36. Gammella E., Cairo G., Tacchini L. Adenosine A2A receptor but not HIF-1 mediates tyrosine hydroxylase induction in hypoxic PC12 cells. Journal of Neurosciences Research 2010, 88:2007-2016.
37. Khan M.S., Tabrez S., Priyadarshini M., Priyamvada S., Khan M.M. Targeting Parkinson's disease-tyrosine hydroxylase and oxidative stress as points of interventions. CNS & Neurological Disorders - Drug Targets 2012, 11:369-380.
38. Tolleson C., Claassen D. The function of tyrosine hydroxylase in the normal and Parkinsonian brain. CNS & Neurological Disorders - Drug Targets 2012, 11:381-386.
39. Chen H., O'Reilly E.J., Schwarzschild M.A., Ascherio A. Peripheral inflammatory biomarkers and risk of Parkinson's disease. American Journal of Epidemiology 2008, 167:90-95.
40. Nagatsu T., Sawada M. Biochemistry of postmortem brains in Parkinson's disease: historical overview and future prospects. Journal of Neural Transmission 2007, (Suppl. 72):113-120.
41. Lofrumento D.D., Saponaro C., Cianciulli A., De Nuccio F., Mitolo V., Nicolardi G., et al. MPTP-induced neuroinflammation increases the expression of pro-inflammatory cytokines and their receptors in mouse brain. Neuroimmunomodulation 2011, 18:79-88.
42. Reale M., Iarlori C., Thomas A., Gambi D., Perfetti B., Di Nicola M., et al. Peripheral cytokines profile in Parkinson's disease. Brain Behavior and Immunity 2009, 23:55-63.
43. Chuang D.M., Leng Y., Marinova Z., Kim H.J., Chiu C.T. Multiple roles of HDAC inhibition in neurodegenerative conditions. Trends in Neurosciences 2009, 32:591-601.
44. Cordato N.J., Halliday G.M., Harding A.J., Hely M.A., Morris J.G. Regional brain atrophy in progressive supranuclear palsy and Lewy body disease. Annals of Neurology 2000, 47:718-728.
45. Camicioli R., Moore M.M., Kinney A., Corbridge E., Glassberg K., Kaye J.A. Parkinson's disease is associated with hippocampal atrophy. Movement Disorders 2003, 18:784-790.
46. Brück A., Kurki T., Kaasinen V., Vahlberg T., Rinne J.O. Hippocampal and prefrontal atrophy in patients with early non-demented Parkinson's disease is related to cognitive impairment. Journal of Neurology, Neurosurgery, and Psychiatry 2004, 75:1467-1469.
47. Carlesimo G.A., Piras F., Assogna F., Pontieri F.E., Caltagirone C., Spalletta G. Hippocampal abnormalities and memory deficits in Parkinson disease. Neurology 2012, 78:1839-1845.
48. Prediger R.D. Effects of caffeine in Parkinson's disease: from neuroprotection in the management of motor and non-motor symptoms. Journal of Alzheimers Disease 2010, 20:S205-S220.
49. Postuma R.B., Lang A.E., Munhoz R.P., Charland K., Pelletier A., Moscovich M., et al. Caffeine for treatment of Parkinson's disease: a randomized control trial. Neurology 2012, 79:651-658.
50. Schwarzschild M.A., Xu K., Oztas E., Petzer J.P., Castangnoli K., Castangnoli N., et al. Neuroprotection by caffeine and more specific A2A receptor antagonists in animal models of Parkinson's disease. Neurology 2003, 61:S55-S61.
51. Kalda A., Yu L., Oztas E., Chen J.F. Novel neuroprotection by caffeine and adenosine A(2A) receptor antagonists in animal models of Parkinson's disease. Journal of Neurological Sciences 2006, 248:9-15.
52. Nobre H.V., Cunha G.M., Vasconcelos L.M., Magalhães H.I., Oliveira Neto R.N., Maia F.D., et al. Caffeine and CSC, adenosine A2A antagonists, offer neuroprotection against 6-OHDA-induced neurotoxicity in rat mesencephalic cells. Neurochemistry International 2010, 56:51-58.
53. Yadav S., Gupta S.P., Srivastava G., Srivastava P.K., Singh M.P. Role of secondary mediators in caffeine-mediated neuroprotection in maneb- and paraquat-induced Parkinson's disease phenotype in the mouse. Neurochemical Research 2012, 37:875-884.
54. Ross G.W., Abbott R.D., Petrovitch H., Morens D.M., Grandinetti A., Tung K.-H., et al. Association of coffee and caffeine intake with the risk of Parkinson disease. JAMA: The Journal of the American Medical Association 2000, 283:2674-2679.
55. Cunha R.A., Agostinho P.M. Chronic caffeine consumption prevents memory disturbance in different animal models of memory decline. Journal of Alzheimers Disease 2010, 20:S95-S116.
56. Chen J.F., Pedata F. Modulation of ischemic brain injury and neuroinflammation by adenosine A2A receptors. Current Pharmaceutical Design 2008, 14:1490-1499.
57. Dai S.S., Zhou Y.G., Li W., An J.H., Li P., Yang N., et al. Local glutamate level dictates adenosine A2A receptor regulation of neuroinflammation and traumatic brain injury. The Journal of Neuroscience 2010, 30:5802-5810.
58. Ritter M., Hohenberger K., Alter P., Herzum M., Tebbe J., Maisch M. Caffeine inhibits cytokine expression in lymphocytes. Cytokine 2005, 30:177-181.
59. Aguiar L.M., Macedo D.S., Vasconcelos S.M., Oliveira A.A., Sousa F.C., Viana G.S. CSC, an adenosine A(2A) receptor antagonist and MAO B inhibitor, reverses behavior, monoamine neurotransmission, and amino acid alterations in the 6-OHDA-lesioned rats. Brain Research 2008, 1101:192-199.
60. Brothers H.M., Marchalant Y., Wenk G.L. Caffeine attenuates lipopolysaccharide-induced neuroinflammation. Neuroscience Letters 2010, 480:97-100.
61. Vignoli J.A., Bassoli D.G., Benassi T.T. Antioxidant activity, polyphenols, caffeine and melanoidins in soluble coffee: the influence of processing conditions and raw material. Food Chemistry 2011, 24:863-868.
62. Kang C.H., Jayasooriya R.G., Dilshara M.G., Choi Y.H., Jeong Y.K., Kim N.D., et al. Caffeine suppresses lipopolysaccharide-stimulated BV2 microglial cells by suppressing Akt-mediated BF-kB activation and ERK phosphorylation. Food Chemistry and Toxicology 2012, 50:4270-4276.
63. Choi D.K., Suk K. Glial Reaction in Parkinson's Diseases: Inflammatory Activation Signaling of Glia as a Potential Therapeutic Target. Current Signal Transduction Therapy 2007, 2:77-90.
64. McCarty M.F. Down-regulation of microglial activation may represent a practical strategy for combating neurodegenerative disorders. Medical Hypotheses 2006, 10.1016/j.mehy.2006.01.013.
65. Hu G., Bidel S., Jousilahti P., Antikainen R., Tuomilehto J. Coffee and tea consumption and the risk of Parkinson's disease. Movement Disorders 2007, 22:2242-2248.
66. Saaksjarvi K., Knekt P., Rissanen H., Laaksonen M.A., Reunanen A., Mannisto S. Prospective study of coffee consumption and risk of Parkinson's disease. European Journal of Clinical Nutrition 2008, 62:908-915.
67. Wills A.M., Eberly S., Tennis M., Lang A.E., Messing S., Togasaki D., et al. Caffeine consumption and risk of dyskinesia in CALM-PD. Movement Disorders 2013, 28:380-383.