Expression, pharmacology and functional activity of adenosine A1 receptors in genetic models of Huntington's disease

Neurobiology of Disease

Volumn 71, Issue , 2014, Pages 193-204

  Ferrante, Antonella ^a   Martire, Alberto ^a   Pepponi, Rita ^a   Varani, Katia ^b   Vincenzi, Fabrizio ^b   Ferraro, Luca ^b   Beggiato, Sarah ^b   Tebano, Maria Teresa ^a   Popoli, Patrizia ^a  

^a ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^b UNIVERSITY OF FERRARA   (Italy)

Author keywords

Huntington's disease; R6 2 mice; Striatum

Indexed keywords

4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; ADENOSINE A1 RECEPTOR; ADENOSINE A1 RECEPTOR AGONIST; CYCLIC AMP; CYCLOPENTYLADENOSINE; GLUTAMIC ACID; MITOGEN ACTIVATED PROTEIN KINASE P38; N METHYL DEXTRO ASPARTIC ACID; UNCLASSIFIED DRUG; 1,3-DIPROPYL-8-CYCLOPENTYLXANTHINE; ADENINE; ADENOSINE A1 RECEPTOR ANTAGONIST; CYCLOPENTANE DERIVATIVE; CYCLOPENTENYLADENINE; ENZYME INHIBITOR; HUNTINGTON PROTEIN, MOUSE; NERVE PROTEIN; NUCLEAR PROTEIN; POTASSIUM CHLORIDE; PROTEIN BINDING; TRITIUM; XANTHINE DERIVATIVE; 6 N CYCLOPENTYLADENOSINE; CYCLIC AMP DEPENDENT PROTEIN KINASE; SYNAPTOPHYSIN;

AMINO ACID SYNTHESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN MEMBRANE; CELL VIABILITY; CONTROLLED STUDY; CORPUS STRIATUM; DEPRESSION; ENZYME ACTIVITY; FEMALE; GENOTYPE; HUNTINGTON CHOREA; IN VITRO STUDY; INTRACELLULAR SIGNALING; MALE; MOUSE; NEOCORTEX; NONHUMAN; PRESYNAPTIC INHIBITION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; RECEPTOR AFFINITY; RECEPTOR BINDING; RECEPTOR DENSITY; RECEPTOR DOWN REGULATION; SIGNAL TRANSDUCTION; SYNAPTIC POTENTIAL; SYNAPTIC TRANSMISSION; WILD TYPE; ACTION POTENTIAL; ANALOGS AND DERIVATIVES; ANIMAL; BRAIN CORTEX; DISEASE MODEL; DOSE RESPONSE; DRUG EFFECTS; ELECTROSTIMULATION; GENE EXPRESSION REGULATION; GENETIC TRANSFECTION; GENETICS; METABOLISM; NERVE CELL; NONPARAMETRIC TEST; PATHOLOGY; SYNAPTOSOME; TRANSGENIC MOUSE; TRINUCLEOTIDE REPEAT; BINDING AFFINITY; BRAIN SLICE; NERVE ENDING; PROTEIN BINDING;

ACTION POTENTIALS; ADENINE; ADENOSINE A1 RECEPTOR ANTAGONISTS; ANIMALS; CEREBRAL CORTEX; CORPUS STRIATUM; CYCLIC AMP; CYCLOPENTANES; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; ELECTRIC STIMULATION; ENZYME INHIBITORS; FEMALE; GENE EXPRESSION REGULATION; GLUTAMIC ACID; HUNTINGTON DISEASE; IN VITRO TECHNIQUES; MALE; MICE; MICE, TRANSGENIC; NERVE TISSUE PROTEINS; NEURONS; NUCLEAR PROTEINS; POTASSIUM CHLORIDE; PROTEIN BINDING; RECEPTOR, ADENOSINE A1; SIGNAL TRANSDUCTION; STATISTICS, NONPARAMETRIC; SYNAPTIC TRANSMISSION; SYNAPTOSOMES; TRANSFECTION; TRINUCLEOTIDE REPEAT EXPANSION; TRITIUM; XANTHINES;

EID: 84906825112     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2014.08.013     Document Type: Article

References (100)

1. Alberch J., Pérez-Navarro E., Canals J.M. Neurotrophic factors in Huntington's disease. Prog. Brain Res. 2004, 146:195-229.
2. Alfinito P.D., Wang S.P., Manzino L., Rijhsinghani S., Zeevalk G.D., Sonsalla P.K. Adenosinergic protection of dopaminergic and GABAergic neurons against mitochondrial inhibition through receptors located in the substantia nigra and striatum, respectively. J. Neurosci. 2003, 23:10982-10987.
3. Anderson W.W., Collingridge G.L. The LTP Program: a data acquisition program for on-line analysis of long-term potentiation and other synaptic events. J. Neurosci. Methods 2001, 15:71-83.
4. Barth A., Newell D.W., Nguyen L.B., Winn H.R., Wender R., Meno J.R., Janigro D. Neurotoxicity in organotypic hippocampal slices mediated by adenosine analogues and nitric oxide. Brain Res. 1997, 762:79-88.
5. Blum D., Gall D., Galas M.C., D'Alcantara P., Bantubungi K., Schiffmann S.N. The adenosine A1 receptor agonist adenosine amine congener exerts a neuroprotective effect against the development of striatal lesions and motor impairments in the 3-nitropropionic acid model of neurotoxicity. J. Neurosci. 2002, 22:9122-9133.
6. Blum D., Galas M.C., Gall D., Cuvelier L., Schiffmann S.N. Striatal and cortical neurochemical changes induced by chronic metabolic compromise in the 3-nitropropionic model of Huntington's disease. Neurobiol. Dis. 2002, 10:410-426.
7. Brust T.B., Cayabyab F.S., Zhou N., MacVicar B.A. p38 mitogen-activated protein kinase contributes to adenosine A1 receptor-mediated synaptic depression in area CA1 of the rat hippocampus. J. Neurosci. 2006, 26:12427-12438.
8. Calabresi P., Centonze D., Pisani A., Bernardi G. Endogenous adenosine mediates the presynaptic inhibition induced by aglycemia at corticostriatal synapses. J. Neurosci. 1997, 17:4509-4516.
9. Cattaneo E., Zuccato C., Tartari M. Normal huntingtin function: an alternative approach to Huntington's disease. Nat. Rev. Neurosci. 2005, 6:919-930.
10. Cepeda C., Ariano M.A., Calvert C.R., Flores-Hernández J., Chandler S.H., Leavitt B.R., Hayden M.R., Levine M.S. NMDA receptor function in mouse models of Huntington disease. J. Neurosci. Res. 2001, 66:525-539.
11. Cha J.H., Frey A.S., Alsdorf S.A., Kerner J.A., Kosinski C.M., Mangiarini L., Penney J.B., Davies S.W., Bates G.P., Young A.B. Altered neurotransmitter receptor expression in transgenic mouse models of Huntington's disease. Philos. Trans. R. Soc. Lond. B Biol. Sci. 1999, 354:981-989.
12. Chang D.T., Rintoul G.L., Pandipati S., Reynolds I.J. Mutant huntingtin aggregates impair mitochondrial movement and trafficking in cortical neurons. Neurobiol. Dis. 2006, 22:388-400.
13. Chou S.Y., Lee Y.C., Chen H.M., Chiang M.C., Lai H.L., Chang H.H., Wu Y.C., Sun C.N., Chien C.L., Lin Y.S., Wang S.C., Tung Y.Y., Chang C., Chern Y. CGS21680 attenuates symptoms of Huntington's disease in a transgenic mouse model. J. Neurochem. 2005, 93:310-320.
14. Ciruela F., Saura C., Canela E.I., Mallol J., Llui's C., Franco R. Adenosine deaminase affects ligand-induced signalling by interacting with cell surface adenosine receptors. FEBS Lett. 1996, 380:219-223.
15. Cobb M.H. MAP kinase pathways. Prog. Biophys. Mol. Biol. 1999, 71:479-500.
16. Cunha R.A. Adenosine as a neuromodulator and as a homeostatic regulator in the nervous system: different roles, different sources and different receptors. Neurochem. Int. 2001, 38:107-125.
17. Cunha R.A. Neuroprotection by adenosine in the brain: from A1 receptor activation to A2A receptor blockade. Purinergic Signal 2005, 1:111-134.
18. Dalpiaz A., Manfredini S. Adenosine A1 receptor: analysis of the potential therapeutic effects obtained by its activation in the central nervous system. Curr. Med. Chem. 2002, 9:1923-1937.
19. Damiano M., Galvan L., Déglon N., Brouillet E. Mitochondria in Huntington's disease. Biochim. Biophys. Acta 2010, 1802:52-61.
20. Dau A., Gladding C.M., Sepers M.D., Raymond L.A. Chronic blockade of extrasynaptic NMDA receptors ameliorates synaptic dysfunction and pro-death signaling in Huntington disease transgenic mice. Neurobiol. Dis. 2014, 62:533-542.
21. de Mendonça A., Sebastiao A.M., Ribeiro J.A. Inhibition of NMDA receptor-mediated currents in isolated rat hippocampal neurones by adenosine A1 receptor activation. Neuroreport 1995, 6:1097-1100.
22. Domenici M.R., Scattoni M.L., Martire A., Lastoria G., Potenza R.L., Borioni A., Venerosi A., Calamandrei G., Popoli P. Behavioral and electrophysiological effects of the adenosine A2A receptor antagonist SCH 58261 in R6/2 Huntington's disease mice. Neurobiol. Dis. 2007, 28:197-205.
23. Dong X.X., Wang Y., Qin Z.H. Molecular mechanisms of excitotoxicity and their relevance to pathogenesis of neurodegenerative diseases. Acta Pharmacol. Sin. 2009, 30:379-387.
24. Dunwiddie T.V., Masino S.A. The role and regulation of adenosine in the central nervous system. Annu. Rev. Neurosci. 2001, 24:31-55.
25. Fan M.M.Y., Raymond L.A. N-methyl-d-aspartate (NMDA) receptor function and excitotoxicity in Huntington's disease. Prog. Neurobiol. 2007, 81:272-293.
26. Fan J., Gladding C.M., Wang L., Zhang L.Y., Kaufman A.M., Milnerwood A.J., Raymond L.A. P38 MAPK is involved in enhanced NMDA receptor-dependent excitotoxicity in YAC transgenic mouse model of Huntington disease. Neurobiol. Dis. 2012, 45:999-1009.
27. Ferrante R.J., Kowall N.W., Beal M.F., Martin J.B., Bird E.D., Richardson E.P. Morphologic and histochemical characteristics of a spared subset of striatal neurons in Huntington's disease. J. Neuropathol. Exp. Neurol. 1987, 46:12-27.
28. 3H]-dopamine efflux from rat striatal synaptosomes; a novel action of cocaine. J. Neural Transm. 2010, 117:593-597.
29. Ferré S., Fredholm B.B., Morelli M., Popoli P., Fuxe K. Adenosine-dopamine receptor-receptor interactions as an integrative mechanism in the basal ganglia. Trends Neurosci. 1997, 20:482-487.
30. Ferrer I., Goutan E., Marín C., Rey M.J., Ribalta T. Brain-derived neurotrophic factor in Huntington disease. Brain Res. 2000, 866:257-261.
31. Fredholm B.B., Dunwiddie T.V. How does adenosine inhibit transmitter release?. Trends Pharmacol. Sci. 1988, 9:130-134.
32. Fredholm B.B., Ijzerman A.P., Jacobson K.A., Klotz K.N., Linden J. International union of pharmacology XXV. Nomenclature and classification of adenosine receptors. Pharmacol. Rev. 2001, 53:527-552.
33. Fredholm B.B., Chen J.F., Cunha R.A., Svenningsson P., Vaugeois J.M. Adenosine and brain function. Int. Rev. Neurobiol. 2005, 63:191-270.
34. Fredholm B.B., IJzerman A.P., Jacobson K.A., Linden J., Müller C.E. International union of basic and clinical pharmacology. LXXXI. Nomenclature and classification of adenosine receptors-an update. Pharmacol. Rev. 2011, 63:1-34.
35. Gauthier L.R., Charrin B.C., Borrell-Pages M., Dompierre J.P., Rangone H., Cordelieres F.P., De May J., MacDonald M.E., Lessmann V., Humbert S., Saudou F. Huntingtin controls neurotrophic support and survival of neurons by enhancing BDNF vesicular transport along microtubules. Cell 2004, 118:127-138.
36. + current, IAHP, by reducing adenylyl cyclase activity in rat CA3 hippocampal neurons. J. Neurophysiol. 1994, 72:2360-2367.
37. Gianfriddo M., Melani A., Turchi D., Giovannini M.G., Pedata F. Adenosine and glutamate extracellular concentrations and mitogen-activated protein kinases in the striatum of Huntington transgenic mice. Selective antagonism of adenosine A2A receptors reduces transmitter outflow. Neurobiol. Dis. 2004, 17:77-88.
38. Giralt A., Saavedra A., Carretòn O., Xifrò X., Alberch J., Pérez-Navarro E. Increased PKA signaling disrupts recognition memory and spatial memory: role in Huntington's disease. Hum. Mol. Genet. 2011, 20:4232-4247.
39. Glass M., Dragunow M., Faull R.L.M. The pattern of neurodegeneration in Huntington's disease: a comparative study of cannabinoid, dopamine, adenosine and GABAA receptor alterations in the human basal ganglia in Huntington's disease. Neuroscience 2000, 97:505-519.
40. Gomez-Lazaro M., Galindo M.F., Melero-Fernandez de Mera R.M., Fernandez-Gómez F.J., Concannon C.G., Segura M.F., Comella J.X., Prehn J.H., Jordan J. Reactive oxygen species and p38 mitogen-activated protein kinase activate Bax to induce mitochondrial cytochrome c release and apoptosis in response to malonate. Mol. Pharmacol. 2007, 71:736-743.
41. 3H](R)-pia binding to the caudate nucleus. J. Neurochem. 2008, 107:161-170.
42. Haas H.L., Selbach O. Functions of neuronal adenosine receptors. Naunyn Schmiedebergs Arch. Pharmacol. 2000, 362:375-381.
43. Harper P.S. The epidemiology of Huntington's disease. Hum. Genet. 1992, 89:365-376.
44. Jacobson K.A., Gao Z.G. Adenosine receptors as therapeutics targets. Nat. Rev. Drug Discov. 2006, 5:247-264.
45. Kumar S., Jiang M.S., Adams J.L., Lee J.C. Pyridinylimidazole compound SB 203580 inhibits the activity but not the activation of p38 mitogen-activated protein kinase. Biochem. Biophys. Res. Commun. 1999, 263:825-831.
46. Legos J.J., McLaughlin B.A., Stephen D., Skaper S.D., Strijbos P.J.L.M., Parsons A.A., Aizenman E., Herin G.A., Barone F.C., Erhardt J.A. The selective p38 inhibitor SB-239063 protects primary neurons from mild to moderate excitotoxic injury. Eur. J. Pharmacol. 2002, 447:37-42.
47. Lennmyr F., Ericsson A., Gerwins P., Ahlström H., Terént A. Increased brain injury and vascular leakage after pretreatment with p38-inhibitor SB203580 in transient ischemia. Acta Neurol. Scand. 2003, 108:339-345.
48. Li S., Li X.J. Multiple pathways contribute to the pathogenesis of Huntington disease. Mol. Neurodegener. 2006, 16:1-19.
49. Luthi-Carter R., Apostol B.L., Dunaha A.W., DeJohna M.M., Farrella L.A., Batesc G.P., Young A.B., Standaert D.G., Thompson L.M., Cha J.H.J. Complex alteration of NMDA receptors in transgenic Huntington's disease mouse brain: analysis of mRNA and protein expression, plasma membrane association, interacting proteins, and phosphorylation. Neurobiol. Dis. 2003, 14:624-636.
50. 2+ channels. Eur. J. Pharmacol. 2004, 499:265-274.
51. 2A receptor agonist CGS21680 in the striatum of Huntington's disease versus wild-type mice. Neurosci. Lett. 2007, 417:78-83.
52. Martire A., Ferrante A., Potenza R.L., Armida M., Ferretti R., Pézzola A., Domenici M.R., Popoli P. Remodeling of striatal NMDA receptors by chronic A2A receptor blockade in Huntington's disease mice. Neurobiol. Dis. 2010, 37:99-105.
53. Martire A., Pepponi R., Domenici M.R., Ferrante A., Chiodi V., Popoli P. BDNF prevents NMDA-induced toxicity in models of Huntington's disease: the effects are genotype specific and adenosine A2A receptor is involved. J. Neurochem. 2013, 125:225-235.
54. Milnerwood A.J., Gladding C.M., Pouladi M.A., Kaufman A.M., Hines R.M., Boyd J.D., Ko R.W.Y., Vasuta O.C., Graham R.K., Hayden M.R. Early increase in extrasynaptic NMDA receptor signaling and expression contributes to phenotype onset in Huntington's disease mice. Neuron 2010, 65:178-190.
55. Mitchell I.J., Cooper A.J., Griffiths M.R. The selective vulnerability of striatopallidal neurons. Prog. Neurobiol. 1999, 59:691-719.
56. Nagahara A.H., Tuszynski M.H. Potential therapeutic uses of BDNF in neurological and psychiatric disorders. Nat. Rev. Drug Discov. 2011, 10:209-219.
57. Nishimura M., Sugino T., Nozaki K., Takagi Y., Hattori I., Hayashi J., Hashimoto N., Moriguchi T., Nishida E. Activation of p38 kinase in the gerbil hippocampus showing ischemic tolerance. J. Cereb. Blood Flow Metab. 2003, 23:1052-1059.
58. Paul S., Elsinga P.H., Ishiwata K., Dierckx R.A., van Waarde A. Adenosine A(1) receptors in the central nervous system: their functions in health and disease, and possible elucidation by PET imaging. Curr. Med. Chem. 2011, 18:4820-4835.
59. Popoli P., Blum D., Martire A., Ledent C., Ceruti S., Abbracchio M.P. Functions, dysfunctions and possible therapeutic relevance of adenosine A2A receptors in Huntington's disease. Prog. Neurobiol. 2007, 81:331-348.
60. Popoli P., Blum D., Domenici M.R., Burnouf S., Chern Y. A critical evaluation of adenosine A2A receptors as potentially "druggable" targets in Huntington's disease. Curr. Pharm. Des. 2008, 14:1500-1512.
61. Rangone H., Poizat G., Troncoso J., Ross C.A., MacDonald M.E., Saudou F., Humbert S. The serum- and glucocorticoid-induced kinase SGK inhibits mutant huntingtin-induced toxicity by phosphorylating serine 421 of huntingtin. Eur. J. Neurosci. 2004, 19:273-279.
62. Raymond L.A., André V.M., Cepeda C., Gladding C.M., Milnerwood A.J., Levine M.S. Pathophysiology of Huntington's disease: time-dependent alterations in synaptic and receptor function. Neuroscience 2011, 198:252-273.
63. Rebola N., Rodrigues R.J., Oliveira C.R., Cunha R.A. Different roles of adenosine A1, A2A and A3 receptors in controlling kainite-induced toxicity in cortical cultured neurons. Neurochem. Int. 2005, 47:317-325.
64. Reddy P.H., Shirendeb U.P. Mutant huntingtin, abnormal mitochondrial dynamics, defective axonal transport of mitochondria, and selective synaptic degeneration in Huntington's disease. Biochim. Biophys. Acta 2012, 1822:101-110.
65. Reddy P.H., Maoa P., Manczaka M. Mitochondrial structural and functional dynamics in Huntington's disease. Brain Res. Rev. 2009, 61:33-48.
66. Robinson A.J., Dickenson J.M. Regulation of p42/p44 MAPK and p38 MAPK by the adenosine A(1) receptor in DDT(1)MF-2 cells. Eur. J. Pharmacol. 2001, 41:151-161.
67. Rosenstock T.R., Duarte A.I., Rego A.C. Mitochondrial-associated metabolic changes and neurodegeneration in Huntington's disease - from clinical features to the bench. Curr. Drug Targets 2010, 11:1218-1236.
68. Saura C.A., Mallol J., Canela E.I., Lluis C., Franco R. Adenosine deaminase and A1 adenosine receptors internalize together following agonist-induced receptor desensitization. J. Biol. Chem. 1998, 273:17610-17617.
69. Scholz K.P., Miller R. Inhibition of quantal transmitter release in the absence of calcium influx by a G protein-linked adenosine receptor at hippocampal synapses. Neuron 1992, 8:1139-1150.
70. Schulz P.E., Cook E.P., Johnston D. Changes in paired-pulse facilitation suggest presynaptic involvement in long-term potentiation. J. Neurosci. 1994, 14:5325-5337.
71. Sebastião A.M., Ribeiro J.A. Tuning and fine-tuning of synapses with adenosine. Curr. Neuropharmacol. 2009, 7:180-194.
72. Sebastiao A.M., de Mendonca A., Moreira T., Ribeiro J.A. Activation of synaptic NMDA receptors by action potential dependent release of transmitter during hypoxia impairs recovery of synaptic transmission on reoxygenation. J. Neurosci. 2001, 21:8564-8571.
73. Seger R., Krebs E.G. The MAPK signalling cascade. FASEB J. 1995, 9:726-735.
74. Starling A.J., André V.M., Cepeda C., de Lima M., Chandler S.H., Levine M.S. Alterations in N-methyl-d-aspartate receptor sensitivity and magnesium blockade occur early in development in the R6/2 mouse model of Huntington's disease. J. Neurosci. Res. 2005, 82:377-386.
75. Stone T.W. Purines and neuroprotection. Adv. Exp. Med. Biol. 2002, 513:249-280.
76. Stone T.W., Ceruti S., Abbracchio M.P. Adenosine receptors and neurological disease: neuroprotection and neurodegeneration. Handb. Exp. Pharmacol. 2009, 193:535-587.
77. Sun W., Cao Y., Jin L., Wang L., Meng F., Zhu X. Modulating effect of adenosine deaminase on function of adenosine A1 receptors. Acta Pharmacol. Sin. 2005, 26:160-165.
78. Tarditi A., Camurri A., Varani K., Borea P.A., Woodman B., Bates G., Cattaneo E., Abbracchio M.P. Early and transient alteration of adenosine A(2A) receptor signaling in a mouse model of Huntington disease. Neurobiol. Dis. 2006, 23:44-53.
79. Taylor D.M., Moser R., Régulier E., Breuillaud L., Dixon M., Beesen A.A., Elliston L., Silva Santos Mde F., Kim J., Jones L., Goldstein D.R., Ferrante R.J., Luthi-Carter R. MAP kinase phosphatase 1 (MKP-1/DUSP1) is neuroprotective in Huntington's disease via additive effects of JNK and p38 Inhibition. J. Neurosci. 2013, 33:2313-2325.
80. 2A receptors enable the synaptic effects of cannabinoid CB1 receptors in the rodent striatum. J. Neurochem. 2009, 110:1921-1930.
81. Tebano M.T., Martire A., Chiodi V., Ferrante A., Popoli P. Role of adenosine A2A receptors in modulating synaptic functions and brain levels of BDNF: a possible key mechanism in the pathophysiology of Huntington's disease. ScientificWorldJournal 2010, 10:1768-1782.
82. The Huntington's Disease Collaborative Research Group A novel gene containing a trinucleotide repeat that is expanded and unstable on Huntington's disease chromosomes. Cell 1993, 72:971-983.
83. Trettel F., Rigamonti D., Hilditch-Maguire P., Wheeler V.C., Sharp A.H., Persichetti F., Cattaneo E., MacDonald M.E. Dominant phenotypes produced by the HD mutation in STHdh(Q111) striatal cells. Hum. Mol. Genet. 2000, 9:2799-2809.
84. Trussell L.O., Jackson M.B. Adenosine-activated potassium conductance in cultured striatal neurons. Proc. Natl. Acad. Sci. U. S. A. 1985, 82:4857-4861.
85. Turner C.P., Blackburn M.R., Rivkees S.A. A1 adenosine receptors mediate hypoglycemia-induced neuronal injury. J. Mol. Endocrinol. 2004, 32:129-144.
86. 2A receptor signaling in striatal cells expressing mutant huntingtin. FASEB J. 2001, 15:1245-1247.
87. 2A receptor function in peripheral blood cells in Huntington's disease. FASEB J. 2003, 17:2148-2150.
88. 1 adenosine receptor allosteric modulator, exhibits anti-nociceptive properties in acute and neuropathic pain models in mice. Neuropharmacology 2014, 81C:6-14.
89. von Lubitz D.K., Dambrosia J.M., Kempski O., Redmond D.J. Cyclohexyl adenosine protects against neuronal death following ischemia in the CA1 region of gerbil hippocampus. Stroke 1988, 19:1133-1139.
90. Wilk-Blaszczak M.A., Stein B., Xu S., Barbosa M.S., Cobb M.H., Belardetti F. The mitogen-activated protein kinase p38-2 is necessary for the inhibition of N-type calcium current by bradykinin. J. Neurosci. 1998, 18:112-118.
91. Wu L.G., Saggau P. Adenosine inhibits evoked synaptic transmission primarily by reducing presynaptic calcium influx in area CA1 of hippocampus. Neuron 1994, 12:1139-1148.
92. Wu L.G., Saggau P. Presynaptic inhibition of elicited neurotransmitter release. Trends Neurosci. 1997, 20(5):204-212.
93. Yan L., Burbiel J.C., Maass A., Muller C.E. Adenosine receptor agonists: from basic medicinal chemistry to clinical development. Expert Opin. Emerg. Drugs 2003, 8:537-576.
94. Zhu Y., Mao X.O., Sun Y., Xia Z., Greenberg D.A. p38 mitogen-activated protein kinase mediates hypoxic regulation of Mdm2 and p53 in neurons. J. Biol. Chem. 2002, 277(25):22909-22914.
95. Zhu P., Zhan L., Zhu T., Hu J., Sun W., Hou Q., Zhou H., Wu B., Wang Y., Xu E. The roles of p38 MAPK/MSK1 signaling pathway in the neuroprotection of hypoxic postconditioning against transient global cerebral ischemia in adult rats. Mol. Neurobiol. 2013, 49:1338-1349.
96. Zuccato C., Cattaneo E. Role of brain-derived neurotrophic factor in Huntington's disease. Prog. Neurobiol. 2007, 81:294-330.
97. Zuccato C., Cattaneo E. Brain-derived neurotrophic factor in neurodegenerative diseases Nat. Rev. Neurol. 2009, 5:311-322.
98. Zuccato C., Ciammola A., Rigamonti D., Leavitt B.R., Goffredo D., Conti L., MacDonald M.E., Friedlander R.M., Silani V., Hayden M.R., Timmusk T., Sipione S., Cattaneo E. Loss of huntingtin-mediated BDNF gene transcription in Huntington's disease. Science 2001, 293:493-498.
99. Zuccato C., Valenza M., Cattaneo E. Molecular mechanisms and potential therapeutical targets in Huntington's disease. Physiol. Rev. 2010, 90:905-981.
100. Zuchora B., Turski W.A., Wielosz M., Urbańska E.M. Protective effect of adenosine receptor agonists in a new model of epilepsy-seizures evoked by mitochondrial toxin, 3-nitropropionic acid, in mice. Neurosci. Lett. 2001, 305:91-94.