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A1 Adenosine Receptor Activation Modulates Central Nervous System Development and Repair

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Abstract

Adenosine is an endogenous, autacoid purine nucleoside which performs many important biological roles, particularly during stressful events. Adenosine can signal through four adenosine receptor (AR) subtypes: A1, A2A, A2B, and A3. Of these, adenosine A1 receptor (A1AR) has a broad, wide distribution throughout different vertebrate cell types and the highest affinity to adenosine. The A1AR-dependent action of adenosine is well documented in reports from numerous studies that have used different selective A1AR agonists and antagonists as well as in animals that have a genetically manipulated A1AR gene. Despite its wide distribution and function, A1AR homo/hetero-oligomerization with other adenosine and non-adenosine receptors extends its biological role during developmental, physiological, and pathological situations. In this review, we initially discuss the A1AR structure and most important signaling pathway triggered by its activation. Next, we summarize some of the most well-known biological effects of A1AR in the central nervous system (CNS) during development and adulthood, in addition to its role in nervous system regeneration and repair.

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References

  1. Engler RL (1991) Adenosine. The signal of life? Circulation 84(2):951–954

    Article  CAS  PubMed  Google Scholar 

  2. Mullane K, Bullough D (1995) Harnessing an endogenous cardioprotective mechanism: cellular sources and sites of action of adenosine. J Mol Cell Cardiol 27(4):1041–1054

    Article  CAS  PubMed  Google Scholar 

  3. Park J, Gupta RS (2013) Adenosine metabolism, adenosine kinase, and evolution. In: Adenosine. Springer. pp. 23–54

  4. Latini S, Pedata F (2001) Adenosine in the central nervous system: release mechanisms and extracellular concentrations. J Neurochem 79(3):463–484

    Article  CAS  PubMed  Google Scholar 

  5. Burnstock G et al (2010) The birth and postnatal development of purinergic signalling. Acta Physiol 199(2):93–147

    Article  CAS  Google Scholar 

  6. Fredholm BB et al (2011) International Union of Basic and Clinical Pharmacology. LXXXI. Nomenclature and classification of adenosine receptors—an update. Pharmacol Rev 63(1):1–34

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Pasini FL, Capecchi P, Di Perri T (2000) Adenosine and chronic ischemia of the lower limbs. Vasc Med 5(4):243–250

    Article  CAS  PubMed  Google Scholar 

  8. Ren H, Stiles GL (1994) Characterization of the human A1 adenosine receptor gene. Evidence for alternative splicing. J Biol Chem 269(4):3104–3110

    CAS  PubMed  Google Scholar 

  9. Linden J, et al. (1987) Agonist and antagonist radioligands and photoaffinity labels for the adenosine A1 receptor. In: Topics and perspectives in adenosine research. Springer. pp. 3–14

  10. Latek D et al (2012) G protein-coupled receptors—recent advances. Acta Biochim Pol 59(4):515–529

    CAS  PubMed  PubMed Central  Google Scholar 

  11. Gilman AG (1987) G proteins: transducers of receptor-generated signals. Annu Rev Biochem 56(1):615–649

    Article  CAS  PubMed  Google Scholar 

  12. Libert F et al (1991) The orphan receptor cDNA RDC7 encodes an A1 adenosine receptor. EMBO J 10(7):1677

    CAS  PubMed  PubMed Central  Google Scholar 

  13. Townsend-Nicholson A, Schofield PR (1994) A threonine residue in the seventh transmembrane domain of the human A1 adenosine receptor mediates specific agonist binding. J Biol Chem 269(4):2373–2376

    CAS  PubMed  Google Scholar 

  14. Olah ME et al (1992) Cloning, expression, and characterization of the unique bovine A1 adenosine receptor. Studies on the ligand binding site by site-directed mutagenesis. J Biol Chem 267(15):10764–10770

    CAS  PubMed  PubMed Central  Google Scholar 

  15. Rivkees SA, Lasbury ME, Barbhaiya H (1995) Identification of domains of the human A1 adenosine receptor that are important for binding receptor subtype-selective ligands using chimeric A1/A2a adenosine receptors. J Biol Chem 270(35):20485–20490

    Article  CAS  PubMed  Google Scholar 

  16. Libert F et al (1991) Chromosomal mapping of A1 and A2 adenosine receptors, VIP receptor, and a new subtype of serotonin receptor. Genomics 11(1):225–227

    Article  CAS  PubMed  Google Scholar 

  17. Mahan LC et al (1991) Cloning and expression of an A1 adenosine receptor from rat brain. Mol Pharmacol 40(1):1–7

    CAS  PubMed  Google Scholar 

  18. Ren H, Stiles GL (1994) Posttranscriptional mRNA processing as a mechanism for regulation of human A1 adenosine receptor expression. Proc Natl Acad Sci 91(11):4864–4866

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Ren H, Stiles GL (1995) Separate promoters in the human A1 adenosine receptor gene direct the synthesis of distinct messenger RNAs that regulate receptor abundance. Mol Pharmacol 48(6):975–980

    CAS  PubMed  Google Scholar 

  20. Ren H, Stiles GL (1999) Dexamethasone stimulates human A1 adenosine receptor (A1AR) gene expression through multiple regulatory sites in promoter B. Mol Pharmacol 55(2):309–316

    CAS  PubMed  Google Scholar 

  21. Nie Z et al (1998) Oxidative stress increases A1 adenosine receptor expression by activating nuclear factor κB. Mol Pharmacol 53(4):663–669

    CAS  PubMed  Google Scholar 

  22. Cordeaux Y, IJzerman AP, Hill SJ (2004) Coupling of the human A1 adenosine receptor to different heterotrimeric G proteins: evidence for agonist-specific G protein activation. Br J Pharmacol 143(6):705–714

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Gerwins P, Fredholm B (1992) ATP and its metabolite adenosine act synergistically to mobilize intracellular calcium via the formation of inositol 1,4,5-trisphosphate in a smooth muscle cell line. J Biol Chem 267(23):16081–16087

    CAS  PubMed  Google Scholar 

  24. Iredale PA, Alexander SP, Hill SJ (1994) Coupling of a transfected human brain A1 adenosine receptor in CHO-K1 cells to calcium mobilisation via a pertussis toxin-sensitive mechanism. Br J Pharmacol 111(4):1252–1256

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Sabourin J et al (2012) Activation of transient receptor potential canonical 3 (TRPC3)-mediated Ca2+ entry by A1 adenosine receptor in cardiomyocytes disturbs atrioventricular conduction. J Biol Chem 287(32):26688–26701

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Robin E et al (2011) Adenosine A1 receptor activation is arrhythmogenic in the developing heart through NADPH oxidase/ERK-and PLC/PKC-dependent mechanisms. J Mol Cell Cardiol 51(6):945–954

    Article  CAS  PubMed  Google Scholar 

  27. Jeong H-J et al (2003) Adenosine A1 receptor-mediated presynaptic inhibition of GABAergic transmission in immature rat hippocampal CA1 neurons. J Neurophysiol 89(3):1214–1222

    Article  CAS  PubMed  Google Scholar 

  28. Li Y et al (2011) Adenosine modulates the excitability of layer II stellate neurons in entorhinal cortex through A1 receptors. Hippocampus 21(3):265–280

    Article  PubMed  CAS  Google Scholar 

  29. Dickenson JM, Blank JL, Hill SJ (1998) Human adenosine A1 receptor and P2Y2-purinoceptor-mediated activation of the mitogen-activated protein kinase cascade in transfected CHO cells. Br J Pharmacol 124(7):1491–1499

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Saura C et al (1996) Adenosine deaminase interacts with A1 adenosine receptors in pig brain cortical membranes. J Neurochem 66(4):1675–1682

    Article  CAS  PubMed  Google Scholar 

  31. Ciruela F et al (1996) Adenosine deaminase affects ligand-induced signalling by interacting with cell surface adenosine receptors. FEBS Lett 380(3):219–223

    Article  CAS  PubMed  Google Scholar 

  32. Saura CA et al (1998) Adenosine deaminase and A1 adenosine receptors internalize together following agonist-induced receptor desensitization. J Biol Chem 273(28):17610–17617

    Article  CAS  PubMed  Google Scholar 

  33. Escriche M et al (2003) Ligand-induced caveolae-mediated internalization of A 1 adenosine receptors: morphological evidence of endosomal sorting and receptor recycling. Exp Cell Res 285(1):72–90

    Article  CAS  PubMed  Google Scholar 

  34. Garrido C et al (2012) The small heat shock proteins family: the long forgotten chaperones. Int J Biochem Cell Biol 44(10):1588–1592

    Article  CAS  PubMed  Google Scholar 

  35. Sarrió S et al (2000) The heat shock cognate protein hsc73 assembles with A1 adenosine receptors to form functional modules in the cell membrane. Mol Cell Biol 20(14):5164–5174

    Article  PubMed  PubMed Central  Google Scholar 

  36. Dongcheng L et al (2004) Cytoskeletal protein 4.1 G binds to the third intracellular loop of the A1 adenosine receptor and inhibits receptor action. Biochem J 377(1):51–59

    Article  Google Scholar 

  37. Prinster SC, Hague C, Hall RA (2005) Heterodimerization of G protein-coupled receptors: specificity and functional significance. Pharmacol Rev 57(3):289–298

    Article  CAS  PubMed  Google Scholar 

  38. Milligan G (2009) G protein-coupled receptor hetero-dimerization: contribution to pharmacology and function. Br J Pharmacol 158(1):5–14

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Kamal M, Jockers R (2011) Biological significance of GPCR heteromerization in the neuro-endocrine system. Frontiers Endocrinol 2

  40. Ciruela F et al (1995) Immunological identification of A1 adenosine receptors in brain cortex. J Neurosci Res 42(6):818–828

    Article  CAS  PubMed  Google Scholar 

  41. Gracia E et al (2013) Homodimerization of adenosine A 1 receptors in brain cortex explains the biphasic effects of caffeine. Neuropharmacology 71:56–69

    Article  CAS  PubMed  Google Scholar 

  42. Ciruela F et al (2006) Presynaptic control of striatal glutamatergic neurotransmission by adenosine A1–A2A receptor heteromers. J Neurosci 26(7):2080–2087

    Article  CAS  PubMed  Google Scholar 

  43. Yoshioka K, Saitoh O, Nakata H (2001) Heteromeric association creates a P2Y-like adenosine receptor. Proc Natl Acad Sci 98(13):7617–7622

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Yoshioka K et al (2002) Hetero-oligomerization of adenosine A 1 receptors with P2Y 1 receptors in rat brains. FEBS Lett 531(2):299–303

    Article  CAS  PubMed  Google Scholar 

  45. Yoshioka K, Saitoh O, Nakata H (2002) Agonist-promoted heteromeric oligomerization between adenosine A 1 and P2Y 1 receptors in living cells. FEBS Lett 523(1):147–151

    Article  CAS  PubMed  Google Scholar 

  46. Tonazzini I et al (2007) Co-localization and functional cross-talk between A1 and P2Y1 purine receptors in rat hippocampus. Eur J Neurosci 26(4):890–902

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Suzuki T et al (2006) Regulation of pharmacology by hetero-oligomerization between A 1 adenosine receptor and P2Y 2 receptor. Biochem Biophys Res Commun 351(2):559–565

    Article  CAS  PubMed  Google Scholar 

  48. Chandrasekera PC et al (2013) Adenosine A 1 receptors heterodimerize with β 1-and β 2-adrenergic receptors creating novel receptor complexes with altered G protein coupling and signaling. Cell Signal 25(4):736–742

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Ciruela F et al (2001) Metabotropic glutamate 1α and adenosine A1 receptors assemble into functionally interacting complexes. J Biol Chem 276(21):18345–18351

    Article  CAS  PubMed  Google Scholar 

  50. Kamikubo Y et al (2013) Functional cooperation of metabotropic adenosine and glutamate receptors regulates postsynaptic plasticity in the cerebellum. J Neurosci 33(47):18661–18671

    Article  CAS  PubMed  Google Scholar 

  51. Kamikubo Y et al (2015) Complex formation and functional interaction between adenosine A1 receptor and type-1 metabotropic glutamate receptor. J Pharmacol Sci 128(3):125–130

    Article  CAS  PubMed  Google Scholar 

  52. Ferré S et al (1998) Adenosine A1 receptor-mediated modulation of dopamine D1 receptors in stably cotransfected fibroblast cells. J Biol Chem 273(8):4718–4724

    Article  PubMed  Google Scholar 

  53. Ginés S et al (2000) Dopamine D1 and adenosine A1 receptors form functionally interacting heteromeric complexes. Proc Natl Acad Sci 97(15):8606–8611

    Article  PubMed  PubMed Central  Google Scholar 

  54. Torvinen M et al (2002) Interactions among adenosine deaminase, adenosine A 1 receptors and dopamine D 1 receptors in stably cotransfected fibroblast cells and neurons. Neuroscience 113(3):709–719

    Article  CAS  PubMed  Google Scholar 

  55. Toda S, Alguacil LF, Kalivas PW (2003) Repeated cocaine administration changes the function and subcellular distribution of adenosine A1 receptor in the rat nucleus accumbens. J Neurochem 87(6):1478–1484

    Article  CAS  PubMed  Google Scholar 

  56. Heiss W-D, Herholz K (2006) Brain receptor imaging. J Nucl Med 47(2):302–312

    CAS  PubMed  Google Scholar 

  57. Bauer A et al (2003) In vivo imaging of adenosine A 1 receptors in the human brain with [18 F] CPFPX and positron emission tomography. NeuroImage 19(4):1760–1769

    Article  PubMed  Google Scholar 

  58. Fukumitsu N et al (2005) Adenosine A1 receptor mapping of the human brain by PET with 8-dicyclopropylmethyl-1-11C-methyl-3-propylxanthine. J Nucl Med 46(1):32–37

    PubMed  Google Scholar 

  59. Svenningsson P et al (1997) Distribution of adenosine receptors in the postmortem human brain: an extended autoradiographic study. Synapse 27(4):322–335

    Article  CAS  PubMed  Google Scholar 

  60. Swanson TH, Drazba JA, Rivkees SA (1995) Adenosine A1 receptors are located predominantly on axons in the rat hippocampal formation. J Comp Neurol 363(4):517–531

    Article  CAS  PubMed  Google Scholar 

  61. Tetzlaff W, Schubert P, Kreutzberg G (1987) Synaptic and extrasynaptic localization of adenosine binding sites in the rat hippocampus. Neuroscience 21(3):869–875

    Article  CAS  PubMed  Google Scholar 

  62. Rebola N et al (2003) Subcellular localization of adenosine A 1 receptors in nerve terminals and synapses of the rat hippocampus. Brain Res 987(1):49–58

    Article  CAS  PubMed  Google Scholar 

  63. Kawamura M, Ruskin DN, Masino SA (2010) Metabolic autocrine regulation of neurons involves cooperation among pannexin hemichannels, adenosine receptors, and KATP channels. J Neurosci 30(11):3886–3895

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Trussell L, Jackson M (1987) Dependence of an adenosine-activated potassium current on a GTP-binding protein in mammalian central neurons. J Neurosci 7(10):3306–3316

    CAS  PubMed  Google Scholar 

  65. Clark BD, Kurth-Nelson ZL, Newman EA (2009) Adenosine-evoked hyperpolarization of retinal ganglion cells is mediated by G-protein-coupled inwardly rectifying K+ and small conductance Ca2+-activated K+ channel activation. J Neurosci 29(36):11237–11245

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Hawryluk JM et al (2012) Adenosine inhibits glutamatergic input to basal forebrain cholinergic neurons. J Neurophysiol 107(10):2769–2781

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Floran B et al (2002) Adenosine A1 receptors control dopamine D1-dependent [3 H] GABA release in slices of substantia nigra pars reticulata and motor behavior in the rat. Neuroscience 115(3):743–751

    Article  CAS  PubMed  Google Scholar 

  68. Okada M et al (1997) Effects of adenosine receptor subtypes on hippocampal extracellular serotonin level and serotonin reuptake activity. J Neurochem 69(6):2581–2588

    Article  CAS  PubMed  Google Scholar 

  69. Oishi Y et al (2008) Adenosine in the tuberomammillary nucleus inhibits the histaminergic system via A1 receptors and promotes non-rapid eye movement sleep. Proc Natl Acad Sci 105(50):19992–19997

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Ross AE, Venton BJ (2015) Adenosine transiently modulates stimulated dopamine release in the caudate–putamen via A1 receptors. J Neurochem 132(1):51–60

    Article  CAS  PubMed  Google Scholar 

  71. O'Neill C et al (2007) Adenosine A1 receptor-mediated inhibition of dopamine release from rat striatal slices is modulated by D1 dopamine receptors. Eur J Neurosci 26(12):3421–3428

    Article  PubMed  Google Scholar 

  72. Porkka-Heiskanen T, Kalinchuk AV (2011) Adenosine as a sleep factor. Sleep and Biological Rhythms 9(s1):18–23

    Article  Google Scholar 

  73. Thakkar MM, Winston S, McCarley RW (2003) A1 receptor and adenosinergic homeostatic regulation of sleep-wakefulness: effects of antisense to the A1 receptor in the cholinergic basal forebrain. J Neurosci 23(10):4278–4287

    CAS  PubMed  PubMed Central  Google Scholar 

  74. Elmenhorst D et al (2007) Sleep deprivation increases A1 adenosine receptor binding in the human brain: a positron emission tomography study. J Neurosci 27(9):2410–2415

    Article  CAS  PubMed  Google Scholar 

  75. Arrigoni E et al (2006) Adenosine inhibits basal forebrain cholinergic and noncholinergic neurons in vitro. Neuroscience 140(2):403–413

    Article  CAS  PubMed  Google Scholar 

  76. Liu Z-W, Gao X-B (2007) Adenosine inhibits activity of hypocretin/orexin neurons by the A1 receptor in the lateral hypothalamus: a possible sleep-promoting effect. J Neurophysiol 97(1):837–848

    Article  CAS  PubMed  Google Scholar 

  77. Thakkar MM (2011) Histamine in the regulation of wakefulness. Sleep Med Rev 15(1):65–74

    Article  PubMed  Google Scholar 

  78. Methippara MM et al (2005) Effects on sleep of microdialysis of adenosine A1 and A2a receptor analogs into the lateral preoptic area of rats. Am J Phys Regul Integr Comp Phys 289(6):R1715–R1723

    CAS  Google Scholar 

  79. Luongo L et al (2014) The A1 adenosine receptor as a new player in microglia physiology. Glia 62(1):122–132

    Article  CAS  PubMed  Google Scholar 

  80. Alloisio S et al (2004) Differential modulation of ATP-induced calcium signalling by A1 and A2 adenosine receptors in cultured cortical astrocytes. Br J Pharmacol 141(6):935–942

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Othman T, Yan H, Rivkees SA (2003) Oligodendrocytes express functional A1 adenosine receptors that stimulate cellular migration. Glia 44(2):166–172

    Article  PubMed  Google Scholar 

  82. Group CS (2008) Maternal caffeine intake during pregnancy and risk of fetal growth restriction: a large prospective observational study. BMJ: Br Med J 337

  83. Rivkees SA (1995) The ontogeny of cardiac and neural A1 adenosine receptor expression in rats. Dev Brain Res 89(2):202–213

    Article  CAS  Google Scholar 

  84. Ådén U et al (2001) Adenosine A 1 receptor agonism in the immature rat brain and heart. Eur J Pharmacol 426(3):185–192

    Article  PubMed  Google Scholar 

  85. Stevens B et al (2002) Adenosine: a neuron-glial transmitter promoting myelination in the CNS in response to action potentials. Neuron 36(5):855–868

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Thevananther S, Rivera A, Rivkees SA (2001) A1 adenosine receptor activation inhibits neurite process formation by Rho kinase-mediated pathways. Neuroreport 12(14):3057–3063

    Article  CAS  PubMed  Google Scholar 

  87. León D et al (2002) Adenosine A1 receptor down-regulation in mothers and fetal brain after caffeine and theophylline treatments to pregnant rats. J Neurochem 82(3):625–634

    Article  PubMed  Google Scholar 

  88. Kranenburg O et al (1999) Activation of RhoA by lysophosphatidic acid and Gα12/13 subunits in neuronal cells: induction of neurite retraction. Mol Biol Cell 10(6):1851–1857

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Bashaw GJ, Klein R (2010) Signaling from axon guidance receptors. Cold Spring Harb Perspect Biol 2(5):a001941

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  90. Brunet I et al (2005) The transcription factor engrailed-2 guides retinal axons. Nature 438(7064):94–98

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Wizenmann A et al (2009) Extracellular engrailed participates in the topographic guidance of retinal axons in vivo. Neuron 64(3):355–366

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Stettler O et al (2012) Engrailed homeoprotein recruits the adenosine A1 receptor to potentiate ephrin A5 function in retinal growth cones. Development 139(1):215–224

    Article  CAS  PubMed  Google Scholar 

  93. Baumann N, Pham-Dinh D (2001) Biology of oligodendrocyte and myelin in the mammalian central nervous system. Physiol Rev 81(2):871–927

    CAS  PubMed  Google Scholar 

  94. Turner CP et al (2003) A1 adenosine receptors mediate hypoxia-induced ventriculomegaly. Proc Natl Acad Sci 100(20):11718–11722

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Damkier HH, Brown PD, Praetorius J (2013) Cerebrospinal fluid secretion by the choroid plexus. Physiol Rev 93(4):1847–1892

    Article  CAS  PubMed  Google Scholar 

  96. Lankford AR et al (2002) Gene expression profile of mouse myocardium with transgenic overexpression of A1 adenosine receptors. Physiol Genomics 11(2):81–89

    Article  CAS  PubMed  Google Scholar 

  97. Han M-E et al (2009) Regulation of cerebrospinal fluid production by caffeine consumption. BMC Neurosci 10(1):110

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  98. Back SA et al (2006) Protective effects of caffeine on chronic hypoxia-induced perinatal white matter injury. Ann Neurol 60(6):696–705

    Article  CAS  PubMed  Google Scholar 

  99. Kim M et al (2005) Susceptibility of the developing brain to acute hypoglycemia involving A1 adenosine receptor activation. American Journal of Physiology-Endocrinology and Metabolism 289(4):E562–E569

    Article  CAS  PubMed  Google Scholar 

  100. Brown P, Dale N (2000) Adenosine A1 receptors modulate high voltage-activated Ca2+ currents and motor pattern generation in the Xenopus embryo. J Physiol 525(3):655–667

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Kochanek PM et al (2006) Adenosine A1 receptor knockout mice develop lethal status epilepticus after experimental traumatic brain injury. J Cereb Blood Flow Metab 26(4):565–575

    Article  CAS  PubMed  Google Scholar 

  102. Fredholm B (2007) Adenosine, an endogenous distress signal, modulates tissue damage and repair. Cell Death & Differentiation 14(7):1315–1323

    Article  CAS  Google Scholar 

  103. Güttinger M et al (2005) Seizure suppression and lack of adenosine A 1 receptor desensitization after focal long-term delivery of adenosine by encapsulated myoblasts. Exp Neurol 193(1):53–64

    Article  PubMed  CAS  Google Scholar 

  104. Fedele DE et al (2006) Adenosine A 1 receptors are crucial in keeping an epileptic focus localized. Exp Neurol 200(1):184–190

    Article  CAS  PubMed  Google Scholar 

  105. Palomero-Gallagher N et al (2012) Multireceptor analysis in human neocortex reveals complex alterations of receptor ligand binding in focal epilepsies. Epilepsia 53(11):1987–1997

    Article  CAS  PubMed  Google Scholar 

  106. Akula KK, Kulkarni S (2014) Effect of curcumin against pentylenetetrazol-induced seizure threshold in mice: possible involvement of adenosine A1 receptors. Phytother Res 28(5):714–721

    Article  CAS  PubMed  Google Scholar 

  107. Wagner AK et al (2010) Adenosine A1 receptor gene variants associated with post-traumatic seizures after severe TBI. Epilepsy Res 90(3):259–272

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Tsutsui S et al (2004) A1 adenosine receptor upregulation and activation attenuates neuroinflammation and demyelination in a model of multiple sclerosis. J Neurosci 24(6):1521–1529

    Article  CAS  PubMed  Google Scholar 

  109. Asghari AA, Mirnajafi-Zadeh SJ, Javan M (2012) Effect of the adenosine A1 receptor agonist on demyelination and remyelination processes in lysolecithin induced demyelination in rat optic chiasm. KAUMS Journal (FEYZ) 16(1):1–8

    Google Scholar 

  110. Mayne M et al (1999) Dysregulation of adenosine A1 receptor-mediated cytokine expression in peripheral blood mononuclear cells from multiple sclerosis patients. Ann Neurol 45(5):633–639

    Article  CAS  PubMed  Google Scholar 

  111. Johnston JB et al (2001) Diminished adenosine A1 receptor expression on macrophages in brain and blood of patients with multiple sclerosis. Ann Neurol 49(5):650–658

    Article  CAS  PubMed  Google Scholar 

  112. Chen GQ et al (2010) Chronic caffeine treatment attenuates experimental autoimmune encephalomyelitis induced by guinea pig spinal cord homogenates in Wistar rats. Brain Res 1309:116–125

    Article  CAS  PubMed  Google Scholar 

  113. Jahromi SR et al (2012) Dietary pattern and risk of multiple sclerosis. Iranian journal of neurology 11(2):47

    PubMed  PubMed Central  Google Scholar 

  114. Hedström A et al (2016) High consumption of coffee is associated with decreased multiple sclerosis risk; results from two independent studies. J Neurol Neurosurg Psychiatry. doi:10.1136/jnnp-2015-312176

    PubMed  PubMed Central  Google Scholar 

  115. Svenningsson P, Fredholm BB (1997) Glucocorticoids regulate the expression of adenosine A1 but not A2A receptors in rat brain. J Pharmacol Exp Ther 280(2):1094–1101

    CAS  PubMed  Google Scholar 

  116. Migita H et al (2008) Activation of adenosine A1 receptor-induced neural stem cell proliferation via MEK/ERK and Akt signaling pathways. J Neurosci Res 86(13):2820–2828

    Article  CAS  PubMed  Google Scholar 

  117. Alvarez-Buylla A, García-Verdugo JM, Tramontin AD (2001) A unified hypothesis on the lineage of neural stem cells. Nat Rev Neurosci 2(4):287–293

    Article  CAS  PubMed  Google Scholar 

  118. Götz M, Huttner WB (2005) The cell biology of neurogenesis. Nat Rev Mol Cell Biol 6(10):777–788

    Article  PubMed  CAS  Google Scholar 

  119. Sim FJ et al (2002) The age-related decrease in CNS remyelination efficiency is attributable to an impairment of both oligodendrocyte progenitor recruitment and differentiation. J Neurosci 22(7):2451–2459

    CAS  PubMed  Google Scholar 

  120. Coppi E et al (2013) Adenosine A 2A receptors inhibit delayed rectifier potassium currents and cell differentiation in primary purified oligodendrocyte cultures. Neuropharmacology 73:301–310

    Article  CAS  PubMed  Google Scholar 

  121. Chittajallu R et al (2002) Regulation of Kv1 subunit expression in oligodendrocyte progenitor cells and their role in G1/S phase progression of the cell cycle. Proc Natl Acad Sci 99(4):2350–2355

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. Vautier F et al (2004) Shaker-type potassium channel subunits differentially control oligodendrocyte progenitor proliferation. Glia 48(4):337–345

    Article  PubMed  Google Scholar 

  123. Daniele S et al (2014) Modulation of A1 and A2B adenosine receptor activity: a new strategy to sensitise glioblastoma stem cells to chemotherapy. Cell Death Dis 5(11):e1539

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  124. Schaddelee MP et al (2005) Pharmacokinetic/pharmacodynamic modelling of the anti-hyperalgesic and anti-nociceptive effect of adenosine A 1 receptor partial agonists in neuropathic pain. Eur J Pharmacol 514(2):131–140

    Article  CAS  PubMed  Google Scholar 

  125. Luongo L et al (2012) 5′-Chloro-5′-deoxy-(±)-ENBA, a potent and selective adenosine A1 receptor agonist, alleviates neuropathic pain in mice through functional glial and microglial changes without affecting motor or cardiovascular functions. Molecules 17(12):13712–13726

    Article  CAS  PubMed  Google Scholar 

  126. Poon A, Sawynok J (1998) Antinociception by adenosine analogs and inhibitors of adenosine metabolism in an inflammatory thermal hyperalgesia model in the rat. Pain 74(2):235–245

    Article  CAS  PubMed  Google Scholar 

  127. Nascimento FP et al (2014) Adenosine A1 receptor-dependent antinociception induced by inosine in mice: pharmacological, genetic and biochemical aspects. Mol Neurobiol 51(3):1368–1378

    Article  PubMed  CAS  Google Scholar 

  128. Gao X et al (2014) Norisoboldine attenuates inflammatory pain via the adenosine A1 receptor. Eur J Pain 18(7):939–948

    Article  CAS  PubMed  Google Scholar 

  129. Wu W-P et al (2005) Increased nociceptive response in mice lacking the adenosine A 1 receptor. Pain 113(3):395–404

    Article  CAS  PubMed  Google Scholar 

  130. Johansson B et al (2001) Hyperalgesia, anxiety, and decreased hypoxic neuroprotection in mice lacking the adenosine A1 receptor. Proc Natl Acad Sci 98(16):9407–9412

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  131. Lima FO et al (2010) Direct blockade of inflammatory hypernociception by peripheral A1 adenosine receptors: involvement of the NO/cGMP/PKG/KATP signaling pathway. Pain 151(2):506–515

    Article  CAS  PubMed  Google Scholar 

  132. Cunha TM et al (2010) Morphine peripheral analgesia depends on activation of the PI3Kγ/AKT/nNOS/NO/KATP signaling pathway. Proc Natl Acad Sci 107(9):4442–4447

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  133. Korboukh I et al (2012) Orally active adenosine A1 receptor agonists with antinociceptive effects in mice. J Med Chem 55(14):6467–6477

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  134. Franchetti P et al (2009) N 6-Cycloalkyl-and N 6-bicycloalkyl-C 5′(C 2′)-modified adenosine derivatives as high-affinity and selective agonists at the human A1 adenosine receptor with antinociceptive effects in mice. J Med Chem 52(8):2393–2406

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Cellular Biotechnology, Cell Science Research Center, Royan Institute for Biotechnology, ACECR, Isfahan, Iran

    Shirin Kashfi, Kamran Ghaedi & Mohammad Hossein Nasr-Esfahani

  2. Department of Developmental Biology, University of Science and Culture, Tehran, Iran

    Shirin Kashfi & Hossein Baharvand

  3. Department of Biology, School of Sciences, University of Isfahan, Isfahan, Iran

    Kamran Ghaedi

  4. Department of Stem Cells and Developmental Biology, Cell Science Research Center, Royan Institute for Stem Cell Biology and Technology, ACECR, Tehran, Iran

    Hossein Baharvand & Mohammad Javan

  5. Department of Physiology, Faculty of Medical Sciences, Tarbiat Modares University, Tehran, Iran

    Mohammad Javan

Authors
  1. Shirin Kashfi
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  2. Kamran Ghaedi
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  3. Hossein Baharvand
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  4. Mohammad Hossein Nasr-Esfahani
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  5. Mohammad Javan
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Correspondence to Mohammad Hossein Nasr-Esfahani or Mohammad Javan.

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Kashfi, S., Ghaedi, K., Baharvand, H. et al. A1 Adenosine Receptor Activation Modulates Central Nervous System Development and Repair. Mol Neurobiol 54, 8128–8139 (2017). https://doi.org/10.1007/s12035-016-0292-6

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  • DOI: https://doi.org/10.1007/s12035-016-0292-6

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