Roles of adenosine and its receptors in sleep-wake regulation

International Review of Neurobiology

Volumn 119, Issue , 2014, Pages 349-371

  Huang, Zhi Li ^a   Zhang, Ze ^a   Qu, Wei Min ^a  

^a FUDAN UNIVERSITY   (China)

Author keywords

Adenosine; Knockout mice; Receptor; Sleep; Wakefulness

Indexed keywords

ADENOSINE; ADENOSINE A1 RECEPTOR; ADENOSINE A2A RECEPTOR; ADENOSINE A2B RECEPTOR; ADENOSINE A3 RECEPTOR; ADENOSINE DEAMINASE; ADENOSINE KINASE; ADENOSINE RECEPTOR; ADENOSINE TRIPHOSPHATE; ADENOSYLHOMOCYSTEINASE; PROSTAGLANDIN D SYNTHASE; PROSTAGLANDIN D2; SNARE PROTEIN;

4 AMINOBUTYRIC ACID RELEASE; ADENOSINE METABOLISM; ADENOSINE TRANSPORT; ARTICLE; BIOSYNTHESIS; CENTRAL NERVOUS SYSTEM; EXTRACELLULAR SPACE; FOREBRAIN; HOMEOSTASIS; HUMAN; MOLECULAR DYNAMICS; NEUROMODULATION; NEUROPHYSIOLOGY; NONHUMAN; NONREM SLEEP; NUCLEUS ACCUMBENS; OPTOGENETICS; PREOPTIC AREA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PURINE METABOLISM; REM SLEEP; SIGNAL TRANSDUCTION; SLEEP DEPRIVATION; SLEEP INDUCTION; SLEEP WAKING CYCLE; SLOW WAVE SLEEP; TRANSPORT AT THE CELLULAR LEVEL; VENTRAL TEGMENTUM; VENTROLATERAL PREOPTIC; ANIMAL; BRAIN; DRUG EFFECTS; METABOLISM; PHYSIOLOGY; SLEEP; WAKEFULNESS;

ADENOSINE; ANIMALS; BRAIN; HUMANS; RECEPTORS, PURINERGIC P1; SLEEP; WAKEFULNESS;

EID: 84906776227     PISSN: 00747742     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-12-801022-8.00014-3     Document Type: Chapter

References (100)

1. Arrigoni E., Chamberlin N., Saper C., McCarley R. Adenosine inhibits basal forebrain cholinergic and noncholinergic neurons in vitro. Neuroscience 2006, 140(2):403-413.
2. Basheer R., Bauer A., Elmenhorst D., Ramesh V., McCarley R.W. Sleep deprivation upregulates A1 adenosine receptors in the rat basal forebrain. Neuroreport 2007, 18(18):1895-1899.
3. Basheer R., Strecker R.E., Thakkar M.M., McCarley R.W. Adenosine and sleep-wake regulation. Progress in Neurobiology 2004, 73(6):379-396.
4. Benington J.H., Kodali S.K., Heller H.C. Stimulation of A1 adenosine receptors mimics the electroencephalographic effects of sleep deprivation. Brain Research 1995, 692(1-2):79-85.
5. Blanco-Centurion C., Xu M., Murillo-Rodriguez E., Gerashchenko D., Shiromani A.M., Salin-Pascual R.J., et al. Adenosine and sleep homeostasis in the basal forebrain. The Journal of Neuroscience 2006, 26(31):8092-8100.
6. Borb A.A., Achermann P. Sleep homeostasis and models of sleep regulation. Journal of Biological Rhythms 1999, 14(6):559-570.
7. Brundege J.M., Diao L., Proctor W.R., Dunwiddie T.V. The role of cyclic AMP as a precursor of extracellular adenosine in the rat hippocampus. Neuropharmacology 1997, 36(9):1201-1210.
8. Burnstock G. Physiology and pathophysiology of purinergic neurotransmission. Physiological Reviews 2007, 87(2):659-797.
9. Christie M.A., Bolortuya Y., Chen L.C., McKenna J.T., McCarley R.W., Strecker R.E. Microdialysis elevation of adenosine in the basal forebrain produces vigilance impairments in the rat psychomotor vigilance task. Sleep 2008, 31(10):1393.
10. Deussen A., Lloyd H.G., Schrader J. Contribution of S-adenosylhomocysteine to cardiac adenosine formation. Journal of Molecular and Cellular Cardiology 1989, 21(8):773-782.
11. Dunwiddie T.V., Masino S.A. The role and regulation of adenosine in the central nervous system. Annual Review of Neuroscience 2001, 24(1):31-55.
12. Durieux P.F., Bearzatto B., Guiducci S., Buch T., Waisman A., Zoli M., et al. D2R striatopallidal neurons inhibit both locomotor and drug reward processes. Nature Neuroscience 2009, 12(4):393-395.
13. Elmenhorst D., Basheer R., McCarley R.W., Bauer A. Sleep deprivation increases A(1) adenosine receptor density in the rat brain. Brain Research 2009, 1258:53-58.
14. Elmenhorst D., Meyer P.T., Winz O.H., Matusch A., Ermert J., Coenen H.H., et al. Sleep deprivation increases A1 adenosine receptor binding in the human brain: A positron emission tomography study. The Journal of Neuroscience 2007, 27(9):2410-2415.
15. El Yacoubi M., Ledent C., Parmentier M., Costentin J., Vaugeois J.M. Caffeine reduces hypnotic effects of alcohol through adenosine A2A receptor blockade. Neuropharmacology 2003, 45(7):977-985.
16. Feldberg W., Sherwood S. Injections of drugs into the lateral ventricle of the cat. The Journal of Physiology 1954, 123(1):148-167.
17. Ferre S., Diamond I., Goldberg S.R., Yao L., Hourani S.M., Huang Z.L., et al. Adenosine A2A receptors in ventral striatum, hypothalamus and nociceptive circuitry implications for drug addiction, sleep and pain. Progress in Neurobiology 2007, 83(5):332-347.
18. Franken P., Chollet D., Tafti M. The homeostatic regulation of sleep need is under genetic control. The Journal of Neuroscience 2001, 21(8):2610-2621.
19. Fredholm B.B. Adenosine, an endogenous distress signal, modulates tissue damage and repair. Cell Death and Differentiation 2007, 14(7):1315-1323.
20. Fredholm B.B., Chen J.F., Cunha R.A., Svenningsson P., Vaugeois J.M. Adenosine and brain function. International Review of Neurobiology 2005, 63:191-270.
21. 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. Pharmacological Reviews 2001, 53(4):527-552.
22. Gallopin T., Luppi P., Cauli B., Urade Y., Rossier J., Hayaishi O., et al. The endogenous somnogen adenosine excites a subset of sleep-promoting neurons via A2A receptors in the ventrolateral preoptic nucleus. Neuroscience 2005, 134(4):1377.
23. Geiger J.D., Fyda D.M. Adenosine transport in nervous system tissues. Adenosine in the nervous system 1991, 1-23. Academic Press, London.
24. Gerashchenko D., Okano Y., Urade Y., Inoué S., Hayaishi O. Strong rebound of wakefulness follows prostaglandin D2-or adenosine A2a receptor agonist-induced sleep. Journal of Sleep Research 2000, 9(1):81-87.
25. Gu J., Foga I., Parkinson F., Geiger J. Involvement of bidirectional adenosine transporters in the release of l-[3H] adenosine from rat brain synaptosomal preparations. Journal of Neurochemistry 1995, 64(5):2105-2110.
26. Halassa M.M., Florian C., Fellin T., Munoz J.R., Lee S.Y., Abel T., et al. Astrocytic modulation of sleep homeostasis and cognitive consequences of sleep loss. Neuron 2009, 61(2):213-219.
27. Hong Z.Y., Huang Z.L., Qu W.M., Eguchi N., Urade Y., Hayaishi O. An adenosine A2A receptor agonist induces sleep by increasing GABA release in the tuberomammillary nucleus to inhibit histaminergic systems in rats. Journal of Neurochemistry 2005, 92(6):1542-1549.
28. Huang Z.L., Qu W.M., Eguchi N., Chen J.F., Schwarzschild M.A., Fredholm B.B., et al. Adenosine A2A, but not A1, receptors mediate the arousal effect of caffeine. Nature Neuroscience 2005, 8(7):858-859.
29. Huang Z.L., Urade Y., Hayaishi O. Prostaglandins and adenosine in the regulation of sleep and wakefulness. Current Opinion in Pharmacology 2007, 7(1):33-38.
30. Huang Z.L., Urade Y., Hayaishi O. The role of adenosine in the regulation of sleep. Current Topics in Medicinal Chemistry 2011, 11(8):1047-1057.
31. Huston J., Haas H., Boix F., Pfister M., Decking U., Schrader J., et al. Extracellular adenosine levels in neostriatum and hippocampus during rest and activity periods of rats. Neuroscience 1996, 73(1):99-107.
32. Islam F., Watanabe Y., Morii H., Hayaishi O. Inhibition of rat brain prostaglandin D synthase by inorganic selenocompounds. Archives of Biochemistry and Biophysics 1991, 289(1):161-166.
33. Jacobson K.A., Gao Z.G. Adenosine receptors as therapeutic targets. Nature Reviews Drug Discovery 2006, 5(3):247-264.
34. Jones B.E. Glia, adenosine, and sleep. Neuron 2009, 61(2):156-157.
35. Jordan W., Tumani H., Cohrs S., Eggert S., Rodenbeck A., Brunner E., et al. Prostaglandin D synthase (beta-trace) in healthy human sleep. Sleep 2004, 27(5):867-874.
36. Jourdain P., Bergersen L.H., Bhaukaurally K., Bezzi P., Santello M., Domercq M., et al. Glutamate exocytosis from astrocytes controls synaptic strength. Nature Neuroscience 2007, 10(3):331-339.
37. Kalinchuk A., McCarley R., Porkka-Heiskanen T., Basheer R. Sleep deprivation triggers inducible nitric oxide-dependent nitric oxide production in wake-active basal forebrain neurons. The Journal of Neuroscience 2010, 30(40):13254.
38. Kalinchuk A.V., McCarley R.W., Stenberg D., Porkka-Heiskanen T., Basheer R. The role of cholinergic basal forebrain neurons in adenosine-mediated homeostatic control of sleep: Lessons from 192 IgG-saporin lesions. Neuroscience 2008, 157(1):238-253.
39. Kaur S., Junek A., Black M.A., Semba K. Effects of ibotenate and 192IgG-saporin lesions of the nucleus basalis magnocellularis/substantia innominata on spontaneous sleep and wake states and on recovery sleep after sleep deprivation in rats. The Journal of Neuroscience 2008, 28(2):491-504.
40. Latini S., Pedata F. Adenosine in the central nervous system: Release mechanisms and extracellular concentrations. Journal of Neurochemistry 2001, 79(3):463-484.
41. Lazarus M., Chen J.F., Urade Y., Huang Z.L. Role of the basal ganglia in the control of sleep and wakefulness. Current Opinion in Neurobiology 2013, 23(5):780-785.
42. Lazarus M., Huang Z.L., Lu J., Urade Y., Chen J.F. How do the basal ganglia regulate sleep-wake behavior?. Trends in Neurosciences 2012, 35(12):723-732.
43. Lazarus M., Shen H.Y., Cherasse Y., Qu W.M., Huang Z.L., Bass C.E., et al. Arousal effect of caffeine depends on adenosine A2A receptors in the shell of the nucleus accumbens. The Journal of Neuroscience 2011, 31(27):10067-10075.
44. Li C.S., Chung S., Lu D.P., Cho Y.K. Descending projections from the nucleus accumbens shell suppress activity of taste-responsive neurons in the hamster parabrachial nuclei. Journal of Neurophysiology 2012, 108(5):1288-1298.
45. Marks G., Shaffery J., Speciale S., Birabil C. Enhancement of rapid eye movement sleep in the rat by actions at A1 and A2a adenosine receptor subtypes with a differential sensitivity to atropine. Neuroscience 2003, 116(3):913-920.
46. Matsumura H., Takahata R., Hayaishi O. Inhibition of sleep in rats by inorganic selenium compounds, inhibitors of prostaglandin D synthase. Proceedings of the National Academy of Sciences of the United States of America 1991, 88(20):9046-9050.
47. McCarley R.W. Neurobiology of REM and NREM sleep. Sleep Medicine 2007, 8(4):302-330.
48. Methippara M.M., Kumar S., Alam M.N., Szymusiak R., McGinty D. Effects on sleep of microdialysis of adenosine A1 and A2a receptor analogs into the lateral preoptic area of rats. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology 2005, 289(6):R1715-R1723.
49. Missale C., Nash S.R., Robinson S.W., Jaber M., Caron M.G. Dopamine receptors: From structure to function. Physiological Reviews 1998, 78(1):189-225.
50. Mizoguchi A., Eguchi N., Kimura K., Kiyohara Y., Qu W.M., Huang Z.L., et al. Dominant localization of prostaglandin D receptors on arachnoid trabecular cells in mouse basal forebrain and their involvement in the regulation of non-rapid eye movement sleep. Proceedings of the National Academy of Sciences of the United States of America 2001, 98(20):11674-11679.
51. Mohri I., Eguchi N., Suzuki K., Urade Y., Taniike M. Hematopoietic prostaglandin D synthase is expressed in microglia in the developing postnatal mouse brain. Glia 2003, 42(3):263-274.
52. Murillo-Rodriguez E., Blanco-Centurion C., Gerashchenko D., Salin-Pascual R., Shiromani P. The diurnal rhythm of adenosine levels in the basal forebrain of young and old rats. Neuroscience 2004, 123(2):361-370.
53. Nagy J., LaBella L., Buss M., Daddona P. Immunohistochemistry of adenosine deaminase: Implications for adenosine neurotransmission. Science 1984, 224(4645):166-168.
54. Narumiya S., Ogorochi T., Nakao K., Hayaishi O. Prostaglandin D2 in rat brain, spinal cord and pituitary: Basal level and regional distribution. Life Sciences 1982, 31(19):2093.
55. Noor Alam M.D., Szymusiak R., McGinty D. Adenosinergic regulation of sleep: Multiple sites of action in the brain. Sleep 2006, 29(11):1384-1385. discussion 1387-1389.
56. Ogorochi T., Narumiya S., Mizuno N., Yamashita K., Miyazaki H., Hayaishi O. Regional distribution of prostaglandins D2, E2, and F2α and related enzymes in postmortem human brain. Journal of Neurochemistry 1984, 43(1):71-82.
57. Oishi Y., Huang Z.L., Fredholm B.B., Urade Y., Hayaishi O. Adenosine in the tuberomammillary nucleus inhibits the histaminergic system via A1 receptors and promotes non-rapid eye movement sleep. Proceedings of the National Academy of Sciences of the United States of America 2008, 105(50):19992-19997.
58. Okada T., Mochizuki T., Huang Z.L., Eguchi N., Sugita Y., Urade Y., et al. Dominant localization of adenosine deaminase in leptomeninges and involvement of the enzyme in sleep. Biochemical and Biophysical Research Communications 2003, 312(1):29-34.
59. Onoe H., Ueno R., Fujita I., Nishino H., Oomura Y., Hayaishi O. Prostaglandin D2, a cerebral sleep-inducing substance in monkeys. Proceedings of the National Academy of Sciences of the United States of America 1988, 85(11):4082-4086.
60. Pandey H.P., Ram A., Matsumura H., Hayaishi O. Concentration of prostaglandin D2 in cerebrospinal fluid exhibits a circadian alteration in conscious rats. Biochemistry and Molecular Biology International 1995, 37(3):431-437.
61. Pascual O., Casper K.B., Kubera C., Zhang J., Revilla-Sanchez R., Sul J.-Y., et al. Astrocytic purinergic signaling coordinates synaptic networks. Science 2005, 310(5745):113-116.
62. Peng L., Huang R., Yu A.C., Fung K.Y., Rathbone M.P., Hertz L. Nucleoside transporter expression and function in cultured mouse astrocytes. Glia 2005, 52(1):25-35.
63. Porkka-Heiskanen T., Strecker R.E., Thakkar M., Bjørkum A.A., Greene R.W., McCarley R.W. Adenosine: A mediator of the sleep-inducing effects of prolonged wakefulness. Science 1997, 276(5316):1265-1268.
64. Qiu M., Qu W., Xu X., Yan M., Urade Y., Huang Z. D (1)/D (2) receptor-targeting l-stepholidine, an active ingredient of the Chinese herb Stephonia, induces non-rapid eye movement sleep in mice. Pharmacology, Biochemistry, and Behavior 2009, 94(1):16.
65. Qu W.M., Huang Z.L., Xu X.H., Aritake K., Eguchi N., Nambu F., et al. Lipocalin-type prostaglandin D synthase produces prostaglandin D2 involved in regulation of physiological sleep. Proceedings of the National Academy of Sciences of the United States of America 2006, 103(47):17949-17954.
66. Qu W.M., Huang Z.L., Xu X.H., Matsumoto N., Urade Y. Dopaminergic D1 and D2 receptors are essential for the arousal effect of modafinil. The Journal of Neuroscience 2008, 28(34):8462-8469.
67. Qu W.M., Xu X.H., Yan M.M., Wang Y.Q., Urade Y., Huang Z.L. Essential role of dopamine D2 receptor in the maintenance of wakefulness, but not in homeostatic regulation of sleep, in mice. The Journal of Neuroscience 2010, 30(12):4382-4389.
68. Radek R.J., Decker M.W., Jarvis M.F. The adenosine kinase inhibitor ABT-702 augments EEG slow waves in rats. Brain Research 2004, 1026(1):74-83.
69. Radulovacki M., Virus R., Djuricic-Nedelson M., Green R. Hypnotic effects of deoxycorformycin in rats. Brain Research 1983, 271(2):392-395.
70. Rai S., Kumar S., Alam M.A., Szymusiak R., McGinty D., Alam M.N. A1 receptor mediated adenosinergic regulation of perifornical-lateral hypothalamic area neurons in freely behaving rats. Neuroscience 2010, 167(1):40.
71. Rainnie D.G., Grunze H.C., McCarley R.W., Greene R.W. Adenosine inhibition of mesopontine cholinergic neurons: Implications for EEG arousal. Science 1994, 263(5147):689.
72. Ram A., Pandey H., Matsumura H., Kasahara-Orita K., Nakajima T., Takahata R., et al. CSF levels of prostaglandins, especially the level of prostaglandin D2, are correlated with increasing propensity towards sleep in rats. Brain Research 1997, 751(1):81.
73. Retey J., Adam M., Honegger E., Khatami R., Luhmann U., Jung H., et al. A functional genetic variation of adenosine deaminase affects the duration and intensity of deep sleep in humans. Proceedings of the National Academy of Sciences of the United States of America 2005, 102(43):15676-15681.
74. Retey J., Adam M., Khatami R., Luhmann U., Jung H., Berger W., et al. A genetic variation in the adenosine A2A receptor gene (ADORA2A) contributes to individual sensitivity to caffeine effects on sleep. Clinical Pharmacology & Therapeutics 2007, 81(5):692-698.
75. Rosenberg P.A., Li Y. Adenylyl cyclase activation underlies intracellular cyclic AMP accumulation, cyclic AMP transport, and extracellular adenosine accumulation evoked by β-adrenergic receptor stimulation in mixed cultures of neurons and astrocytes derived from rat cerebral cortex. Brain Research 1995, 692(1):227-232.
76. Sala-Newby G.B., Skladanowski A.C., Newby A.C. The mechanism of adenosine formation in cells. Cloning of cytosolic 5'-nucleotidase-I. Journal of Biological Chemistry 1999, 274(25):17789-17793.
77. Saper C.B., Fuller P.M., Pedersen N.P., Lu J., Scammell T.E. Sleep state switching. Neuron 2010, 68(6):1023-1042.
78. Saper C.B., Scammell T.E., Lu J. Hypothalamic regulation of sleep and circadian rhythms. Nature 2005, 437(7063):1257-1263.
79. Satoh S., Matsumura H., Hayaishi O. Involvement of adenosine A2A receptor in sleep promotion. The European Journal of Neuroscience 1998, 351(2):155-162.
80. Satoh S., Matsumura H., Koike N., Tokunaga Y., Maeda T., Hayaishi O. Region-dependent difference in the sleep-promoting potency of an adenosine A2A receptor agonist. European Journal of Neuroscience 1999, 11(5):1587-1597.
81. Satoh S., Matsumura H., Suzuki F., Hayaishi O. Promotion of sleep mediated by the A2a-adenosine receptor and possible involvement of this receptor in the sleep induced by prostaglandin D2 in rats. Proceedings of the National Academy of Sciences of the United States of America 1996, 93(12):5980-5984.
82. Sawynok J., Liu X.J. Adenosine in the spinal cord and periphery: Release and regulation of pain. Progress in Neurobiology 2003, 69(5):313-340.
83. Scammell T., Gerashchenko D., Mochizuki T., McCarthy M., Estabrooke I., Sears C., et al. An adenosine A2a agonist increases sleep and induces Fos in ventrolateral preoptic neurons. Neuroscience 2001, 107(4):653-663.
84. Schwierin B., Borbely A.A., Tobler I. Effects of N6-cyclopentyladenosine and caffeine on sleep regulation in the rat. European Journal of Pharmacology 1996, 300(3):163-171.
85. Sharma R., Engemann S.C., Sahota P., Thakkar M.M. Effects of ethanol on extracellular levels of adenosine in the basal forebrain: An in vivo microdialysis study in freely behaving rats. Alcoholism, Clinical and Experimental Research 2010, 34(5):813-818.
86. Sherin J.E., Elmquist J.K., Torrealba F., Saper C.B. Innervation of histaminergic tuberomammillary neurons by GABAergic and galaninergic neurons in the ventrolateral preoptic nucleus of the rat. The Journal of Neuroscience 1998, 18(12):4705-4721.
87. Strecker R.E., Morairty S., Thakkar M.M., Porkka-Heiskanen T., Basheer R., Dauphin L.J., et al. Adenosinergic modulation of basal forebrain and preoptic/anterior hypothalamic neuronal activity in the control of behavioral state. Behavioural Brain Research 2000, 115(2):183-204.
88. Takahata R., Matsumura H., Kantha S.S., Kubo E., Kawase K., Sakai T., et al. Intravenous administration of inorganic selenium compounds, inhibitors of prostaglandin D synthase, inhibits sleep in freely moving rats. Brain Research 1993, 623(1):65-71.
89. Thakkar M.M., Engemann S.C., Sharma R., Sahota P. Role of wake-promoting basal forebrain and adenosinergic mechanisms in sleep-promoting effects of ethanol. Alcoholism, Clinical and Experimental Research 2010, 34(6):997-1005.
90. Thakkar M.M., Winston S., McCarley R.W. Orexin neurons of the hypothalamus express adenosine A1 receptors. Brain Research 2002, 944(1):190-194.
91. Thakkar M.M., Winston S., McCarley R.W. A1 receptor and adenosinergic homeostatic regulation of sleep-wakefulness: Effects of antisense to the A1 receptor in the cholinergic basal forebrain. The Journal of Neuroscience 2003, 23(10):4278-4287.
92. Ueno R., Honda K., Inoué S., Hayaishi O. Prostaglandin D2, a cerebral sleep-inducing substance in rats. Proceedings of the National Academy of Sciences of the United States of America 1983, 80(6):1735-1737.
93. Ueno R., Ishikawa Y., Nakayama T., Hayaishi O. Prostaglandin D2 induces sleep when microinjected into the preoptic area of conscious rats. Biochemical and Biophysical Research Communications 1982, 109(2):576.
94. Urade Y., Eguchi N., Qu W.M., Sakata M., Huang Z.L., Chen J.F., et al. Sleep regulation in adenosine A2A receptor-deficient mice. Neurology 2003, 61(11 Suppl. 6):S94-S96.
95. Urade Y., Kitahama K., Ohishi H., Kaneko T., Mizuno N., Hayaishi O. Dominant expression of mRNA for prostaglandin D synthase in leptomeninges, choroid plexus, and oligodendrocytes of the adult rat brain. Proceedings of the National Academy of Sciences of the United States of America 1993, 90(19):9070-9074.
96. Williams P.T., Vranizan K.M., Austin M.A., Krauss R.M. Associations of age, adiposity, alcohol intake, menstrual status, and estrogen therapy with high-density lipoprotein subclasses. Arteriosclerosis and Thrombosis 1993, 13(11):1654-1661.
97. Yaar R., Jones M., Chen J.F., Ravid K. Animal models for the study of adenosine receptor function. Journal of Cellular Physiology 2005, 202(1):9-20.
98. Zhang Z., Chen G., Zhou W., Song A., Xu T., Luo Q., et al. Regulated ATP release from astrocytes through lysosome exocytosis. Nature Cell Biology 2007, 9(8):945-953.
99. Zhang J.P., Xu Q., Yuan X.S., Cherasse Y., Schiffmann S.N., de Kerchove d'Exaerde A., et al. Projections of nucleus accumbens adenosine A2A receptor neurons in the mouse brain and their implications in mediating sleep-wake regulation. Frontiers in Neuroanatomy 2013, 7:43.
100. Zimmermann H. Extracellular metabolism of ATP and other nucleotides. Naunyn-Schmiedeberg's Archives of Pharmacology 2000, 362(4):299-309.