Astrocyte-derived adenosine modulates increased sleep pressure during inflammatory response

GLIA

Volumn 61, Issue 5, 2013, Pages 724-731

  Nadjar, Agnes ^a,b,c   Blutstein, Tamara ^c   Aubert, Agnes ^a,b   Laye, Sophie ^a,b   Haydon, Philip G ^c  

^a UNIVERSITÉ DE BORDEAUX   (France)

^b NutriNeuro Bordeaux University   (France)

^c TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Adenosine; Glia; Inflammation; Lipopolysaccharide; Sleep

Indexed keywords

ADENOSINE; LIPOPOLYSACCHARIDE; ADENOSINE A1 RECEPTOR; SNARE PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; ASTROCYTE; BEHAVIOR CHANGE; CONTROLLED STUDY; IMMUNE RESPONSE; IMMUNOREACTIVITY; INFLAMMATION; INTRACEREBROVENTRICULAR DRUG ADMINISTRATION; MOUSE; NEUROTRANSMISSION; NONHUMAN; NONREM SLEEP; PHENOTYPE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SLOW WAVE SLEEP; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CHEMICALLY INDUCED; DRUG EFFECTS; ELECTROENCEPHALOGRAPHY; GENETICS; METABOLISM; PATHOLOGY; PHYSIOLOGY; PROCEDURES; SLEEP; TOXICITY; TRANSGENIC MOUSE;

ADENOSINE; ANIMALS; ASTROCYTES; ELECTROENCEPHALOGRAPHY; INFLAMMATION; LIPOPOLYSACCHARIDES; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; RECEPTOR, ADENOSINE A1; SLEEP; SNARE PROTEINS;

EID: 84882747260     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.22465     Document Type: Article

References (43)

1. Andre C, O'Connor JC, Kelley KW, Lestage J, Dantzer R, Castanon N. Spatio-temporal differences in the profile of murine brain expression of proinflammatory cytokines and indoleamine 2,3-dioxygenase in response to peripheral lipopolysaccharide administration. J Neuroimmunol 2008;200: 90-99.
2. Basheer R, Strecker RE, Thakkar MM, McCarley RW. Adenosine and sleepwake regulation. Prog Neurobiol 2004;73:379-396.
3. Bjorness TE, Kelly CL, Gao T, Poffenberger V, Greene RW. Control and function of the homeostatic sleep response by adenosine A1 receptors. J Neurosci 2009;29:1267-1276.
4. Borbely AA. A two process model of sleep regulation. Hum Neurobiol 1982; 1:195-204.
5. Brambilla R, Bracchi-Ricard V, Hu WH, Frydel B, Bramwell A, Karmally S, Green EJ, Bethea JR. Inhibition of astroglial nuclear factor kappaB reduces inflammation and improves functional recovery after spinal cord injury. J Exp Med 2005;202:145-156.
6. Chakravarty S, Herkenham M. Toll-like receptor 4 on nonhematopoietic cells sustains CNS inflammation during endotoxemia, independent of systemic cytokines. J Neurosci 2005;25:1788-1796.
7. Cirelli C, Huber R, Gopalakrishnan A, Southard TL, Tononi G. Locus ceruleus control of slow-wave homeostasis. J Neurosci 2005;25:4503-4511.
8. Damm J, Luheshi GN, Gerstberger R, Roth J, Rummel C. Spatiotemporal nuclear factor interleukin-6 expression in the rat brain during lipopolysaccharide-induced fever is linked to sustained hypothalamic inflammatory target gene induction. J Comp Neurol 2011;519:480-505.
9. Dantzer R, Bluthe RM, Gheusi G, Cremona S, Laye S, Parnet P, Kelley KW. Molecular basis of sickness behavior. Ann N Y Acad Sci 1998;856:132-138.
10. Farina C, Aloisi F, Meinl E. Astrocytes are active players in cerebral innate immunity. Trends Immunol 2007;28:138-145.
11. Gautron L, Lafon P, Chaigniau M, Tramu G, Laye S. Spatiotemporal analysis of signal transducer and activator of transcription 3 activation in rat brain astrocytes and pituitary following peripheral immune challenge. Neuroscience 2002;112:717-729.
12. Gourine AV, Dale N, Llaudet E, Poputnikov DM, Spyer KM, Gourine VN. Release of ATP in the central nervous system during systemic inflammation: Real-time measurement in the hypothalamus of conscious rabbits. J Physiol 2007;585:305-316.
13. Halassa MM, Fellin T, Haydon PG. The tripartite synapse: Roles for gliotransmission in health and disease. Trends Mol Med 2007;13:54-63.
14. Halassa MM, Florian C, Fellin T, Munoz JR, Lee SY, Abel T, Haydon PG, Frank MG. Astrocytic modulation of sleep homeostasis and cognitive consequences of sleep loss. Neuron 2009;61:213-219.
15. Harre EM, Roth J, Gerstberger R, Hubschle T. Interleukin-6 mediates lipopolysaccharide-induced nuclear STAT3 translocation in astrocytes of rat sensory circumventricular organs. Brain Res 2003;980:151-155.
16. Herkenham M, Lee HY, Baker RA. Temporal and spatial patterns of c-fos mRNA induced by intravenous interleukin-1: A cascade of non-neuronal cellular activation at the blood-brain barrier. J Comp Neurol 1998;400: 175-196.
17. Jhaveri KA, Toth LA, Sekino Y, Ramkumar V. Nitric oxide serves as an endogenous regulator of neuronal adenosine A1 receptor expression. J Neurochem 2006;99:42-53.
18. Justicia C, Gabriel C, Planas AM. Activation of the JAK/STAT pathway following transient focal cerebral ischemia: Signaling through Jak1 and Stat3 in astrocytes. Glia 2000;30:253-270.
19. Kapas L, Hansen MK, Chang HY, Krueger JM. Vagotomy attenuates but does not prevent the somnogenic and febrile effects of lipopolysaccharide in rats. Am J Physiol 1998;274:R406-R411.
20. Krueger JM. The role of cytokines in sleep regulation. Curr Pharm Des 2008; 14:3408-3416.
21. Krueger JM, Bacsik J, Garcia-Arraras J. Sleep-promoting material from human urine and its relation to factor S from brain. Am J Physiol 1980;238: E116-E123.
22. Krueger JM, Kubillus S, Shoham S, Davenne D. Enhancement of slow-wave sleep by endotoxin and lipid A. Am J Physiol 1986;251:R591-R597.
23. Krueger JM, Obal FJ, Fang J, Kubota T, Taishi P. The role of cytokines in physiological sleep regulation. Ann N Y Acad Sci 2001;933:211-221.
24. Lancel M, Cronlein J, Muller-Preuss P, Holsboer F. Lipopolysaccharide increases EEG delta activity within non-REM sleep and disrupts sleep continuity in rats. Am J Physiol 1995;268:R1310-R1318.
25. Laye S, Parnet P, Goujon E, Dantzer R. Peripheral administration of lipopolysaccharide induces the expression of cytokine transcripts in the brain and pituitary of mice. Brain Res Mol Brain Res 1994;27:157-162.
26. Majde JA, Krueger JM. Links between the innate immune system and sleep. J Allergy Clin Immunol 2005;116:1188-1198.
27. Morairty S, Rainnie D, McCarley R, Greene R. Disinhibition of ventrolateral preoptic area sleep-active neurons by adenosine: A new mechanism for sleep promotion. Neuroscience 2004;123:451-457.
28. Morrow JD, Opp MR. Diurnal variation of lipopolysaccharide-induced alterations in sleep and body temperature of interleukin-6-deficient mice. Brain Behav Immun 2005;19:40-51.
29. Mullington J, Korth C, Hermann DM, Orth A, Galanos C, Holsboer F, Pollmacher T. Dose-dependent effects of endotoxin on human sleep. Am J Physiol Regul Integr Comp Physiol 2000;278:R947-R955.
30. Nadjar A, Combe C, Laye S, Tridon V, Dantzer R, Amedee T, Parnet P. Nuclear factor kappaB nuclear translocation as a crucial marker of brain response to interleukin-1. A study in rat and interleukin-1 type I deficient mouse. J Neurochem 2003;87:1024-1036.
31. Opp MR, Toth LA. Somnogenic and pyrogenic effects of interleukin-1beta and lipopolysaccharide in intact and vagotomized rats. Life Sci 1998;62: 923-936.
32. Pascual O, Ben Achour S, Rostaing P, Triller A, Bessis A. Microglia activation triggers astrocyte-mediated modulation of excitatory neurotransmission. Proc Natl Acad Sci USA 2011;109:E197-E205.
33. Pascual O, Casper KB, Kubera C, Zhang J, Revilla-Sanchez R, Sul JY, Takano H, Moss SJ, McCarthy K, Haydon PG. Astrocytic purinergic signaling coordinates synaptic networks. Science 2005;310:113-116.
34. Porkka-Heiskanen T, Strecker RE, Thakkar M, Bjorkum AA, Greene RW, McCarley RW. Adenosine: A mediator of the sleep-inducing effects of prolonged wakefulness. Science 1997;276:1265-1268.
35. Quan N, Whiteside M, Kim L, Herkenham M. Induction of inhibitory factor kappaBalpha mRNA in the central nervous system after peripheral lipopolysaccharide administration: An in situ hybridization histochemistry study in the rat. Proc Natl Acad Sci USA 1997;94:10985-10990.
36. Rohleder N, Aringer M, Boentert M. Role of interleukin-6 in stress, sleep, and fatigue. Ann N Y Acad Sci 2012;1261:88-96.
37. Rummel C, Voss T, Matsumura K, Korte S, Gerstberger R, Roth J, Hubschle T. Nuclear STAT3 translocation in guinea pig and rat brain endothelium during systemic challenge with lipopolysaccharide and interleukin-6. J Comp Neurol 2005;491:1-14.
38. Santello M, Bezzi P, Volterra A. TNFalpha controls glutamatergic gliotransmission in the hippocampal dentate gyrus. Neuron 2011;69: 988-1001.
39. Santello M, Cali C, Bezzi P. Gliotransmission and the tripartite synapse. Adv Exp Med Biol 2012;970:307-331.
40. Saper CB, Chou TC, Scammell TE. The sleep switch: hypothalamic control of sleep and wakefulness. Trends Neurosci 2001;24:726-731.
41. Schwaiger FW, Hager G, Schmitt AB, Horvat A, Hager G, Streif R, Spitzer C, Gamal S, Breuer S, Brook GA, Nacimiento W, Kreutzberg GW. Peripheral but not central axotomy induces changes in Janus kinases (JAK) and signal transducers and activators of transcription (STAT). Eur J Neurosci 2000;12: 1165-1176.
42. Thakkar MM, Winston S, McCarley RW. A1 receptor and adenosinergic homeostatic regulation of sleep-wakefulness: Effects of antisense to the A1 receptor in the cholinergic basal forebrain. J Neurosci 2003;23:4278-4287.
43. Volterra A, Meldolesi J. Astrocytes, from brain glue to communication elements: The revolution continues. Nat Rev Neurosci 2005;6:626-640.