Staying awake - a genetic region that hinders α2 adrenergic receptor agonist-induced sleep

European Journal of Neuroscience

Volumn 40, Issue 1, 2014, Pages 2311-2319

  Gelegen, Cigdem ^a   Gent, Thomas C ^a   Ferretti, Valentina ^a   Zhang, Zhe ^a   Yustos, Raquel ^a   Lan, Fei ^a   Yang, Qianzi ^a   Overington, Dorothy W U ^a   Vyssotski, Alexei L ^b   van Lith, Hein A ^c,d   Wisden, William ^a   Franks, Nicholas P ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF ZURICH   (Switzerland)

^c UTRECHT UNIVERSITY   (Netherlands)

^d UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

Alpha2a adrenergic receptor; Sedation; Sleep; Wakefulness

Indexed keywords

ALPHA 2 ADRENERGIC RECEPTOR STIMULATING AGENT; DEXMEDETOMIDINE; ADRA2A PROTEIN, MOUSE; ALPHA 2 ADRENERGIC RECEPTOR; ALPHA ADRENERGIC RECEPTOR STIMULATING AGENT; HYPNOTIC SEDATIVE AGENT;

ALPHA ADRENERGIC STIMULATION; ANIMAL EXPERIMENT; ARTICLE; CHROMOSOME 4; CONTROLLED STUDY; DEXMEDETOMIDINE INDUCED HYPNOSIS; DRUG INDUCED DISEASE; GENE LOCUS; GENETIC ASSOCIATION; LINKAGE ANALYSIS; MOUSE; MOUSE STRAIN; NONHUMAN; PRIORITY JOURNAL; PROGENY; QUANTITATIVE ANALYSIS; RIGHTING REFLEX; SLEEP DISORDER; UNCONSCIOUSNESS; WAKEFULNESS; 129 MOUSE; ANIMAL; BRAIN; C57BL MOUSE; CHROMOSOME; DOMINANT GENE; DRUG EFFECTS; ELECTROENCEPHALOGRAPHY; GENETICS; GENOME-WIDE ASSOCIATION STUDY; METABOLISM; PHARMACOGENETICS; PHYSICAL STIMULATION; PHYSIOLOGY; ROTAROD TEST; SLEEP; SPECIES DIFFERENCE;

ADRENERGIC ALPHA-AGONISTS; ANIMALS; BRAIN; CHROMOSOMES, MAMMALIAN; DEXMEDETOMIDINE; ELECTROENCEPHALOGRAPHY; GENES, DOMINANT; GENOME-WIDE ASSOCIATION STUDY; HYPNOTICS AND SEDATIVES; MICE, 129 STRAIN; MICE, INBRED C57BL; PHARMACOGENETICS; PHYSICAL STIMULATION; RECEPTORS, ADRENERGIC, ALPHA-2; REFLEX, RIGHTING; ROTAROD PERFORMANCE TEST; SLEEP; SPECIES SPECIFICITY; WAKEFULNESS;

EID: 84903884394     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/ejn.12570     Document Type: Article

References (52)

1. Anderson, S.L., Coli, R., Daly, I.W., Kichula, E.A., Rork, M.J., Volpi, S.A., Ekstein, J. & Rubin, B.Y. (2001) Familial dysautonomia is caused by mutations of the IKAP gene. Am. J. Hum. Genet., 68, 753-758.
2. Andretic, R., Franken, P. & Tafti, M. (2008) Genetics of sleep. Annu. Rev. Genet., 42, 361-388.
3. Arends, D., Prins, P., Jansen, R.C. & Broman, K.W. (2010) R/qtl: high-throughput multiple QTL mapping. Bioinformatics, 26, 2990-2992.
4. Avsaroglu, H., Bull, S., Maas-Bakker, R.F., Scherpenisse, P., Van Lith, H.A., Bergwerff, A.A., Hellebrekers, L.J., Van Zutphen, L.F. & Fink-Gremmels, J. (2008) Differences in hepatic cytochrome P450 activity correlate with the strain-specific biotransformation of medetomidine in AX/JU and IIIVO/JU inbred rabbits. J. Vet. Pharmacol. Ther., 31, 368-377.
5. Berridge, C.W., Schmeichel, B.E. & Espana, R.A. (2012) Noradrenergic modulation of wakefulness/arousal. Sleep Med. Rev., 16, 187-197.
6. Broman, K.W. & Sen, S. (2009) A Guide to QTL Mapping with R/qtl. Springer Science+Business Media, New York.
7. Crawley, J.N., Belknap, J.K., Collins, A., Crabbe, J.C., Frankel, W., Henderson, N., Hitzemann, R.J., Maxson, S.C., Miner, L.L., Silva, A.J., Wehner, J.M., Wynshaw-Boris, A. & Paylor, R. (1997) Behavioral phenotypes of inbred mouse strains: implications and recommendations for molecular studies. Psychopharmacology, 132, 107-124.
8. Drew, G.M., Gower, A.J. & Marriott, A.S. (1979) Alpha 2-adrenoceptors mediate clonidine-induced sedation in the rat. Brit. J. Pharmacol., 67, 133-141.
9. Duhamel, M.C., Troncy, E. & Beaudry, F. (2010) Metabolic stability and determination of cytochrome P450 isoenzymes' contribution to the metabolism of medetomidine in dog liver microsomes. Biomed. Chromatogr., 24, 868-877.
10. Franken, P., Malafosse, A. & Tafti, M. (1998) Genetic variation in EEG activity during sleep in inbred mice. Am. J. Physiol., 275, R1127-R1137.
11. Franks, N.P. (2008) General anaesthesia: from molecular targets to neuronal pathways of sleep and arousal. Nat. Rev. Neurosci., 9, 370-386.
12. Gilsbach, R., Roser, C., Beetz, N., Brede, M., Hadamek, K., Haubold, M., Leemhuis, J., Philipp, M., Schneider, J., Urbanski, M., Szabo, B., Weinshenker, D. & Hein, L. (2009) Genetic dissection of alpha2-adrenoceptor functions in adrenergic versus nonadrenergic cells. Mol. Pharmacol., 75, 1160-1170.
13. Hart, D.E. & Ruvolo, M. (2012) The Genetic Basis of Complex Traits in Genetics of Genes and Genomes. Jones and Bartlett, London.
14. Hessel, E.V., van Lith, H.A., Wolterink-Donselaar, I.G., de Wit, M., Hendrickx, D.A., Kas, M.J. & de Graan, P.N. (2012) Mapping an X-linked locus that influences heat-induced febrile seizures in mice. Epilepsia, 53, 1399-1410.
15. Homanics, G.E., Quinlan, J.J. & Firestone, L.L. (1999) Pharmacologic and behavioral responses of inbred C57BL/6J and strain 129/SvJ mouse lines. Pharmacol. Biochem. Be., 63, 21-26.
16. Huber, R., Deboer, T. & Tobler, I. (2000) Effects of sleep deprivation on sleep and sleep EEG in three mouse strains: empirical data and simulations. Brain Res., 857, 8-19.
17. Kamibayashi, T. & Maze, M. (2000) Clinical uses of alpha2 -adrenergic agonists. Anesthesiology, 93, 1345-1349.
18. Kas, M.J., de Mooij-van Malsen, J.G., de Krom, M., van Gassen, K.L., van Lith, H.A., Olivier, B., Oppelaar, H., Hendriks, J., de Wit, M., Groot Koerkamp, M.J., Holstege, F.C., van Oost, B.A. & de Graan, P.N. (2009) High-resolution genetic mapping of mammalian motor activity levels in mice. Genes Brain Behav., 8, 13-22.
19. Kitchigina, V.F., Kutyreva, E.V. & Brazhnik, E.S. (2003) Modulation of theta rhythmicity in the medial septal neurons and the hippocampal electroencephalogram in the awake rabbit via actions at noradrenergic alpha2-receptors. Neuroscience, 120, 509-521.
20. Korpi, E.R., Koikkalainen, P., Vekovischeva, O.Y., Makela, R., Kleinz, R., Uusi-Oukari, M. & Wisden, W. (1999) Cerebellar granule-cell-specific GABAA receptors attenuate benzodiazepine-induced ataxia: evidence from alpha 6-subunit-deficient mice. Eur. J. Neurosci., 11, 233-240.
21. Kuo, Y.M., Zhou, B., Cosco, D. & Gitschier, J. (2001) The copper transporter CTR1 provides an essential function in mammalian embryonic development. Proc. Natl. Acad. Sci. USA, 98, 6836-6841.
22. Lakhlani, P.P., MacMillan, L.B., Guo, T.Z., McCool, B.A., Lovinger, D.M., Maze, M. & Limbird, L.E. (1997) Substitution of a mutant alpha2a-adrenergic receptor via "hit and run" gene targeting reveals the role of this subtype in sedative, analgesic, and anesthetic-sparing responses in vivo. Proc. Natl. Acad. Sci. USA, 94, 9950-9955.
23. Linden, A.M., Aller, M.I., Leppa, E., Vekovischeva, O., Aitta-Aho, T., Veale, E.L., Mathie, A., Rosenberg, P., Wisden, W. & Korpi, E.R. (2006) The in vivo contributions of TASK-1-containing channels to the actions of inhalation anesthetics, the alpha(2) adrenergic sedative dexmedetomidine, and cannabinoid agonists. J. Pharmacol. Exp. Ther., 317, 615-626.
24. Logue, S.F., Owen, E.H., Rasmussen, D.L. & Wehner, J.M. (1997) Assessment of locomotor activity, acoustic and tactile startle, and prepulse inhibition of startle in inbred mouse strains and F1 hybrids: implications of genetic background for single gene and quantitative trait loci analyses. Neuroscience, 80, 1075-1086.
25. Maret, S., Franken, P., Dauvilliers, Y., Ghyselinck, N.B., Chambon, P. & Tafti, M. (2005) Retinoic acid signaling affects cortical synchrony during sleep. Science, 310, 111-113.
26. Mason, K.P., O'Mahony, E., Zurakowski, D. & Libenson, M.H. (2009) Effects of dexmedetomidine sedation on the EEG in children. Paediatr. Anaesth., 19, 1175-1183.
27. Maze, M. & Regan, J.W. (1991) Role of signal transduction in anesthetic action. Alpha 2 adrenergic agonists. Ann. NY Acad. Sci., 625, 409-422.
28. Nelson, L.E., Lu, J., Guo, T., Saper, C.B., Franks, N.P. & Maze, M. (2003) The alpha2-adrenoceptor agonist dexmedetomidine converges on an endogenous sleep-promoting pathway to exert its sedative effects. Anesthesiology, 98, 428-436.
29. Nicholas, A.P., Pieribone, V. & Hokfelt, T. (1993) Distributions of mRNAs for alpha-2 adrenergic receptor subtypes in rat brain: an in situ hybridization study. J. Comp. Neurol., 328, 575-594.
30. Pang, D.S., Robledo, C.J., Carr, D.R., Gent, T.C., Vyssotski, A.L., Caley, A., Zecharia, A.Y., Wisden, W., Brickley, S.G. & Franks, N.P. (2009) An unexpected role for TASK-3 potassium channels in network oscillations with implications for sleep mechanisms and anesthetic action. Proc. Natl. Acad. Sci. USA, 106, 17546-17551.
31. Philipp, M. & Hein, L. (2004) Adrenergic receptor knockout mice: distinct functions of 9 receptor subtypes. Pharmacol. Therapeut., 101, 65-74.
32. Prows, D.R., Hafertepen, A.P., Winterberg, A.V., Gibbons, W.J. Jr., Liu, C. & Nick, T.G. (2007) Genetic analysis of hyperoxic acute lung injury survival in reciprocal intercross mice. Physiol. Genomics, 30, 271-281.
33. Ralph, M.R. & Menaker, M. (1988) A mutation of the circadian system in golden hamsters. Science, 241, 1225-1227.
34. Sainsbury, R.S. & Partlo, L.A. (1991) The effects of alpha 2 agonists and antagonists on hippocampal theta activity in the freely moving rat. Brain Res. Bull., 26, 37-42.
35. Saper, C.B., Fuller, P.M., Pedersen, N.P., Lu, J. & Scammell, T.E. (2010) Sleep state switching. Neuron, 68, 1023-1042.
36. Schmeichel, B.E. & Berridge, C.W. (2013) Wake-promoting actions of noradrenergic alpha1 - and beta-receptors within the lateral hypothalamic area. Eur. J. Neurosci., 37, 891-900.
37. Szabadi, E. (2013) Functional neuroanatomy of the central noradrenergic system. J. Psychopharmacol., 27, 659-693.
38. Tafti, M., Petit, B., Chollet, D., Neidhart, E., de Bilbao, F., Kiss, J.Z., Wood, P.A. & Franken, P. (2003) Deficiency in short-chain fatty acid beta-oxidation affects theta oscillations during sleep. Nat. Genet., 34, 320-325.
39. Tan, C.M., Wilson, M.H., MacMillan, L.B., Kobilka, B.K. & Limbird, L.E. (2002) Heterozygous alpha 2A-adrenergic receptor mice unveil unique therapeutic benefits of partial agonists. Proc. Natl. Acad. Sci. USA, 99, 12471-12476.
40. Valatx, J.L., Bugat, R. & Jouvet, M. (1972) Genetic studies of sleep in mice. Nature, 238, 226-227.
41. Venn, R.M. & Grounds, R.M. (2001) Comparison between dexmedetomidine and propofol for sedation in the intensive care unit: patient and clinician perceptions. Brit. J. Anaesth., 87, 684-690.
42. Vyssotski, A.L., Dell'Omo, G., Dell'Ariccia, G., Abramchuk, A.N., Serkov, A.N., Latanov, A.V., Loizzo, A., Wolfer, D.P. & Lipp, H.P. (2009) EEG responses to visual landmarks in flying pigeons. Curr. Biol., 19, 1159-1166.
43. Wang, R., Macmillan, L.B., Fremeau, R.T., Magnuson, M.A., Lindner, J. & Limbird, L.E. (1996) Expression of alpha(2)-adrenergic receptor subtypes in the mouse brain: evaluation of spatial and temporal information imparted by 3 kb of 5' regulatory sequence for the alpha(2A)AR-receptor gene in transgenic animals. Neuroscience, 74, 199-218.
44. Waud, D.R. (1972) On biological assays involving quantal responses. J. Pharmacol. Exp. Ther., 183, 577-607.
45. Weber, J.N., Peterson, B.K. & Hoekstra, H.E. (2013) Discrete genetic modules are responsible for complex burrow evolution in Peromyscus mice. Nature, 493, 402-405.
46. Winrow, C.J., Williams, D.L., Kasarskis, A., Millstein, J., Laposky, A.D., Yang, H.S., Mrazek, K., Zhou, L., Owens, J.R., Radzicki, D., Preuss, F., Schadt, E.E., Shimomura, K., Vitaterna, M.H., Zhang, C., Koblan, K.S., Renger, J.J. & Turek, F.W. (2009) Uncovering the genetic landscape for multiple sleep-wake traits. PLoS ONE, 4, e5161.
47. Winsky-Sommerer, R., Vyazovskiy, V.V., Homanics, G.E. & Tobler, I. (2007) The EEG effects of THIP (Gaboxadol) on sleep and waking are mediated by the GABA(A)delta-subunit-containing receptors. Eur. J. Neurosci., 25, 1893-1899.
48. Wisden, W. & Morris, B. (1994). In Situ Hybridization Protocols for the Brain. Academic Press, London.
49. Wrighton, S.A. & Stevens, J.C. (1992) The human hepatic cytochromes P450 involved in drug metabolism. Crit. Rev. Toxicol., 22, 1-21.
50. Wrzosek, M., Nicpon, J., Bergamasco, L., Sammartano, F., Cizinauskas, S. & Jaggy, A. (2009) Visual and quantitative electroencephalographic analysis of healthy young and adult cats under medetomidine sedation. Vet. J., 180, 221-230.
51. A receptors. Nat. Neurosci., 10, 923-929.
52. Zecharia, A.Y., Yu, X., Gotz, T., Ye, Z., Carr, D.R., Wulff, P., Bettler, B., Vyssotski, A.L., Brickley, S.G., Franks, N.P. & Wisden, W. (2012) GABAergic inhibition of histaminergic neurons regulates active waking but not the sleep-wake switch or propofol-induced loss of consciousness. J. Neurosci., 32, 13062-13075.