Mice with astrocyte-directed inactivation of connexin43 exhibit increased exploratory behaviour, impaired motor capacities, and changes in brain acetylcholine levels

European Journal of Neuroscience

Volumn 18, Issue 8, 2003, Pages 2313-2318

  Frisch, Christian ^a,b   Theis, Martin ^b,d   De Souza Silva, Maria A ^a   Dere, Ekrem ^a   Söhl, Goran ^b   Teubner, Barbara ^b   Namestkova, Katerina ^c   Willecke, Klaus ^b   Huston, Joseph R ^a  

^a HEINRICH HEINE UNIVERSITY   (Germany)

^b UNIVERSITY OF BONN   (Germany)

^c INSTITUTE OF EXPERIMENTAL BOTANY   (Czech Republic)

^d Howard Hughes Medical Institute   (United States)

Author keywords

Behaviour; Cre loxP; Gap junctions; Neuron glia interactions

Indexed keywords

CONNEXIN 30; CONNEXIN 43;

ACETYLCHOLINE BRAIN LEVEL; ANIMAL EXPERIMENT; ARTICLE; ASTROCYTE; BEHAVIORAL SCIENCE; CELL ACTIVATION; CELL FUNCTION; CONTROLLED STUDY; DRUG EFFECT; EMOTION; EXPLORATORY BEHAVIOR; GENE DELETION; HABITUATION; LEARNING; MAZE TEST; MOTOR ACTIVITY; MOTOR DYSFUNCTION; MOUSE; NEUROCHEMISTRY; NONHUMAN; OPEN FIELD BEHAVIOR; PRIORITY JOURNAL; TASK PERFORMANCE; TRAINING; TRANQUILIZING ACTIVITY;

3,4-DIHYDROXYPHENYLACETIC ACID; ACETYLCHOLINE; ANIMALS; ASTROCYTES; BRAIN; BRAIN CHEMISTRY; CHOLINE; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CONNEXIN 43; EXPLORATORY BEHAVIOR; GLIAL FIBRILLARY ACIDIC PROTEIN; GROOMING; HABITUATION, PSYCHOPHYSIOLOGIC; HYDROXYINDOLEACETIC ACID; LOCOMOTION; MICE; MICE, TRANSGENIC; MOTOR ACTIVITY; PSYCHOMOTOR PERFORMANCE; RETENTION (PSYCHOLOGY); ROTAROD PERFORMANCE TEST; SEROTONIN; TIME FACTORS;

EID: 1642545215     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1460-9568.2003.02971.x     Document Type: Article

References (40)

1. Alvarez-Maubecin, V., García-Hernández, F., Williams, J.T. & Van Bockstaele, E.J. (2000) Functional coupling between neurons and glia. J. Neurosci., 20, 4091-4098.
2. Araque, A., Parpura, V., Sanzgiri, R.P. & Haydon, P.G. (1999) Tripartite synapses: glia, the unacknowledged partner. Trends Neurosci., 22, 208-215.
3. Blomstrand, F., Aberg, N.D., Eriksson, P.S., Hansson, E. & Rönnbäck, L. (1999) Extent of intercellular calcium wave propagation is related to gap junction permeability and level of connexin-43 expression in astrocytes in primary cultures from four brain regions. Neuroscience, 92, 255-265.
4. Buzsaki, G. (1989) Two-stage model of memory trace formation: a role for 'noisy' brain states. Neuroscience, 31, 551-570.
5. Buzsaki, G. & Chrobak, J.J. (1995) Temporal structure in spatially organized neuronal ensembles: a role for interneuronal networks. Curr. Opin. Neurobiol., 5, 504-510.
6. Carola, V., D'Olimpio, F., Brunamonti, E., Mangia, F & Renzi, P. (2002) Evaluation of the elevated plus-maze and open-field tests for the assessment of anxiety-related behaviour in inbred mice. Behav. Brain Res., 134, 49-57.
7. Damsma, G., Lammerts van Bueren, D., Westerink, B.H.C. & Horn, A.S. (1987) Determination of acetylcholine and choline in the femtomole range by means of HPLC, a post-column enzyme reactor, and electrochemical detection. Chromatographia, 24, 827-831.
8. De Souza Silva, M.A., Mattern, C., Häcker, R., Nogueira, PJ.C., Huston, J.P. & Schwarting, R.K.W. (1997) Intranasal administration of the dopaminergic agonists 1-dopa, amphetamine, and cocaine increases activity in the neostriatum: a microdialysis study in the rat. J. Neurochem., 68, 233-239.
9. Dere, E., De Souza Silva, M.A., Frisch, C., Teubner, B., Söhl, G., Willecke, K. & Huston, J.P. (2003) Connexin30 deficient mice show increased emotionality and decreased rearing activity in the open field along with neurochemical changes. Eur. J. Neurosci. 18, 629-638.
10. Dermietzel, R. (1998) Diversification of gap junction proteins (connexins) in the central nervous system and the concept of functional compartments. Cell Biol. Int., 22, 719-730.
11. Frisch, C., Dere, E., De Souza Silva, M.A., Gödecke, A., Schader, J. & Huston, J.P. (2000) Superior water maze performance and increase in fear-related behavior in the endotehlial nitric oxide synthase-deficient mouse together with monoamine changes in cerebellum and ventral striatum. J. Neurosci., 20, 6694-6700.
12. 2+]i in rat astrocytes through activation of peripheral-type benzodiazepine receptors. Glia, 35, 90-100.
13. Goodlett, C.R., Thomas, J.D. & West, J.R. (1991) Long-term deficits in cerebellar growth and rotarod performance of rats following 'binge-like' alcohol exposure during the neonatal brain growth spurt. Neurotoxicol. Teratol., 13, 69-74.
14. Irwin, I.N. (2001) Gene expression in the hippocampus of behaviorally stimulated rats: analysis by DNA microarray. Mol. Brain Res., 96, 163-169.
15. +. Neuroscience, 93. 285-292.
16. McCall, M.A., Gregg, R.G., Behringer, R.R., Brenner, M., Delaney, C.L., Galbraeth, F.J., Zhang, C.L., Pearce, R.A., Chiu, S.Y. & Messing, A. (1996) Targeted deletion in astrocyte intermediate filament (GFAP) alters neuronal physiology. Proc. Natl A cad. Sci. USA, 93, 6361-6366.
17. Nagy, J.I., Patel, D., Ochalski, P.A.Y. & Stelmack, G.L. (1998) Connexin 30 in rodent, cat and human brain: selective expression in gray matter astrocytes, co-localization with connexin43 at gap junctions and late developmental appearance. Neuroscience, 88, 447-468.
18. Nagy, J. & Rash, J.E. (2000) Connexins and gap junctions of astrocytes and oligodendrocytes in the CNS. Brain Res. Rev., 32, 29-44.
19. Naus, C.C.G., Bechberger, J.F., Venance, L., Yamasaki, H., Zhang, Y., Juneja, S.C., Kidder, G.M. & Giaume, C. (1997) Altered gap junctional communication, intercellular signaling, and growth in cultured astrocytes deficient in connexin43. J. Neurosci. Res., 49, 528-540.
20. Nishiyama, H., Knöpfel, T., Endo, S. & Itohara, S. (2002) Glial protein S100B modulates long-term neuronal synaptic plasticity. Proc. Natl Acad. Sci. USA, 99, 4037-4042.
21. Pasti, L., Volterra, A., Pozzan, T. & Carmignoto, G. (1997) Intracellular calcium oscillations in astrocytes: a highly plastic, bidirectional form of communication between neurons and astrocytes in situ. J. Neurosci. 17, 7817-7830.
22. Rao, V.L., Bowen, K.K., Rao, A.M. & Dempsey, R.J. (2001) Up-regulation of the peripheral-type benzodiazepine receptor expression and [(3)H]PK11195 binding in gerbil hippocampus after transient forebrain ischemia. J. Neurosci. Res., 64, 493-500.
23. Rash, J.E., Yasumura, T., Dudek, F.E. & Nagy, J.I. (2001) Cell-specific expression of connexins and evidence of restricted gap junctional coupling between glial cells and between neurons. J. Neurosci., 21, 1983-2000.
24. Reaume, A.G., De Sousa, P.A., Kulkarni, S., Langille, B.L., Zhu, D., Davies, T.C., Juneja, S.C., Kidder, G.M. & Rossant, J. (1995) Cardiac malformation in neonatal mice lacking connexin43. Science, 267, 1831-1834.
25. Roder, J.K., Roder, J.C. & Gerlai, R. (1996) Conspecific exploration in the T-maze: abnormalities in S100 beta transgenic mice. Physiol. Behav., 60, 31-36.
26. Rouach, N., Glowinski, J. & Giaume, C. (2000) Activity-dependent neuronal control of gap-junctional communication in astrocytes. J. Cell Biol., 149, 1513-1526.
27. Sarter, M. & Bruno, J.P. (1997) Cognitive functions of cortical acetylcholine: toward a unifying hypothesis. Brain Res. Rev., 23, 28-46.
28. Sastry, B.R., Maretic, H., Morishita, W. & Xie, Z. (1990) Modulation of the induction of long-term potentiation in the hippocampus. Adv. Exp. Med. Biol., 268, 377-386.
29. Scemes, E., Dermietzel, R. & Spray, D.C. (1998) Calcium waves between astrocytes from Cx43 knockout mice. Glia, 24, 65-73.
30. Sethy, V.M. & Francis, J.W. (1988) Regulation of brain acetylcholine concentration by muscarinic receptors. J. Pharmacol. Exp. Ther., 246, 243-248.
31. Somjen, G.G. (2001) Mechanisms of spreading depression and hypoxic spreading depression-like depolarization. Physiol. Rev., 81, 1065-1096.
32. Theis, M., de Wit, C., Schlaeger, T.M., Eckardt, D., Krüger, O., Döring, B., Risau, W., Deutsch, U., Pohl, U. & Willecke, K. (2001). Endothelium-specific replacement of the connexin43 coding region by a lacZ reporter gene. Genesis, 29, 1-13.
33. Theis, M., Jauch, R., Zhuo, L., Speidel, D., Wallraff, A., Döring, B., Frisch, C., Sohl, G., Teubner, B., Euwens, C., Huston, J., Steinhaeuser. C., Messing, A., Heinemann, U. & Willecke, K. (2003) Accelerated hippocampal spreading depression and enhanced locomotory activity in mice with astrocyte-directed inactivation of connexin43. J. Neurosci., 23, 766-776.
34. Thiel, CM., Huston, J.P. & Schwarting, R.K. (1998) Hippocampal acetylcholine and habituation learning. Neuroscience, 85, 1253-1262.
35. Tsacopoulos, M. & Magistretti, P.J. (1996) Metabolic coupling between glia and neurons. J. Neurosci., 16, 877-885.
36. Verkhratsky, A. & Kettenmann, H. (1996) Calcium signalling in glial cells. Trends Neurosci., 19, 346-352.
37. Whitaker-Azmitia, P.M., Clarke, C. & Azmitia, E.C. (1993) Localization of 5-HT1A receptors to astroglial cells in adult rats: implications for neuronalglial interactions and psychoactive drug mechanism of action. Synapse, 14, 201-215.
38. Wolfer, D.P., Mohajeri, H.M., Lipp, H.P. & Schachner, M. (1998) Increased flexibility and selectivity in spatial learning of transgenic mice ectopically expressing the neural cell adhesion molecule L1 in astrocytes. Eur. J. Neurosci., 10, 708-717.
39. Zhao, Z., Hertz, L. & Code, W.E. (1996) Effects of benzodiazepines on potassium-induced increase in free cytosolic calcium concentration in astrocytes: interactions with nifedipine and the peripheral-type benzodiazepine antagonist PK 11195. Can. J. Physiol. Pharmacol., 74, 273-277.
40. Zhuo, L., Theis, M., Alvarez-Maya, I., Brenner. M., Willecke, K. & Messing, A. (2001) hGFAP-cre transgenic mice for manipulation of glial and neuronal function in vivo. Genesis, 31, 85-94.