Hippocampal astrocytes exhibit Ca2+-elevating muscarinic cholinergic and histaminergic receptors in situ

Journal of Neurochemistry

Volumn 74, Issue 2, 2000, Pages 555-563

  Shelton, Marilee K ^a   McCarthy, Ken D ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

Brain slices; Carbachol; Cholinergic receptors; Glia; Histamine; Receptors

Indexed keywords

1 AMINO 1,3 CYCLOPENTANEDICARBOXYLIC ACID; ALPHA 2 ADRENERGIC RECEPTOR; ATROPINE; CALCIUM ION; CARBACHOL; CHLORPHENIRAMINE; G PROTEIN COUPLED RECEPTOR; GLUTAMIC ACID; HISTAMINE; HISTAMINE RECEPTOR; METABOTROPIC RECEPTOR; MUSCARINIC RECEPTOR; PIRENZEPINE; TETRODOTOXIN;

ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN SLICE; CALCIUM CELL LEVEL; CONTROLLED STUDY; HIPPOCAMPUS; IMMUNOCYTOCHEMISTRY; NEUROTRANSMITTER RELEASE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; RAT;

AGING; ANIMALS; ANIMALS, NEWBORN; ASTROCYTES; CALCIUM; HIPPOCAMPUS; KINETICS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, HISTAMINE; RECEPTORS, MUSCARINIC;

EID: 0033978239     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.2000.740555.x     Document Type: Article

References (67)

1. Andre C., Dos Santos G., and Koulakoff A. (1994) Muscarinic receptor profiles of mouse brain astrocytes in culture vary with their tissue of origin but differ from those of neurons. Eur. J. Neurosci. 6, 1702-1709.
2. Araque A., Parpura V., Sanzgiri R. P., and Haydon P. G. (1998a) Glutamate-dependent astrocyte modulation of synaptic transmission between cultured hippocampal neurons. Eur. J. Neurosci. 10, 2129-2142.
3. Araque A., Sanzgiri R. P., Parpura V., and Haydon P. G. (1998b) Calcium elevation in astrocytes causes an NMDA receptor-dependent increase in the frequency of miniature synaptic currents in cultured hippocampal neurons. J. Neurosci. 18, 6822-6829.
4. Augelli-Szafran C. E., Blankley C. J., Jaen J. C., Moreland D. W., Nelson C. B., Penvose-Yi J. R., Schwarz R. D., and Thomas A. J. (1999) Identification and characterization of m1 selective muscarinic receptor. J. Med. Chem. 42, 356-363.
5. Behrends J. C. and ten Bruggencate G. (1993) Cholinergic modulation of synaptic inhibition in the guinea pig hippocampus in vitro: excitation of GABAergic interneurons and inhibition of GABA-release. J. Neurophysiol. 69, 626-629.
6. Beldhuis H. J., Everts H. G., Van der Zee E. A., Luiten P. G., and Bohus B. (1992) Amygdala kindling-induced seizures selectively impair spatial memory. 2. Effects on hippocampal neuronal and glial muscarinic acetylcholine receptor. Hippocampus 2, 411-419.
7. Bernstein M., Lyons S. A., Moller T., and Kettenmann H. (1996) Receptor-mediated calcium signalling in glial cells from mouse corpus callosum slices. J. Neurosci. Res. 46, 152-163.
8. Bezzi P., Carmignoto G., Pasti L., Vesce S., Rossi D., Rizzini B. L., Pozzan T., and Volterra A. (1998) Prostaglandins stimulate calcium-dependent glutamate release in astrocytes. Nature 391, 281-285.
9. Brown R. E. and Haas H. L. (1999) On the mechanism of histaminergic inhibition of glutamate release in the rat dentate gyrus. J. Physiol. (Lond.) 515, 777-786.
10. Cai Z. and Kimelberg H. K. (1997) Glutamate receptor-mediated calcium responses in acutely isolated hippocampal astrocytes Glia 21, 380-389.
11. Cornell-Bell A. H., Finkbeiner S. M., Cooper M. S., and Smith S. J. (1990) Glutamate induces calcium waves in cultured astrocytes: long-range glial signaling. Science 247, 470-473.
12. 2+ and filopodial responses to glutamate in cultured astrocytes and neurons. Can. J. Physiol. Pharmacol. 70 (Suppl.), S206-S218.
13. Cotrina M. L., Lin J. H., Alves-Rodrigues A., Liu S., Li J., Azmi-Ghadimi H., Kang J., Naus C. C., and Nedergaard M. (1998a) Connexins regulate calcium signaling by controlling ATP release. Proc. Natl. Acad. Sci. USA 95, 15735-15740.
14. Cotrina M. L., Lin J. H., and Nedergaard M. (1998b) Cytoskeletal assembly and ATP release regulate astrocytic calcium signaling. J. Neurosci. 18, 8794-8804.
15. Dermietzel R., Hertberg E. L., Kessler J. A., and Spray D. C. (1991) Gap junctions between cultured astrocytes: immunocytochemical, molecular, and electrophysiological analysis. J. Neurosci. 11, 1421-1432.
16. Dingledine R. (1983) N-Methyl aspartate activates voltage-dependent calcium conductance in rat hippocampal pyramidal cells. J. Physiol. (Lond.) 343, 385-340.
17. Duffy S. and MacVicar B. A. (1995) Adrenergic calcium signaling in astrocyte networks within the hippocampal slice. J. Neurosci. 15, 5535-5550.
18. ++ channels. J. Pharmacol. Exp. Ther. 269, 221-229.
19. Enkvist M. O. K. and McCarthy K. D. (1992) Activation of protein kinase C blocks astroglial gap junction communication and inhibits the spread of calcium waves. J. Neurochem. 59, 519-526.
20. + concentration. J. Neurochem. 62, 489-495.
21. Freund T. F. and Buzsaki G. (1996) Interneurons of the hippocampus. Hippocampus 6, 347-470.
22. Frotscher M., Schiander M., and Leranth C. (1986) Cholinergic neurons in the hippocampus. A combined light- and electron-microscopic immunocytochemical study in the rat. Cell Tissue Res. 246, 293-301.
23. Giaume C., Fromaget C., et Aoumari A., Cordier J., Glowinski J., and Gros D. (1991) Gap junctions in cultured astrocytes: single-channel currents and characterization of channel-forming protein. Neuron 6, 133-143.
24. Guthrie P. B., Knappenberger J., Segal M., Bennett M. V. L., Charles A. C., and Kater S. B. (1999) ATP released from astrocytes mediates glial calcium waves. J. Neurosci. 19, 520-528.
25. Hayashi H., Takagi H., Takeda N., Kubota Y., Tohyama M., Watanabe T., and Wada H. (1984) Fine structure of histaminergic neurons in the caudal magnocellular nucleus of the rat as demonstrated by immunocytochemistry using histidine decarboxylase as a marker. J. Comp. Neurol. 229, 233-241.
26. Hosli E. and Hosli L. (1988) Autoradiographic localization of binding sites for muscarinic and nicotinic agonists and antagonists on cultured astrocytes. Exp. Brain Res. 71, 450-454.
27. Hosli E., Ledergerber M., Kofler A., and Hosli L. (1997) Evidence for the existence of galanin receptors on cultured astrocytes of rat CNS: colocalization with cholinergic receptors. J. Chem. Neuroanat. 13, 95-103.
28. Hosli L., Hosli E., Della Briotta G., Quadri L., and Heuss L. (1988) Action of acetylcholine, muscarine, nicotine and antagonists on the membrane potential of astrocytes in cultured rat brainstem and spinal cord. Neurosci. Lett. 92, 165-170.
29. Jeftinija S. D., Jeftinija K. V., Stefanovic G., and Liu F. (1996) Neuroligand-evoked calcium-dependent release of excitatory amino acids from cultured astrocytes. J. Neurochem. 66, 676-684.
30. Kang J., Jiang L., Goldman S. A., and Nedergaard M. (1998) Astrocyte-mediated potentiation of inhibitory synaptic transmission. Nat. Neurosci. 1, 683-692.
31. Katz B. and Miledi R. (1967) A study of synaptic transmission in the absence of nerve impulses. J. Physiol. (Lond.) 192, 407-436.
32. Kawabata S., Tsutsumi R., Kohara A., Yamaguchi T., Nakanishi S., and Okada M. (1996) Control of calcium oscillations by phosphorylation of metabotropic glutamate receptors. Nature 383, 89-91.
33. Kettenmann H. and Ransom B. R. (1988) Electrical coupling between astrocytes and between oligodendrocytes studied in mammalian cell cultures. Glia 1, 64-73.
34. Kimelberg H. K., Cai Z., Rastogi P., Charniga C. J., Goderie S., Dave V., and Jalonen T. O. (1997) Transmitter-induced calcium responses differ in astrocytes acutely isolated from rat brain and in culture. J. Neurochem. 68, 1088-1098.
35. Kirischuk S., Tuschick S., Verkhratsky A., and Kettenmann H. (1996) Calcium signalling in mouse Bergmann glial cells mediated by alpha1-adrenoreceptors and H1 histamine receptors. Eur. J. Neurosci. 8, 1198-1208.
36. Konietzko U. and Muller C. M. (1994) Astrocytic dye coupling in rat hippocampus: topography, developmental onset, and modulation by protein kinase C. Hippocampus 4, 297-306.
37. Lerea L. S. and McCarthy K. D. (1990) Neuron-associated astroglial cells express beta- and alpha 1-adrenergic receptors in vitro. Brain Res. 521, 7-14.
38. Lewis P. R. and Shute C. C. (1967) The cholinergic limbic system: projections to hippocampal formation, medial cortex, nuclei of the ascending cholinergic reticular system, and the subfornical organ and supra-optic crest. Brain 90, 521-540.
39. Matsumoto T., Kanaide H., Nishimura J., Shogakiuchi Y., Kobayashi S., and Nakamura M. (1986) Histamine activates H1-receptors to induce cytosolic free calcium transients in cultured vascular smooth muscie cells from rat aorta. Biochem. Biophys. Res. Commun. 135, 172-177.
40. Muller T., Moller T., Neuhaus J., and Kettenmann H. (1996) Electrical coupling among Bergmann glial cells and its modulation by glutamate receptor activation. Glia 17, 274-284.
41. Murphy S., Pearce B., and Morrow C. (1986) Astrocytes have both M1 and M2 muscarinic receptor subtypes. Brain Res. 364, 177-180.
42. Nedergaard M. (1994) Direct signaling from astrocytes to neurons in cultures of mammalian brain cells. Science 263, 1768-1771.
43. Newman E. A. and Zahs K. R. (1997) Calcium waves in retinal glial cells. Science 275, 844-847.
44. Newman E. A. and Zahs K. R. (1998) Modulation of neuronal activity by glial cells in the retina. J. Neurosci. 18, 4022-4028.
45. O'Connor E. R. and Kimelberg H. K. (1993) Role of calcium in astrocyte volume regulation and in the release of ions and amino acids. J. Neurosci. 13, 2638-2650.
46. Parpura V., Basarsky T. A., Liu F., Jeftinija K., Jeftinija S., and Haydon P. G. (1994) Glutamate-mediated astrocyte-neuron signalling. Nature 369, 744-747.
47. Parpura V., Liu F., Brethorst S., Jeftinija K., Jeftinija S., and Haydon P. G. (1995) Alpha-latrotoxin stimulates glutamate release from cortical astrocytes in cell culture FEBS Lett. 360, 266-270.
48. Pasti L., Pozzan T., and Carmignoto G. (1995) Long-lasting changes of calcium oscillations in astrocytes. J. Biol. Chem. 270, 15203-15210.
49. Pasti L., Volterra A., Pozzan T., and 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.
50. i oscillations. Soc. Neurosci. Abstr. 24, 1753.
51. i in hippocampal astrocytes in situ. J. Neurochem. 65, 1515-1523.
52. i. Glia 13, 101-112.
53. Porter J. T. and McCarthy K. D. (1996) Hippocampal astrocytes in situ respond to glutamate released from synaptic terminals. J. Neurosci. 16, 5073-5081.
54. Porter J. T. and McCarthy K. D. (1997) Astrocytic neurotransmitter receptors in situ and in vivo. Prog. Neurobiol. 51, 439-455.
55. Quandt F. N. and MacVicar B. A. (1986) Calcium activated potassium channels in cultured astrocytes. Neuroscience 19, 29-41.
56. Schlicker E., Malinowska B., Kathmann M., and Gothert M. (1994) Modulation of neurotransmitter release via histamine H3 heteroreceptors. Fundam. Clin. Pharmacol. 8, 128-137.
57. Schwartz J. C., Arrang J. M., Garbarg M., Pollard H., and Ruat M. (1991) Histaminergic transmission in the mammalian brain. Physiol Rev. 71, 1-51.
58. Shao Y. and McCarthy K. D. (1993) Regulation of astroglial responsiveness to neuroligands in primary culture. Neuroscience 55, 991-1001.
59. Shelton M. K. and McCarthy K. D. (1999) Mature hippocampal astrocytes exhibit functional metabotropic and ionotropic glutamate receptors in situ. Glia 26, 1-11.
60. Sheridan R. D. and Sutor B. (1990) Presynaptic M1 muscarinic cholinoceptors mediate inhibition of excitatory synaptic transmission in the hippocampus in vitro. Neurosci. Lett. 108, 273-278.
61. Takagi H., Morishima Y., Matsuyama T., Hayashi H., Watanabe T., and Wada H. (1986) Histaminergic axons in the neostriatum and cerebral cortex of the rat: a correlated light and electron microscopic immunocytochemical study using histidine decarboxylase as a marker. Brain Res. 364, 114-123.
62. Van der Zee E. A., Matsuyama T., Strosberg A. D., Traber J., and Luiten P. G. (1989) Demonstration of muscarinic acetylcholine receptor-like immunoreactivity in the rat forebrain and upper brainstem. Histochemistry 92, 475-485.
63. Van der Zee E. A., De Jong G. I., Strosberg A. D., and Luiten P. G. (1993) Muscarinic acetylcholine receptor-expression in astrocytes in the cortex of young and aged rats. Glia 8, 42-50.
64. Verkhratsky A., Orkand R. K., and Kettenmann H. (1998) Glial calcium: homeostasis and signaling function. Physiol. Rev. 78, 99-141.
65. Walz W. (1995) Acetylcholine and serotonin receptor activation, in Neuroglia (Kettenmann H. and Ransom B. R., eds), pp. 3-22. Oxford, New York.
66. Woolf N. J., Eckenstein F., and Butcher L. L. (1984) Cholinergic systems in the rat brain: I. Projections to the limbic telencephalon. Brain Res. Bull. 13, 751-784.
67. Zahs K. R. (1998) Heterotypic coupling between glial cells of the mammalian central nervous system. Glia 24, 85-96.