Regulation of the astrocyte resting membrane potential by cyclic AMP and protein kinase A

GLIA

Volumn 54, Issue 4, 2006, Pages 316-328

  Bolton, Sally ^a   Greenwood, Kirsty ^b   Hamilton, Nicola ^b   Butt, Arthur M ^a  

^a UNIVERSITY OF PORTSMOUTH   (United Kingdom)

^b KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

Astrocyte; cAMP; Glia; Inward rectifying potassium channels; Kir 4.1; Protein kinase A; Resting membrane potential

Indexed keywords

ADENOSINE TRIPHOSPHATE; BARIUM CHLORIDE; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; DIAZOXIDE; FORSKOLIN; GLIBENCLAMIDE; POTASSIUM CHANNEL; ROLIPRAM;

ANIMAL CELL; ARTICLE; ASTROCYTE; CELL MATURATION; CONTROLLED STUDY; DRUG EFFECT; FEMALE; HYPERPOLARIZATION; MALE; MEMBRANE STEADY POTENTIAL; NONHUMAN; OPTIC NERVE; PHENOTYPE; PRIORITY JOURNAL; RAT;

ANIMALS; ASTROCYTES; CELL SHAPE; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; ELECTROPHYSIOLOGY; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; GLIAL FIBRILLARY ACIDIC PROTEIN; IMMUNOHISTOCHEMISTRY; MEMBRANE POTENTIALS; MICE; MICE, INBRED C57BL; MICROELECTRODES; OPTIC NERVE; POTASSIUM; POTASSIUM CHANNEL BLOCKERS; POTASSIUM CHANNELS, INWARDLY RECTIFYING; RATS; RATS, WISTAR;

EID: 33748187164     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.20384     Document Type: Article

References (55)

1. Balazs R, Miller S, Chun Y, O'Toole J, Cotman CW. 1998. Metabotropic glutamate receptor agonists potentiate cyclic AMP formation induced by forskolin or β-adrenergic receptor activation in cerebral cortical astrocytes in culture. J Neurochem 70:2446-2458.
2. + buffer capacity and morphology of glial cells in the corpus callosum slice. J Neurosci 11:3008-3024.
3. Bolton S, Butt AM. 2005. The optic nerve: A model for axon-glial interactions. J Pharmacol Toxicol Methods 51:221-233.
4. Bordey A, Sontheimer H. 1997. Postnatal development of ionic currents in rat hippocampal astrocytes in situ. J Neurophysiol 78:461-477.
5. Bordey A, Sontheimer H. 1998. Passive glial cells, fact or artifact? J Membr Biol 166:213-222.
6. + channels in ontogeny and gliosis. A hypothesis based upon studies in Müller cells. Glia 29:35-44.
7. Brockhaus J, Deitmer J. 2000. Developmental downregulation of ATP-sensitive potassium conductance in astrocytes in situ. Glia 32:205-213.
8. Butt AM, Colquhoun K, Berry M. 1994a. Confocal imaging of glial cells in the intact rat optic nerve. Glia 10:315-322.
9. Butt AM, Duncan A, Berry M. 1994b. Astrocyte associations with nodes of Ranvier: Ultrastructural analysis of HRP-filled astrocytes in the mouse optic nerve. J Neurocytol 23:486-499.
10. Butt AM, Duncan A, Hornby MF, Kirvell SL, Hunter A, Levine JM, Berry M. 1999. Cells expressing the NG2 antigen contact nodes of Ranvier in adult CNS white matter. Glia 26:84-91.
11. Butt AM, Greenwood K, Bolton S. 2005a. Evidence of a role for Kir4.1 on setting the resting membrane potential of optic nerve glia. J Anat 206:493
12. Butt AM, Hamilton N, Hubbard P, Pugh M, Ibrahim M. 2005b. Synantocytes: The fifth element. J Anat 297:695-706.
13. Butt AM, Kalsi A. 2006. Inwardly rectifying potassium channels (Kir) in CNS glia: A special role for Kir4.1 in glial functions. J Cell Mol Med, in press.
14. Butt AM, Ransom BR. 1993. Morphology of astrocytes and oligodendrocytes during development in the intact rat optic nerve. J Comp Neurol 338:141-158.
15. Chvatal A, Pastor A, Mauch M, Sykova E, Kettenmann H. 1995. Distinct populations of identified glial cells in the developing rat spinal cord slice: Ion channel properties and cell morphology. Eur J Neurosci 7:129-142.
16. + accumulation in the developing rat optic nerve. Science 216:1341-1343.
17. D'Ambrosio R, Wenzel J, Schwartzkroin PA, McKhann GM, Janigro D. 1998. Functional specialization and topographic segregation of hippocampal astrocytes. J Neurosci 18:4425-4438.
18. Dennis MJ, Gerschenfeld HM. 1969. Some physiological properties of identified mammalian neuroglial cells. J Physiol 203:211-222.
19. Grass D, Pawlowski PG, Hirrlinger J, Papadopoulos N, Richter DW, Kirchhoff F, Hülsmann S. 2004. Diversity of functional astroglial properties in the respiratory network. J Neurosci 24:1358-1365.
20. + channel subunits, Kir4.1 and Kir5.1, in brain astrocytes. J Biol Chem 279:44065-44073.
21. Higashi K, Fujita A, Inanobe A, Tanemoto M, Doi K, Kako T, Kurachi Y. 2001. An inwardly rectifying K(+) channel, Kir4.1, expressed in astrocytes surrounds synapses and blood vessels in brain. Am J Cell Physiol 281:C922-931.
22. Jackson WF. 2005. Potassium channels in the peripheral microcirculation. Microcirculation 12:113-127.
23. Jeffery G, Sharp C, Malitschek B, Salt TE, Kuhn R, Knopfel T. 1996. Cellular localisation of metabotropic glutamate receptors in the mammalian optic nerve: A mechanism for axon-glia communication. Brain Res 741:75-81.
24. Kalsi AS, Greenwood K, Wilkin G, Butt AM. 2004. Kir4.1 expression by astrocytes and oligodendrocytes in CNS white matter: A developmental study in the rat optic nerve. J Anat 204:475-485.
25. Kofuji P, Biedermann B, Siddharthan V, Raap M, Iandiev I, Milenkovic I, Thomzig A, Veh RW, Bringmann A, Reichenbach A. 2002. Kir potassium channel subunit expression in retinal glial cells: Implications for spatial potassium buffering. Glia 39:292-303.
26. Kofuji P, Ceelen P, Zahs KR, Surbeck LW, Lester HA, Newman EA. 2000. Genetic inactivation of an inwardly rectifying potassium channel (Kir4.1 subunit) in mice: Phenotypic impact in retina. J Neurosci 20:5733-5740.
27. Kofuji P, Newman EA. 2004. Potassium buffering in the central nervous system. Neuroscience 129:1045-1056.
28. Koizumi A, Jakobs TC, Masland RH. 2004. Inward rectifying currents stabilize the membrane potential in dendrites of mouse amacrine cells: Patch-clamp recordings and single-cell RT-PCR. Mol Vis 10: 328-340.
29. + conductances in glial cells of mouse hippocampal brain slices. Glia 15:173-187.
30. Kuffler SW, Nicholls JG, Orkand RK. 1966. Physiological properties of glial cells in the central nervous system of amphibia. J Neurophysiol 29:768-787.
31. Leonoudakis D, Mailliard W, Wingerd K, Clegg D, Vandenberg C. 2001. Inward rectifier potassium channel Kir2.2 is associated with synapse-associated protein SAP97. J Cell Sci 114:987-998.
32. Levine JM, Card JP. 1987. Light and electron microscopic localization of a cell surface antigen (NG2) in the rat cerebellum: Association with smooth protoplasmic astrocytes. J Neurosci 7:2711-2720.
33. Mantyh PW, Rogers SD, Allen CJ, Catton MD, Ghilardi JR, Levin LA, Maggio JE, Vigna SR. 1995. Beta 2-adrenergic receptors are expressed by glia in vivo in the normal and injured central nervous system in the rat, rabbit, and human. J Neurosci 15:152-164.
34. Matthias K, Kirchhoff F, Seifert G, Huttmann K, Matyash M, Kettenmann H, Steinhauser C. 2003. Segregated expression of AMPA-type glutamate receptors and glutamate transporters defines distinct astrocyte populations in the mouse hippocampus. J Neurosci 23:1750-1758.
35. McKhann GM, D'Ambrosio R, Janigro D. 1997. Heterogeneity of astrocyte resting membrane potentials and intercellular coupling revealed by whole-cell and gramicidin-perforated patch recordings from cultured neocortical and hippocampal slice astrocytes. J Neurosci 17: 6850-6863.
36. Neusch C, Rozengurt N, Jacobs RE, Lester HA, Kofuji P. 2001. Kir4.1 potassium channel subunit is crucial for oligodendrocyte development and in vivo myelination. J Neurosci 21:5429-5438.
37. + siphoning. Science 225:1174-1175.
38. Newman EA. 1986. High potassium conductance in astrocyte endfeet. Science 2333:453-454.
39. Newman EA. 1993. Inward-rectifying potassium channels in retinal glial (Müller) cells. J Neurosci 13:3333-3345.
40. Orkand RK, Nicholls JG, Kuffler SW. 1966. Effect of nerve impulses on the membrane potential of glial cells in the central nervous system of amphibia. J Neurophysiol 29:788-806.
41. + channel, Kir4.1, in adult rat CNS. Glia 30:362-372.
42. Ransom BR, Goldring S. 1973. Ionic determinants of membrane potential of cells presumed to be glia in cerebral cortex of cat. J Neurophysiol 36:855-868.
43. Roy ML, Sontheimer H. 1995. Beta-adrenergic modulation of glial inwardly rectifying potassium channels. J Neurochem 64:1576-1584.
44. + channels. Eur J Physiol 441:1-11.
45. Schools GP, Zhou M, Kimelberg HK. 2003. Electrophysiologically "complex" glial cells freshly isolated from the hippocampus are immunopositive for the chondroitin sulfate proteoglycan NG2. J Neurosci Res 73:765-777.
46. + channels. Neuroreport 10:1323-1327.
47. Sontheimer H. 1994. Voltage-dependent ion channels in glial cells. Glia 11:156-172.
48. Steinhauser C, Berger T, Frotscher M, Kettenmann H. 1992. Heterogeneity in the membrane current pattern of identified glial cells in the hippocampal slice. Eur J Neurosci 4:472-484.
49. Steinhauser C. 1993. Electrophysiologic characteristics of glial cells. Hippocampus 3:113-123.
50. Verkhratsky A, Steinhauser C. 2000. Ion channels in glial cells. Brain Res Rev 32:380-412.
51. Walz W. 2000. Controversy surrounding the existence of discrete functional classes of astrocytes in adult gray matter. Glia 31:95-103.
52. Wroblewska B, Santi MR, Neale JH. 1998. N-acetylaspartylglutamate activates cyclic AMP-coupled metabotropic glutamate receptors in cerebellar astrocytes. Glia 24:172-179.
53. o uptake capabilities. J Neurophysiol 84:2746-2757.
54. Zhou M, Kimelberg HK. 2001. Freshly isolated hippocampal CA1 astrocytes comprise two populations differing in glutamate transporter and AMPA receptor expression. J Neurosci 21:7901-7908.
55. Zhou M, Schools GP, Kimelberg HK. 2006. Development of GLAST(+) astrocytes and NG2(+) glia in rat hippocampus CA1: Mature astrocytes are electrophysiologically passive. J Neurophysiol 95:134-143.