Specificity of Cell-cell Coupling in Rat Optic Nerve Astrocytes in Vitro

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 1990 Dec 1

PMID 2263634

Citations 5

Authors

H Sontheimer

J E Minturn

J A Black

S G Waxman

B R Ransom

Affiliations

Soon will be listed here.

Abstract

Intercellular coupling was studied in cultured rat optic nerve astrocytes individually characterized by A2B5 antibody staining. The presence of cell coupling was assessed by injecting single cells with the low molecular weight fluorescent dye Lucifer yellow and noting dye passage into adjacent cells; cell coupling was also studied by analyzing the decay phase of current transients recorded in response to small voltage steps using whole-cell patch-clamp recording. Cell coupling was restricted to A2B5- astrocytes, the majority of which had a flat fibroblast-like appearance and was never observed in A2B5+ stellate-shaped astrocytes. Furthermore, A2B5- astrocytes showed coupling only to A2B5- and never to A2B5+ astrocytes. Analysis of current transients provided an additional indicator for cell coupling. Astrocytes that showed dye coupling to at least one neighboring cell required the sum of two exponential functions to fit current transients, whereas a single exponential function sufficed to fit transients in cells that were not dye coupled. The specificity of cell coupling in cultured rat optic nerve astrocytes suggests that predominantly A2B5- astrocytes comprise a coupled glial syncytium; this physiological feature of these cells may be a specialized adaptation for "spatial buffering," the transport of K+ away from areas of focal extracellular accumulation. On the other hand, A2B5+ astrocytes form an uncoupled subpopulation of rat optic nerve glial cells that may serve different functions.

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References

Gutnick M, Connors B, Ransom B . Dye-coupling between glial cells in the guinea pig neocortical slice. Brain Res. 1981; 213(2):486-92. DOI: 10.1016/0006-8993(81)90259-6. View

Hamill O, Marty A, Neher E, Sakmann B, Sigworth F . Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch. 1981; 391(2):85-100. DOI: 10.1007/BF00656997. View

Barres B, Chun L, Corey D . Glial and neuronal forms of the voltage-dependent sodium channel: characteristics and cell-type distribution. Neuron. 1989; 2(4):1375-88. DOI: 10.1016/0896-6273(89)90076-7. View

Stewart W . Functional connections between cells as revealed by dye-coupling with a highly fluorescent naphthalimide tracer. Cell. 1978; 14(3):741-59. DOI: 10.1016/0092-8674(78)90256-8. View

Minturn J, Black J, Angelides K, Waxman S . Sodium channel expression detected with antibody 7493 in A2B5+ and A2B5- astrocytes from rat optic nerve in vitro. Glia. 1990; 3(5):358-67. DOI: 10.1002/glia.440030507. View

Loewenstein W . Junctional intercellular communication: the cell-to-cell membrane channel. Physiol Rev. 1981; 61(4):829-913. DOI: 10.1152/physrev.1981.61.4.829. View

NEWMAN E . Regional specialization of retinal glial cell membrane. Nature. 1984; 309(5964):155-7. PMC: 2693194. DOI: 10.1038/309155a0. View

Fischer G, Kettenmann H . Cultured astrocytes form a syncytium after maturation. Exp Cell Res. 1985; 159(2):273-9. DOI: 10.1016/s0014-4827(85)80001-x. View

CONNER J, Detwiler P, Sarthy P . Ionic and electrophysiological properties of retinal Müller (glial) cells of the turtle. J Physiol. 1985; 362:79-92. PMC: 1192883. DOI: 10.1113/jphysiol.1985.sp015664. View

10.

Spray D, Bennett M . Physiology and pharmacology of gap junctions. Annu Rev Physiol. 1985; 47:281-303. DOI: 10.1146/annurev.ph.47.030185.001433. View

11.

Miller R, Fulton B, Raff M . A Novel Type of Glial Cell Associated with Nodes of Ranvier in Rat Optic Nerve. Eur J Neurosci. 1989; 1(2):172-180. DOI: 10.1111/j.1460-9568.1989.tb00785.x. View

12.

Levi G, Gallo V, Ciotti M . Bipotential precursors of putative fibrous astrocytes and oligodendrocytes in rat cerebellar cultures express distinct surface features and "neuron-like" gamma-aminobutyric acid transport. Proc Natl Acad Sci U S A. 1986; 83(5):1504-8. PMC: 323105. DOI: 10.1073/pnas.83.5.1504. View

13.

Bennett M . Physiology of electrotonic junctions. Ann N Y Acad Sci. 1966; 137(2):509-39. DOI: 10.1111/j.1749-6632.1966.tb50178.x. View

14.

Raff M, Abney E, Cohen J, Lindsay R, Noble M . Two types of astrocytes in cultures of developing rat white matter: differences in morphology, surface gangliosides, and growth characteristics. J Neurosci. 1983; 3(6):1289-1300. PMC: 6564607. View

15.

Kettenmann H, ORKAND R, Schachner M . Coupling among identified cells in mammalian nervous system cultures. J Neurosci. 1983; 3(3):506-16. PMC: 6564554. View

16.

Butt A, Ransom B . Visualization of oligodendrocytes and astrocytes in the intact rat optic nerve by intracellular injection of lucifer yellow and horseradish peroxidase. Glia. 1989; 2(6):470-5. DOI: 10.1002/glia.440020609. View

17.

Waxman S, Black J . Freeze-fracture ultrastructure of the perinodal astrocyte and associated glial junctions. Brain Res. 1984; 308(1):77-87. DOI: 10.1016/0006-8993(84)90919-3. View

18.

Anders J . Lactic acid inhibition of gap junctional intercellular communication in in vitro astrocytes as measured by fluorescence recovery after laser photobleaching. Glia. 1988; 1(6):371-9. DOI: 10.1002/glia.440010604. View

19.

Ransom B, Kettenmann H . Electrical coupling, without dye coupling, between mammalian astrocytes and oligodendrocytes in cell culture. Glia. 1990; 3(4):258-66. DOI: 10.1002/glia.440030405. View

20.

Murphy A, Hadley R, Kater S . Axotomy-induced parallel increases in electrical and dye coupling between identified neurons of Helisoma. J Neurosci. 1983; 3(7):1422-29. PMC: 6564434. View