Home LiteratureArticle Details
PMID: 11264297 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Propagation of intercellular calcium waves in retinal astrocytes and Müller cells.

Newman EA

Abstract

Intercellular Ca(2+) waves are believed to propagate through networks of glial cells in culture in one of two ways: by diffusion of IP(3) between cells through gap junctions or by release of ATP, which functions as an extracellular messenger. Experiments were conducted to determine the mechanism of Ca(2+) wave propagation between glial cells in an intact CNS tissue. Calcium waves were imaged in the acutely isolated rat retina with the Ca(2+) indicator dye fluo-4. Mechanical stimulation of astrocyte somata evoked Ca(2+) waves that propagated through both astrocytes and Müller cells. Octanol (0.5 mm), which blocks coupling between astrocytes and Müller cells, did not reduce propagation into Müller cells. Purinergic receptor antagonists suramin (100 microm), PPADS (20-50 microm), and apyrase (80 U/ml), in contrast, substantially reduced wave propagation into Müller cells (wave radii reduced to 16-61% of control). Suramin also reduced wave propagation from Müller cell to Müller cell (51% of control). Purinergic antagonists reduced wave propagation through astrocytes to a lesser extent (64-81% of control). Mechanical stimulation evoked the release of ATP, imaged with the luciferin-luciferase bioluminescence assay. Peak ATP concentration at the surface of the retina averaged 78 microm at the stimulation site and 6.8 microm at a distance of 100 microm. ATP release propagated outward from the stimulation site with a velocity of 41 microm/sec, somewhat faster than the 28 microm/sec velocity of Ca(2+) waves. Ejection of 3 microm ATP onto the retinal surface evoked propagated glial Ca(2+) waves. Together, these results indicate that Ca(2+) waves are propagated through retinal glial cells by two mechanisms. Waves are propagated through astrocytes principally by diffusion of an internal messenger, whereas waves are propagated from astrocytes to Müller cells and from Müller cells to other Müller cells primarily by the release of ATP.

MeSH Terms
Adenosine Triphosphate/metabolism Animals Astrocytes/physiology Calcium/metabolism,physiology Calcium Channels/physiology Evoked Potentials/physiology Mice Rats Rats, Long-Evans Retina/cytology,physiology
Chemicals
Calcium Channels Adenosine Triphosphate Calcium
Authors & Affiliations
1 authors, click to expand affiliations / ORCID
Newman E A
Department of Neuroscience, University of Minnesota, Minneapolis, Minnesota 55455, USA. ean@tc.umn.edu
References (42)
42 references, click to expand
  1. P2Y(1) purinoceptor-mediated Ca(2+) signaling and Ca(2+) wave propagation in dorsal spinal cord astrocytes.
    J Neurosci. 2000 Apr 15;20(8):2800-8 PMID: 10751431
  2. ATP-mediated glia signaling.
    J Neurosci. 2000 Apr 15;20(8):2835-44 PMID: 10751435
  3. Evidence for P2X(3), P2X(4), P2X(5) but not for P2X(7) containing purinergic receptors in Müller cells of the rat retina.
    Brain Res Mol Brain Res. 2000 Mar 29;76(2):205-10 PMID: 10762695
  4. Direct observation of calcium-independent intercellular ATP signaling in astrocytes.
    Anal Chem. 2000 May 1;72(9):2001-7 PMID: 10815957
  5. P2X7 receptors in Müller glial cells from the human retina.
    J Neurosci. 2000 Aug 15;20(16):5965-72 PMID: 10934244
  6. Membrane physiology of retinal glial (Müller) cells.
    J Neurosci. 1985 Aug;5(8):2225-39 PMID: 3874934
  7. Neuronal activity triggers calcium waves in hippocampal astrocyte networks.
    Neuron. 1992 Mar;8(3):429-40 PMID: 1347996
  8. Calcium waves in astrocytes-filling in the gaps.
    Neuron. 1992 Jun;8(6):1101-8 PMID: 1351732
  9. Intercellular calcium signaling via gap junctions in glioma cells.
    J Cell Biol. 1992 Jul;118(1):195-201 PMID: 1320034
  10. Activation of protein kinase C blocks astroglial gap junction communication and inhibits the spread of calcium waves.
    J Neurochem. 1992 Aug;59(2):519-26 PMID: 1629725
  11. Intercellular propagation of calcium waves mediated by inositol trisphosphate.
    Science. 1992 Oct 9;258(5080):292-5 PMID: 1411526
  12. Mechanisms of intercellular calcium signaling in glial cells studied with dantrolene and thapsigargin.
    Glia. 1993 Feb;7(2):134-45 PMID: 8094375
  13. Glial calcium: homeostasis and signaling function.
    Physiol Rev. 1998 Jan;78(1):99-141 PMID: 9457170
  14. Prostaglandins stimulate calcium-dependent glutamate release in astrocytes.
    Nature. 1998 Jan 15;391(6664):281-5 PMID: 9440691
  15. The sleep-inducing lipid oleamide deconvolutes gap junction communication and calcium wave transmission in glial cells.
    J Cell Biol. 1997 Dec 29;139(7):1785-92 PMID: 9412472
  16. Glial calcium.
    Glia. 1993 Oct;9(2):83-104 PMID: 8244537
  17. Asymmetric gap junctional coupling between glial cells in the rat retina.
    Glia. 1997 May;20(1):10-22 PMID: 9145301
  18. Expression of the P2X2 receptor subunit of the ATP-gated ion channel in the retina.
    Neuroreport. 1997 Mar 24;8(5):1083-8 PMID: 9175089
  19. Modulation of neuronal activity by glial cells in the retina.
    J Neurosci. 1998 Jun 1;18(11):4022-8 PMID: 9592083
  20. Calcium elevation in astrocytes causes an NMDA receptor-dependent increase in the frequency of miniature synaptic currents in cultured hippocampal neurons.
    J Neurosci. 1998 Sep 1;18(17):6822-9 PMID: 9712653
  21. Modulation of [3H]acetylcholine release from cultured amacrine-like neurons by adenosine A1 receptors.
    J Neurochem. 1998 Sep;71(3):1086-94 PMID: 9721733
  22. Glutamate-dependent astrocyte modulation of synaptic transmission between cultured hippocampal neurons.
    Eur J Neurosci. 1998 Jun;10(6):2129-42 PMID: 9753099
  23. Receptors for purines and pyrimidines.
    Pharmacol Rev. 1998 Sep;50(3):413-92 PMID: 9755289
  24. Cytoskeletal assembly and ATP release regulate astrocytic calcium signaling.
    J Neurosci. 1998 Nov 1;18(21):8794-804 PMID: 9786986
  25. Modulation of synaptic efficacy and synaptic depression by glial cells at the frog neuromuscular junction.
    Neuron. 1998 Oct;21(4):847-55 PMID: 9808470
  26. Connexins regulate calcium signaling by controlling ATP release.
    Proc Natl Acad Sci U S A. 1998 Dec 22;95(26):15735-40 PMID: 9861039
  27. ATP released from astrocytes mediates glial calcium waves.
    J Neurosci. 1999 Jan 15;19(2):520-8 PMID: 9880572
  28. Astrocyte-mediated potentiation of inhibitory synaptic transmission.
    Nat Neurosci. 1998 Dec;1(8):683-92 PMID: 10196584
  29. Ca2+-permeable P2X receptor channels in cultured rat retinal ganglion cells.
    J Neurosci. 1999 May 1;19(9):3353-66 PMID: 10212295
  30. IL-1beta differentially regulates calcium wave propagation between primary human fetal astrocytes via pathways involving P2 receptors and gap junction channels.
    Proc Natl Acad Sci U S A. 1999 Sep 28;96(20):11613-8 PMID: 10500225
  31. Prostaglandin E(2) stimulates glutamate receptor-dependent astrocyte neuromodulation in cultured hippocampal cells.
    J Neurobiol. 1999 Nov 5;41(2):221-9 PMID: 10512979
  32. Mechanisms and function of intercellular calcium signaling.
    Mol Cell Endocrinol. 1994 Jan;98(2):173-87 PMID: 8143927
  33. Glutamate-mediated astrocyte-neuron signalling.
    Nature. 1994 Jun 30;369(6483):744-7 PMID: 7911978
  34. Extracellular ATP-induced currents in astrocytes: involvement of a cation channel.
    J Neurosci Res. 1994 May 1;38(1):12-8 PMID: 7520086
  35. Evidence for glutamate-mediated activation of hippocampal neurons by glial calcium waves.
    J Neurobiol. 1995 Oct;28(2):159-70 PMID: 8537822
  36. P2 purinoceptors in rat cortical astrocytes: expression, calcium-imaging and signalling studies.
    Neuroscience. 1996 Oct;74(4):1187-96 PMID: 8895885
  37. Imaging extracellular waves of glutamate during calcium signaling in cultured astrocytes.
    J Neurosci. 2000 Mar 1;20(5):1800-8 PMID: 10684881
  38. Intercellular communication in spinal cord astrocytes: fine tuning between gap junctions and P2 nucleotide receptors in calcium wave propagation.
    J Neurosci. 2000 Feb 15;20(4):1435-45 PMID: 10662834
  39. An eyecup preparation for the rat and mouse.
    J Neurosci Methods. 1999 Nov 15;93(2):169-75 PMID: 10634502
  40. The effects of temperature, pH, and magnesium on the diffusion coefficient of ATP in solutions of physiological ionic strength.
    Biochim Biophys Acta. 1996 Oct 24;1291(2):115-21 PMID: 8898871
  41. An extracellular signaling component in propagation of astrocytic calcium waves.
    Proc Natl Acad Sci U S A. 1996 Nov 12;93(23):13268-73 PMID: 8917580
  42. Calcium waves in retinal glial cells.
    Science. 1997 Feb 7;275(5301):844-7 PMID: 9012354
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
1529-2401
Published
2001-04-01
Pages
2215-23
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC2409971
Subset
IM
Grants
NEI NIH HHS · R01 EY004077 · United States
NEI NIH HHS · R01 EY004077-21 · United States
NEI NIH HHS · EY04077 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com