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PMID: 10500225 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

IL-1beta differentially regulates calcium wave propagation between primary human fetal astrocytes via pathways involving P2 receptors and gap junction channels.

John GR, Scemes E, Suadicani SO, Liu JS, Charles PC, Lee SC, Spray DC, Brosnan CF

Abstract

In mammalian astrocytes, calcium waves are transmitted between cells via both a gap junction-mediated pathway and an extracellular, P2 receptor-mediated pathway, which link the cells into a syncytium. Calcium waves in astrocytes have also been shown to evoke calcium transients in neurons, and activity in neurons can elicit calcium waves in astrocytes. In this study, we show that in primary human fetal astrocytes, the P2 receptor-mediated and gap junction-mediated pathways are differentially regulated by the cytokine IL-1beta. Confocal microscopy of astrocytes loaded with Indo-1 demonstrated that intercellular calcium wave transmission in IL-1beta-treated cultures was potentiated compared with controls. However, transmission of calcium waves via the gap junction-mediated pathway was strikingly reduced. The major component of functional gap junctions in human fetal astrocytes was demonstrated to be connexin43 (Cx43), and there was a marked reduction of junctional conductance, loss of dye coupling, loss of Cx43 protein, and down-regulation of Cx43 mRNA expression after IL-1beta treatment of cultures. Conversely, transmission of calcium waves via the P2 receptor-mediated pathway was potentiated in IL-1beta-treated cultures compared with controls. This potentiation was associated with an increase in the number of cells responsive to UTP, and with a transient increase in expression of the P2Y(2) purinoceptor mRNA. Because in inflammatory conditions of the human central nervous system IL-1beta is produced both by resident glia and by invading cells of the immune system, our results suggest that inflammatory events may have a significant impact on coordination of astrocytic function and on information processing in the central nervous system.

MeSH Terms
Astrocytes/metabolism Calcium/metabolism Cell Communication/drug effects Cells, Cultured Connexin 43/genetics Fetus/metabolism Gap Junctions/physiology Humans Interleukin-1/pharmacology RNA, Messenger/analysis Receptors, Purinergic P2/genetics,physiology Uridine Triphosphate/pharmacology
Chemicals
Connexin 43 Interleukin-1 RNA, Messenger Receptors, Purinergic P2 Calcium Uridine Triphosphate
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
John G R
Department of Pathology, Albert Einstein College of Medicine, 1300 Morris Park Avenue, Bronx, NY 10461, USA.
Scemes E
Suadicani S O
Liu J S
Charles P C
Lee S C
Spray D C
Brosnan C F
References (38)
38 references, click to expand
  1. Differential phosphorylation of the gap junction protein connexin43 in junctional communication-competent and -deficient cell lines.
    J Cell Biol. 1990 Nov;111(5 Pt 1):2077-88 PMID: 2172261
  2. Gap-junction-mediated propagation and amplification of cell injury.
    Nat Neurosci. 1998 Oct;1(6):494-500 PMID: 10196547
  3. Intercellular signaling in glial cells: calcium waves and oscillations in response to mechanical stimulation and glutamate.
    Neuron. 1991 Jun;6(6):983-92 PMID: 1675864
  4. Neuronal activity triggers calcium waves in hippocampal astrocyte networks.
    Neuron. 1992 Mar;8(3):429-40 PMID: 1347996
  5. Cytokine expression in the brain during the acquired immunodeficiency syndrome.
    Ann Neurol. 1992 Apr;31(4):349-60 PMID: 1586135
  6. Calcium waves in astrocytes-filling in the gaps.
    Neuron. 1992 Jun;8(6):1101-8 PMID: 1351732
  7. Cell-to-cell spread of calcium signals mediated by ATP receptors in mast cells.
    Nature. 1992 Sep 17;359(6392):241-4 PMID: 1388246
  8. Intercellular propagation of calcium waves mediated by inositol trisphosphate.
    Science. 1992 Oct 9;258(5080):292-5 PMID: 1411526
  9. Characterization of primary human fetal dissociated central nervous system cultures with an emphasis on microglia.
    Lab Invest. 1992 Oct;67(4):465-76 PMID: 1359193
  10. Expression cloning of an ATP receptor from mouse neuroblastoma cells.
    Proc Natl Acad Sci U S A. 1993 Jun 1;90(11):5113-7 PMID: 7685114
  11. Cloning and functional expression of a brain G-protein-coupled ATP receptor.
    FEBS Lett. 1993 Jun 14;324(2):219-25 PMID: 8508924
  12. Mechanisms and function of intercellular calcium signaling.
    Mol Cell Endocrinol. 1994 Jan;98(2):173-87 PMID: 8143927
  13. Cloning and expression of a human P2U nucleotide receptor, a target for cystic fibrosis pharmacotherapy.
    Proc Natl Acad Sci U S A. 1994 Apr 12;91(8):3275-9 PMID: 8159738
  14. Glutamate-mediated astrocyte-neuron signalling.
    Nature. 1994 Jun 30;369(6483):744-7 PMID: 7911978
  15. Molecular cloning of two human cardiac gap junction proteins, connexin40 and connexin45.
    J Mol Cell Cardiol. 1994 Jul;26(7):861-8 PMID: 7966354
  16. Interleukin-1 immunoreactive innervation of the human hypothalamus.
    Science. 1988 Apr 15;240(4850):321-4 PMID: 3258444
  17. Hepatocyte gap junctions are permeable to the second messenger, inositol 1,4,5-trisphosphate, and to calcium ions.
    Proc Natl Acad Sci U S A. 1989 Apr;86(8):2708-12 PMID: 2784857
  18. Brain interleukin 1 and S-100 immunoreactivity are elevated in Down syndrome and Alzheimer disease.
    Proc Natl Acad Sci U S A. 1989 Oct;86(19):7611-5 PMID: 2529544
  19. Glutamate induces calcium waves in cultured astrocytes: long-range glial signaling.
    Science. 1990 Jan 26;247(4941):470-3 PMID: 1967852
  20. Neuronal domains in developing neocortex: mechanisms of coactivation.
    Neuron. 1995 Jan;14(1):7-17 PMID: 7826643
  21. The adhesion molecule and cytokine profile of multiple sclerosis lesions.
    Ann Neurol. 1995 Apr;37(4):424-35 PMID: 7536402
  22. Cytokines and the nervous system. I: Expression and recognition.
    Trends Neurosci. 1995 Feb;18(2):83-8 PMID: 7537419
  23. Calcium signaling in cultured rat oligodendrocytes.
    Glia. 1995 Jul;14(3):225-36 PMID: 7591034
  24. Cloning and functional expression of a human uridine nucleotide receptor.
    J Biol Chem. 1995 Dec 29;270(52):30849-52 PMID: 8537336
  25. Expression of type II nitric oxide synthase in primary human astrocytes and microglia: role of IL-1beta and IL-1 receptor antagonist.
    J Immunol. 1996 Oct 15;157(8):3569-76 PMID: 8871657
  26. P2 purinoceptors in rat cortical astrocytes: expression, calcium-imaging and signalling studies.
    Neuroscience. 1996 Oct;74(4):1187-96 PMID: 8895885
  27. 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
  28. Calcium waves in retinal glial cells.
    Science. 1997 Feb 7;275(5301):844-7 PMID: 9012354
  29. Down-regulation of P2U-purinergic nucleotide receptor messenger RNA expression during in vitro differentiation of human myeloid leukocytes by phorbol esters or inflammatory activators.
    Mol Pharmacol. 1997 Jan;51(1):97-108 PMID: 9016351
  30. Interleukin-1 enhances the ATP-evoked release of arachidonic acid from mouse astrocytes.
    J Neurosci. 1997 May 1;17(9):2939-46 PMID: 9096130
  31. Gap junctions equalize intracellular Na+ concentration in astrocytes.
    Glia. 1997 Aug;20(4):299-307 PMID: 9262234
  32. 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
  33. Calcium waves between astrocytes from Cx43 knockout mice.
    Glia. 1998 Sep;24(1):65-73 PMID: 9700490
  34. Regulation by retinoids of P2Y2 nucleotide receptor mRNA in human uterine cervical cells.
    Am J Physiol. 1998 Sep;275(3 Pt 1):C758-65 PMID: 9730959
  35. Pyrimidinoceptor-mediated potentiation of inducible nitric-oxide synthase induction in J774 macrophages. Role of intracellular calcium.
    J Biol Chem. 1998 Nov 6;273(45):29754-63 PMID: 9792689
  36. The kinase TAK1 can activate the NIK-I kappaB as well as the MAP kinase cascade in the IL-1 signalling pathway.
    Nature. 1999 Mar 18;398(6724):252-6 PMID: 10094049
  37. Positive and negative regulation of IkappaB kinase activity through IKKbeta subunit phosphorylation.
    Science. 1999 Apr 9;284(5412):309-13 PMID: 10195894
  38. Gap junctions between cultured astrocytes: immunocytochemical, molecular, and electrophysiological analysis.
    J Neurosci. 1991 May;11(5):1421-32 PMID: 1851221
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
1999-09-28
Pages
11613-8
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC18082
Subset
IM
Grants
NINDS NIH HHS · NS11920 · United States
NIMH NIH HHS · R01 MH055477 · United States
NIGMS NIH HHS · T32GM07288 · United States
NINDS NIH HHS · P50 NS011920 · United States
NIGMS NIH HHS · T32 GM007288 · United States
NINDS NIH HHS · R01 NS062703 · United States
NIMH NIH HHS · MH55477 · United States
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