Sphingosine-1-phosphate mediates calcium signaling in guinea pig enteroglial cells

B. J. Segura; W. Zhang; L. Xiao; D. Turner; R. A. Cowles; C. Logsdon; M. W. Mulholland

doi:10.1016/S0022-4804(03)00281-6

Sphingosine-1-phosphate mediates calcium signaling in guinea pig enteroglial cells

B. J. Segura
, W. Zhang
, L. Xiao
, D. Turner
, R. A. Cowles
, C. Logsdon
, M. W. Mulholland

Surgery

Research output: Contribution to journal › Article › peer-review

17 Scopus citations

Abstract

The enteric nervous system, which regulates multiple aspects of digestive activity, is composed of two major cell types, neurons and glial cells. Enteric glia, but not enteric neurons, respond to bioactive lipids with calcium signaling. The sphingomyelin metabolite sphingosine-1-phosphate (S1P) caused dose-dependent calcium (Ca²⁺) signaling using extracellular and intracellular Ca²⁺. The signal transduction cascade was pertussis toxin-insensitive and involved an extracellular receptor since repetitive exposure yielded diminished responsiveness. Inhibition of either phospholipase C or the inositol 1,4,5-trisphosphate receptor abolished S1P effects. RT-PCR analysis demonstrated the presence of S1P-coupled endothelial differentiation gene (EDG) receptor mRNAs (EDG-1, EDG-3, and EDG-5) within the enteric nervous system. Immunocytochemical analysis demonstrated strong expression of both EDG-1 and EDG-3 and weak expression of EDG-5 in enteric glial cells. Other sphingomyelin cycle components, including sphingomyelin, sphingomyelinase, and sphingosine caused Ca²⁺ transients in enteric glia. Related lipids lysophosphatidic acid and sphingosylphosphorylcholine also induced Ca ²⁺ signaling in enteric glia, suggesting that multiple lipid-activated signaling mechanisms exist in these cells.

Original language	English (US)
Pages (from-to)	42-54
Number of pages	13
Journal	Journal of Surgical Research
Volume	116
Issue number	1
DOIs	https://doi.org/10.1016/S0022-4804(03)00281-6
State	Published - Jan 2004

Bibliographical note

Funding Information:
This research was supported by the National Institutes of Health (DK41204 and accompanying Minority Supplemental Grant, and Systems & Integrative Biology training grant GM08322–11) and by a pre-doctoral fellowship from the Horace Rackham School of Graduate Studies, University of Michigan.

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

SDG 3 Good Health and Well-being

Keywords

Enteroglial cells
Nervous system
Sphingosine-1-phosphate

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10.1016/S0022-4804(03)00281-6

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title = "Sphingosine-1-phosphate mediates calcium signaling in guinea pig enteroglial cells",

abstract = "The enteric nervous system, which regulates multiple aspects of digestive activity, is composed of two major cell types, neurons and glial cells. Enteric glia, but not enteric neurons, respond to bioactive lipids with calcium signaling. The sphingomyelin metabolite sphingosine-1-phosphate (S1P) caused dose-dependent calcium (Ca2+) signaling using extracellular and intracellular Ca2+. The signal transduction cascade was pertussis toxin-insensitive and involved an extracellular receptor since repetitive exposure yielded diminished responsiveness. Inhibition of either phospholipase C or the inositol 1,4,5-trisphosphate receptor abolished S1P effects. RT-PCR analysis demonstrated the presence of S1P-coupled endothelial differentiation gene (EDG) receptor mRNAs (EDG-1, EDG-3, and EDG-5) within the enteric nervous system. Immunocytochemical analysis demonstrated strong expression of both EDG-1 and EDG-3 and weak expression of EDG-5 in enteric glial cells. Other sphingomyelin cycle components, including sphingomyelin, sphingomyelinase, and sphingosine caused Ca2+ transients in enteric glia. Related lipids lysophosphatidic acid and sphingosylphosphorylcholine also induced Ca 2+ signaling in enteric glia, suggesting that multiple lipid-activated signaling mechanisms exist in these cells.",

keywords = "Enteroglial cells, Nervous system, Sphingosine-1-phosphate",

author = "Segura, \{B. J.\} and W. Zhang and L. Xiao and D. Turner and Cowles, \{R. A.\} and C. Logsdon and Mulholland, \{M. W.\}",

note = "Funding Information: This research was supported by the National Institutes of Health (DK41204 and accompanying Minority Supplemental Grant, and Systems \& Integrative Biology training grant GM08322–11) and by a pre-doctoral fellowship from the Horace Rackham School of Graduate Studies, University of Michigan.",

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AU - Segura, B. J.

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AU - Xiao, L.

AU - Turner, D.

AU - Cowles, R. A.

AU - Logsdon, C.

AU - Mulholland, M. W.

N1 - Funding Information: This research was supported by the National Institutes of Health (DK41204 and accompanying Minority Supplemental Grant, and Systems & Integrative Biology training grant GM08322–11) and by a pre-doctoral fellowship from the Horace Rackham School of Graduate Studies, University of Michigan.

PY - 2004/1

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N2 - The enteric nervous system, which regulates multiple aspects of digestive activity, is composed of two major cell types, neurons and glial cells. Enteric glia, but not enteric neurons, respond to bioactive lipids with calcium signaling. The sphingomyelin metabolite sphingosine-1-phosphate (S1P) caused dose-dependent calcium (Ca2+) signaling using extracellular and intracellular Ca2+. The signal transduction cascade was pertussis toxin-insensitive and involved an extracellular receptor since repetitive exposure yielded diminished responsiveness. Inhibition of either phospholipase C or the inositol 1,4,5-trisphosphate receptor abolished S1P effects. RT-PCR analysis demonstrated the presence of S1P-coupled endothelial differentiation gene (EDG) receptor mRNAs (EDG-1, EDG-3, and EDG-5) within the enteric nervous system. Immunocytochemical analysis demonstrated strong expression of both EDG-1 and EDG-3 and weak expression of EDG-5 in enteric glial cells. Other sphingomyelin cycle components, including sphingomyelin, sphingomyelinase, and sphingosine caused Ca2+ transients in enteric glia. Related lipids lysophosphatidic acid and sphingosylphosphorylcholine also induced Ca 2+ signaling in enteric glia, suggesting that multiple lipid-activated signaling mechanisms exist in these cells.

AB - The enteric nervous system, which regulates multiple aspects of digestive activity, is composed of two major cell types, neurons and glial cells. Enteric glia, but not enteric neurons, respond to bioactive lipids with calcium signaling. The sphingomyelin metabolite sphingosine-1-phosphate (S1P) caused dose-dependent calcium (Ca2+) signaling using extracellular and intracellular Ca2+. The signal transduction cascade was pertussis toxin-insensitive and involved an extracellular receptor since repetitive exposure yielded diminished responsiveness. Inhibition of either phospholipase C or the inositol 1,4,5-trisphosphate receptor abolished S1P effects. RT-PCR analysis demonstrated the presence of S1P-coupled endothelial differentiation gene (EDG) receptor mRNAs (EDG-1, EDG-3, and EDG-5) within the enteric nervous system. Immunocytochemical analysis demonstrated strong expression of both EDG-1 and EDG-3 and weak expression of EDG-5 in enteric glial cells. Other sphingomyelin cycle components, including sphingomyelin, sphingomyelinase, and sphingosine caused Ca2+ transients in enteric glia. Related lipids lysophosphatidic acid and sphingosylphosphorylcholine also induced Ca 2+ signaling in enteric glia, suggesting that multiple lipid-activated signaling mechanisms exist in these cells.

KW - Enteroglial cells

KW - Nervous system

KW - Sphingosine-1-phosphate

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Sphingosine-1-phosphate mediates calcium signaling in guinea pig enteroglial cells

Abstract

Bibliographical note

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Keywords

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