Ubiquitous [Na+]i/[K+]i-sensitive transcriptome in mammalian cells: evidence for Ca(2+)i-independent excitation-transcription coupling.

Stimulus-dependent elevation of intracellular Ca(2+) ([Ca(2+)](i)) affects the expression of numerous genes--a phenomenon known as excitation-transcription coupling. Recently, we found that increases in [Na(+)](i) trigger c-Fos expression via a novel Ca(2+) (i)-independent pathway. In the present st...

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Autores principales:	Svetlana V Koltsova, Yulia Trushina, Mounsif Haloui, Olga A Akimova, Johanne Tremblay, Pavel Hamet, Sergei N Orlov
Formato:	article
Lenguaje:	EN
Publicado:	Public Library of Science (PLoS) 2012
Materias:	Medicine R Science Q
Acceso en línea:	https://doaj.org/article/72fdc3bfb05a4583b13bb504ccdfb00d
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spelling	oai:doaj.org-article:72fdc3bfb05a4583b13bb504ccdfb00d2021-11-18T07:17:04ZUbiquitous [Na+]i/[K+]i-sensitive transcriptome in mammalian cells: evidence for Ca(2+)i-independent excitation-transcription coupling.1932-620310.1371/journal.pone.0038032https://doaj.org/article/72fdc3bfb05a4583b13bb504ccdfb00d2012-01-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/22666440/?tool=EBIhttps://doaj.org/toc/1932-6203Stimulus-dependent elevation of intracellular Ca(2+) ([Ca(2+)](i)) affects the expression of numerous genes--a phenomenon known as excitation-transcription coupling. Recently, we found that increases in [Na(+)](i) trigger c-Fos expression via a novel Ca(2+) (i)-independent pathway. In the present study, we identified ubiquitous and tissue-specific [Na(+)](i)/[K(+)](i)-sensitive transcriptomes by comparative analysis of differentially expressed genes in vascular smooth muscle cells from rat aorta (RVSMC), the human adenocarcinoma cell line HeLa, and human umbilical vein endothelial cells (HUVEC). To augment [Na(+)](i) and reduce [K(+)](i), cells were treated for 3 hrs with the Na(+),K(+)-ATPase inhibitor ouabain or placed for the same time in the K(+)-free medium. Employing Affymetrix-based technology, we detected changes in expression levels of 684, 737 and 1839 transcripts in HeLa, HUVEC and RVSMC, respectively, that were highly correlated between two treatments (p<0.0001; R(2)>0.62). Among these Na(+) (i)/K(+) (i)-sensitive genes, 80 transcripts were common for all three types of cells. To establish if changes in gene expression are dependent on increases in [Ca(2+)](i), we performed identical experiments in Ca(2+)-free media supplemented with extracellular and intracellular Ca(2+) chelators. Surprisingly, this procedure elevated rather than decreased the number of ubiquitous and cell-type specific Na(+) (i)/K(+) (i)-sensitive genes. Among the ubiquitous Na(+) (i)/K(+) (i)-sensitive genes whose expression was regulated independently of the presence of Ca(2+) chelators by more than 3-fold, we discovered several transcription factors (Fos, Jun, Hes1, Nfkbia), interleukin-6, protein phosphatase 1 regulatory subunit, dual specificity phosphatase (Dusp8), prostaglandin-endoperoxide synthase 2, cyclin L1, whereas expression of metallopeptidase Adamts1, adrenomedulin, Dups1, Dusp10 and Dusp16 was detected exclusively in Ca(2+)-depleted cells. Overall, our findings indicate that Ca(2+) (i)-independent mechanisms of excitation-transcription coupling are involved in transcriptomic alterations triggered by elevation of the [Na(+)](i)/[K(+)](i) ratio. There results likely have profound implications for normal and pathological regulation of mammalian cells, including sustained excitation of neuronal cells, intensive exercise and ischemia-triggered disorders.Svetlana V KoltsovaYulia TrushinaMounsif HalouiOlga A AkimovaJohanne TremblayPavel HametSergei N OrlovPublic Library of Science (PLoS)articleMedicineRScienceQENPLoS ONE, Vol 7, Iss 5, p e38032 (2012)
institution	DOAJ
collection	DOAJ
language	EN
topic	Medicine R Science Q
spellingShingle	Medicine R Science Q Svetlana V Koltsova Yulia Trushina Mounsif Haloui Olga A Akimova Johanne Tremblay Pavel Hamet Sergei N Orlov Ubiquitous [Na+]i/[K+]i-sensitive transcriptome in mammalian cells: evidence for Ca(2+)i-independent excitation-transcription coupling.
description	Stimulus-dependent elevation of intracellular Ca(2+) ([Ca(2+)](i)) affects the expression of numerous genes--a phenomenon known as excitation-transcription coupling. Recently, we found that increases in [Na(+)](i) trigger c-Fos expression via a novel Ca(2+) (i)-independent pathway. In the present study, we identified ubiquitous and tissue-specific [Na(+)](i)/[K(+)](i)-sensitive transcriptomes by comparative analysis of differentially expressed genes in vascular smooth muscle cells from rat aorta (RVSMC), the human adenocarcinoma cell line HeLa, and human umbilical vein endothelial cells (HUVEC). To augment [Na(+)](i) and reduce [K(+)](i), cells were treated for 3 hrs with the Na(+),K(+)-ATPase inhibitor ouabain or placed for the same time in the K(+)-free medium. Employing Affymetrix-based technology, we detected changes in expression levels of 684, 737 and 1839 transcripts in HeLa, HUVEC and RVSMC, respectively, that were highly correlated between two treatments (p<0.0001; R(2)>0.62). Among these Na(+) (i)/K(+) (i)-sensitive genes, 80 transcripts were common for all three types of cells. To establish if changes in gene expression are dependent on increases in [Ca(2+)](i), we performed identical experiments in Ca(2+)-free media supplemented with extracellular and intracellular Ca(2+) chelators. Surprisingly, this procedure elevated rather than decreased the number of ubiquitous and cell-type specific Na(+) (i)/K(+) (i)-sensitive genes. Among the ubiquitous Na(+) (i)/K(+) (i)-sensitive genes whose expression was regulated independently of the presence of Ca(2+) chelators by more than 3-fold, we discovered several transcription factors (Fos, Jun, Hes1, Nfkbia), interleukin-6, protein phosphatase 1 regulatory subunit, dual specificity phosphatase (Dusp8), prostaglandin-endoperoxide synthase 2, cyclin L1, whereas expression of metallopeptidase Adamts1, adrenomedulin, Dups1, Dusp10 and Dusp16 was detected exclusively in Ca(2+)-depleted cells. Overall, our findings indicate that Ca(2+) (i)-independent mechanisms of excitation-transcription coupling are involved in transcriptomic alterations triggered by elevation of the [Na(+)](i)/[K(+)](i) ratio. There results likely have profound implications for normal and pathological regulation of mammalian cells, including sustained excitation of neuronal cells, intensive exercise and ischemia-triggered disorders.
format	article
author	Svetlana V Koltsova Yulia Trushina Mounsif Haloui Olga A Akimova Johanne Tremblay Pavel Hamet Sergei N Orlov
author_facet	Svetlana V Koltsova Yulia Trushina Mounsif Haloui Olga A Akimova Johanne Tremblay Pavel Hamet Sergei N Orlov
author_sort	Svetlana V Koltsova
title	Ubiquitous [Na+]i/[K+]i-sensitive transcriptome in mammalian cells: evidence for Ca(2+)i-independent excitation-transcription coupling.
title_short	Ubiquitous [Na+]i/[K+]i-sensitive transcriptome in mammalian cells: evidence for Ca(2+)i-independent excitation-transcription coupling.
title_full	Ubiquitous [Na+]i/[K+]i-sensitive transcriptome in mammalian cells: evidence for Ca(2+)i-independent excitation-transcription coupling.
title_fullStr	Ubiquitous [Na+]i/[K+]i-sensitive transcriptome in mammalian cells: evidence for Ca(2+)i-independent excitation-transcription coupling.
title_full_unstemmed	Ubiquitous [Na+]i/[K+]i-sensitive transcriptome in mammalian cells: evidence for Ca(2+)i-independent excitation-transcription coupling.
title_sort	ubiquitous [na+]i/[k+]i-sensitive transcriptome in mammalian cells: evidence for ca(2+)i-independent excitation-transcription coupling.
publisher	Public Library of Science (PLoS)
publishDate	2012
url	https://doaj.org/article/72fdc3bfb05a4583b13bb504ccdfb00d
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Ubiquitous [Na+]i/[K+]i-sensitive transcriptome in mammalian cells: evidence for Ca(2+)i-independent excitation-transcription coupling.

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