Phosphorylation of mRNA decapping protein Dcp1a by the ERK signaling pathway during early differentiation of 3T3-L1 preadipocytes.

<h4>Background</h4>Turnover of mRNA is a critical step in the regulation of gene expression, and an important step in mRNA decay is removal of the 5' cap. We previously demonstrated that the expression of some immediate early gene mRNAs is controlled by RNA stability during early di...

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Autores principales:	Pei-Yu Chiang, Yu-Fang Shen, Yu-Lun Su, Ching-Han Kao, Nien-Yi Lin, Pang-Hung Hsu, Ming-Daw Tsai, Shun-Chang Wang, Geen-Dong Chang, Sheng-Chung Lee, Ching-Jin Chang
Formato:	article
Lenguaje:	EN
Publicado:	Public Library of Science (PLoS) 2013
Materias:	Medicine R Science Q
Acceso en línea:	https://doaj.org/article/6a5bff4fe9ad46d0907fcc1b9c418f5d
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spelling	oai:doaj.org-article:6a5bff4fe9ad46d0907fcc1b9c418f5d2021-11-18T07:48:52ZPhosphorylation of mRNA decapping protein Dcp1a by the ERK signaling pathway during early differentiation of 3T3-L1 preadipocytes.1932-620310.1371/journal.pone.0061697https://doaj.org/article/6a5bff4fe9ad46d0907fcc1b9c418f5d2013-01-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/23637887/?tool=EBIhttps://doaj.org/toc/1932-6203<h4>Background</h4>Turnover of mRNA is a critical step in the regulation of gene expression, and an important step in mRNA decay is removal of the 5' cap. We previously demonstrated that the expression of some immediate early gene mRNAs is controlled by RNA stability during early differentiation of 3T3-L1 preadipocytes.<h4>Methodology/principal findings</h4>Here we show that the mouse decapping protein Dcp1a is phosphorylated via the ERK signaling pathway during early differentiation of preadipocytes. Mass spectrometry analysis and site-directed mutagenesis combined with a kinase assay identified ERK pathway-mediated dual phosphorylation at Ser 315 and Ser 319 of Dcp1a. To understand the functional effects of Dcp1a phosphorylation, we examined protein-protein interactions between Dcp1a and other decapping components with co-immunoprecipitation. Dcp1a interacted with Ddx6 and Edc3 through its proline-rich C-terminal extension, whereas the conserved EVH1 (enabled vasodilator-stimulated protein homology 1) domain in the N terminus of Dcp1a showed a stronger interaction with Dcp2. Once ERK signaling was activated, the interaction between Dcp1a and Ddx6, Edc3, or Edc4 was not affected by Dcp1a phosphorylation. Phosphorylated Dcp1a did, however, enhanced interaction with Dcp2. Protein complexes immunoprecipitated with the recombinant phosphomimetic Dcp1a(S315D/S319D) mutant contained more Dcp2 than did those immunoprecipitated with the nonphosphorylated Dcp1a(S315A/S319A) mutant. In addition, Dcp1a associated with AU-rich element (ARE)-containing mRNAs such as MAPK phosphatase-1 (MKP-1), whose mRNA stability was analyzed under the overexpression of Dcp1a constructs in the Dcp1a knockdown 3T3-L1 cells.<h4>Conclusions/significance</h4>Our findings suggest that ERK-phosphorylated Dcp1a enhances its interaction with the decapping enzyme Dcp2 during early differentiation of 3T3-L1 cells.Pei-Yu ChiangYu-Fang ShenYu-Lun SuChing-Han KaoNien-Yi LinPang-Hung HsuMing-Daw TsaiShun-Chang WangGeen-Dong ChangSheng-Chung LeeChing-Jin ChangPublic Library of Science (PLoS)articleMedicineRScienceQENPLoS ONE, Vol 8, Iss 4, p e61697 (2013)
institution	DOAJ
collection	DOAJ
language	EN
topic	Medicine R Science Q
spellingShingle	Medicine R Science Q Pei-Yu Chiang Yu-Fang Shen Yu-Lun Su Ching-Han Kao Nien-Yi Lin Pang-Hung Hsu Ming-Daw Tsai Shun-Chang Wang Geen-Dong Chang Sheng-Chung Lee Ching-Jin Chang Phosphorylation of mRNA decapping protein Dcp1a by the ERK signaling pathway during early differentiation of 3T3-L1 preadipocytes.
description	<h4>Background</h4>Turnover of mRNA is a critical step in the regulation of gene expression, and an important step in mRNA decay is removal of the 5' cap. We previously demonstrated that the expression of some immediate early gene mRNAs is controlled by RNA stability during early differentiation of 3T3-L1 preadipocytes.<h4>Methodology/principal findings</h4>Here we show that the mouse decapping protein Dcp1a is phosphorylated via the ERK signaling pathway during early differentiation of preadipocytes. Mass spectrometry analysis and site-directed mutagenesis combined with a kinase assay identified ERK pathway-mediated dual phosphorylation at Ser 315 and Ser 319 of Dcp1a. To understand the functional effects of Dcp1a phosphorylation, we examined protein-protein interactions between Dcp1a and other decapping components with co-immunoprecipitation. Dcp1a interacted with Ddx6 and Edc3 through its proline-rich C-terminal extension, whereas the conserved EVH1 (enabled vasodilator-stimulated protein homology 1) domain in the N terminus of Dcp1a showed a stronger interaction with Dcp2. Once ERK signaling was activated, the interaction between Dcp1a and Ddx6, Edc3, or Edc4 was not affected by Dcp1a phosphorylation. Phosphorylated Dcp1a did, however, enhanced interaction with Dcp2. Protein complexes immunoprecipitated with the recombinant phosphomimetic Dcp1a(S315D/S319D) mutant contained more Dcp2 than did those immunoprecipitated with the nonphosphorylated Dcp1a(S315A/S319A) mutant. In addition, Dcp1a associated with AU-rich element (ARE)-containing mRNAs such as MAPK phosphatase-1 (MKP-1), whose mRNA stability was analyzed under the overexpression of Dcp1a constructs in the Dcp1a knockdown 3T3-L1 cells.<h4>Conclusions/significance</h4>Our findings suggest that ERK-phosphorylated Dcp1a enhances its interaction with the decapping enzyme Dcp2 during early differentiation of 3T3-L1 cells.
format	article
author	Pei-Yu Chiang Yu-Fang Shen Yu-Lun Su Ching-Han Kao Nien-Yi Lin Pang-Hung Hsu Ming-Daw Tsai Shun-Chang Wang Geen-Dong Chang Sheng-Chung Lee Ching-Jin Chang
author_facet	Pei-Yu Chiang Yu-Fang Shen Yu-Lun Su Ching-Han Kao Nien-Yi Lin Pang-Hung Hsu Ming-Daw Tsai Shun-Chang Wang Geen-Dong Chang Sheng-Chung Lee Ching-Jin Chang
author_sort	Pei-Yu Chiang
title	Phosphorylation of mRNA decapping protein Dcp1a by the ERK signaling pathway during early differentiation of 3T3-L1 preadipocytes.
title_short	Phosphorylation of mRNA decapping protein Dcp1a by the ERK signaling pathway during early differentiation of 3T3-L1 preadipocytes.
title_full	Phosphorylation of mRNA decapping protein Dcp1a by the ERK signaling pathway during early differentiation of 3T3-L1 preadipocytes.
title_fullStr	Phosphorylation of mRNA decapping protein Dcp1a by the ERK signaling pathway during early differentiation of 3T3-L1 preadipocytes.
title_full_unstemmed	Phosphorylation of mRNA decapping protein Dcp1a by the ERK signaling pathway during early differentiation of 3T3-L1 preadipocytes.
title_sort	phosphorylation of mrna decapping protein dcp1a by the erk signaling pathway during early differentiation of 3t3-l1 preadipocytes.
publisher	Public Library of Science (PLoS)
publishDate	2013
url	https://doaj.org/article/6a5bff4fe9ad46d0907fcc1b9c418f5d
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Phosphorylation of mRNA decapping protein Dcp1a by the ERK signaling pathway during early differentiation of 3T3-L1 preadipocytes.

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