Cargando…

Src Family Tyrosine Kinase Signaling Regulates FilGAP through Association with RBM10

FilGAP is a Rac-specific GTPase-activating protein (GAP) that suppresses lamellae formation. In this study, we have identified RBM10 (RNA Binding Motif domain protein 10) as a FilGAP-interacting protein. Although RBM10 is mostly localized in the nuclei in human melanoma A7 cells, forced expression o...

Descripción completa

Detalles Bibliográficos
Autores principales: Yamada, Hazuki, Tsutsumi, Koji, Nakazawa, Yuki, Shibagaki, Yoshio, Hattori, Seisuke, Ohta, Yasutaka
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4709192/
https://www.ncbi.nlm.nih.gov/pubmed/26751795
http://dx.doi.org/10.1371/journal.pone.0146593
_version_ 1782409609583001600
author Yamada, Hazuki
Tsutsumi, Koji
Nakazawa, Yuki
Shibagaki, Yoshio
Hattori, Seisuke
Ohta, Yasutaka
author_facet Yamada, Hazuki
Tsutsumi, Koji
Nakazawa, Yuki
Shibagaki, Yoshio
Hattori, Seisuke
Ohta, Yasutaka
author_sort Yamada, Hazuki
collection PubMed
description FilGAP is a Rac-specific GTPase-activating protein (GAP) that suppresses lamellae formation. In this study, we have identified RBM10 (RNA Binding Motif domain protein 10) as a FilGAP-interacting protein. Although RBM10 is mostly localized in the nuclei in human melanoma A7 cells, forced expression of Src family tyrosine kinase Fyn induced translocation of RBM10 from nucleus into cell peripheries where RBM10 and FilGAP are co-localized. The translocation of RBM10 from nucleus appears to require catalytic activity of Fyn since kinase-negative Fyn mutant failed to induce translocation of RBM10 in A7 cells. When human breast carcinoma MDA-MB-231 cells are spreading on collagen-coated coverslips, endogenous FilGAP and RBM10 were localized at the cell periphery with tyrosine-phosphorylated proteins. RBM10 appears to be responsible for targeting FilGAP at the cell periphery because depletion of RBM10 by siRNA abrogated peripheral localization of FilGAP during cell spreading. Association of RBM10 with FilGAP may stimulate RacGAP activity of FilGAP. First, forced expression of RBM10 suppressed FilGAP-mediated cell spreading on collagen. Conversely, depletion of endogenous RBM10 by siRNA abolished FilGAP-mediated suppression of cell spreading on collagen. Second, FilGAP suppressed formation of membrane ruffles induced by Fyn and instead produced spiky cell protrusions at the cell periphery. This protrusive structure was also induced by depletion of Rac, suggesting that the formation of protrusions may be due to suppression of Rac by FilGAP. We found that depletion of RBM10 markedly reduced the formation of protrusions in cells transfected with Fyn and FilGAP. Finally, depletion of RBM10 blocked FilGAP-mediated suppression of ruffle formation induced by EGF. Taken together, these results suggest that Src family tyrosine kinase signaling may regulate FilGAP through association with RBM10.
format Online
Article
Text
id pubmed-4709192
institution National Center for Biotechnology Information
language English
publishDate 2016
publisher Public Library of Science
record_format MEDLINE/PubMed
spelling pubmed-47091922016-01-15 Src Family Tyrosine Kinase Signaling Regulates FilGAP through Association with RBM10 Yamada, Hazuki Tsutsumi, Koji Nakazawa, Yuki Shibagaki, Yoshio Hattori, Seisuke Ohta, Yasutaka PLoS One Research Article FilGAP is a Rac-specific GTPase-activating protein (GAP) that suppresses lamellae formation. In this study, we have identified RBM10 (RNA Binding Motif domain protein 10) as a FilGAP-interacting protein. Although RBM10 is mostly localized in the nuclei in human melanoma A7 cells, forced expression of Src family tyrosine kinase Fyn induced translocation of RBM10 from nucleus into cell peripheries where RBM10 and FilGAP are co-localized. The translocation of RBM10 from nucleus appears to require catalytic activity of Fyn since kinase-negative Fyn mutant failed to induce translocation of RBM10 in A7 cells. When human breast carcinoma MDA-MB-231 cells are spreading on collagen-coated coverslips, endogenous FilGAP and RBM10 were localized at the cell periphery with tyrosine-phosphorylated proteins. RBM10 appears to be responsible for targeting FilGAP at the cell periphery because depletion of RBM10 by siRNA abrogated peripheral localization of FilGAP during cell spreading. Association of RBM10 with FilGAP may stimulate RacGAP activity of FilGAP. First, forced expression of RBM10 suppressed FilGAP-mediated cell spreading on collagen. Conversely, depletion of endogenous RBM10 by siRNA abolished FilGAP-mediated suppression of cell spreading on collagen. Second, FilGAP suppressed formation of membrane ruffles induced by Fyn and instead produced spiky cell protrusions at the cell periphery. This protrusive structure was also induced by depletion of Rac, suggesting that the formation of protrusions may be due to suppression of Rac by FilGAP. We found that depletion of RBM10 markedly reduced the formation of protrusions in cells transfected with Fyn and FilGAP. Finally, depletion of RBM10 blocked FilGAP-mediated suppression of ruffle formation induced by EGF. Taken together, these results suggest that Src family tyrosine kinase signaling may regulate FilGAP through association with RBM10. Public Library of Science 2016-01-11 /pmc/articles/PMC4709192/ /pubmed/26751795 http://dx.doi.org/10.1371/journal.pone.0146593 Text en © 2016 Yamada et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Yamada, Hazuki
Tsutsumi, Koji
Nakazawa, Yuki
Shibagaki, Yoshio
Hattori, Seisuke
Ohta, Yasutaka
Src Family Tyrosine Kinase Signaling Regulates FilGAP through Association with RBM10
title Src Family Tyrosine Kinase Signaling Regulates FilGAP through Association with RBM10
title_full Src Family Tyrosine Kinase Signaling Regulates FilGAP through Association with RBM10
title_fullStr Src Family Tyrosine Kinase Signaling Regulates FilGAP through Association with RBM10
title_full_unstemmed Src Family Tyrosine Kinase Signaling Regulates FilGAP through Association with RBM10
title_short Src Family Tyrosine Kinase Signaling Regulates FilGAP through Association with RBM10
title_sort src family tyrosine kinase signaling regulates filgap through association with rbm10
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4709192/
https://www.ncbi.nlm.nih.gov/pubmed/26751795
http://dx.doi.org/10.1371/journal.pone.0146593
work_keys_str_mv AT yamadahazuki srcfamilytyrosinekinasesignalingregulatesfilgapthroughassociationwithrbm10
AT tsutsumikoji srcfamilytyrosinekinasesignalingregulatesfilgapthroughassociationwithrbm10
AT nakazawayuki srcfamilytyrosinekinasesignalingregulatesfilgapthroughassociationwithrbm10
AT shibagakiyoshio srcfamilytyrosinekinasesignalingregulatesfilgapthroughassociationwithrbm10
AT hattoriseisuke srcfamilytyrosinekinasesignalingregulatesfilgapthroughassociationwithrbm10
AT ohtayasutaka srcfamilytyrosinekinasesignalingregulatesfilgapthroughassociationwithrbm10