Identification of a unique endoplasmic retention motif in the Xenopus GIRK5 channel and its contribution to oocyte maturation

G protein‐activated inward‐rectifying potassium (K+) channels (Kir3/GIRK) participate in cell excitability. The GIRK5 channel is present in Xenopus laevis oocytes. In an attempt to investigate the physiological role of GIRK5, we identified a noncanonical di‐arginine endoplasmic reticulum (ER) retent...

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Main Authors: Claudia I. Rangel‐Garcia, Carolina Salvador, Karla Chavez‐Garcia, Beatriz Diaz‐Bello, Zinaeli Lopez‐Gonzalez, Lourdes Vazquez‐Cruz, Julio Angel Vazquez‐Martinez, Vianney Ortiz‐Navarrete, Hector Riveros‐Rosas, Laura I. Escobar
Format: Article
Language:English
Published: Wiley 2021-04-01
Series:FEBS Open Bio
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Online Access:https://doi.org/10.1002/2211-5463.13113
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author Claudia I. Rangel‐Garcia
Carolina Salvador
Karla Chavez‐Garcia
Beatriz Diaz‐Bello
Zinaeli Lopez‐Gonzalez
Lourdes Vazquez‐Cruz
Julio Angel Vazquez‐Martinez
Vianney Ortiz‐Navarrete
Hector Riveros‐Rosas
Laura I. Escobar
author_facet Claudia I. Rangel‐Garcia
Carolina Salvador
Karla Chavez‐Garcia
Beatriz Diaz‐Bello
Zinaeli Lopez‐Gonzalez
Lourdes Vazquez‐Cruz
Julio Angel Vazquez‐Martinez
Vianney Ortiz‐Navarrete
Hector Riveros‐Rosas
Laura I. Escobar
author_sort Claudia I. Rangel‐Garcia
collection DOAJ
description G protein‐activated inward‐rectifying potassium (K+) channels (Kir3/GIRK) participate in cell excitability. The GIRK5 channel is present in Xenopus laevis oocytes. In an attempt to investigate the physiological role of GIRK5, we identified a noncanonical di‐arginine endoplasmic reticulum (ER) retention motif (KRXY). This retention motif is located at the N‐terminal region of GIRK5, coded by two small exons found only in X. laevis and X. tropicalis. These novel exons are expressed through use of an alternative transcription start site. Mutations in the sequence KRXY produced functional channels and induced progesterone‐independent oocyte meiotic progression. The chimeric proteins enhanced green fluorescent protein (EGFP)‐GIRK5‐WT and the EGFP‐GIRK5K13AR14A double mutant, were localized to the ER and the plasma membrane of the vegetal pole of the oocyte, respectively. Silencing of GIRK5 or blocking of this channel by external barium prevented progesterone‐induced meiotic progression. The endogenous level of GIRK5 protein decreased through oocyte stages in prophase I augmenting by progesterone. In conclusion, we have identified a unique mechanism by which the expression pattern of a K+ channel evolved to control Xenopus oocyte maturation.
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spelling doaj.art-06dcd182319048a5bae86159bcb70a232022-12-21T19:57:57ZengWileyFEBS Open Bio2211-54632021-04-011141093110810.1002/2211-5463.13113Identification of a unique endoplasmic retention motif in the Xenopus GIRK5 channel and its contribution to oocyte maturationClaudia I. Rangel‐Garcia0Carolina Salvador1Karla Chavez‐Garcia2Beatriz Diaz‐Bello3Zinaeli Lopez‐Gonzalez4Lourdes Vazquez‐Cruz5Julio Angel Vazquez‐Martinez6Vianney Ortiz‐Navarrete7Hector Riveros‐Rosas8Laura I. Escobar9Departamento de Fisiologia Facultad de Medicina Universidad Nacional Autonoma de Mexico Ciudad de Mexico MexicoDepartamento de Fisiologia Facultad de Medicina Universidad Nacional Autonoma de Mexico Ciudad de Mexico MexicoDepartamento de Fisiologia Facultad de Medicina Universidad Nacional Autonoma de Mexico Ciudad de Mexico MexicoDepartamento de Fisiologia Facultad de Medicina Universidad Nacional Autonoma de Mexico Ciudad de Mexico MexicoDepartamento de Fisiologia Facultad de Medicina Universidad Nacional Autonoma de Mexico Ciudad de Mexico MexicoDepartamento de Fisiologia Facultad de Medicina Universidad Nacional Autonoma de Mexico Ciudad de Mexico MexicoDepartamento de Biomedicina Molecular Centro de Investigacion y de Estudios Avanzados del Instituto Politecnico Nacional Mexico City MexicoDepartamento de Biomedicina Molecular Centro de Investigacion y de Estudios Avanzados del Instituto Politecnico Nacional Mexico City MexicoDepartamento de Bioquimica Facultad de Medicina Universidad Nacional Autonoma de Mexico Ciudad de Mexico MexicoDepartamento de Fisiologia Facultad de Medicina Universidad Nacional Autonoma de Mexico Ciudad de Mexico MexicoG protein‐activated inward‐rectifying potassium (K+) channels (Kir3/GIRK) participate in cell excitability. The GIRK5 channel is present in Xenopus laevis oocytes. In an attempt to investigate the physiological role of GIRK5, we identified a noncanonical di‐arginine endoplasmic reticulum (ER) retention motif (KRXY). This retention motif is located at the N‐terminal region of GIRK5, coded by two small exons found only in X. laevis and X. tropicalis. These novel exons are expressed through use of an alternative transcription start site. Mutations in the sequence KRXY produced functional channels and induced progesterone‐independent oocyte meiotic progression. The chimeric proteins enhanced green fluorescent protein (EGFP)‐GIRK5‐WT and the EGFP‐GIRK5K13AR14A double mutant, were localized to the ER and the plasma membrane of the vegetal pole of the oocyte, respectively. Silencing of GIRK5 or blocking of this channel by external barium prevented progesterone‐induced meiotic progression. The endogenous level of GIRK5 protein decreased through oocyte stages in prophase I augmenting by progesterone. In conclusion, we have identified a unique mechanism by which the expression pattern of a K+ channel evolved to control Xenopus oocyte maturation.https://doi.org/10.1002/2211-5463.13113endoplasmic retention motifG protein‐activated potassium channelnested genesoocyteXenopus
spellingShingle Claudia I. Rangel‐Garcia
Carolina Salvador
Karla Chavez‐Garcia
Beatriz Diaz‐Bello
Zinaeli Lopez‐Gonzalez
Lourdes Vazquez‐Cruz
Julio Angel Vazquez‐Martinez
Vianney Ortiz‐Navarrete
Hector Riveros‐Rosas
Laura I. Escobar
Identification of a unique endoplasmic retention motif in the Xenopus GIRK5 channel and its contribution to oocyte maturation
FEBS Open Bio
endoplasmic retention motif
G protein‐activated potassium channel
nested genes
oocyte
Xenopus
title Identification of a unique endoplasmic retention motif in the Xenopus GIRK5 channel and its contribution to oocyte maturation
title_full Identification of a unique endoplasmic retention motif in the Xenopus GIRK5 channel and its contribution to oocyte maturation
title_fullStr Identification of a unique endoplasmic retention motif in the Xenopus GIRK5 channel and its contribution to oocyte maturation
title_full_unstemmed Identification of a unique endoplasmic retention motif in the Xenopus GIRK5 channel and its contribution to oocyte maturation
title_short Identification of a unique endoplasmic retention motif in the Xenopus GIRK5 channel and its contribution to oocyte maturation
title_sort identification of a unique endoplasmic retention motif in the xenopus girk5 channel and its contribution to oocyte maturation
topic endoplasmic retention motif
G protein‐activated potassium channel
nested genes
oocyte
Xenopus
url https://doi.org/10.1002/2211-5463.13113
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