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Misoprostol treatment prevents hypoxia-induced cardiac dysfunction through a 14-3-3 and PKA regulatory motif on Bnip3

Systemic hypoxia is a common element in most perinatal emergencies and is a known driver of Bnip3 expression in the neonatal heart. Bnip3 plays a prominent role in the evolution of necrotic cell death, disrupting ER calcium homeostasis and initiating mitochondrial permeability transition (MPT). Emer...

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Autores principales: Martens, Matthew D., Seshadri, Nivedita, Nguyen, Lucas, Chapman, Donald, Henson, Elizabeth S., Xiang, Bo, Falk, Landon, Mendoza, Arielys, Rattan, Sunil, Field, Jared T., Kawalec, Philip, Gibson, Spencer B., Keijzer, Richard, Saleem, Ayesha, Hatch, Grant M., Doucette, Christine A., Karch, Jason M., Dolinsky, Vernon W., Dixon, Ian M., West, Adrian R., Rampitsch, Christof, Gordon, Joseph W.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8617186/
https://www.ncbi.nlm.nih.gov/pubmed/34824192
http://dx.doi.org/10.1038/s41419-021-04402-3
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author Martens, Matthew D.
Seshadri, Nivedita
Nguyen, Lucas
Chapman, Donald
Henson, Elizabeth S.
Xiang, Bo
Falk, Landon
Mendoza, Arielys
Rattan, Sunil
Field, Jared T.
Kawalec, Philip
Gibson, Spencer B.
Keijzer, Richard
Saleem, Ayesha
Hatch, Grant M.
Doucette, Christine A.
Karch, Jason M.
Dolinsky, Vernon W.
Dixon, Ian M.
West, Adrian R.
Rampitsch, Christof
Gordon, Joseph W.
author_facet Martens, Matthew D.
Seshadri, Nivedita
Nguyen, Lucas
Chapman, Donald
Henson, Elizabeth S.
Xiang, Bo
Falk, Landon
Mendoza, Arielys
Rattan, Sunil
Field, Jared T.
Kawalec, Philip
Gibson, Spencer B.
Keijzer, Richard
Saleem, Ayesha
Hatch, Grant M.
Doucette, Christine A.
Karch, Jason M.
Dolinsky, Vernon W.
Dixon, Ian M.
West, Adrian R.
Rampitsch, Christof
Gordon, Joseph W.
author_sort Martens, Matthew D.
collection PubMed
description Systemic hypoxia is a common element in most perinatal emergencies and is a known driver of Bnip3 expression in the neonatal heart. Bnip3 plays a prominent role in the evolution of necrotic cell death, disrupting ER calcium homeostasis and initiating mitochondrial permeability transition (MPT). Emerging evidence suggests a cardioprotective role for the prostaglandin E1 analog misoprostol during periods of hypoxia, but the mechanisms for this protection are not completely understood. Using a combination of mouse and cell models, we tested if misoprostol is cardioprotective during neonatal hypoxic injury by altering Bnip3 function. Here we report that hypoxia elicits mitochondrial-fragmentation, MPT, reduced ejection fraction, and evidence of necroinflammation, which were abrogated with misoprostol treatment or Bnip3 knockout. Through molecular studies we show that misoprostol leads to PKA-dependent Bnip3 phosphorylation at threonine-181, and subsequent redistribution of Bnip3 from mitochondrial Opa1 and the ER through an interaction with 14-3-3 proteins. Taken together, our results demonstrate a role for Bnip3 phosphorylation in the regulation of cardiomyocyte contractile/metabolic dysfunction, and necroinflammation. Furthermore, we identify a potential pharmacological mechanism to prevent neonatal hypoxic injury.
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spelling pubmed-86171862021-12-10 Misoprostol treatment prevents hypoxia-induced cardiac dysfunction through a 14-3-3 and PKA regulatory motif on Bnip3 Martens, Matthew D. Seshadri, Nivedita Nguyen, Lucas Chapman, Donald Henson, Elizabeth S. Xiang, Bo Falk, Landon Mendoza, Arielys Rattan, Sunil Field, Jared T. Kawalec, Philip Gibson, Spencer B. Keijzer, Richard Saleem, Ayesha Hatch, Grant M. Doucette, Christine A. Karch, Jason M. Dolinsky, Vernon W. Dixon, Ian M. West, Adrian R. Rampitsch, Christof Gordon, Joseph W. Cell Death Dis Article Systemic hypoxia is a common element in most perinatal emergencies and is a known driver of Bnip3 expression in the neonatal heart. Bnip3 plays a prominent role in the evolution of necrotic cell death, disrupting ER calcium homeostasis and initiating mitochondrial permeability transition (MPT). Emerging evidence suggests a cardioprotective role for the prostaglandin E1 analog misoprostol during periods of hypoxia, but the mechanisms for this protection are not completely understood. Using a combination of mouse and cell models, we tested if misoprostol is cardioprotective during neonatal hypoxic injury by altering Bnip3 function. Here we report that hypoxia elicits mitochondrial-fragmentation, MPT, reduced ejection fraction, and evidence of necroinflammation, which were abrogated with misoprostol treatment or Bnip3 knockout. Through molecular studies we show that misoprostol leads to PKA-dependent Bnip3 phosphorylation at threonine-181, and subsequent redistribution of Bnip3 from mitochondrial Opa1 and the ER through an interaction with 14-3-3 proteins. Taken together, our results demonstrate a role for Bnip3 phosphorylation in the regulation of cardiomyocyte contractile/metabolic dysfunction, and necroinflammation. Furthermore, we identify a potential pharmacological mechanism to prevent neonatal hypoxic injury. Nature Publishing Group UK 2021-11-26 /pmc/articles/PMC8617186/ /pubmed/34824192 http://dx.doi.org/10.1038/s41419-021-04402-3 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Martens, Matthew D.
Seshadri, Nivedita
Nguyen, Lucas
Chapman, Donald
Henson, Elizabeth S.
Xiang, Bo
Falk, Landon
Mendoza, Arielys
Rattan, Sunil
Field, Jared T.
Kawalec, Philip
Gibson, Spencer B.
Keijzer, Richard
Saleem, Ayesha
Hatch, Grant M.
Doucette, Christine A.
Karch, Jason M.
Dolinsky, Vernon W.
Dixon, Ian M.
West, Adrian R.
Rampitsch, Christof
Gordon, Joseph W.
Misoprostol treatment prevents hypoxia-induced cardiac dysfunction through a 14-3-3 and PKA regulatory motif on Bnip3
title Misoprostol treatment prevents hypoxia-induced cardiac dysfunction through a 14-3-3 and PKA regulatory motif on Bnip3
title_full Misoprostol treatment prevents hypoxia-induced cardiac dysfunction through a 14-3-3 and PKA regulatory motif on Bnip3
title_fullStr Misoprostol treatment prevents hypoxia-induced cardiac dysfunction through a 14-3-3 and PKA regulatory motif on Bnip3
title_full_unstemmed Misoprostol treatment prevents hypoxia-induced cardiac dysfunction through a 14-3-3 and PKA regulatory motif on Bnip3
title_short Misoprostol treatment prevents hypoxia-induced cardiac dysfunction through a 14-3-3 and PKA regulatory motif on Bnip3
title_sort misoprostol treatment prevents hypoxia-induced cardiac dysfunction through a 14-3-3 and pka regulatory motif on bnip3
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8617186/
https://www.ncbi.nlm.nih.gov/pubmed/34824192
http://dx.doi.org/10.1038/s41419-021-04402-3
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