Parasympathetic and sympathetic axons are bundled in the cardiac ventricles and undergo physiological reinnervation during heart regeneration

Summary: Sympathetic innervation influences homeostasis, repair, and pathology in the cardiac ventricles; in contrast, parasympathetic innervation is considered to have minimal contribution and influence in the ventricles. Here, we use genetic models, whole-mount imaging, and three-dimensional model...

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Main Authors: Rebecca J. Salamon, Poorva Halbe, William Kasberg, Jiyoung Bae, Anjon Audhya, Ahmed I. Mahmoud
Format: Article
Language:English
Published: Elsevier 2023-10-01
Series:iScience
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2589004223017868
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author Rebecca J. Salamon
Poorva Halbe
William Kasberg
Jiyoung Bae
Anjon Audhya
Ahmed I. Mahmoud
author_facet Rebecca J. Salamon
Poorva Halbe
William Kasberg
Jiyoung Bae
Anjon Audhya
Ahmed I. Mahmoud
author_sort Rebecca J. Salamon
collection DOAJ
description Summary: Sympathetic innervation influences homeostasis, repair, and pathology in the cardiac ventricles; in contrast, parasympathetic innervation is considered to have minimal contribution and influence in the ventricles. Here, we use genetic models, whole-mount imaging, and three-dimensional modeling to define cardiac nerve architecture during development, disease, and regeneration. Our approach reveals that parasympathetic nerves extensively innervate the cardiac ventricles. Furthermore, we identify that parasympathetic and sympathetic axons develop synchronously and are bundled throughout the ventricles. We further investigate cardiac nerve remodeling in the regenerative neonatal and the non-regenerative postnatal mouse heart. Our results show that the regenerating myocardium undergoes a unique process of physiological reinnervation, where proper nerve distribution and architecture is reestablished, in stark contrast to the non-regenerating heart. Mechanistically, we demonstrate that physiological reinnervation during regeneration is dependent on collateral artery formation. Our results reveal clinically significant insights into cardiac nerve plasticity which can identify new therapies for cardiac disease.
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spelling doaj.art-1f2a10dadd3b4802ac12db390773597c2023-10-28T05:08:09ZengElsevieriScience2589-00422023-10-012610107709Parasympathetic and sympathetic axons are bundled in the cardiac ventricles and undergo physiological reinnervation during heart regenerationRebecca J. Salamon0Poorva Halbe1William Kasberg2Jiyoung Bae3Anjon Audhya4Ahmed I. Mahmoud5Department of Cell and Regenerative Biology, University of Wisconsin School of Medicine and Public Health, Madison, WI 53705, USADepartment of Cell and Regenerative Biology, University of Wisconsin School of Medicine and Public Health, Madison, WI 53705, USADepartment of Biomolecular Chemistry, University of Wisconsin School of Medicine and Public Health, Madison, WI 53705, USADepartment of Nutritional Sciences, Oklahoma State University, Stillwater, OK 74078, USADepartment of Biomolecular Chemistry, University of Wisconsin School of Medicine and Public Health, Madison, WI 53705, USADepartment of Cell and Regenerative Biology, University of Wisconsin School of Medicine and Public Health, Madison, WI 53705, USA; Corresponding authorSummary: Sympathetic innervation influences homeostasis, repair, and pathology in the cardiac ventricles; in contrast, parasympathetic innervation is considered to have minimal contribution and influence in the ventricles. Here, we use genetic models, whole-mount imaging, and three-dimensional modeling to define cardiac nerve architecture during development, disease, and regeneration. Our approach reveals that parasympathetic nerves extensively innervate the cardiac ventricles. Furthermore, we identify that parasympathetic and sympathetic axons develop synchronously and are bundled throughout the ventricles. We further investigate cardiac nerve remodeling in the regenerative neonatal and the non-regenerative postnatal mouse heart. Our results show that the regenerating myocardium undergoes a unique process of physiological reinnervation, where proper nerve distribution and architecture is reestablished, in stark contrast to the non-regenerating heart. Mechanistically, we demonstrate that physiological reinnervation during regeneration is dependent on collateral artery formation. Our results reveal clinically significant insights into cardiac nerve plasticity which can identify new therapies for cardiac disease.http://www.sciencedirect.com/science/article/pii/S2589004223017868Molecular biologyNeuroscienceCell biology
spellingShingle Rebecca J. Salamon
Poorva Halbe
William Kasberg
Jiyoung Bae
Anjon Audhya
Ahmed I. Mahmoud
Parasympathetic and sympathetic axons are bundled in the cardiac ventricles and undergo physiological reinnervation during heart regeneration
iScience
Molecular biology
Neuroscience
Cell biology
title Parasympathetic and sympathetic axons are bundled in the cardiac ventricles and undergo physiological reinnervation during heart regeneration
title_full Parasympathetic and sympathetic axons are bundled in the cardiac ventricles and undergo physiological reinnervation during heart regeneration
title_fullStr Parasympathetic and sympathetic axons are bundled in the cardiac ventricles and undergo physiological reinnervation during heart regeneration
title_full_unstemmed Parasympathetic and sympathetic axons are bundled in the cardiac ventricles and undergo physiological reinnervation during heart regeneration
title_short Parasympathetic and sympathetic axons are bundled in the cardiac ventricles and undergo physiological reinnervation during heart regeneration
title_sort parasympathetic and sympathetic axons are bundled in the cardiac ventricles and undergo physiological reinnervation during heart regeneration
topic Molecular biology
Neuroscience
Cell biology
url http://www.sciencedirect.com/science/article/pii/S2589004223017868
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