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The familial dysautonomia disease gene IKBKAP is required in the developing and adult mouse central nervous system

Hereditary sensory and autonomic neuropathies (HSANs) are a genetically and clinically diverse group of disorders defined by peripheral nervous system (PNS) dysfunction. HSAN type III, known as familial dysautonomia (FD), results from a single base mutation in the gene IKBKAP that encodes a scaffold...

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Autores principales: Chaverra, Marta, George, Lynn, Mergy, Marc, Waller, Hannah, Kujawa, Katharine, Murnion, Connor, Sharples, Ezekiel, Thorne, Julian, Podgajny, Nathaniel, Grindeland, Andrea, Ueki, Yumi, Eiger, Steven, Cusick, Cassie, Babcock, A. Michael, Carlson, George A., Lefcort, Frances
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Company of Biologists Ltd 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5451171/
https://www.ncbi.nlm.nih.gov/pubmed/28167615
http://dx.doi.org/10.1242/dmm.028258
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author Chaverra, Marta
George, Lynn
Mergy, Marc
Waller, Hannah
Kujawa, Katharine
Murnion, Connor
Sharples, Ezekiel
Thorne, Julian
Podgajny, Nathaniel
Grindeland, Andrea
Ueki, Yumi
Eiger, Steven
Cusick, Cassie
Babcock, A. Michael
Carlson, George A.
Lefcort, Frances
author_facet Chaverra, Marta
George, Lynn
Mergy, Marc
Waller, Hannah
Kujawa, Katharine
Murnion, Connor
Sharples, Ezekiel
Thorne, Julian
Podgajny, Nathaniel
Grindeland, Andrea
Ueki, Yumi
Eiger, Steven
Cusick, Cassie
Babcock, A. Michael
Carlson, George A.
Lefcort, Frances
author_sort Chaverra, Marta
collection PubMed
description Hereditary sensory and autonomic neuropathies (HSANs) are a genetically and clinically diverse group of disorders defined by peripheral nervous system (PNS) dysfunction. HSAN type III, known as familial dysautonomia (FD), results from a single base mutation in the gene IKBKAP that encodes a scaffolding unit (ELP1) for a multi-subunit complex known as Elongator. Since mutations in other Elongator subunits (ELP2 to ELP4) are associated with central nervous system (CNS) disorders, the goal of this study was to investigate a potential requirement for Ikbkap in the CNS of mice. The sensory and autonomic pathophysiology of FD is fatal, with the majority of patients dying by age 40. While signs and pathology of FD have been noted in the CNS, the clinical and research focus has been on the sensory and autonomic dysfunction, and no genetic model studies have investigated the requirement for Ikbkap in the CNS. Here, we report, using a novel mouse line in which Ikbkap is deleted solely in the nervous system, that not only is Ikbkap widely expressed in the embryonic and adult CNS, but its deletion perturbs both the development of cortical neurons and their survival in adulthood. Primary cilia in embryonic cortical apical progenitors and motile cilia in adult ependymal cells are reduced in number and disorganized. Furthermore, we report that, in the adult CNS, both autonomic and non-autonomic neuronal populations require Ikbkap for survival, including spinal motor and cortical neurons. In addition, the mice developed kyphoscoliosis, an FD hallmark, indicating its neuropathic etiology. Ultimately, these perturbations manifest in a developmental and progressive neurodegenerative condition that includes impairments in learning and memory. Collectively, these data reveal an essential function for Ikbkap that extends beyond the peripheral nervous system to CNS development and function. With the identification of discrete CNS cell types and structures that depend on Ikbkap, novel strategies to thwart the progressive demise of CNS neurons in FD can be developed.
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spelling pubmed-54511712017-06-01 The familial dysautonomia disease gene IKBKAP is required in the developing and adult mouse central nervous system Chaverra, Marta George, Lynn Mergy, Marc Waller, Hannah Kujawa, Katharine Murnion, Connor Sharples, Ezekiel Thorne, Julian Podgajny, Nathaniel Grindeland, Andrea Ueki, Yumi Eiger, Steven Cusick, Cassie Babcock, A. Michael Carlson, George A. Lefcort, Frances Dis Model Mech Research Articles Hereditary sensory and autonomic neuropathies (HSANs) are a genetically and clinically diverse group of disorders defined by peripheral nervous system (PNS) dysfunction. HSAN type III, known as familial dysautonomia (FD), results from a single base mutation in the gene IKBKAP that encodes a scaffolding unit (ELP1) for a multi-subunit complex known as Elongator. Since mutations in other Elongator subunits (ELP2 to ELP4) are associated with central nervous system (CNS) disorders, the goal of this study was to investigate a potential requirement for Ikbkap in the CNS of mice. The sensory and autonomic pathophysiology of FD is fatal, with the majority of patients dying by age 40. While signs and pathology of FD have been noted in the CNS, the clinical and research focus has been on the sensory and autonomic dysfunction, and no genetic model studies have investigated the requirement for Ikbkap in the CNS. Here, we report, using a novel mouse line in which Ikbkap is deleted solely in the nervous system, that not only is Ikbkap widely expressed in the embryonic and adult CNS, but its deletion perturbs both the development of cortical neurons and their survival in adulthood. Primary cilia in embryonic cortical apical progenitors and motile cilia in adult ependymal cells are reduced in number and disorganized. Furthermore, we report that, in the adult CNS, both autonomic and non-autonomic neuronal populations require Ikbkap for survival, including spinal motor and cortical neurons. In addition, the mice developed kyphoscoliosis, an FD hallmark, indicating its neuropathic etiology. Ultimately, these perturbations manifest in a developmental and progressive neurodegenerative condition that includes impairments in learning and memory. Collectively, these data reveal an essential function for Ikbkap that extends beyond the peripheral nervous system to CNS development and function. With the identification of discrete CNS cell types and structures that depend on Ikbkap, novel strategies to thwart the progressive demise of CNS neurons in FD can be developed. The Company of Biologists Ltd 2017-05-01 /pmc/articles/PMC5451171/ /pubmed/28167615 http://dx.doi.org/10.1242/dmm.028258 Text en © 2017. Published by The Company of Biologists Ltd http://creativecommons.org/licenses/by/3.0This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
spellingShingle Research Articles
Chaverra, Marta
George, Lynn
Mergy, Marc
Waller, Hannah
Kujawa, Katharine
Murnion, Connor
Sharples, Ezekiel
Thorne, Julian
Podgajny, Nathaniel
Grindeland, Andrea
Ueki, Yumi
Eiger, Steven
Cusick, Cassie
Babcock, A. Michael
Carlson, George A.
Lefcort, Frances
The familial dysautonomia disease gene IKBKAP is required in the developing and adult mouse central nervous system
title The familial dysautonomia disease gene IKBKAP is required in the developing and adult mouse central nervous system
title_full The familial dysautonomia disease gene IKBKAP is required in the developing and adult mouse central nervous system
title_fullStr The familial dysautonomia disease gene IKBKAP is required in the developing and adult mouse central nervous system
title_full_unstemmed The familial dysautonomia disease gene IKBKAP is required in the developing and adult mouse central nervous system
title_short The familial dysautonomia disease gene IKBKAP is required in the developing and adult mouse central nervous system
title_sort familial dysautonomia disease gene ikbkap is required in the developing and adult mouse central nervous system
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5451171/
https://www.ncbi.nlm.nih.gov/pubmed/28167615
http://dx.doi.org/10.1242/dmm.028258
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