A systematic review and embryological perspective of pluripotent stem cell-derived autonomic postganglionic neuron differentiation for human disease modeling

Human autonomic neuronal cell models are emerging as tools for modeling diseases such as cardiac arrhythmias. In this systematic review, we compared 33 articles applying 14 different protocols to generate sympathetic neurons and 3 different procedures to produce parasympathetic neurons. All methods...

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Main Authors: Thomas A Bos, Elizaveta Polyakova, Janine Maria van Gils, Antoine AF de Vries, Marie-José Goumans, Christian Freund, Marco C DeRuiter, Monique RM Jongbloed
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Language:English
Published: eLife Sciences Publications Ltd 2025-03-01
Series:eLife
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Online Access:https://elifesciences.org/articles/103728
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author Thomas A Bos
Elizaveta Polyakova
Janine Maria van Gils
Antoine AF de Vries
Marie-José Goumans
Christian Freund
Marco C DeRuiter
Monique RM Jongbloed
author_facet Thomas A Bos
Elizaveta Polyakova
Janine Maria van Gils
Antoine AF de Vries
Marie-José Goumans
Christian Freund
Marco C DeRuiter
Monique RM Jongbloed
author_sort Thomas A Bos
collection DOAJ
description Human autonomic neuronal cell models are emerging as tools for modeling diseases such as cardiac arrhythmias. In this systematic review, we compared 33 articles applying 14 different protocols to generate sympathetic neurons and 3 different procedures to produce parasympathetic neurons. All methods involved the differentiation of human pluripotent stem cells, and none employed permanent or reversible cell immortalization. Almost all protocols were reproduced in multiple pluripotent stem cell lines, and over half showed evidence of neural firing capacity. Common limitations in the field are a lack of three-dimensional models and models that include multiple cell types. Sympathetic neuron differentiation protocols largely mirrored embryonic development, with the notable absence of migration, axon extension, and target-specificity cues. Parasympathetic neuron differentiation protocols may be improved by including several embryonic cues promoting cell survival, cell maturation, or ion channel expression. Moreover, additional markers to define parasympathetic neurons in vitro may support the validity of these protocols. Nonetheless, four sympathetic neuron differentiation protocols and one parasympathetic neuron differentiation protocol reported more than two-thirds of cells expressing autonomic neuron markers. Altogether, these protocols promise to open new research avenues of human autonomic neuron development and disease modeling.
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spelling doaj-art-f5ea30b6a950455f82ff19b416bfbb982025-08-20T01:54:54ZengeLife Sciences Publications LtdeLife2050-084X2025-03-011410.7554/eLife.103728A systematic review and embryological perspective of pluripotent stem cell-derived autonomic postganglionic neuron differentiation for human disease modelingThomas A Bos0https://orcid.org/0000-0003-2837-7355Elizaveta Polyakova1https://orcid.org/0000-0002-9615-2871Janine Maria van Gils2Antoine AF de Vries3Marie-José Goumans4Christian Freund5Marco C DeRuiter6Monique RM Jongbloed7https://orcid.org/0000-0002-9132-0418Department of Anatomy and Embryology, Leiden University Medical Centre, Leiden, NetherlandsDepartment of Anatomy and Embryology, Leiden University Medical Centre, Leiden, NetherlandsDepartment of Anatomy and Embryology, Leiden University Medical Centre, Leiden, NetherlandsDepartment of Cardiology, Leiden University Medical Centre, Leiden, NetherlandsDepartment of Cell and Chemical Biology, Leiden University Medical Centre, Leiden, NetherlandsDepartment of Anatomy and Embryology, Leiden University Medical Centre, Leiden, Netherlands; Leiden hiPSC Centre, Leiden University Medical Centre, Leiden, NetherlandsDepartment of Anatomy and Embryology, Leiden University Medical Centre, Leiden, Netherlands; Centre for Congenital Heart Disease Amsterdam-Leiden (CAHAL), Leiden, NetherlandsDepartment of Anatomy and Embryology, Leiden University Medical Centre, Leiden, Netherlands; Department of Cardiology, Leiden University Medical Centre, Leiden, Netherlands; Centre for Congenital Heart Disease Amsterdam-Leiden (CAHAL), Leiden, NetherlandsHuman autonomic neuronal cell models are emerging as tools for modeling diseases such as cardiac arrhythmias. In this systematic review, we compared 33 articles applying 14 different protocols to generate sympathetic neurons and 3 different procedures to produce parasympathetic neurons. All methods involved the differentiation of human pluripotent stem cells, and none employed permanent or reversible cell immortalization. Almost all protocols were reproduced in multiple pluripotent stem cell lines, and over half showed evidence of neural firing capacity. Common limitations in the field are a lack of three-dimensional models and models that include multiple cell types. Sympathetic neuron differentiation protocols largely mirrored embryonic development, with the notable absence of migration, axon extension, and target-specificity cues. Parasympathetic neuron differentiation protocols may be improved by including several embryonic cues promoting cell survival, cell maturation, or ion channel expression. Moreover, additional markers to define parasympathetic neurons in vitro may support the validity of these protocols. Nonetheless, four sympathetic neuron differentiation protocols and one parasympathetic neuron differentiation protocol reported more than two-thirds of cells expressing autonomic neuron markers. Altogether, these protocols promise to open new research avenues of human autonomic neuron development and disease modeling.https://elifesciences.org/articles/103728sympathetic neuronsparasympathetic neuronspluripotent stem cellsembryologyhumansystematic review
spellingShingle Thomas A Bos
Elizaveta Polyakova
Janine Maria van Gils
Antoine AF de Vries
Marie-José Goumans
Christian Freund
Marco C DeRuiter
Monique RM Jongbloed
A systematic review and embryological perspective of pluripotent stem cell-derived autonomic postganglionic neuron differentiation for human disease modeling
eLife
sympathetic neurons
parasympathetic neurons
pluripotent stem cells
embryology
human
systematic review
title A systematic review and embryological perspective of pluripotent stem cell-derived autonomic postganglionic neuron differentiation for human disease modeling
title_full A systematic review and embryological perspective of pluripotent stem cell-derived autonomic postganglionic neuron differentiation for human disease modeling
title_fullStr A systematic review and embryological perspective of pluripotent stem cell-derived autonomic postganglionic neuron differentiation for human disease modeling
title_full_unstemmed A systematic review and embryological perspective of pluripotent stem cell-derived autonomic postganglionic neuron differentiation for human disease modeling
title_short A systematic review and embryological perspective of pluripotent stem cell-derived autonomic postganglionic neuron differentiation for human disease modeling
title_sort systematic review and embryological perspective of pluripotent stem cell derived autonomic postganglionic neuron differentiation for human disease modeling
topic sympathetic neurons
parasympathetic neurons
pluripotent stem cells
embryology
human
systematic review
url https://elifesciences.org/articles/103728
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