Combinatorial transcriptional regulation establishes subtype-appropriate synaptic properties in auditory neurons

Summary: Neurons develop diverse synapses that vary in content, morphology, and size. Although transcriptional regulators of neurotransmitter identity are known, it remains unclear how synaptic features are patterned among neuronal subtypes. In the auditory system, glutamatergic synaptic properties...

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Main Authors: Isle Bastille, Lucy Lee, Cynthia Moncada-Reid, Wei-Ming Yu, Austen Sitko, Andrea Yung, Mina Zamani, Nele Christophersen, Reza Maroofian, Hamid Galehdari, Norbert Babai, Barbara Vona, Tobias Moser, Lisa Goodrich
Format: Article
Language:English
Published: Elsevier 2025-06-01
Series:Cell Reports
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Online Access:http://www.sciencedirect.com/science/article/pii/S2211124725005674
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author Isle Bastille
Lucy Lee
Cynthia Moncada-Reid
Wei-Ming Yu
Austen Sitko
Andrea Yung
Mina Zamani
Nele Christophersen
Reza Maroofian
Hamid Galehdari
Norbert Babai
Barbara Vona
Tobias Moser
Lisa Goodrich
author_facet Isle Bastille
Lucy Lee
Cynthia Moncada-Reid
Wei-Ming Yu
Austen Sitko
Andrea Yung
Mina Zamani
Nele Christophersen
Reza Maroofian
Hamid Galehdari
Norbert Babai
Barbara Vona
Tobias Moser
Lisa Goodrich
author_sort Isle Bastille
collection DOAJ
description Summary: Neurons develop diverse synapses that vary in content, morphology, and size. Although transcriptional regulators of neurotransmitter identity are known, it remains unclear how synaptic features are patterned among neuronal subtypes. In the auditory system, glutamatergic synaptic properties vary across three spiral ganglion neuron (SGN) subtypes that collectively encode sound. Here, we demonstrate that Maf transcription factors combinatorially shape synaptic properties in SGNs. SGN subtypes express different ratios of c-Maf and Mafb, which act redundantly to impart subtype identities and individually to shape subtype-appropriate gene expression programs. On their own, c-Maf and Mafb have independent and opposing effects on synaptic features and hearing. A mutation in the MAFB leucine zipper domain causes deafness in humans, underscoring the importance of regulated Maf activity for hearing. Thus, functional diversity and coordinated action of Maf family members enable flexible and robust control of gene expression needed to generate synaptic heterogeneity across neuronal subtypes.
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spelling doaj-art-ca74d44ad9eb416a9d38952b0bcf3be22025-08-20T02:31:00ZengElsevierCell Reports2211-12472025-06-0144611579610.1016/j.celrep.2025.115796Combinatorial transcriptional regulation establishes subtype-appropriate synaptic properties in auditory neuronsIsle Bastille0Lucy Lee1Cynthia Moncada-Reid2Wei-Ming Yu3Austen Sitko4Andrea Yung5Mina Zamani6Nele Christophersen7Reza Maroofian8Hamid Galehdari9Norbert Babai10Barbara Vona11Tobias Moser12Lisa Goodrich13Department of Neurobiology, Harvard Medical School, Boston, MA, USADepartment of Neurobiology, Harvard Medical School, Boston, MA, USADepartment of Neurobiology, Harvard Medical School, Boston, MA, USADepartment of Neurobiology, Harvard Medical School, Boston, MA, USA; Department of Biology, Loyola University Chicago, Chicago, IL, USADepartment of Neurobiology, Harvard Medical School, Boston, MA, USADepartment of Neurobiology, Harvard Medical School, Boston, MA, USA; Genentech, South San Francisco, CA, USADepartment of Biology, Faculty of Sciences, Shahid Chamran University of Ahvaz, Ahvaz, Iran; Narges Medical Genetics and Prenatal Diagnosis Laboratory, Kianpars, Ahvaz, Iran; Department of Neuromuscular Diseases, Queen Square, Institute of Neurology, University College London, London, UKInstitute of Human Genetics, University Medical Center Göttingen, Göttingen, Germany; Institute for Auditory Neuroscience and InnerEarLab, University Medical Center Göttingen, Göttingen, GermanyDepartment of Neuromuscular Diseases, Queen Square, Institute of Neurology, University College London, London, UKDepartment of Biology, Faculty of Sciences, Shahid Chamran University of Ahvaz, Ahvaz, IranInstitute for Auditory Neuroscience and InnerEarLab, University Medical Center Göttingen, Göttingen, GermanyInstitute of Human Genetics, University Medical Center Göttingen, Göttingen, Germany; Institute for Auditory Neuroscience and InnerEarLab, University Medical Center Göttingen, Göttingen, GermanyInstitute for Auditory Neuroscience and InnerEarLab, University Medical Center Göttingen, Göttingen, GermanyDepartment of Neurobiology, Harvard Medical School, Boston, MA, USA; Corresponding authorSummary: Neurons develop diverse synapses that vary in content, morphology, and size. Although transcriptional regulators of neurotransmitter identity are known, it remains unclear how synaptic features are patterned among neuronal subtypes. In the auditory system, glutamatergic synaptic properties vary across three spiral ganglion neuron (SGN) subtypes that collectively encode sound. Here, we demonstrate that Maf transcription factors combinatorially shape synaptic properties in SGNs. SGN subtypes express different ratios of c-Maf and Mafb, which act redundantly to impart subtype identities and individually to shape subtype-appropriate gene expression programs. On their own, c-Maf and Mafb have independent and opposing effects on synaptic features and hearing. A mutation in the MAFB leucine zipper domain causes deafness in humans, underscoring the importance of regulated Maf activity for hearing. Thus, functional diversity and coordinated action of Maf family members enable flexible and robust control of gene expression needed to generate synaptic heterogeneity across neuronal subtypes.http://www.sciencedirect.com/science/article/pii/S2211124725005674CP: Neuroscience
spellingShingle Isle Bastille
Lucy Lee
Cynthia Moncada-Reid
Wei-Ming Yu
Austen Sitko
Andrea Yung
Mina Zamani
Nele Christophersen
Reza Maroofian
Hamid Galehdari
Norbert Babai
Barbara Vona
Tobias Moser
Lisa Goodrich
Combinatorial transcriptional regulation establishes subtype-appropriate synaptic properties in auditory neurons
Cell Reports
CP: Neuroscience
title Combinatorial transcriptional regulation establishes subtype-appropriate synaptic properties in auditory neurons
title_full Combinatorial transcriptional regulation establishes subtype-appropriate synaptic properties in auditory neurons
title_fullStr Combinatorial transcriptional regulation establishes subtype-appropriate synaptic properties in auditory neurons
title_full_unstemmed Combinatorial transcriptional regulation establishes subtype-appropriate synaptic properties in auditory neurons
title_short Combinatorial transcriptional regulation establishes subtype-appropriate synaptic properties in auditory neurons
title_sort combinatorial transcriptional regulation establishes subtype appropriate synaptic properties in auditory neurons
topic CP: Neuroscience
url http://www.sciencedirect.com/science/article/pii/S2211124725005674
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