Sociosexual behavior requires both activating and repressive roles of Tfap2e/AP-2ε in vomeronasal sensory neurons

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Data availability
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Abstract

Neuronal identity dictates the position in an epithelium, and the ability to detect, process, and transmit specific signals to specified targets. Transcription factors (TFs) determine cellular identity via direct modulation of genetic transcription and recruiting chromatin modifiers. However, our understanding of the mechanisms that define neuronal identity and their magnitude remain a critical barrier to elucidate the etiology of congenital and neurodegenerative disorders. The rodent vomeronasal organ provides a unique system to examine in detail the molecular mechanisms underlying the differentiation and maturation of chemosensory neurons. Here we demonstrated that the identity of postmitotic/maturing vomeronasal sensory neurons (VSNs), and vomeronasal dependent behaviors can be reprogrammed through the rescue of Tfap2e/AP-2e expression in the Tfap2e^Null mice, and partially reprogrammed by inducing ectopic Tfap2e expression in mature apical VSNs. We suggest that the transcription factor Tfap2e can reprogram VSNs bypassing cellular plasticity restrictions, and that it directly controls the expression of batteries of vomeronasal genes.

Data availability

All data generated or analyzed during this study are included in the manuscript and supporting file; Source Data files have been provided for Figures 1 and 6.The scRNA-seq data discussed in this publication have been deposited in NCBI's Gene Expression Omnibus and are accessible through GEO series accession number GSE192746 (https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE192746). We also utilized previously published data from (Katreddi et al., 2021), available through GEO series accession number GSE190330 (https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE190330).The data from this CUT&RUN experiment has been deposited into the NCBI's Expression Omnibus and are accessible through GEO series accession number GSE193139 (https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE193139).

The following data sets were generated

1. Lin JM
2. Taroc EZ
3. Katreddi RR
4. Forni PE
(2022) Single cell RNA sequencing of P10 and adult vomeronasal organ of OMPCreR26AP2e and Controls
NCBI's Expression Omnibus, GSE192746.

https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE192746
1. Lin JM
2. Mitchell TA
3. Rothstein M
4. Pehl A
5. Taroc EZ
6. Katreddi RR
7. Parra KE
8. Zuloaga DG
9. Simoes-Costa M
10. Forni PE
(2022) Tfap2e/AP-2ε has both activating and repressive roles in controlling genetic programs of vomeronasal sensory neurons that underly sociosexual behavior in mice
NCBI's Expression Omnibus, GS193139.

https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE193139

The following previously published data sets were used

1. Katreddi R
2. Lin JM
3. Taroc EZ
4. Hicks SM
5. Forni PE
(2022) single cell RNA sequencing of adult (P60) vomeronasal organ
NCBI's Expression Omnibus, GSE190330.

https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE190330

Article and author information

Author details

Jennifer M Lin

Department of Biological Sciences, University at Albany, State University of New York, Albany, United States

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-9197-0816
Tyler A Mitchell

Department of Biological Sciences, University at Albany, State University of New York, Albany, United States

Competing interests
The authors declare that no competing interests exist.
Megan Rothstein

Department of Molecular Biology and Genetics, Cornell University, Ithaca, United States

Competing interests
The authors declare that no competing interests exist.
Alison Pehl

Department of Biological Sciences, University at Albany, State University of New York, Albany, United States

Competing interests
The authors declare that no competing interests exist.
Ed Zandro M Taroc

Department of Biological Sciences, University at Albany, State University of New York, Albany, United States

Competing interests
The authors declare that no competing interests exist.
Raghu R Katreddi

Department of Biological Sciences, University at Albany, State University of New York, Albany, United States

Competing interests
The authors declare that no competing interests exist.
Katherine E Parra

Department of Psychology, University at Albany, State University of New York, Albany, United States

Competing interests
The authors declare that no competing interests exist.
Damian G Zuloaga

Department of Psychology, University at Albany, State University of New York, Albany, United States

Competing interests
The authors declare that no competing interests exist.
Marcos Simoes-Costa

Department of Molecular Biology and Genetics, Cornell University, Ithaca, United States

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0003-1452-7068
Paolo Emanuele Forni

Department of Biological Sciences, University at Albany, State University of New York, Albany, United States

For correspondence
pforni@albany.edu

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0001-6547-3464

Funding

Eunice Kennedy Shriver National Institute of Child Health and Human Development (R01-HD097331/HD/NICHD)

Paolo Emanuele Forni

National Institute on Deafness and Other Communication Disorders (R01-DC017149)

Paolo Emanuele Forni

National Institute of Dental and Craniofacial Research (R01DE028576)

Marcos Simoes-Costa

National Institute of Mental Health (R15-MH118692)

Damian G Zuloaga

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: All mouse studies were performed according to the approved Institutional Animal Care and Use Committee (IACUC) protocols (#20-002, #19-001) of the University at Albany.

Copyright

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.