Sex-Dependent Sensory Phenotypes and Related Transcriptomic Expression Profiles Are Differentially Affected by Angelman Syndrome

  • Lee Koyavski
  • Julia Panov
  • Lilach Simchi
  • Prudhvi Raj Rayi
  • Lital Sharvit
  • Yonatan Feuermann
  • Hanoch KaphzanEmail author


Angelman syndrome (AS) is a genetic disorder which entails autism, intellectual disability, lack of speech, motor deficits, and seizure susceptibility. It is caused by the lack of UBE3A protein expression, which is an E3-ubiquitin ligase. Despite AS equal prevalence in males and females, not much data on how sex affects the syndrome was reported. In the herein study, we thoroughly characterized many behavioral phenotypes of AS mice. The behavioral data acquired was analyzed with respect to sex. In addition, we generated a new mRNA sequencing dataset. We analyzed the coding transcriptome expression profiles with respect to the effects of genotype and sex observed in the behavioral phenotypes. We identified several neurobehavioral aspects, especially sensory perception, where AS mice either lack the male-to-female differences observed in wild-type littermates or even show opposed differences. However, motor phenotypes did not show male-to-female variation between wild-type (WT) and AS mice. In addition, by utilizing the mRNA sequencing, we identified genes and isoforms with expression profiles that mirror the sensory perception results. These genes are differentially regulated in the two sexes with inverse expression profiles in AS mice compared to WT littermates. Some of these are known pain-related and estrogen-dependent genes. The observed differences in sex-dependent neurobehavioral phenotypes and the differential transcriptome expression profiles in AS mice strengthen the evidence for molecular cross talk between Ube3a protein and sex hormone receptors or their elicited pathways. These interactions are essential for understanding Ube3a deletion effects, beyond its E3-ligase activity.


Angelman syndrome Ube3a Sex Behavioral phenotypes Transcriptome Bioinformatics analyses 



Angelman syndrome


wild type


contextual fear conditioning


Morris water maze


open-field arena


simple odor discrimination


sex-related opposite interaction


Comparative Toxicogenomics Database



We thank the Tauber Bioinformatics Research Center at the University of Haifa for their help and assistance in the bioinformatics analyses.

Author’s contributions

HK initiated the study. LK and HK designed the behavioral experiments. LK performed the experiments and supplied the data for analysis. PRR, LK, and HK analyzed the behavioral data. LS (Simchi) and LS (Sharvit) produced the biological material for RNA sequencing. JP, YF, and HK performed the bioinformatics analyses. LK, JP, YF, PRR, and HK wrote the manuscript.


This work was supported by personal grants from the Angelman Syndrome Foundation and by the Israel Science Foundation, Grant Number 287/15.

Compliance with Ethical Standards

Ethical Approval

All procedures were performed in strict accordance with the University of Haifa regulations and the US National Institutes of Health guidelines (NIH publication number 8023). All experiments and breeding protocols were approved by the animal welfare committee of the University of Haifa and the Israeli ministry of health.

Conflict of Interest

The authors declare that they have no conflict of interest.

Consent for Publication

Not applicable.

Supplementary material

12035_2019_1503_MOESM1_ESM.docx (333 kb)
ESM 1 (DOCX 332 kb)


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Authors and Affiliations

  1. 1.Laboratory for Neurobiology of Psychiatric Disorders, Sagol Department of NeurobiologyUniversity of HaifaHaifaIsrael

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