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[Preprint]. 2024 Oct 19:2024.10.14.618205. [Version 2] doi: 10.1101/2024.10.14.618205

An iPSC model of fragile X syndrome reflects clinical phenotypes and reveals m 6 A-mediated epi-transcriptomic dysregulation underlying synaptic dysfunction

Lu Lu, Avijite Kumer Sarkar, Lan Dao, Yanchen Liu, Chunlong Ma, Phyo Han Thwin, Xuyao Chang, George Yoshida, Annie Li, Cenjing Wang, Crace Westerkamp, Lauren Schmitt, Maag Chelsey, Monzon Stephanie, Yu Zhao, Yaping Liu, Xiong Wang, Ling-Qiang Zhu, Dan Liu, Jason Tchieu, Makoto Miyakoshi, Haining Zhu, Christina Gross, Ernest Pedapati, Nathan Salomonis, Craig Erickson, Ziyuan Guo
PMCID: PMC11507714  PMID: 39464060

Abstract

Fragile X syndrome (FXS), the leading genetic cause of intellectual disability, arises from FMR1 gene silencing and loss of the FMRP protein. N6-methyladenosine (m 6 A) is a prevalent mRNA modification essential for post-transcriptional regulation. FMRP is known to bind to and regulate the stability of m 6 A-containing transcripts. However, how loss of FMRP impacts on transcriptome-wide m 6 A modifications in FXS patients remains unknown. To answer this question, we generated cortical neurons differentiated from induced pluripotent stem cells (iPSC) derived from healthy subjects and FXS patients. In electrophysiology recordings, we validated that synaptic and neuronal network defects in iPSC-derived FXS neurons corresponded to the clinical EEG data of the patients from which the corresponding iPSC line was derived. In analysis of transcriptome-wide methylation, we show that FMRP deficiency led to increased translation of m 6 A writers, resulting in hypermethylation that primarily affecting synapse-associated transcripts and increased mRNA decay. Conversely, in the presence of an m 6 A writer inhibitor, synaptic defects in FXS neurons were rescued. Taken together, our findings uncover that an FMRP-dependent epi-transcriptomic mechanism contributes to FXS pathogenesis by disrupting m 6 A modifications in FXS, suggesting a promising avenue for m 6 A-targeted therapies.

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