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Recruitment of CTCF to the SIRT1 promoter after Oxidative Stress mediates Cardioprotective Transcription

Wagner, T.; Priyanka, P.; Micheletti, R.; Friedman, M. J.; Nair, S. J.; Gamliel, A.; Taylor, H.; Song, X.; Cho, M.; Oh, S.; Li, W.; Han, J.; Ohgi, K. A.; Abrass, M.; D'Antonio-Chronowska, A.; D'Antonio, M.; Hazuda, H.; Duggirala, R.; Blangero, J.; Ding, S.; Guzmann, C.; Frazer, K.; Aggarwal, A. K.; Zemljic-Harpf, A. E.; Rosenfeld, M. G.; Suh, Y.

2024-05-19 cell biology
10.1101/2024.05.17.594600 bioRxiv
Show abstract

Because most DNA-binding transcription factors (dbTFs), including the architectural regulator CTCF, bind RNA and exhibit di-/multimerization, a central conundrum is whether these distinct properties are regulated post-transcriptionally to modulate transcriptional programs. Here, investigating stress-dependent activation of SIRT1, encoding an evolutionarily-conserved protein deacetylase, we show that induced phosphorylation of CTCF acts as a rheostat to permit CTCF occupancy of low-affinity promoter DNA sites to precisely the levels necessary. This CTCF recruitment to the SIRT1 promoter is eliciting a cardioprotective cardiomyocyte transcriptional activation program and provides resilience against the stress of the beating heart in vivo. Mice harboring a mutation in the conserved low-affinity CTCF promoter binding site exhibit an altered, cardiomyocyte-specific transcriptional program and a systolic heart failure phenotype. This transcriptional role for CTCF reveals that a covalent dbTF modification regulating signal-dependent transcription serves as a previously unsuspected component of the oxidative stress response.

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