SMARCAD1 Contributes to the Regulation of Naive Pluripotency by Interacting with Histone Citrullination

Xiao, Shu Dong; Lee, Jia; Sridhar, Bharat; Cao, Xiaoyi; Yu, Pengfei; Zhao, Tianyi; Chen, Chieh Chun; McDee, Darina; Sloofman, Laura; Wang, Yan; Rivas‐Astroza, Marcelo; Telugu, Bhanu P.; Levasseur, Dana N.; Zhang, Kang; Liang, Han; Zhao, Jing; Tanaka, Tetsuya; Stormo, Gary D.; Zhong, Sheng

doi:10.1016/j.celrep.2017.02.070

Cited by 44 publications

(59 citation statements)

References 40 publications

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“…In the course of vertebrate evolution, citrullination was thus expanded in scope and adapted to a variety of cellular contexts, ranging from neutrophil extracellular trap release to stem cell potency, and from oligodendrocytes to bone marrow and keratinocytes 30 . The emerging physiological roles of the vertebrate PADIs, such as in the regulation of pluripotency and embryonic development 8,24,92,93 , or the newly described role of the fish PADI in tissue regeneration 94 , point to possible selective advantages conferred to metazoans by PADIs and offer a possible explanation for the fact that PADIs were retained so widely 95 . In a similar vein, it is interesting to consider our findings in light of the proposal that genes with a role antimicrobial defence are amenable to co-option by eukaryotic innate immune systems 46 .…”

Section: Discussionmentioning

confidence: 99%

Protein citrullination was introduced into animals by horizontal gene transfer from cyanobacteria

Cummings

Gori²,

Sánchez‐Pulido

et al. 2020

Preprint

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Protein post-translational modifications (PTMs) add an enormous amount of sophistication to biological systems but their origins are largely unexplored. Citrullination, a key regulatory mechanism in human physiology and pathophysiology, is particularly enigmatic in an evolutionary context. The citrullinating enzymes peptidylarginine deiminases (PADIs) are ubiquitous across vertebrates but absent from yeast, worms and flies. Here, we map the surprising evolutionary trajectory of PADIs into the animal lineage. We present strong phylogenetic support for a clade encompassing animal and cyanobacterial PADIs that excludes fungal and other bacterial homologues. The animal and cyanobacterial PADIs share unique, functionally relevant synapomorphies that are absent from all other homologues. Molecular clock calculations and sequence divergence analyses using the fossil record estimate the last common ancestor of the cyanobacterial and animal PADIs to be approximately 1 billion years old, far younger than the 3.35-4.52 billion years known to separate bacterial and eukaryotic lineages. Under an assumption of vertical descent, PADI sequence change is anachronistically slow during this evolutionary time frame, even when compared to mitochondrial proteins, products of likely endosymbiont gene transfer and some of the most highly conserved proteins in life. The consilience of evidence indicates that PADIs were introduced from cyanobacteria into animals by horizontal gene transfer (HGT). The ancestral cyanobacterial protein is enzymatically active and can citrullinate eukaryotic proteins, suggesting that the PADI HGT event introduced a new catalytic capability into the regulatory repertoire of animals. This study reveals the unusual evolution of a pleiotropic protein modification with clear relevance in human physiology and disease.

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Section: Discussionmentioning

confidence: 99%

Protein citrullination was introduced into animals by horizontal gene transfer from cyanobacteria

Cummings

Gori²,

Sánchez‐Pulido

et al. 2020

Preprint

View full text Add to dashboard Cite

show abstract

“…An unexpected role of another embryonic tissue-enriched SWI/SNF family member SMARCAD1 was discovered in a screen for factors binding deiminated histone 3 arginine 26 (H3R26Cit), a mark important for early embryonic development (Christophorou et al, 2014). SMARCAD1 is enriched in S/L-cultured ESCs compared with EpiSCs and its depletion results in the appearance of some EpiSC features (Xiao et al, 2017). SMARCAD1 chromatin binding and H3R26Cit counteract H3K9me3 deposition; however, it is unclear how this mechanism links to gene expression changes observed upon SMARCAD1 depletion and to what degree nucleosome remodeling is involved.…”

Section: The Swi/snf Familymentioning

confidence: 99%

Epigenetic control of transcriptional regulation in pluripotency and early differentiation

Gökbuget

Blelloch

2019

Development

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Pluripotent stem cells give rise to all cells of the adult organism, making them an invaluable tool in regenerative medicine. In response to differentiation cues, they can activate markedly distinct lineagespecific gene networks while turning off or rewiring pluripotency networks. Recent innovations in chromatin and nuclear structure analyses combined with classical genetics have led to novel insights into the transcriptional and epigenetic mechanisms underlying these networks. Here, we review these findings in relation to their impact on the maintenance of and exit from pluripotency and highlight the many factors that drive these processes, including histone modifying enzymes, DNA methylation and demethylation, nucleosome remodeling complexes and transcription factor-mediated enhancer switching.

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“…These findings do not exclude the possibility that there are sites in the genome that are bound by SMARCAD1 independently of KAP1. For example, additional mechanisms could involve histone modifications; one potential candidate is citrullinated histone H3 Arg-26, which SMARCAD1 interacts with in ESCs (10).…”

Section: Smarcad1 Genomic Localization Via Kap1mentioning

confidence: 99%

The CUE1 domain of the SNF2-like chromatin remodeler SMARCAD1 mediates its association with KRAB-associated protein 1 (KAP1) and KAP1 target genes

Ding

Bergmaier

Sachs

et al. 2018

Journal of Biological Chemistry

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Chromatin in embryonic stem cells (ESCs) differs markedly from that in somatic cells, with ESCs exhibiting a more open chromatin configuration. Accordingly, ATP-dependent chromatin remodeling complexes are important regulators of ESC homeostasis. Depletion of the remodeler SMARCAD1, an ATPase of the SNF2 family, has been shown to affect stem cell state, but the mechanistic explanation for this effect is unknown. Here, we set out to gain further insights into the function of SMARCAD1 in mouse ESCs. We identified KRAB-associated protein 1 (KAP1) as the stoichiometric binding partner of SMARCAD1 in ESCs. We found that this interaction occurs on chromatin and that SMARCAD1 binds to different classes of KAP1 target genes, including zinc finger protein (ZFP) and imprinted genes. We also found that the RING B-box coiled-coil (RBCC) domain in KAP1 and the proximal coupling of ubiquitin conjugation to ER degradation (CUE) domain in SMARCAD1 mediate their direct interaction. Of note, retention of SMARCAD1 in the nucleus depended on KAP1 in both mouse ESCs and human somatic cells. Mutations in the CUE1 domain of SMARCAD1 perturbed the binding to KAP1 and Accordingly, an intact CUE1 domain was required for tethering this remodeler to the nucleus. Moreover, mutation of the CUE1 domain compromised SMARCAD1 binding to KAP1 target genes. Taken together, our results reveal a mechanism that localizes SMARCAD1 to genomic sites through the interaction of SMARCAD1's CUE1 motif with KAP1.

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SMARCAD1 Contributes to the Regulation of Naive Pluripotency by Interacting with Histone Citrullination

Cited by 44 publications

References 40 publications

Protein citrullination was introduced into animals by horizontal gene transfer from cyanobacteria

Protein citrullination was introduced into animals by horizontal gene transfer from cyanobacteria

Epigenetic control of transcriptional regulation in pluripotency and early differentiation

The CUE1 domain of the SNF2-like chromatin remodeler SMARCAD1 mediates its association with KRAB-associated protein 1 (KAP1) and KAP1 target genes

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