Bookmarking by specific and nonspecific binding of FoxA1 pioneer factor to mitotic chromosomes

Caravaca, Juan Manuel; Donahue, Greg; Becker, Justin S.; Zaret, Kenneth S.

doi:10.1186/1756-8935-6-s1-p94

Cited by 43 publications

(94 citation statements)

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“…Interestingly, the mitotic-retained sites of binding in GATA1 and FoxA1 are not associated with a particular histone modification. The one correlate that was observed is that the mitotic-retained FoxA1 sites are those with a higher predicted intrinsic nucleosome occupancy (Caravaca et al 2013). This is consistent with the above discussion about how predicted nucleosome occupancy is a prominent feature at genomic regulatory sequences and underscores the nucleosome-binding pioneer feature for mitotic bookmarking.…”

Section: Pioneer Factors As Bookmarking Factors In Mitosissupporting

confidence: 77%

“…Notably, the genes associated with GATA1 and FoxA1 binding in mitosis were among the first to be reactivated during mitotic exit (Kadauke et al 2012;Caravaca et al 2013). A careful experiment in which GATA1 was destroyed specifically in mitosis proved definitively that mitotic retention was crucial for timely gene reactivation during mitotic exit (Kadauke et al 2012).…”

Section: Pioneer Factors As Bookmarking Factors In Mitosismentioning

confidence: 99%

“…In the time since this initial discovery, it has become appreciated that the mitotic-retaining bookmarking factors are typically those classified as pioneer transcription factors, including GATA1 and FoxA1 (Table 1; Kadauke et al 2012;Caravaca et al 2013). Genome-wide binding studies of GATA1 and FoxA1 in mitosis show that only a minority of their interphase binding sites are retained in mitotic chromatin (Kadauke et al 2012;Caravaca et al 2013). Interestingly, the mitotic-retained sites of binding in GATA1 and FoxA1 are not associated with a particular histone modification.…”

Section: Pioneer Factors As Bookmarking Factors In Mitosismentioning

confidence: 99%

“…Chromatin decompaction Fakhouri et al 2010 Mitotic bookmarking (human) Binding to mitotic chromatin Caravaca et al 2013 Hormone-dependent cancer progression (human) Recruitment of hormone receptor Zaret and Carroll 2011;Jozwik and Carroll 2012 In vitro reconstituted nucleosome or nucleosome array…”

Section: Updike and Mango 2006mentioning

confidence: 99%

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Pioneer transcription factors in cell reprogramming

2014

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A subset of eukaryotic transcription factors possesses the remarkable ability to reprogram one type of cell into another. The transcription factors that reprogram cell fate are invariably those that are crucial for the initial cell programming in embryonic development. To elicit cell programming or reprogramming, transcription factors must be able to engage genes that are developmentally silenced and inappropriate for expression in the original cell. Developmentally silenced genes are typically embedded in ''closed'' chromatin that is covered by nucleosomes and not hypersensitive to nuclease probes such as DNase I. Biochemical and genomic studies have shown that transcription factors with the highest reprogramming activity often have the special ability to engage their target sites on nucleosomal DNA, thus behaving as ''pioneer factors'' to initiate events in closed chromatin. Other reprogramming factors appear dependent on pioneer factors for engaging nucleosomes and closed chromatin. However, certain genomic domains in which nucleosomes are occluded by higher-order chromatin structures, such as in heterochromatin, are resistant to pioneer factor binding. Understanding the means by which pioneer factors can engage closed chromatin and how heterochromatin can prevent such binding promises to advance our ability to reprogram cell fates at will and is the topic of this review.Cell fate control represents the most extreme form of gene regulation. Genes specific to the function of a particular type of cell may be antagonistic to the function of another type of cell, so nature has evolved diverse regulatory mechanisms to ensure stable patterns of gene activation and repression. In prokaryotes, self-sustaining regulatory networks of transcription factors bound to DNA can be sufficient to regulate gene activation and repression (Ptashne 2011). In eukaryotes, ;200-base-pair (bp) segments of the genome are wound nearly twice around an octamer of the four core histones to form nucleosomes, providing steric constraints on how transcription factors can bind DNA (Kornberg and Lorch 1999). As described below, pioneer transcription factors have the special property of being able to overcome such constraints, enabling the factors to engage closed chromatin that is not accessible by other types of transcription factors (Fig. 1). However, further higher-order packaging of nucleosomes into heterochromatin can occlude access to DNA altogether, presenting an additional barrier to cell fate conversion (Fig. 1). This review focuses on the most recent studies of pioneer factors in cell programming and reprogramming, how pioneer factors have special chromatinbinding properties, and facilitators and impediments to chromatin binding. We project that such knowledge will greatly aid future efforts to change the fates of cells at will for research, diagnostic, and therapeutic purposes.

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Section: Pioneer Factors As Bookmarking Factors In Mitosissupporting

confidence: 77%

Section: Pioneer Factors As Bookmarking Factors In Mitosismentioning

confidence: 99%

Section: Pioneer Factors As Bookmarking Factors In Mitosismentioning

confidence: 99%

Section: Updike and Mango 2006mentioning

confidence: 99%

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Pioneer transcription factors in cell reprogramming

2014

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“…FOXA1 is a pioneer transcription factor that binds to mitotic chromosomes and enables other factors to bind (61,62). The DBD of FOXA1 protein binds specific DNA and is required for its localization to mitotic chromosomes only when a nuclear localization signal is present (63,64). Interestingly, we have found a sequence in Orc1 that is similar to the chromatin-binding domain of the FOXA1 protein.…”

Section: Generation and Characterization Of Monoclonal Antibodies Agamentioning

confidence: 63%

Orc1 Binding to Mitotic Chromosomes Precedes Spatial Patterning during G1 Phase and Assembly of the Origin Recognition Complex in Human Cells

Kara

Hossain

Prasanth

et al. 2015

Journal of Biological Chemistry

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Background: Orc1 is the largest subunit of the origin recognition complex that promotes genome duplication. Results: We studied the dynamics of Orc1 during the cell division cycle. Conclusion: Orc1 binds to mitotic chromosomes, and during G 1 phase in the daughter cells it then forms spatial-temporal patterns in the nucleus. Significance: The large subunit of ORC orchestrates the earliest stages of chromosome inheritance.

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Transcription factor retention on mitotic chromosomes: regulatory mechanisms and impact on cell fate decisions

Raccaud

Suter

2017

FEBS Letters

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Edited by Wilhelm JustDuring mitosis, gene transcription stops, and the bulk of DNA-binding proteins are excluded from condensed chromosomes. While most gene-specific transcription factors are largely evicted from mitotic chromosomes, a subset remains bound to specific and non-specific DNA sites. Here, we review the current knowledge on the mechanisms leading to the retention of a subset of transcription factors on mitotic chromosomes and discuss the implications in gene expression regulation and their potential as an epigenetic mechanism controlling stem cell self-renewal and differentiation.

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Bookmarking by specific and nonspecific binding of FoxA1 pioneer factor to mitotic chromosomes

Abstract: Caravaca et al.: Bookmarking by specific and nonspecific binding of FoxA1 pioneer factor to mitotic chromosomes.

Cited by 43 publications

References 0 publications

Pioneer transcription factors in cell reprogramming

Pioneer transcription factors in cell reprogramming

Orc1 Binding to Mitotic Chromosomes Precedes Spatial Patterning during G1 Phase and Assembly of the Origin Recognition Complex in Human Cells

Transcription factor retention on mitotic chromosomes: regulatory mechanisms and impact on cell fate decisions

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