The DOI matches its Crossref record; 197 of the 197 references it cites were found in a registry or an index; none of the 202 sources its claims cite is checked for support yet.
Pioneer transcription factors: establishing competence for gene expression
Open accessAbstract
Transcription factors are adaptor molecules that detect regulatory sequences in the DNA and target the assembly of protein complexes that control gene expression. Yet much of the DNA in the eukaryotic cell is in nucleosomes and thereby occluded by histones, and can be further occluded by higher-order chromatin structures and repressor complexes. Indeed, genome-wide location analyses have revealed that, for all transcription factors tested, the vast majority of potential DNA-binding sites are unoccupied, demonstrating the inaccessibility of most of the nuclear DNA. This raises the question of how target sites at silent genes become bound de novo by transcription factors, thereby initiating regulatory events in chromatin. Binding cooperativity can be sufficient for many kinds of factors to simultaneously engage a target site in chromatin and activate gene expression. However, in cases in which the binding of a series of factors is sequential in time and thus not initially cooperative, special “pioneer transcription factors” can be the first to engage target sites in chromatin. Such initial binding can passively enhance transcription by reducing the number of additional factors that are needed to bind the DNA, culminating in activation. In addition, pioneer factor binding can actively open up the local chromatin and directly make it competent for other factors to bind. Passive and active roles for the pioneer factor FoxA occur in embryonic development, steroid hormone induction, and human cancers. Herein we review the field and describe how pioneer factors may enable cellular reprogramming.
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In the paper
“Simple target site affinity was not a predictor of FoxA occupancy, at least in terminally differentiated cells.”
§ Pioneer transcription factors: establishing competence for gene expression > Initiating events in chromatin: pioneer factors bind first
What the sources say
- Not checked yetcites Tuteja et al. 2008
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In the paper
“Genome-wide location analyses have shown that all known transcription factors physically occupy less than a few percent of their consensus target sites in the genome (Carr and Biggin 1999;Iyer et al. 2001;Yang et al. 2006;Joseph et al. 2010;Kaplan et al. 2011).”
§ Pioneer transcription factors: establishing competence for gene expression > Abstract
What the sources say
- Not checked yetcites Carr and Biggin 1999
- Not checked yetcites Iyer et al. 2001
- Not checked yetcites Yang et al. 2006
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In the paper
“The ability to genetically reprogram cells in the absence of DNA replication (Chiu and Blau 1984) means that the problem is not generally solved by simply having increased accessibility during chromatin assembly in S phase.”
§ Pioneer transcription factors: establishing competence for gene expression > Abstract
What the sources say
- Not checked yetcites Chiu and Blau 1984
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In the paper
“Passive and active roles for the pioneer factor FoxA occur in embryonic development, steroid hormone induction, and human cancers.”
§ Pioneer transcription factors: establishing competence for gene expression > Abstract
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In the paper
“On the other hand, careful analysis of genome-wide FoxA binding in the adult mouse liver revealed that FoxA target sites with a medium or weak consensus binding sequence were at genes that are much more liver-specific than genes with a strong consensus sequence (Tuteja et al. 2008).”
§ Pioneer transcription factors: establishing competence for gene expression > Initiating events in chromatin: pioneer factors bind first
What the sources say
- Not checked yetcites Tuteja et al. 2008
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In the paper
“Six binding sites were occupied at the same sequence in nascent liver buds in mouse embryos (Gualdi et al. 1996).”
§ Pioneer transcription factors: establishing competence for gene expression > Initiating events in chromatin: pioneer factors bind first
What the sources say
- Not checked yetcites Gualdi et al. 1996
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In the paper
“For example, in vivo footprinting analysis of the liverspecific enhancer of the Alb1 gene in adult mouse liver revealed a continuous array of five factor-binding sites occupied over a 120-base-pair (bp) region that is important for enhancer activity (Liu et al. 1991;McPherson et al. 1993).”
§ Pioneer transcription factors: establishing competence for gene expression > Initiating events in chromatin: pioneer factors bind first
What the sources say
- Not checked yetcites Liu et al. 1991
- Not checked yetcites McPherson et al. 1993
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In the paper
“In addition, pioneer factor binding can actively open up the local chromatin and directly make it competent for other factors to bind.”
§ Pioneer transcription factors: establishing competence for gene expression > Abstract
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In the paper
“Furthermore, as described below, pioneer factors have the special property of being able to bind their target sites in condensed chromatin.”
§ Pioneer transcription factors: establishing competence for gene expression > Initiating events in chromatin: pioneer factors bind first
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In the paper
“Furthermore, in adult liver tissue, FoxA1 and FoxA2 binding was not required to maintain local nucleosome organization (Z Li et al. 2011).”
§ Pioneer transcription factors: establishing competence for gene expression > Initiating events in chromatin: pioneer factors bind first
What the sources say
- Not checked yetcites Z Li et al. 2011
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- It may state two separate claims as one. 71
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In the paper
“By these criteria, FoxA and GATA are initial and important chromatin-binding factors, and as such were termed pioneer factors.”
§ Pioneer transcription factors: establishing competence for gene expression > Initiating events in chromatin: pioneer factors bind first
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In the paper
“GATA-4 and GATA-6 are redundantly expressed in the foregut endoderm and are necessary for early liver development (Holtzinger and Evans 2005;Zhao et al. 2005;Watt et al. 2007).”
§ Pioneer transcription factors: establishing competence for gene expression > Initiating events in chromatin: pioneer factors bind first
What the sources say
- Not checked yetcites Holtzinger and Evans 2005
- Not checked yetcites Zhao et al. 2005
- Not checked yetcites Watt et al. 2007
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In the paper
“FoxA1 and FoxA2 are redundantly expressed in the foregut endoderm and are necessary for liver induction (Lee et al. 2005).”
§ Pioneer transcription factors: establishing competence for gene expression > Initiating events in chromatin: pioneer factors bind first
What the sources say
- Not checked yetcites Lee et al. 2005
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In the paper
“The importance of cooperative binding is reflected by the observation that many transcription factors individually cannot occupy their target sites on nucleosomal DNA in vitro, but cooperative interactions among a group of such factors can allow nucleosome binding (Adams and Workman 1995;Steger and Workman 1997).”
§ Pioneer transcription factors: establishing competence for gene expression > Abstract
What the sources say
- Not checked yetcites Adams and Workman 1995
- Not checked yetcites Steger and Workman 1997
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In the paper
“To summarize, many or most regulatory regions do not coincide with DNA sequence that assembles into intrinsically unstable nucleosomes.Thus, other mechanisms are needed to expose the DNA.”
§ Pioneer transcription factors: establishing competence for gene expression > Abstract
plain- Asserted: passes — The authors put it forward as true.
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In the paper
“Tuteja et al. (2008) did find that medium-and lower-affinity, liver-specific targets were highly enriched for binding of other hepatic nuclear factors, suggesting a role for cooperative binding during the maintenance of differentiation.”
§ Pioneer transcription factors: establishing competence for gene expression > Initiating events in chromatin: pioneer factors bind first
What the sources say
- Not checked yetcites Tuteja et al. 2008
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In the paper
“A distinction about the designation of pioneer factors is that they not only perform a genetic function early in the activation of transcription, but they have been physically shown to bind to the genome for a period prior to activation and prior to other factors binding and, as such, impart competence for activity (Fig. 1).”
§ Pioneer transcription factors: establishing competence for gene expression > Initiating events in chromatin: pioneer factors bind first
boosteddirect- Asserted: passes — The authors put it forward as true.
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In the paper
“However, all of the above observations do not address how general coregulators, chromatin modifiers, histone modifications, and hypersensitivity become localized to genomic sites in the first place and thus fail to resolve the issue of how regulatory events are initiated at particular genomic locations.”
§ Pioneer transcription factors: establishing competence for gene expression > Abstract
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In the paper
“While the specific dimethyl sulfate protection technique used for in vivo footprinting could have failed to detect other factors, FoxA and GATA site occupancy clearly preceded occupancy of the other enhancer-binding factors in nascent liver and occurred in progenitor cells prior to gene activation.”
§ Pioneer transcription factors: establishing competence for gene expression > Initiating events in chromatin: pioneer factors bind first
What the sources say
- Not checked yetcites Gualdi et al. 1996
boostedcorrelational- Asserted: passes — The authors put it forward as true.
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- Rests on an assumption: The dimethyl sulfate protection technique used for in vivo footprinting did not miss other factors that bound the Alb1 enhancer before FoxA and GATA.
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In the paper
“The binding sites were for FoxA and GATA factors, which are expressed in the endoderm and nascent liver (Ang et al. 1993;Arceci et al. 1993;Monaghan et al. 1993;Laverriere et al. 1994) and whose binding sites are crucial for Alb1 enhancer function (Liu et al. 1991;Bossard and Zaret 1998).”
§ Pioneer transcription factors: establishing competence for gene expression > Initiating events in chromatin: pioneer factors bind first
What the sources say
- Not checked yetcites Ang et al. 1993
- Not checked yetcites Arceci et al. 1993
- Not checked yetcites Liu et al. 1991
plaincorrelational- Asserted: passes — The authors put it forward as true.
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In the paper
“genome-wide location analyses have revealed that, for all transcription factors tested, the vast majority of potential DNA-binding sites are unoccupied, demonstrating the inaccessibility of most of the nuclear DNA.”
§ Pioneer transcription factors: establishing competence for gene expression > Abstract
boosteddirect- Asserted: passes — The authors put it forward as true.
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In the paper
“With regard to FoxA1, a C-terminal domain of the protein, independent of the central, DNA-binding domain, binds to core histones and is necessary for chromatin opening in vitro (Cirillo et al. 2002).”
§ Pioneer transcription factors: establishing competence for gene expression > Active and passive means by which pioneer factors are useful in development
What the sources say
- Not checked yetcites Cirillo et al. 2002
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In the paper
“While the two factors together are also not necessary for late fetal hepatocyte differentiation (Li et al. 2009), they are absolutely essential for the embryonic initiation of hepatic differentiation (Lee et al. 2005).”
§ Pioneer transcription factors: establishing competence for gene expression > Initiating events in chromatin: pioneer factors bind first
What the sources say
- Not checked yetcites Li et al. 2009
- Not checked yetcites Lee et al. 2005
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In the paper
“The FoxA factor was more active than the GATA factor in this regard, and studies of FoxE and FoxO have shown that they can similarly open compacted chromatin (Cuesta et al. 2007;Hatta and Cirillo 2007).”
§ Pioneer transcription factors: establishing competence for gene expression > Active and passive means by which pioneer factors are useful in development
What the sources say
- Not checked yetcites Cuesta et al. 2007
- Not checked yetcites Hatta and Cirillo 2007
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In the paper
“Chromatin opening properties have also been seen for the basic helix-loop-helix (bHLH) factor TFE3, which, in vitro, induces hypersensitivity in chromatin and mediates local nucleosome positioning (Ishii et al. 2004).”
§ Pioneer transcription factors: establishing competence for gene expression > Active and passive means by which pioneer factors are useful in development
What the sources say
- Not checked yetcites Ishii et al. 2004
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In the paper
“PU.1 and RUNX1 prime transcription of the c-fms/ csf1R gene, with RUNX1 being needed only transiently (Krysinska et al. 2007;Hoogenkamp et al. 2009).”
§ Pioneer transcription factors: establishing competence for gene expression > Initiating events in chromatin: pioneer factors bind first
What the sources say
- Not checked yetcites Krysinska et al. 2007
- Not checked yetcites Hoogenkamp et al. 2009
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In the paper
“Also, like linker histone, FoxA and other Fox family members are retained on mitotic chromosomes and thus could serve as ''bookmarking'' proteins in mitosis (Yan et al. 2006;Zaret et al. 2011).”
§ Pioneer transcription factors: establishing competence for gene expression > Active and passive means by which pioneer factors are useful in development
What the sources say
- Not checked yetcites Yan et al. 2006
- Not checked yetcites Zaret et al. 2011
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In the paper
“For example, direct assessments of FoxA1 and GATA-4, in comparison with other Alb1 enhancer-binding proteins, showed that these pioneer factors were uniquely capable of binding to their target sites in highly compacted chromatin in vitro and generating a local region of DNase or restriction enzyme sensitivity (Cirillo et al. 2002).”
§ Pioneer transcription factors: establishing competence for gene expression > Active and passive means by which pioneer factors are useful in development
What the sources say
- Not checked yetcites Cirillo et al. 2002
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In the paper
“In conclusion, the structure of the FoxA DNA-binding domain appears intermediate between that of linker histone and other transcription factors, and this feature contributes to pioneer activity.”
§ Pioneer transcription factors: establishing competence for gene expression > Active and passive means by which pioneer factors are useful in development
hedgeddirect- Asserted: passes — The authors put it forward as true.
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In the paper
“Also, from the fetal stages onward, a third homolog, FoxA3, is expressed in the liver and apparently provides compensation ( Z Li et al. 2011).”
§ Pioneer transcription factors: establishing competence for gene expression > Initiating events in chromatin: pioneer factors bind first
What the sources say
- Not checked yetcites Z Li et al. 2011
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In the paper
“An example of this is at the aforementioned Alb1 enhancer, where FoxA and GATA factor sites are bound in the endoderm, allowing a rapid and synchronous transcriptional response in the cell population receiving liver-inductive signals.”
§ Pioneer transcription factors: establishing competence for gene expression > Active and passive means by which pioneer factors are useful in development
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In the paper
“Indeed, FoxA proteins can bind their target sites on a nucleosome core particle in vitro and in vivo, and the DNA-binding domain alone is sufficient for such binding (Cirillo et al. 1998;Chaya et al. 2001).”
§ Pioneer transcription factors: establishing competence for gene expression > Active and passive means by which pioneer factors are useful in development
What the sources say
- Not checked yetcites Cirillo et al. 1998
- Not checked yetcites Chaya et al. 2001
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In the paper
“While FoxA factors lack the requisite basic residues on the ''back'' side of the globular domain to enable such binding, conversion of analogously positioned residues to basic residues in FoxA enables the factor to bind nucleosomes more tightly, similar to linker histone (Cirillo et al. 1998).”
§ Pioneer transcription factors: establishing competence for gene expression > Active and passive means by which pioneer factors are useful in development
What the sources say
- Not checked yetcites Cirillo et al. 1998
plaindirect- Asserted: passes — The authors put it forward as true.
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In the paper
“Notably, FoxA proteins move in nuclear chromatin much more slowly than other factors tested, implicating unusually tight chromatin binding in vivo (Sekiya et al. 2009).”
§ Pioneer transcription factors: establishing competence for gene expression > Active and passive means by which pioneer factors are useful in development
What the sources say
- Not checked yetcites Sekiya et al. 2009
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In the paper
“Notably, FoxD3 was shown to block methylation of an underlying CpG sequence at the silent Alb1 gene in ES cells, demonstrating that pioneer factor occupancy can modulate the local epigenetic state of chromatin (Xu et al. 2009).”
§ Pioneer transcription factors: establishing competence for gene expression > Initiating events in chromatin: pioneer factors bind first
What the sources say
- Not checked yetcites Xu et al. 2009
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In the paper
“The rate of association of FoxA for nucleosomes is low, apparently due to the need for proper rotational phasing of the target site on the nucleosome surface (Sekiya et al. 2009), but the rate of dissociation is much lower than that for free DNA (Cirillo and Zaret 1999).”
§ Pioneer transcription factors: establishing competence for gene expression > Active and passive means by which pioneer factors are useful in development
What the sources say
- Not checked yetcites Sekiya et al. 2009
- Not checked yetcites Cirillo and Zaret 1999
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In the paper
“PU.1 itself can expand the linker region between nucleosomes and promote local histone modifications, likely contributing to its ability to enhance binding of other factors (Ghisletti et al. 2010;Heinz et al. 2010).”
§ Pioneer transcription factors: establishing competence for gene expression > Initiating events in chromatin: pioneer factors bind first
What the sources say
- Not checked yetcites Ghisletti et al. 2010
- Not checked yetcites Heinz et al. 2010
hedgedconditional- Asserted: passes — The authors put it forward as true.
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In the paper
“While the FoxA factors have base-specific contacts with DNA that are necessary for site-specific binding (Clark et al. 1993;Sekiya et al. 2009), linker histone lacks such contacts and does not bind DNA sites specifically.”
§ Pioneer transcription factors: establishing competence for gene expression > Active and passive means by which pioneer factors are useful in development
What the sources say
- Not checked yetcites Clark et al. 1993
- Not checked yetcites Sekiya et al. 2009
plaindirect- Asserted: passes — The authors put it forward as true.
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In the paper
“Thus, binding of FoxA1 can help stabilize a nucleosome position (Shim et al. 1998), which in turn can phase other local binding sites on and off of nucleosomes to modulate factor binding.”
§ Pioneer transcription factors: establishing competence for gene expression > Active and passive means by which pioneer factors are useful in development
What the sources say
- Not checked yetcites Shim et al. 1998
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In the paper
“Interestingly, while Grg3 tetramers by themselves avidly bind chromatin, they do not elicit closing, herein defined as conferring resistance to nuclease access (Sekiya and Zaret 2007).”
§ Pioneer transcription factors: establishing competence for gene expression > Pioneer factors recruiting corepressor complexes
What the sources say
- Not checked yetcites Sekiya and Zaret 2007
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In the paper
“Undifferentiated embryonic endoderm cells express Grg1 and Grg3 when the albumin gene is silent, and both Grgs are markedly down-regulated during hepatic specification when the albumin gene is activated (Santisteban et al. 2010).”
§ Pioneer transcription factors: establishing competence for gene expression > Pioneer factors recruiting corepressor complexes
What the sources say
- Not checked yetcites Santisteban et al. 2010
plaincorrelational- Asserted: passes — The authors put it forward as true.
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None of the sources cited for this claim have been checked yet.
In the paper
“The yeast Rap1 protein can bind target sites in chromatin and open the domain for other factors (Yu and Morse 1999;Koerber et al. 2009).”
§ Pioneer transcription factors: establishing competence for gene expression > Active and passive means by which pioneer factors are useful in development
What the sources say
- Not checked yetcites Yu and Morse 1999
- Not checked yetcites Koerber et al. 2009
plaindirect- Asserted: passes — The authors put it forward as true.
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It may state two separate claims as one.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Pioneer factors can thus actively help initiate the assembly of regulatory factors on the DNA by either opening the chromatin locally, positioning nucleosomes, enabling intrinsic cooperative binding effects among other DNA-binding factors, or directly recruiting other chromatin modifiers and coregulators.”
§ Pioneer transcription factors: establishing competence for gene expression > Active and passive means by which pioneer factors are useful in development
plainconditional- Asserted: passes — The authors put it forward as true.
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In the paper
“Taken together, it appears that FoxA may recruit a corepressor to maintain the silent, competent state, and loss of the corepressor contributes to activation that is enabled by FoxA and additional factors that bind the enhancer during liver induction (Gualdi et al. 1996).”
§ Pioneer transcription factors: establishing competence for gene expression > Pioneer factors recruiting corepressor complexes
What the sources say
- Not checked yetcites Gualdi et al. 1996
hedgedconditional- Asserted: passes — The authors put it forward as true.
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In the paper
“The yeast Gal4 protein's DNA-binding domain can bind nucleosomal DNA in vitro and in vivo, the latter without replication, and stabilize distinct nucleosome positions (Taylor et al. 1991;Pazin et al. 1998;Balasubramanian and Morse 1999).”
§ Pioneer transcription factors: establishing competence for gene expression > Active and passive means by which pioneer factors are useful in development
What the sources say
- Not checked yetcites Taylor et al. 1991
- Not checked yetcites Pazin et al. 1998
- Not checked yetcites Balasubramanian and Morse 1999
plaindirect- Asserted: passes — The authors put it forward as true.
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In the paper
“ER is a member of the nuclear hormone receptor family of transcription factors, a subset of which, including the androgen receptor (AR) and the GR, is not stably bound to chromatin in unstimulated cells”
§ Pioneer transcription factors: establishing competence for gene expression > Pioneer factors enabling hormone induction in differentiated cells
What the sources say
- Not checked yetcites Glass and Rosenfeld 2000
- Not checked yetcites Hager et al. 2004
plain- Asserted: passes — The authors put it forward as true.
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In the paper
“Finally, FoxA proteins have an N-terminal, trans-activation domain (Fig. 3; Pani et al. 1992) that presumably recruits coregulators, which in turn can facilitate other factors to enter the chromatin.”
§ Pioneer transcription factors: establishing competence for gene expression > Active and passive means by which pioneer factors are useful in development
What the sources say
- Not checked yetcites Pani et al. 1992
hedgedconditional- Asserted: passes — The authors put it forward as true.
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In the paper
“FoxA1 binding is required for genes that are either induced or repressed by ER, as well as for ER binding in the presence of both an agonist (estrogen) and an antagonist (tamoxifen)”
§ Pioneer transcription factors: establishing competence for gene expression > Pioneer factors enabling hormone induction in differentiated cells
What the sources say
- Not checked yetcites Malik et al. 2010
- Not checked yetcites Hurtado et al. 2011
plaindirect- Asserted: passes — The authors put it forward as true.
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In the paper
“Although such target sequences may be a minority for GR at the genomic level (John et al. 2011), the sites where GR induces hypersensitivity are where other factors can subsequently enter the chromatin and therefore represent regions where GR serves as a pioneer factor (Voss et al. 2011).”
§ Pioneer transcription factors: establishing competence for gene expression > Active and passive means by which pioneer factors are useful in development
What the sources say
- Not checked yetcites John et al. 2011
- Not checked yetcites Voss et al. 2011
plaindirect- Asserted: passes — The authors put it forward as true.
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A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“The dependency of significant ER binding on FoxA1 illustrates that the latter functions as a pioneer factor for ER in breast cancer cells.”
§ Pioneer transcription factors: establishing competence for gene expression > Pioneer factors enabling hormone induction in differentiated cells
plaindirect- Asserted: passes — The authors put it forward as true.
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In the paper
“ER can positively regulate FoxA1 expression (and that of GATA3)”
§ Pioneer transcription factors: establishing competence for gene expression > Pioneer factors enabling hormone induction in differentiated cells
What the sources say
- Not checked yetcites Laganiere et al. 2005
plaindirect- Asserted: passes — The authors put it forward as true.
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In the paper
“expression of FoxA1 in ER-negative cells results in opportunistic binding of FoxA1 to numerous regions lacking H3K4me1 or H3K4me2 marks, followed by subsequent methylation of these histone residues”
§ Pioneer transcription factors: establishing competence for gene expression > Genomic analysis of FoxA1 and chromatin modifications at target sites
What the sources say
- Not checked yetcites Serandour et al. 2011
plaindirect- Asserted: passes — The authors put it forward as true.
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In the paper
“its expression negatively correlates with tumor grade and is associated with better survival”
§ Pioneer transcription factors: establishing competence for gene expression > Pioneer factors enabling hormone induction in differentiated cells
What the sources say
- Not checked yetcites Laganiere et al. 2005
- Not checked yetcites Thorat et al. 2008
- Not checked yetcites Albergaria et al. 2009
plaincorrelational- Asserted: passes — The authors put it forward as true.
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A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“we conclude that there are defined features of chromatin that can facilitate FoxA1 binding in breast cancer cells”
§ Pioneer transcription factors: establishing competence for gene expression > Genomic analysis of FoxA1 and chromatin modifications at target sites
plainconditional- Asserted: passes — The authors put it forward as true.
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In the paper
“Specific silencing of FoxA1 decreases the hypersensitivity of specific ER-and FoxA1-binding regions without affecting H3K4me1 or H3K4me2 levels”
§ Pioneer transcription factors: establishing competence for gene expression > Genomic analysis of FoxA1 and chromatin modifications at target sites
What the sources say
- Not checked yetcites Lupien et al. 2008
plaindirect- Asserted: passes — The authors put it forward as true.
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None of the sources cited for this claim have been checked yet.
In the paper
“;1 million predicted EREs exist in the human genome”
§ Pioneer transcription factors: establishing competence for gene expression > Genomic analysis of FoxA1 and chromatin modifications at target sites
What the sources say
- Not checked yetcites Vega et al. 2006
- Not checked yetcites Joseph et al. 2010
plain- Asserted: passes — The authors put it forward as true.
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A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“FoxA1 both positively and negatively regulates AR-binding potential”
§ Pioneer transcription factors: establishing competence for gene expression > Interaction between FoxA1 and diverse nuclear receptors
plaindirect- Asserted: passes — The authors put it forward as true.
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A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“implying that the presence of the H3K4me1 and H3K4me2 marks is important for FoxA1 binding (Lupien et al. 2008) and, therefore, ER binding”
§ Pioneer transcription factors: establishing competence for gene expression > Genomic analysis of FoxA1 and chromatin modifications at target sites
hedgeddirect- Asserted: passes — The authors put it forward as true.
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In the paper
“Expression of FoxA1 in U20S-ER cells can induce ER binding to regions previously only observed in the breast cancer cells, and this alters the genes that estrogen-ER can transcribe”
§ Pioneer transcription factors: establishing competence for gene expression > Genomic analysis of FoxA1 and chromatin modifications at target sites
What the sources say
- Not checked yetcites Hurtado et al. 2011
plaindirect- Asserted: passes — The authors put it forward as true.
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A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“A role for FoxA1 as a nuclear receptor regulatory protein and pioneer factor is not limited to ER and appears to be a more general phenomenon observed for other hormoneresponsive nuclear receptors.”
§ Pioneer transcription factors: establishing competence for gene expression > Interaction between FoxA1 and diverse nuclear receptors
hedgeddirect- Asserted: passes — The authors put it forward as true.
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It may state two separate claims as one.
- Rests on an assumption: FoxA1 and FoxA2 interact with the androgen receptor in prostate cancer cells.
None of the sources cited for this claim have been checked yet.
In the paper
“Molecular apocrine breast cancers are ER À AR + but express a gene expression pattern resembling an ER + breast cancer”
§ Pioneer transcription factors: establishing competence for gene expression > Interaction between FoxA1 and diverse nuclear receptors
What the sources say
- Not checked yetcites Farmer et al. 2005
- Not checked yetcites Doane et al. 2006
plaincorrelational- Asserted: passes — The authors put it forward as true.
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A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“heavily methylated regions may negatively impact ERand/or FoxA1-binding potential”
§ Pioneer transcription factors: establishing competence for gene expression > Genomic analysis of FoxA1 and chromatin modifications at target sites
hedgedconditional- Asserted: passes — The authors put it forward as true.
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It may state two separate claims as one.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“This establishes a stable platform for recruitment of ER-associated cofactors and mediating chromatin loops with promoters of target genes.”
§ Pioneer transcription factors: establishing competence for gene expression > Genomic analysis of FoxA1 and chromatin modifications at target sites
plaindirect- Asserted: passes — The authors put it forward as true.
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A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Upon FoxA1 binding, chromatin condensation is relieved further, thereby allowing ER to bind to local EREs”
§ Pioneer transcription factors: establishing competence for gene expression > Genomic analysis of FoxA1 and chromatin modifications at target sites
plaindirect- Asserted: passes — The authors put it forward as true.
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It may state two separate claims as one.
None of the sources cited for this claim have been checked yet.
In the paper
“In molecular apocrine breast cancer cells, AR substitutes for ER and uses FoxA1 to bind to the regulatory regions normally occupied by ER”
§ Pioneer transcription factors: establishing competence for gene expression > Interaction between FoxA1 and diverse nuclear receptors
What the sources say
- Not checked yetcites Ni et al. 2011
- Not checked yetcites Robinson et al. 2011
plaindirect- Asserted: passes — The authors put it forward as true.
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It may state two separate claims as one.
None of the sources cited for this claim have been checked yet.
In the paper
“it is possible that their accompanying pioneer factors may constitute therapeutic targets”
§ Pioneer transcription factors: establishing competence for gene expression > Pioneer factors as drug targets in cancer
What the sources say
- Not checked yetcites Nakshatri and Badve 2007
- Not checked yetcites Fu et al. 2011
- Not checked yetcites Hurtado et al. 2011
hedgedconditional- Asserted: passes — The authors put it forward as true.
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Probably not a substantial claim.
In the paper
“GATA proteins can bind to condensed chromatin and can induce local nuclease hypersensitivity, albeit more weakly than that by FoxA1”
§ Pioneer transcription factors: establishing competence for gene expression > GATA and other pioneer factors for nuclear receptors
What the sources say
- Not checked yetcites Cirillo et al. 2002
plaindirect- Asserted: passes — The authors put it forward as true.
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It may state two separate claims as one.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“the emerging picture involves multiple pioneer factors that contribute to ER-chromatin interactions, with an interplay and dependency existing between the factors”
§ Pioneer transcription factors: establishing competence for gene expression > GATA and other pioneer factors for nuclear receptors
plaincorrelational- Asserted: passes — The authors put it forward as true.
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It may state two separate claims as one.
None of the sources cited for this claim have been checked yet.
In the paper
“ER binding is redirected to different regions in the genome (Krum et al. 2008), and this is mediated by GATA4”
§ Pioneer transcription factors: establishing competence for gene expression > GATA and other pioneer factors for nuclear receptors
What the sources say
- Not checked yetcites Krum et al. 2008
- Not checked yetcites Miranda-Carboni et al. 2011
plaindirect- Asserted: passes — The authors put it forward as true.
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The paper states this without a source or data behind it here, so there is nothing to check it against. The quote shows it is in the paper.
In the paper
“In many of the gene transduction studies, multiple factors are required for the cellular conversion, and in cases in which a single ectopic factor has been used, it converts cells from related germ layer lineages.”
§ Pioneer transcription factors: establishing competence for gene expression > Summary and perspectives for cellular reprogramming
plaindirect- Asserted: passes — The authors put it forward as true.
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A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“FoxA factors still bind chromatin sites when other factors cannot, and enable other factors to bind”
§ Pioneer transcription factors: establishing competence for gene expression > Summary and perspectives for cellular reprogramming
plaindirect- Asserted: passes — The authors put it forward as true.
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In the paper
“is essential for ER-mediated transcription of target genes and for growth of MCF-7 breast cancer cells”
§ Pioneer transcription factors: establishing competence for gene expression > GATA and other pioneer factors for nuclear receptors
What the sources say
- Not checked yetcites Eeckhoute et al. 2007
plaindirect- Asserted: passes — The authors put it forward as true.
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It may state two separate claims as one.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Pioneer factors, including FoxA proteins, can initiate such regulatory events, at least in part due to their resemblance to linker histone, and, hence, special nucleosome-and chromatinbinding properties”
§ Pioneer transcription factors: establishing competence for gene expression > Summary and perspectives for cellular reprogramming
hedgedconditional- Asserted: passes — The authors put it forward as true.
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None of the sources cited for this claim have been checked yet.
In the paper
“Specific silencing of FoxA1 inhibits the proliferation of tamoxifen-resistant MCF-7 cells”
§ Pioneer transcription factors: establishing competence for gene expression > Pioneer factors as drug targets in cancer
What the sources say
- Not checked yetcites Hurtado et al. 2011
- Not checked yetcites Yamaguchi et al. 2008
plaindirect- Asserted: passes — The authors put it forward as true.
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In the paper
“GATA motifs are also enriched in AR-binding events in LnCaP prostate cancer cells, and GATA2 is shown to be recruited to several AR-binding regions, where it is required for effective AR-chromatin interactions”
§ Pioneer transcription factors: establishing competence for gene expression > GATA and other pioneer factors for nuclear receptors
What the sources say
- Not checked yetcites Wang et al. 2007
plaindirect- Asserted: passes — The authors put it forward as true.
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A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“genes can exist in stable states where they are transcriptionally silent, yet competent for expression”
§ Pioneer transcription factors: establishing competence for gene expression > Summary and perspectives for cellular reprogramming
plain- Asserted: passes — The authors put it forward as true.
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In the paper
“there are numerous genomic sites where such ''pioneer'' binding creates local hypersensitivity and promotes the recruitment of other transcription factors”
§ Pioneer transcription factors: establishing competence for gene expression > Interaction between FoxA1 and diverse nuclear receptors
What the sources say
- Not checked yetcites Voss et al. 2011
plaindirect- Asserted: passes — The authors put it forward as true.
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The paper states this without a source or data behind it here, so there is nothing to check it against. The quote shows it is in the paper.
In the paper
“While FoxA binding to target sequences on nucleosomes is efficient in vitro with unmodified histones, in vivo the factor exhibits preferences for particular modified domains”
§ Pioneer transcription factors: establishing competence for gene expression > Summary and perspectives for cellular reprogramming
plaincorrelational- Asserted: passes — The authors put it forward as true.
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It may state two separate claims as one.
In the paper
“Following FoxA1 and GR recruitment to the MMTV promoter, associated transcription factors, including NF1 and Oct1, can get recruited and increase transcriptional activity, but this can be dependent on the presence of FoxA1”
§ Pioneer transcription factors: establishing competence for gene expression > Interaction between FoxA1 and diverse nuclear receptors
What the sources say
- Not checked yetcites Belikov et al. 2009
plainconditional- Asserted: passes — The authors put it forward as true.
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In the paper
“AP-2g binds to a significant fraction of ER-binding events, where it is essential for estrogenmediated transcription and ER binding”
§ Pioneer transcription factors: establishing competence for gene expression > GATA and other pioneer factors for nuclear receptors
What the sources say
- Not checked yetcites Tan et al. 2011
plaindirect- Asserted: passes — The authors put it forward as true.
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None of the sources cited for this claim have been checked yet.
In the paper
“GATA3 is required for mammary gland development (Asselin-Labat et al. 2007) and maintains cellular differentiation in the adult”
§ Pioneer transcription factors: establishing competence for gene expression > GATA and other pioneer factors for nuclear receptors
What the sources say
- Not checked yetcites Asselin-Labat et al. 2007
- Not checked yetcites Kouros-Mehr et al. 2006
plaindirect- Asserted: passes — The authors put it forward as true.
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In the paper
“Increasing the number of cell divisions during reprogramming increases the time for stochastic events to occur, and thus enhances reprogramming efficiency”
§ Pioneer transcription factors: establishing competence for gene expression > Summary and perspectives for cellular reprogramming
What the sources say
- Not checked yetcites Hanna et al. 2009
plaindirect- Asserted: passes — The authors put it forward as true.
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In the paper
“Only a small subset of the targeted cells becomes converted, suggesting that either a subset of the cells are competent or stochastic parameters are involved”
§ Pioneer transcription factors: establishing competence for gene expression > Summary and perspectives for cellular reprogramming
What the sources say
- Not checked yetcites Yamanaka 2009
hedgedconditional- Asserted: passes — The authors put it forward as true.
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It may state two separate claims as one.
The paper relies on this without support.
The dimethyl sulfate protection technique used for in vivo footprinting did not miss other factors that bound the Alb1 enhancer before FoxA and GATA.
“While the specific dimethyl sulfate protection technique used for in vivo footprinting could have failed to detect other factors, FoxA and GATA site occupancy clearly preceded occupancy of the other enhancer-binding factors in nascent liver and occurred in progenitor cells prior to gene activation.”
The paper relies on this without support.
FoxA1 and FoxA2 interact with the androgen receptor in prostate cancer cells.
“It has been well established that both FoxA1 and FoxA2 interact with the AR, the driving transcription factor in prostate cancer cells.”
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“By the ability to enter closed chromatin at its own high-affinity sites, and by its functional role in controlling chromatin accessibility at other sites, PU.1 meets the criteria for “pioneer” factor activity in early pro-T cells (98)”
From Mechanisms of Action of Hematopoietic Transcription Factor PU.1 in Initiation of T-Cell Development (2019) · cites this paper as [98]
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“These reports, together with ours, challenge the concept that NF-κB and other signal-activated TFs are restricted to enhancer regions pre-activated by lineage-determining factors58.”
From Synergistic gene expression during the acute phase response is characterized by transcription factor assisted loading (2017) · cites this paper as [58]
Experimental — accuracy not yet measuredThe cited source says what the claim attributes to it.
In the citing paper
“However, these TFs (termed pioneer factors) were attributed with special properties that separated them functionally from the rest of TFs58.”
From Synergistic gene expression during the acute phase response is characterized by transcription factor assisted loading (2017) · cites this paper as [58]
The cited source says what the claim attributes to it.
In the citing paper
“FOXAs have a structural similarity to linker histories and are able to bind condensed chromatin, where they can either passively act as placeholders for recruitment of factors later in development or actively recruit other factors for transcriptional initiation (Sekiya et al., 2009; Zaret and Carroll, 2011).”
From Hippo Signaling Influences HNF4A and FOXA2 Enhancer Switching during Hepatocyte Differentiation (2014) · cites this paper as Zaret and Carroll, 2011
The cited source says what the claim attributes to it.
In the citing paper
“Often, pioneer factors must recruit additional non-pioneer sequence-specific TFs for efficient enhancer activation [30, 31].”
From Transcriptional enhancers and their communication with gene promoters (2021) · cites this paper as [31]
The cited source says what the claim attributes to it.
In the citing paper
“A subset of TFs known as pioneer factors are capable of overcoming this constraint through chromatin remodelling (reviewed in [31, 32]).”
From Transcriptional enhancers and their communication with gene promoters (2021) · cites this paper as [31]
In the citing paper
“FOXA2 is a pioneer transcription factor (Zaret and Carroll, 2011), and therefore, the age-dependent increase in FOXA2 binding likely causes the eviction of nucleosomes from these regions.”
From The Aging Epigenome (2016) · cites this paper as Zaret and Carroll, 2011
In the citing paper
“A typical characteristic of pioneer TFs is their ability to bind directly to heterochromatic DNA and recruit other factors to change the status to euchromatin to initiate transcription105,106.”
From Transcription factors as readers and effectors of DNA methylation (2016) · cites this paper as [106]
In the citing paper
“Indeed, we observed a large overlap between known pioneer TFs and proteins that bind to methylated DNA (for example, forkhead box protein A (FOXA) and GATA families, which are the best-studied pioneer factors)106,108–110.”
From Transcription factors as readers and effectors of DNA methylation (2016) · cites this paper as [106]
In the citing paper
“Pioneer TFs are a unique subset of TFs that drive these chromatin changes.”
From Transcription factors as readers and effectors of DNA methylation (2016) · cites this paper as [106]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
Each contradiction between two passages listed here was confirmed by an independent check.
Rated minor: it would not touch a result — a value no result rests on, a p-value that stays on the same side of the significance level, or a conflict that is clerical, resolved elsewhere in the paper, or outside its own findings.
In the paper
§ Pioneer transcription factors: establishing competence for gene expression > References
“184. Zaret KS, Yamamoto KR. 1984. Reversible and persistent changes in chromatin structure accompany activation of a glucocoriticoid-dependent enhancer element. Cell 258: 1780-1784.”
§ Pioneer transcription factors: establishing competence for gene expression > References
“166. Voss TC, Schiltz RL, Sung MH, Yen PM, Stamatoyannopoulos JA, Biddie SC, Johnson TA, Miranda TB, John S, Hager GL. 2011. Dynamic exchange at regulatory elements during chromatin remodeling underlies assisted loading mecha- nism. Cell 146: 544-554.”
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Proietti, C. J., Izzo, F., Flaqué, M. C. D., Russo, R. I. C., Venturutti, L., Mercogliano, M. F., Martino, M. D., Pineda, V., Muñoz, S., Guzmán, P., et al. (2015) · Molecular Endocrinology · doi:10.1210/me.2015-1170 · Cited by 15
Mori, H., Chen, J. Q., Cardiff, R. D., Pénzváltó, Z., Hubbard, N. E., Schuetter, L., Hovey, R. C., Trott, J. F., & Borowsky, A. D. (2017) · Breast Cancer Research · doi:10.1186/s13058-017-0892-8 · Cited by 15
Proietti, C. J., Cenciarini, M. E., & Elizalde, P. V. (2018) · Steroids · doi:10.1016/j.steroids.2017.12.015 · Cited by 15
Xu, D., Yang, H., Zhuo, Z., Lu, B., Hu, J., & Yang, F. (2020) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2020.12.098 · Cited by 15
Metadata
- Authors
- Zaret, K. S., & Carroll, J. S.
- Affiliations
- University of Pennsylvania (US)
- University of Cambridge (GB)
- Venue
- Genes & Development
- Publisher
- Cold Spring Harbor Laboratory
- Published
- 2011-11-01
- Volume
- 25
- Issue
- 21
- Pages
- 2227-2241
- ISSN
- 0890-9369 (ISSN-L)
- 1549-5477
- PMC
- PMC3219227
- OpenAlex
- W2122097157
- Semantic Scholar
- f9d723b94bcaa230978b0c3de2e657ed1c636702
- Cited by
- 1,589
- References
- 196
- Citations by year
- 2026: 75 · 2025: 68 · 2024: 59 · 2023: 94 · 2022: 114 · 2021: 130 · 2020: 131 · 2019: 121 · 2018: 126 · 2017: 119 · 2016: 141 · 2015: 112 · 2014: 128 · 2013: 107 · 2012: 60
- Type
- posted content
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Genes & Development (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Cancer Research UK (15602)
- National Institutes of Health (R37GM36477)
- National Institute of General Medical Sciences (R37GM36477, R37GM036477)
- National Institute of Diabetes and Digestive and Kidney Diseases (R01DK082623)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Chromatin Remodeling and Cancer
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Keywords
- pioneer transcription factors, chromatin accessibility, histone-DNA interactions, chromatin remodeling, FoxA, cooperative binding, gene expression regulation, cellular reprogramming, embryonic development, cancer
- MeSH terms
- Histones, Humans, Oxidoreductases, N-Demethylating, Protein Binding, Substrate Specificity, Transcription Factors, Gene Expression, Protein Structure, Tertiary
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
A language model drew the claims from the paper on 2026-10-06, under version 3 of the claim definition (model deepseek-v4.1-flash, prompt extract-v3).
A second model labelled each claim on 2026-10-06 (model jev-1.13-20260917, definition revision gold-guideline-v0.2).
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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