Context-dependent Function of Regulatory Elements and a Switch in Chromatin Occupancy between GATA3 and GATA2 Regulate Gata2 Transcription during Trophoblast Differentiation

Ray, Soma; Dutta, Debasree; Rumi, M.A. Karim; Kent, Lindsey N.; Soares, Michael J.; Paul, Soumen

doi:10.1074/jbc.m807329200

Cited by 61 publications

(62 citation statements)

References 58 publications

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“…It was recently reported that switching in chromatin occupancy between GATA2 and GATA3 is an important mechanism for the transcriptional regulation of GATA2 gene expression and trophoblast differentiation [40]. These results indicate that changes and/or a balance in expression levels of GATA2 and GATA3 may be important in determining the expression of trophoblast-specific factor genes.…”

Section: Discussionmentioning

confidence: 68%

Regulation of Trophoblast-Specific Factors by GATA2 and GATA3 in Bovine Trophoblast CT-1 Cells

et al. 2011

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Abstract. Numerous transcription factors that regulate trophoblast developmental processes have been identified; however, the regulation of trophoblast-specific gene expression has not been definitively characterized. While a new role of Gata3 in trophoblast development was being demonstrated in mice, we examined effects of GATA transcription factors on conceptus interferon tau (IFNT), a major trophectoderm factor in ruminants. In this study, expression patterns of trophoblast ASCL2, CDX2, CSH1, ELF5, HAND1, IFNT, and TKDP1 mRNAs were initially examined, from which ASCL2, CDX2, IFNT, and TKDP1 mRNAs were found to be similar to those of GATA2 and GATA3 in days 17, 20, and 22 (day 0=day of estrus) bovine conceptuses. A chromatin immunoprecipitation (ChIP) assay revealed that endogenous GATA2 and GATA3 occupied GATA binding sites on the upstream regions of CSH1, IFNT, and TKDP1 genes and on the intron 1 region of CDX2 gene in bovine trophoblast CT-1 cells. In transient transfection analyses of the upstream region of bovine CSH1, and IFNT or the intron 1 region of CDX2 gene, over-expression of GATA2 induced transactivation of these trophoblast-specific genes in bovine non-trophoblast ear fibroblast EF cells, but over-expression of GATA3 did not substantially affect their transactivation. In CT-1 cells, endogenous CDX2 and IFNT mRNAs were down-regulated by GATA2 siRNA, while endogenous ASCL2 and CDX2 mRNAs were down-regulated by GATA3 siRNA. Our results indicate that in addition to trophectoderm lineage specification, GATA2 and/or GATA3 are involved in the regulation of trophoblast-specific gene transcription in bovine trophoblast CT-1 cells. Key words: Bovine, GATA factors, Gene regulation, Trophoblast cells (J. Reprod. Dev. 57: [518][519][520][521][522][523][524][525] 2011) uring mammalian development, the first lineage decision is to establish the trophectoderm (TE) and inner cell mass (ICM). The outer TE layer attaches to and invades the maternal endometrium and eventually forms placental structures. It has been well established that caudal-type homeobox transcription factor 2 (Cdx2) serves as a lineage determining factor for the murine trophectoderm [1,2]. Quite recently, one of the GATA transcription factors, Gata3, was found to specify the trophectoderm lineage [3].In addition to these factors, there are numerous factors that are expressed in the trophoblasts during trophectoderm cell differentiation. These are E74-like factor 5 (Elf5), heart and neural crest derivatives expressed 1 (Hand1), a mammalian achaete scute-like homolog 2 (Ascl2), placental lactogens (PLs, CSHs) in many mammalian species, and interferon tau (IFNT) and trophoblast Kunitz domain proteins (TKDPs) in ruminant ungulates. Elf5 is necessary to maintain expression of the trophoblast stem cell genes Cdx2 and Eomes, and thereby reinforces trophoblast cell fate [4]. Hand1 and Ascl2, basic helix-loop-helix (bHLH) transcription factor genes, are essential for trophoblast proliferation and differentiation in mice [5,6]. CSHs belong to the growt...

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Section: Discussionmentioning

confidence: 68%

Regulation of Trophoblast-Specific Factors by GATA2 and GATA3 in Bovine Trophoblast CT-1 Cells

et al. 2011

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“…ChIP-Real time PCR-based quantitative ChIP analysis was performed using our protocol described previously (12,13). Briefly, cells were trypsinized, cross-linked with formaldehyde (1%), and sonicated to generate chromatin fragments.…”

Section: Methodsmentioning

confidence: 99%

Inhibition of Protein Kinase C Signaling Maintains Rat Embryonic Stem Cell Pluripotency*

Rajendran

Dutta

Hong

et al. 2013

Journal of Biological Chemistry

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Background: Signaling mechanisms regulating rat embryonic stem cell (rESC) pluripotency are understood poorly. Results: Inhibition of PKC signaling promotes rESC self-renewal without compromising developmental potency. Conclusion: PKC signaling contributes to the balance of self-renewal versus differentiation of rESCs. Significance: PKC signaling could be targeted to derive rat pluripotent stem cells to establish transgenic models and for regenerative studies.

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“…S2a). Although both are putative transcriptional activators, some repressor activity has been reported (Takaki et al 2008;Ray et al 2009). Consistent with our data, we suggest that pStat6 and Gata-3 repress zfp157 expression.…”

Section: Zfp157 Is a Stat6-regulated Krab Domain Zinc Finger Proteinmentioning

confidence: 99%

The Stat6-regulated KRAB domain zinc finger protein Zfp157 regulates the balance of lineages in mammary glands and compensates for loss of Gata-3

Oliver¹,

Khaled²,

Frend³

et al. 2012

Genes Dev.

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Lineage commitment studies in mammary glands have focused on identifying cell populations that display stem or progenitor properties. However, the mechanisms that control cell fate have been incompletely explored. Herein we show that zinc finger protein 157 (Zfp157) is required to establish the balance between luminal alveolar pStat5-and Gata-3-expressing cells in the murine mammary gland. Using mice in which the zfp157 gene was disrupted, we found that alveologenesis was accelerated concomitantly with a dramatic skewing of the proportion of pStat5-expressing cells relative to Gata-3 + cells. This suppression of the Gata-3 + lineage was associated with increased expression of the inhibitor of helix-loop-helix protein Id2. Surprisingly, Gata-3 becomes dispensable in the absence of Zfp157, as mice deficient for both Zfp157 and Gata-3 lactate normally, although the glands display a mild epithelial dysplasia. These data suggest that the luminal alveolar compartment of the mammary gland is comprised of a number of distinct cell populations that, although interdependant, exhibit considerable cell fate plasticity.

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Context-dependent Function of Regulatory Elements and a Switch in Chromatin Occupancy between GATA3 and GATA2 Regulate Gata2 Transcription during Trophoblast Differentiation

Cited by 61 publications

References 58 publications

Regulation of Trophoblast-Specific Factors by GATA2 and GATA3 in Bovine Trophoblast CT-1 Cells

Regulation of Trophoblast-Specific Factors by GATA2 and GATA3 in Bovine Trophoblast CT-1 Cells

Inhibition of Protein Kinase C Signaling Maintains Rat Embryonic Stem Cell Pluripotency*

The Stat6-regulated KRAB domain zinc finger protein Zfp157 regulates the balance of lineages in mammary glands and compensates for loss of Gata-3

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