Maternal expression and early induction of histone gene transcription factor Hinfp sustains development in pre-implantation embryos

Prachi N. Ghule, Rong Lin Xie, Jennifer L. Colby, Jaime A. Rivera-Pérez, Stephen N. Jones, Jane B. Lian, Janet L. Stein, Andre J van Wijnen, Gary S. Stein

Research output: Contribution to journalArticle

4 Citations (Scopus)

Abstract

Fidelity of histone gene expression is important for normal cell growth and differentiation that is stringently controlled during development but is compromised during tumorigenesis. Efficient production of histones for packaging newly replicated DNA is particularly important for proper cell division and epigenetic control during the initial pre-implantation stages of embryonic development. Here, we addressed the unresolved question of when the machinery for histone gene transcription is activated in the developing zygote to accommodate temporal demands for histone gene expression. We examined induction of Histone Nuclear Factor P (HINFP), the only known transcription factor required for histone H4 gene expression, that binds directly to a unique H4 promoter-specific element to regulate histone H4 transcription. We show that Hinfp gene transcripts are stored in oocytes and maternally transmitted to the zygote. Transcripts from the paternal Hinfp gene, which reflect induction of zygotic gene expression, are apparent at the 4- to 8-cell stage, when most maternal mRNA pools are depleted. Loss of Hinfp expression due to gene ablation reduces cell numbers in E3.5 stage embryos and compromises implantation. Reduced cell proliferation is attributable to severe reduction in histone mRNA levels accompanied by reduced cell survival and genomic damage as measured by cleaved Caspase 3 and phospho-H2AX staining, respectively. We conclude that transmission of maternal Hinfp transcripts and zygotic activation of the Hinfp gene together are necessary to control H4 gene expression in early pre-implantation embryos in order to support normal embryonic development.

Original languageEnglish (US)
Pages (from-to)311-320
Number of pages10
JournalDevelopmental Biology
Volume419
Issue number2
DOIs
StatePublished - Nov 15 2016

Fingerprint

Histones
Embryonic Development
Transcription Factors
Mothers
Genes
Gene Expression
Zygote
Stored Messenger RNA
Product Packaging
Epigenomics
Caspase 3
Cell Division
Transcriptional Activation
Oocytes
Cell Differentiation
Cell Survival
Carcinogenesis
Cell Count
Cell Proliferation
Staining and Labeling

Keywords

  • Hinfp
  • Histone H4
  • HLB
  • Mouse embryonic development
  • NPAT

ASJC Scopus subject areas

  • Molecular Biology
  • Developmental Biology
  • Cell Biology

Cite this

Ghule, P. N., Xie, R. L., Colby, J. L., Rivera-Pérez, J. A., Jones, S. N., Lian, J. B., ... Stein, G. S. (2016). Maternal expression and early induction of histone gene transcription factor Hinfp sustains development in pre-implantation embryos. Developmental Biology, 419(2), 311-320. https://doi.org/10.1016/j.ydbio.2016.09.003

Maternal expression and early induction of histone gene transcription factor Hinfp sustains development in pre-implantation embryos. / Ghule, Prachi N.; Xie, Rong Lin; Colby, Jennifer L.; Rivera-Pérez, Jaime A.; Jones, Stephen N.; Lian, Jane B.; Stein, Janet L.; van Wijnen, Andre J; Stein, Gary S.

In: Developmental Biology, Vol. 419, No. 2, 15.11.2016, p. 311-320.

Research output: Contribution to journalArticle

Ghule, PN, Xie, RL, Colby, JL, Rivera-Pérez, JA, Jones, SN, Lian, JB, Stein, JL, van Wijnen, AJ & Stein, GS 2016, 'Maternal expression and early induction of histone gene transcription factor Hinfp sustains development in pre-implantation embryos', Developmental Biology, vol. 419, no. 2, pp. 311-320. https://doi.org/10.1016/j.ydbio.2016.09.003
Ghule, Prachi N. ; Xie, Rong Lin ; Colby, Jennifer L. ; Rivera-Pérez, Jaime A. ; Jones, Stephen N. ; Lian, Jane B. ; Stein, Janet L. ; van Wijnen, Andre J ; Stein, Gary S. / Maternal expression and early induction of histone gene transcription factor Hinfp sustains development in pre-implantation embryos. In: Developmental Biology. 2016 ; Vol. 419, No. 2. pp. 311-320.
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