The Caenorhabditis elegans histone hairpin-binding protein is required for core histone gene expression and is essential for embryonic and postembryonic cell division

Jonathan Pettitt, Catriona Crombie, Daniel Schümperli, Berndt Marino Muller

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36 Citations (Scopus)

Abstract

As in all metazoans, the replication-dependent histone genes of Caenorhabditis elegans lack introns and contain a short hairpin structure in the 3' untranslated region. This hairpin structure is a key element for post-transcriptional regulation of histone gene expression and determines mRNA 3' end formation, nuclear export, translation and mRNA decay. All these steps contribute to the S-phase-specific expression of the replication-dependent histone genes. The hairpin structure is the binding site for histone hairpin-binding protein that is required for hairpin-dependent regulation. Here, we demonstrate that the C. elegans histone hairpin-binding protein gene is transcribed in dividing cells during embryogenesis and postembryonic development. Depletion of histone hairpin-binding protein (HBP) function in early embryos using RNA-mediated interference leads to an embryonic-lethal phenotype brought about by defects in chromosome condensation. A similar phenotype was obtained by depleting histones H3 and H4 in early embryos, indicating that the defects in hairpin-binding protein-depleted embryos are caused by reduced histone biosynthesis. We have confirmed this by showing that HBP depletion reduces histone gene expression. Depletion of HBP during postembryonic development also results in defects in cell division during late larval development. In addition, we have observed defects in the specification of vulval cell fate in animals depleted for histone H3 and H4, which indicates that histone proteins are required for cell fate regulation during vulval development.
Original languageEnglish
Pages (from-to)857-866
Number of pages10
JournalJournal of Cell Science
Volume115
Issue number4
Publication statusPublished - 15 Feb 2002

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Caenorhabditis elegans
Cell Division
Histones
Carrier Proteins
Gene Expression
Embryonic Structures
Genes
Phenotype
Cell Nucleus Active Transport
RNA Stability
Gene Expression Regulation
3' Untranslated Regions
RNA Interference
S Phase
Introns
Radioactivity
Embryonic Development
Chromosomes
Binding Sites

Keywords

  • 3' Untranslated Regions
  • Amino Acid Sequence
  • Animals
  • Base Sequence
  • Caenorhabditis elegans
  • Caenorhabditis elegans Proteins
  • Carrier Proteins
  • Cell Division
  • Chromosomal Proteins, Non-Histone
  • Conserved Sequence
  • Gene Expression Regulation, Developmental
  • Green Fluorescent Proteins
  • Histones
  • Humans
  • Larva
  • Luminescent Proteins
  • Molecular Sequence Data
  • RNA, Helminth
  • RNA-Binding Proteins
  • S Phase
  • Development
  • Histone gene expression
  • Mitosis

Cite this

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title = "The Caenorhabditis elegans histone hairpin-binding protein is required for core histone gene expression and is essential for embryonic and postembryonic cell division",
abstract = "As in all metazoans, the replication-dependent histone genes of Caenorhabditis elegans lack introns and contain a short hairpin structure in the 3' untranslated region. This hairpin structure is a key element for post-transcriptional regulation of histone gene expression and determines mRNA 3' end formation, nuclear export, translation and mRNA decay. All these steps contribute to the S-phase-specific expression of the replication-dependent histone genes. The hairpin structure is the binding site for histone hairpin-binding protein that is required for hairpin-dependent regulation. Here, we demonstrate that the C. elegans histone hairpin-binding protein gene is transcribed in dividing cells during embryogenesis and postembryonic development. Depletion of histone hairpin-binding protein (HBP) function in early embryos using RNA-mediated interference leads to an embryonic-lethal phenotype brought about by defects in chromosome condensation. A similar phenotype was obtained by depleting histones H3 and H4 in early embryos, indicating that the defects in hairpin-binding protein-depleted embryos are caused by reduced histone biosynthesis. We have confirmed this by showing that HBP depletion reduces histone gene expression. Depletion of HBP during postembryonic development also results in defects in cell division during late larval development. In addition, we have observed defects in the specification of vulval cell fate in animals depleted for histone H3 and H4, which indicates that histone proteins are required for cell fate regulation during vulval development.",
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TY - JOUR

T1 - The Caenorhabditis elegans histone hairpin-binding protein is required for core histone gene expression and is essential for embryonic and postembryonic cell division

AU - Pettitt, Jonathan

AU - Crombie, Catriona

AU - Schümperli, Daniel

AU - Muller, Berndt Marino

PY - 2002/2/15

Y1 - 2002/2/15

N2 - As in all metazoans, the replication-dependent histone genes of Caenorhabditis elegans lack introns and contain a short hairpin structure in the 3' untranslated region. This hairpin structure is a key element for post-transcriptional regulation of histone gene expression and determines mRNA 3' end formation, nuclear export, translation and mRNA decay. All these steps contribute to the S-phase-specific expression of the replication-dependent histone genes. The hairpin structure is the binding site for histone hairpin-binding protein that is required for hairpin-dependent regulation. Here, we demonstrate that the C. elegans histone hairpin-binding protein gene is transcribed in dividing cells during embryogenesis and postembryonic development. Depletion of histone hairpin-binding protein (HBP) function in early embryos using RNA-mediated interference leads to an embryonic-lethal phenotype brought about by defects in chromosome condensation. A similar phenotype was obtained by depleting histones H3 and H4 in early embryos, indicating that the defects in hairpin-binding protein-depleted embryos are caused by reduced histone biosynthesis. We have confirmed this by showing that HBP depletion reduces histone gene expression. Depletion of HBP during postembryonic development also results in defects in cell division during late larval development. In addition, we have observed defects in the specification of vulval cell fate in animals depleted for histone H3 and H4, which indicates that histone proteins are required for cell fate regulation during vulval development.

AB - As in all metazoans, the replication-dependent histone genes of Caenorhabditis elegans lack introns and contain a short hairpin structure in the 3' untranslated region. This hairpin structure is a key element for post-transcriptional regulation of histone gene expression and determines mRNA 3' end formation, nuclear export, translation and mRNA decay. All these steps contribute to the S-phase-specific expression of the replication-dependent histone genes. The hairpin structure is the binding site for histone hairpin-binding protein that is required for hairpin-dependent regulation. Here, we demonstrate that the C. elegans histone hairpin-binding protein gene is transcribed in dividing cells during embryogenesis and postembryonic development. Depletion of histone hairpin-binding protein (HBP) function in early embryos using RNA-mediated interference leads to an embryonic-lethal phenotype brought about by defects in chromosome condensation. A similar phenotype was obtained by depleting histones H3 and H4 in early embryos, indicating that the defects in hairpin-binding protein-depleted embryos are caused by reduced histone biosynthesis. We have confirmed this by showing that HBP depletion reduces histone gene expression. Depletion of HBP during postembryonic development also results in defects in cell division during late larval development. In addition, we have observed defects in the specification of vulval cell fate in animals depleted for histone H3 and H4, which indicates that histone proteins are required for cell fate regulation during vulval development.

KW - 3' Untranslated Regions

KW - Amino Acid Sequence

KW - Animals

KW - Base Sequence

KW - Caenorhabditis elegans

KW - Caenorhabditis elegans Proteins

KW - Carrier Proteins

KW - Cell Division

KW - Chromosomal Proteins, Non-Histone

KW - Conserved Sequence

KW - Gene Expression Regulation, Developmental

KW - Green Fluorescent Proteins

KW - Histones

KW - Humans

KW - Larva

KW - Luminescent Proteins

KW - Molecular Sequence Data

KW - RNA, Helminth

KW - RNA-Binding Proteins

KW - S Phase

KW - Development

KW - Histone gene expression

KW - Mitosis

M3 - Article

C2 - 11865041

VL - 115

SP - 857

EP - 866

JO - Journal of Cell Science

JF - Journal of Cell Science

SN - 0021-9533

IS - 4

ER -