Histone gene expression and histone mRNA 3' end structure in Caenorhabditis elegans

Rebecca Keall, Sandra Whitelaw, Jonathan Pettitt, Berndt Muller

Research output: Contribution to journalArticle

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Abstract

Background: Histone protein synthesis is essential for cell proliferation and required for the packaging of DNA into chromatin. In animals, histone proteins are provided by the expression of multicopy replication- dependent histone genes. Histone mRNAs that are processed by a histonespecific mechanism to end after a highly conserved RNA hairpin element, and lack a poly( A) tail. In vertebrates and Drosophila, their expression is dependent on HBP/ SLBP that binds to the RNA hairpin element. We showed previously that these cis and trans acting regulators of histone gene expression are conserved in C. elegans. Here we report the results of an investigation of the histone mRNA 3' end structure and of histone gene expression during C. elegans development.

Results: Sequence analysis of replication- dependent histone genes revealed the presence of several highly conserved sequence elements in the 3' untranslated region of histone pre- mRNAs, including an RNA hairpin element and a polyadenylation signal. To determine whether in C. elegans histone mRNA 3' end formation occurs at this polyadenylation signal and results in polyadenylated histone mRNA, we investigated the mRNA 3' end structure of histone mRNA. Using poly( A) selection, RNAse protection and sequencing of histone mRNA ends, we determined that a majority of C. elegans histone mRNAs lack a poly( A) tail and end three to six nucleotides after the hairpin structure, after an A or a U, and have a 3' OH group. RNAi knock down of CDL- 1, the C. elegans HBP/ SLBP, does not significantly affect histone mRNA levels but severely depletes histone protein levels. Histone gene expression varies during development and is reduced in L3 animals compared to L1 animals and adults. In adults, histone gene expression is restricted to the germ line, where cell division occurs.

Conclusion: Our findings indicate that the expression of C. elegans histone genes is subject to control mechanisms similar to the ones in other animals: the structure of C. elegans histone mRNA 3' ends is compatible with histone- specific mRNA 3' end processing; CDL- 1 functions in posttranscriptional control of histone gene expression; and C. elegans histone mRNA levels are elevated at periods of active cell division, indicating that histone gene expression is linked to DNA replication.

Original languageEnglish
Article number51
Number of pages12
JournalBMC Molecular Biology
Volume8
DOIs
Publication statusPublished - 14 Jun 2007

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Caenorhabditis elegans
Histones
Gene Expression
Messenger RNA
Polyadenylation
RNA
Cell Division
DNA Packaging
Genes
Animal Structures

Keywords

  • loop-binding-protein
  • polyadenylation factor CPSF-73
  • cell-cycle progression
  • in-vitro
  • U7 SNRNP
  • translation
  • drosophila
  • proliferation
  • oocytes
  • site

Cite this

Histone gene expression and histone mRNA 3' end structure in Caenorhabditis elegans. / Keall, Rebecca; Whitelaw, Sandra; Pettitt, Jonathan; Muller, Berndt.

In: BMC Molecular Biology, Vol. 8, 51, 14.06.2007.

Research output: Contribution to journalArticle

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T1 - Histone gene expression and histone mRNA 3' end structure in Caenorhabditis elegans

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N2 - Background: Histone protein synthesis is essential for cell proliferation and required for the packaging of DNA into chromatin. In animals, histone proteins are provided by the expression of multicopy replication- dependent histone genes. Histone mRNAs that are processed by a histonespecific mechanism to end after a highly conserved RNA hairpin element, and lack a poly( A) tail. In vertebrates and Drosophila, their expression is dependent on HBP/ SLBP that binds to the RNA hairpin element. We showed previously that these cis and trans acting regulators of histone gene expression are conserved in C. elegans. Here we report the results of an investigation of the histone mRNA 3' end structure and of histone gene expression during C. elegans development.Results: Sequence analysis of replication- dependent histone genes revealed the presence of several highly conserved sequence elements in the 3' untranslated region of histone pre- mRNAs, including an RNA hairpin element and a polyadenylation signal. To determine whether in C. elegans histone mRNA 3' end formation occurs at this polyadenylation signal and results in polyadenylated histone mRNA, we investigated the mRNA 3' end structure of histone mRNA. Using poly( A) selection, RNAse protection and sequencing of histone mRNA ends, we determined that a majority of C. elegans histone mRNAs lack a poly( A) tail and end three to six nucleotides after the hairpin structure, after an A or a U, and have a 3' OH group. RNAi knock down of CDL- 1, the C. elegans HBP/ SLBP, does not significantly affect histone mRNA levels but severely depletes histone protein levels. Histone gene expression varies during development and is reduced in L3 animals compared to L1 animals and adults. In adults, histone gene expression is restricted to the germ line, where cell division occurs.Conclusion: Our findings indicate that the expression of C. elegans histone genes is subject to control mechanisms similar to the ones in other animals: the structure of C. elegans histone mRNA 3' ends is compatible with histone- specific mRNA 3' end processing; CDL- 1 functions in posttranscriptional control of histone gene expression; and C. elegans histone mRNA levels are elevated at periods of active cell division, indicating that histone gene expression is linked to DNA replication.

AB - Background: Histone protein synthesis is essential for cell proliferation and required for the packaging of DNA into chromatin. In animals, histone proteins are provided by the expression of multicopy replication- dependent histone genes. Histone mRNAs that are processed by a histonespecific mechanism to end after a highly conserved RNA hairpin element, and lack a poly( A) tail. In vertebrates and Drosophila, their expression is dependent on HBP/ SLBP that binds to the RNA hairpin element. We showed previously that these cis and trans acting regulators of histone gene expression are conserved in C. elegans. Here we report the results of an investigation of the histone mRNA 3' end structure and of histone gene expression during C. elegans development.Results: Sequence analysis of replication- dependent histone genes revealed the presence of several highly conserved sequence elements in the 3' untranslated region of histone pre- mRNAs, including an RNA hairpin element and a polyadenylation signal. To determine whether in C. elegans histone mRNA 3' end formation occurs at this polyadenylation signal and results in polyadenylated histone mRNA, we investigated the mRNA 3' end structure of histone mRNA. Using poly( A) selection, RNAse protection and sequencing of histone mRNA ends, we determined that a majority of C. elegans histone mRNAs lack a poly( A) tail and end three to six nucleotides after the hairpin structure, after an A or a U, and have a 3' OH group. RNAi knock down of CDL- 1, the C. elegans HBP/ SLBP, does not significantly affect histone mRNA levels but severely depletes histone protein levels. Histone gene expression varies during development and is reduced in L3 animals compared to L1 animals and adults. In adults, histone gene expression is restricted to the germ line, where cell division occurs.Conclusion: Our findings indicate that the expression of C. elegans histone genes is subject to control mechanisms similar to the ones in other animals: the structure of C. elegans histone mRNA 3' ends is compatible with histone- specific mRNA 3' end processing; CDL- 1 functions in posttranscriptional control of histone gene expression; and C. elegans histone mRNA levels are elevated at periods of active cell division, indicating that histone gene expression is linked to DNA replication.

KW - loop-binding-protein

KW - polyadenylation factor CPSF-73

KW - cell-cycle progression

KW - in-vitro

KW - U7 SNRNP

KW - translation

KW - drosophila

KW - proliferation

KW - oocytes

KW - site

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DO - 10.1186/1471-2199-8-51

M3 - Article

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JO - BMC Molecular Biology

JF - BMC Molecular Biology

SN - 1471-2199

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