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Metabolism and regulation of canonical histone mRNAs: life without a poly(A) tail

Key Points

  • Replication-dependent histone mRNAs, which encode the most abundant histone proteins, are the only known cellular mRNAs that are not polyadenylated. Instead they end in a conserved stem–loop that interacts with stem–loop binding protein (SLBP), a factor involved in several steps of histone mRNA metabolism: pre-mRNA processing, translation and mRNA degradation.

  • Replication-dependent histone genes contain no introns, and the only pre-mRNA processing step is an endonucleoytic cleavage to form the 3′ end of the mRNA. By contrast, the replacement variant histone genes (H3.3 and H2A.Z) contain introns and their mRNAs are polyadenylated.

  • A complex containing SLBP, U7 small nuclear ribonucleoprotein and a cleavage factor processes the 3′ end of the histone mRNA. The cleavage factor contains some of the same components required for cleavage and polyadenylation, and one of these, CPSF73 (cleavage and polyadenylation specificity factor subunit 73), catalyses the cleavage of both histone pre-mRNAs and polyadenylated pre-mRNAs.

  • Histone genes are clustered in the genome and a nuclear organelle located near the histone genes contains many of the components required for histone gene expression. In vertebrates this organelle is a subset of Cajal bodies, whereas in Drosophila melanogaster it comprises a distinct structure called the histone locus body.

  • Recent studies suggest an unexpected connection between the ability to process replication-dependent histone mRNAs and the variant histone proteins H3.3 and H2A.Z that serves to help balance the proper amounts of the two types of histone proteins.

  • Replication-dependent histone mRNAs are present at high levels only in S phase cells, and in mammalian cells the stem–loop is the major cis element responsible for cell cycle regulation. SLBP is also cell-cycle-regulated, and is abundant only in S phase cells.

  • A diverse set of strategies, all involving the unique 3′ end of histone mRNA, have evolved for regulation of histone mRNA during oogenesis and early embryogenesis in metazoans.

  • Stem–loops in histone mRNAs and SLBP have recently been found in representatives of a broad range of unicellular eukaryotes, suggesting that the distinct structure of histone mRNAs is ancient.

Abstract

The canonical histone proteins are encoded by replication-dependent genes and must rapidly reach high levels of expression during S phase. In metazoans the genes that encode these proteins produce mRNAs that, instead of being polyadenylated, contain a unique 3′ end structure. By contrast, the synthesis of the variant, replication-independent histones, which are encoded by polyadenylated mRNAs, persists outside of S phase. Accurate positioning of both histone types in chromatin is essential for proper transcriptional regulation, the demarcation of heterochromatic boundaries and the epigenetic inheritance of gene expression patterns. Recent results suggest that the coordinated synthesis of replication-dependent and variant histone mRNAs is achieved by signals that affect formation of the 3′ end of the replication-dependent histone mRNAs.

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Figure 1: Structure and formation of canonical histone mRNAs.
Figure 2: Global view of histone mRNA metabolism in mammalian cells.
Figure 3: The Cajal body and the histone locus body (HLB).
Figure 4: Cell-cycle regulation of canonical histone mRNA.
Figure 5: Two models for histone variant function in core histone mRNA 3′ end formation.
Figure 6: Strategies for supplying canonical histones in early embryogenesis.

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Correspondence to William F. Marzluff.

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Glossary

Small nuclear RNA

(snRNA). A series of small nuclear RNAs are involved in pre-mRNA processing.

Cajal body

An organelle in the nucleus, characterized by the presence of the protein coilin, that contains many factors needed for snRNA biosynthesis and in vertebrates also contains U7 snRNP.

Spliceosome

The complex of small nuclear ribonucleoproteins and associated proteins that removes introns from pre-mRNAs.

Nucleolus

An organelle in the nucleus that primarily functions in ribosome biosynthesis.

Nurse cells

There are 16 germ cells in each D. melanogaster egg chamber (or follicle). One differentiates into the oocyte and the other 15 become highly polyploid nurse cells that synthesize much of the RNA and protein incorporated into the oocyte.

Endoreplication

Process of polyploidization of the genome in which repeated rounds of S phase occur without an intervening mitosis.

Germinal vesicle

The oocyte nucleus (4C) before meiosis.

Pronucleus

The haploid nucleus (1C) present in the egg after meiosis.

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Marzluff, W., Wagner, E. & Duronio, R. Metabolism and regulation of canonical histone mRNAs: life without a poly(A) tail. Nat Rev Genet 9, 843–854 (2008). https://doi.org/10.1038/nrg2438

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