Two Types of Polyadenated mRNAs are Synthesized from <i>Drosophila</i> Replication‐Dependent Histone Genes

Akhmanova, Anna; Miedema, Koos; Kremer, Hannie; Hennig, Wolfgang

doi:10.1111/j.1432-1033.1997.00294.x

Cited by 18 publications

(13 citation statements)

References 44 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Curiously, clones with the poly(A) sequence starting in the stem-loop of both histone H1 and H3 mRNAs were also recovered at low frequency from the RT-PCR. The origin of these RT-PCR products is unclear, but they have also been observed by others (2).…”

Section: Resultsmentioning

confidence: 92%

Developmental Control of Histone mRNA and dSLBP Synthesis duringDrosophilaEmbryogenesis and the Role of dSLBP in Histone mRNA 3′ End Processing In Vivo

Lanzotti¹,

Kaygun²,

Yang

et al. 2002

Molecular and Cellular Biology

182

View full text Add to dashboard Cite

In metazoans, the 3 end of histone mRNA is not polyadenylated but instead ends with a stem-loop structure that is required for cell cycle-regulated expression. The sequence of the stem-loop in the Drosophila melanogaster histone H2b, H3, and H4 genes is identical to the consensus sequence of other metazoan histone mRNAs, but the sequence of the stem-loop in the D. melanogaster histone H2a and H1 genes is novel. dSLBP binds to these novel stem-loop sequences as well as the canonical stem-loop with similar affinity. Eggs derived from females containing a viable, hypomorphic mutation in dSLBP store greatly reduced amounts of all five histone mRNAs in the egg, indicating that dSLBP is required in the maternal germ line for production of each histone mRNA. Embryos deficient in zygotic dSLBP function accumulate poly(A)؉ versions of all five histone mRNAs as a result of usage of polyadenylation signals located 3 of the stem-loop in each histone gene. Since the 3 ends of adjacent histone genes are close together, these polyadenylation signals may ensure the termination of transcription in order to prevent read-through into the next gene, which could possibly disrupt transcription or produce antisense histone mRNA that might trigger RNA interference. During early wild-type embryogenesis, ubiquitous zygotic histone gene transcription is activated at the end of the syncytial nuclear cycles during S phase of cycle 14, silenced during the subsequent G 2 phase, and then reactivated near the end of that G 2 phase in the well-described mitotic domain pattern. There is little or no dSLBP protein provided maternally in wild-type embryos, and zygotic expression of dSLBP is immediately required to process newly made histone pre-mRNA.

show abstract

Section: Resultsmentioning

confidence: 92%

Developmental Control of Histone mRNA and dSLBP Synthesis duringDrosophilaEmbryogenesis and the Role of dSLBP in Histone mRNA 3′ End Processing In Vivo

Lanzotti¹,

Kaygun²,

Yang

et al. 2002

Molecular and Cellular Biology

182

View full text Add to dashboard Cite

show abstract

“…We also fractionated the RNA on oligo(dT) cellulose prior to the S1 nuclease assay. There is a previous report that some histone mRNAs in Drosophila ovaries are polyadenylated (Akhmanova et al 1997). Akhmanova and coworkers cloned some of these polyadenylated mRNAs after RT-PCR, and many of the A-tails started at nucleotides within the 3 ′ side of the stem rather than 3 ′ of the stem-loop.…”

Section: Sequencingmentioning

confidence: 99%

EnD-Seq and AppEnD: sequencing 3′ ends to identify nontemplated tails and degradation intermediates

Welch

Slevin

Tatomer³

et al. 2015

RNA

View full text Add to dashboard Cite

Existing methods for detecting RNA intermediates resulting from exonuclease degradation are low-throughput and laborious. In addition, mapping the 3 ′ ends of RNA molecules to the genome after high-throughput sequencing is challenging, particularly if the 3 ′ ends contain post-transcriptional modifications. To address these problems, we developed EnD-Seq, a high-throughput sequencing protocol that preserves the 3 ′ end of RNA molecules, and AppEnD, a computational method for analyzing highthroughput sequencing data. Together these allow determination of the 3 ′ ends of RNA molecules, including nontemplated additions. Applying EnD-Seq and AppEnD to histone mRNAs revealed that a significant fraction of cytoplasmic histone mRNAs end in one or two uridines, which have replaced the 1-2 nt at the 3 ′ end of mature histone mRNA maintaining the length of the histone transcripts. Histone mRNAs in fly embryos and ovaries show the same pattern, but with different tail nucleotide compositions. We increase the sensitivity of EnD-Seq by using cDNA priming to specifically enrich low-abundance tails of known sequence composition allowing identification of degradation intermediates. In addition, we show the broad applicability of our computational approach by using AppEnD to gain insight into 3 ′ additions from diverse types of sequencing data, including data from small capped RNA sequencing and some alternative polyadenylation protocols.

show abstract

“…The transcripts are longer than normal and bind to oligo(dT), suggesting that they are polyadenylated. In the absence of sufficient dSLBP, it is likely that transcription continues past the normal 3Ј end of the histone mRNA, resulting in subsequent processing at cryptic polyA sites (Akhmanova et al 1997). In mammalian cells, artificially polyadenylated histone mRNA has an increased half-life and is not subject to normal posttranscriptional regulation (Pandey and Marzluff 1987).…”

Section: Genes and Development 181mentioning

confidence: 99%

Drosophilastem loop binding protein coordinates accumulation of mature histone mRNA with cell cycle progression

Sullivan¹,

Santiago²,

Parker³

et al. 2001

Genes Dev.

129

202

View full text Add to dashboard Cite

Replication-associated histone genes encode the only metazoan mRNAs that lack polyA tails, ending instead in a conserved 26-nt sequence that forms a stem-loop. Most of the regulation of mammalian histone mRNA is posttranscriptional and mediated by this unique 3 end. Stem-loop-binding protein (SLBP) binds to the histone mRNA 3 end and is thought to participate in all aspects of histone mRNA metabolism, including cell cycle regulation. To examine SLBP function genetically, we have cloned the gene encoding Drosophila SLBP (dSLBP) by a yeast three-hybrid method and have isolated mutations in dSLBP. dSLBP function is required both zygotically and maternally. Strong dSLBP alleles cause zygotic lethality late in development and result in production of stable histone mRNA that accumulates in nonreplicating cells. These histone mRNAs are cytoplasmic and have polyadenylated 3 ends like other polymerase II transcripts. Hypomorphic dSLBP alleles support zygotic development but cause female sterility. Eggs from these females contain dramatically reduced levels of histone mRNA, and mutant embryos are not able to complete the syncytial embryonic cycles. This is in part because of a failure of chromosome condensation at mitosis that blocks normal anaphase. These data demonstrate that dSLBP is required in vivo for 3 end processing of histone pre-mRNA, and that this is an essential function for development. Moreover, dSLBP-dependent processing plays an important role in coupling histone mRNA production with the cell cycle.

show abstract

Two Types of Polyadenated mRNAs are Synthesized from Drosophila Replication‐Dependent Histone Genes

Cited by 18 publications

References 44 publications

Developmental Control of Histone mRNA and dSLBP Synthesis duringDrosophilaEmbryogenesis and the Role of dSLBP in Histone mRNA 3′ End Processing In Vivo

Developmental Control of Histone mRNA and dSLBP Synthesis duringDrosophilaEmbryogenesis and the Role of dSLBP in Histone mRNA 3′ End Processing In Vivo

EnD-Seq and AppEnD: sequencing 3′ ends to identify nontemplated tails and degradation intermediates

Drosophilastem loop binding protein coordinates accumulation of mature histone mRNA with cell cycle progression

Contact Info

Product

Resources

About