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. 2009 Jun 1;23(11):1247-69.
doi: 10.1101/gad.1792809.

Transcription termination by nuclear RNA polymerases

Patricia Richard  1 , James L Manley
Affiliations

Transcription termination by nuclear RNA polymerases

Patricia Richard et al. Genes Dev. .

Abstract

Gene transcription in the cell nucleus is a complex and highly regulated process. Transcription in eukaryotes requires three distinct RNA polymerases, each of which employs its own mechanisms for initiation, elongation, and termination. Termination mechanisms vary considerably, ranging from relatively simple to exceptionally complex. In this review, we describe the present state of knowledge on how each of the three RNA polymerases terminates and how mechanisms are conserved, or vary, from yeast to human.

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Figures

Figure 1.
Figure 1.
Mammalian RNAPII termination at protein-coding genes. Poly(A) site recognition leads to changes in the EC. Some factors associated with RNAPII through elongation that may function as anti-terminators are released (Paf1C, PC4) upon passage through the poly(A) site. At the same time, other factors, such as Xrn2, are recruited to the EC. After cleavage, Xrn2, most likely recruited by p54nrb/PSF, degrades the downstream RNA, “catches up” with RNAPII, and, perhaps with the aid of the helicase SETX, terminates transcription by releasing RNAPII from the template DNA. Involvement of chromatin remodeling factors and pausing sequences and factors are depicted. The RNAPII subunits Rpb3 and Rpb11 are also shown to play a role in termination by perhaps transducing a “termination signal.” The possible involvement of SR proteins in termination is also indicated.
Figure 2.
Figure 2.
Yeast RNAPII termination at snoRNA genes. Termination at terminator I (TI), the major termination site, is Nrd1-binding-dependent. The Nrd1 complex interacts with the Ser5-phosphorylated CTD and with the TRAMP and exosome complexes. The cleavage/polyadenylation machinery (CPF and CFIA) is not required for termination at TI (drawn as blurry complexes). Termination at terminator II (TII) involves cleavage/polyadenylation factors, while the Nrd1–TRAMP–exosome complex appears inactive in that process (blurry complexes). SnoRNA transcription couples termination with RNA surveillance. After release of the precursor, Trf4 and Pap1 adenylates the pre-snoRNA that will be processed by the exosome. Other factors shown to have a role in snoRNA termination are indicated. These include Pcf11, Paf1C, and the RNAPII subunits Rpb3 and Rpb11.
Figure 3.
Figure 3.
Organization of the rDNA genes in yeast and mouse. The rDNA transcription unit is 9.1-kb long in yeast and 43-kb long in human. It consists of a 35S precursor in yeast and 45S in human. The precursor contains the sequences of the mature 18S, 5.8S, and 25S/28S rRNAs separated by two ITSs, ITS1 and ITS2, and is flanked by two ETSs, the 5′ETS and 3′ETS. In yeast, the IGS is interrupted by the 5S rDNA gene, which is transcribed by RNAPIII in the opposite orientation. In yeast, RNAPI terminates predominantly at the T1 terminator, apparently dependent on Reb1 and located ∼90 bp downstream from the 25S sequence, in IGS1 (IGS upstream of the 5S gene). The “fail-safe” terminator (T2) is located ∼250 bp downstream from the 25S sequence. The RFB that binds Fob1 is located downstream from T2. In mouse, the major terminator (Sal box 1) is located ∼550 nt downstream from the 28S RNA. The origin of bidirectional replication (OBR) in mouse and the autonomously replicating sequence (ARS) in yeast are indicated, as well as the Rnt1 cleavage and the T0 terminator.
Figure 4.
Figure 4.
Mammalian RNAPI termination. Transcription terminates at the transcript release element composed of a stretch of Ts, upstream of the TTF-I-mediated pause site. The release factor PTRF, which interacts with RNAPI and TTF-I, recognizes the transcript release element and most likely binds the stretch of Us on the nascent RNA. The RNAPI-specific subunit Rpa12 also plays a role in yeast RNAPI termination that is possibly conserved in mammals. After cleavage of the precursor downstream from the 28S gene, Xrn2 degrades the downstream RNA, “catches up” with RNAPI, and participates in RNAPI release, possibly in conjunction with SETX. An unidentified 3′–5′ exonuclease might be involved in processing of the rRNA precursor.
Figure 5.
Figure 5.
RNAPIII termination. Most of the termination activity is triggered by RNAPIII itself. The subunits C37 and C53 are essential for termination. The heterodimer C37–C53 might play a role in reducing the elongation rate of RNAPIII, allowing for an increased pausing time at the terminator, composed of a stretch of four to five Ts in the coding DNA strand. Several auxiliary factors, such as La, PC4, Topoisomerase I, or TFIIIC, are proposed to participate in RNAPIII termination in mammals.
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