RNA polymerases stall and/or prematurely terminate nearby both early and late promoters on polyomavirus DNA

Skarnes, William C.; Tessier, Daniel C.; Acheson, Nicholas H.

doi:10.1016/0022-2836(88)90099-x

Journal of Molecular Biology

1988

DOI: 10.1016/0022-2836(88)90099-x

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RNA polymerases stall and/or prematurely terminate nearby both early and late promoters on polyomavirus DNA

William C. Skarnes

Daniel C. Tessier²,

Nicholas H. Acheson³

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1991

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Cited by 46 publications

(32 citation statements)

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“…Premature termination termed attenuation, has been shown to regulate the quantity of mRNA of several animal viruses, including simian virus 40 (SV40) (1,14,15,48,49), polyomavirus (47), the parvovirus minute virus of mice (2,40), adenovirus type 2 (Ad2) (23,24,45), and human immunodeficiency virus types 1 and 2 (21,54). These observations indicate that regulation of gene expression can be exerted at the level of elongation by RNA polymerase II.…”

mentioning

confidence: 99%

Role of the mammalian transcription factors IIF, IIS, and IIX during elongation by RNA polymerase II.

Bengal¹,

Flores²,

Krauskopf³

et al. 1991

Mol. Cell. Biol.

149

133

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We have used a recently developed system that allows the isolation of complexes competent for RNA polymerase II elongation (E. Bengal, A. Goldring, and Y. Aloni, J. Biol. Chem. 264:18926-18932, 1989). Pulse-labeled transcription complexes were formed at the adenovirus major late promoter with use of HeLa cell extracts. Elongation-competent complexes were purified from most of the proteins present in the extract, as well as from loosely bound elongation factors, by high-salt gel filtration chromatography. We found that under these conditions the nascent RNA was displaced from the DNA during elongation. These column-purified complexes were used to analyze the activities of different transcription factors during elongation by RNA polymerase II. We found that transcription factor IIS (TFIIS), TFIIF, and TFIIX affected the efficiency of elongation through the adenovirus major late promoter attenuation site and a synthetic attenuation site composed of eight T residues. These factors have distinct activities that depend on whether they are added before RNA polymerase has reached the attenuation site or at the time when the polymerase is pausing at the attenuation site. TFIIS was found to have antiattenuation activity, while TFIIF and TFIIX stimulated the rate of elongation. In comparison with TFIIF, TFIIS is loosely bound to the elongation complex. We also found that the activities of the factors are dependent on the nature of the attenuator. These results indicate that at least three factors play a major role during elongation by RNA polymerase II.RNA polymerase II sequentially utilizes several accessory factors during the multistage process of transcription (27). These factors can be functionally classified into three groups: (i) regulatory factors, which either directly bind to specific DNA sequences (18,26) or regulate the activity of specific DNA binding proteins (18); (ii) general transcription factors, which together with RNA polymerase II constitute the basic transcription machinery required for basal levels of transcription (27, 44); and (iii) factors that affect elongation and termination by RNA polymerase 11 (21,30,34,37,50).Recent studies have shown that the expression of several genes can be regulated by premature termination (1,32,41). Interestingly, it has been shown that premature termination during transcription of the mouse 13-major globin gene (33), the c-myc gene (5), and the Drosophila heat shock gene hsp-70 (43) can vary with the physiological state of the cells. Premature termination termed attenuation, has been shown to regulate the quantity of mRNA of several animal viruses, including simian virus 40 (SV40) (1,14,15,48,49), polyomavirus (47), the parvovirus minute virus of mice (2, 40), adenovirus type 2 (Ad2) (23,24,45), and human immunodeficiency virus types 1 and 2 (21, 54). These observations indicate that regulation of gene expression can be exerted at the level of elongation by RNA polymerase II. The findings that 3'-end formation of Ul and U2 small nuclear RNAs requires promoter elements...

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mentioning

confidence: 99%

Role of the mammalian transcription factors IIF, IIS, and IIX during elongation by RNA polymerase II.

Bengal¹,

Flores²,

Krauskopf³

et al. 1991

Mol. Cell. Biol.

149

133

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“…Examples of eukaryotic genes include the cellular proto-oncogenes human and murine c-myc (4, 13,30,43), human L-myc (33), murine c-myb (2,63), rat, murine, and hamster c-fos (15,34), the human and murine adenosine deaminase (ADA) genes (6-8, 26, 35, 38, 45), the human histone H3.3 gene (50), the human epidermal growth factor receptor gene (18), and the Drosophila heat shock genes (53,54) as well as several other Drosophila genes (54). Some viral transcription units also contain elongation controls; examples include human immunodeficiency virus (28), simian virus 40 (22,23), adenovirus type 2 (20,39,42,64), polyomavirus (60), and minute virus of mice (1,51). Two mechanisms can lead to premature transcription arrest.…”

mentioning

confidence: 99%

Functional analysis of a stable transcription arrest site in the first intron of the murine adenosine deaminase gene.

et al. 1993

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Transcription arrest plays a role in regulating the expression of a number of genes, including the murine adenosine deaminase (ADA) gene. We have previously identified two prominent arrest sites at the 5' end of the ADA gene: one in the first exon and one in the first intron (J. W. Innis and R. E. Kellems, Mol. Cell. Biol. 11:5398-5409, 1991 (4,13,30,43), human L-myc (33), murine c-myb (2, 63), rat, murine, and hamster c-fos (15, 34), the human and murine adenosine deaminase (ADA) genes (6-8, 26, 35, 38, 45), the human histone H3.3 gene (50), the human epidermal growth factor receptor gene (18), and the Drosophila heat shock genes (53, 54) as well as several other Drosophila genes (54). Some viral transcription units also contain elongation controls; examples include human immunodeficiency virus (28), simian virus 40 (22, 23), adenovirus type 2 (20,39,42,64), polyomavirus (60), and minute virus of mice (1, 51). Two mechanisms can lead to premature transcription arrest. First, the polymerase may stop but not be released from the template, resulting in a pause. This is the case for the Drosophila heat shock genes, in which sequences in the promoter are capable of setting up a paused polymerase complex (36). Upon heat shock induction, the block to elongation is overcome, resulting in the production of full-length transcripts. One transcription elongation factor, SII (3,46,48,56), has been shown to promote readthrough of several pause sites, including those in the histone H3.3 gene (59) and the adenovirus major late promoter transcription unit (46, 48). The second mechanism involves RNA polymerase II dissociation from the template accompanied by the release of the nascent transcript, or premature termination. In the case of human immunodeficiency virus, prematurely terminated transcripts are produced by the inducer of short transcripts, which is located between -3 and +82 relative to the cap site (62). These transcripts can also be detected in vivo in the absence of Tat (28).In some cases, multiple elongation blocks have been described within a gene. For example, in the murine c-fos * Corresponding author. gene, a negative regulatory element (the FIRE, or fosintragenic regulatory element) which lies in the first exon has been identified (34). This block can be released by the titration of a putative factor, as shown by the release of the block in a p-fos-4acZ test construct upon coinjection of the FIRE sequence into rat fibroblasts (34). Within the first intron of the c-fos gene, a block to elongation which is calcium dependent has been found in murine macrophages. Functional analysis of this block has revealed that a 103-nucleotide (nt)-long intron 1 sequence is sufficient for obtaining the block in vitro (41). Similarly, in the c-myc gene, the site of transcription arrest has been mapped to two locations, one in the first exon (TI) and one in the first intron (TII) (5,13,30,37). Site T, is preceded by dyad symmetry and contains a uridine stretch (5). If this signal is similar to the rho-independent termination s...

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“…Examples of RNA polymerase II genes which are controlled at the level of transcription elongation include proto-oncogenes c-myc, c-fos, c-myb, L-myc, and N-myc (2,12,26,36,37,57), the human adenosine deaminase gene (10), the epidermal growth factor receptor gene (14), the 13-globin gene (30), the Drosophila hsp7O gene (28,46), and a number of genes of viruses such as the human immunodeficiency virus (HIV) (22,27), adenovirus (25), simian virus 40 (43), and polyomavirus (50). For reviews, see references 23 and 53.…”

mentioning

confidence: 99%

Transcription elongation in the human c-myc gene is governed by overall transcription initiation levels in Xenopus oocytes.

Spencer¹,

Kilvert²

1993

Mol. Cell. Biol.

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Both transcription initiation and transcription elongation contribute to the regulation of steady-state c-myc RNA levels. We have used the Xenopus oocyte transcription assay to study premature transcription termination which occurs in the first exon and intron of the human c-myc gene. Previous studies showed that after injection into Xenopus oocytes transcription from the c-myc PI promoter resulted in read-through transcripts whereas transcription from the stronger P2 promoter resulted in a combination of prematurely terminated and read-through transcripts. We now demonstrate that this promoter-specific processivity results from the overall amount of RNA polymerase TI transcription occurring from either promoter. Parameters that reduce the amount of transcription from P1 or P2, such as decreased concentration of template injected or decreased incubation time, result in a reduction in the ratio of terminated to read-through c-myc transcripts. Conversely, when transcription levels are increased by higher concentrations of injected template, increased incubation time, or coinjection with competing template, the ratio of terminated to read-through transcripts increases. We hypothesize that an RNA polymerase IT processivity function is depleted above a threshold level of transcription initiation, resulting in high levels of premature transcription termination. These findings account for the promoter-specific effects on transcription elongation previously seen in this assay system and suggest a mechanism whereby limiting transcription elongation factors may contribute to transcription regulation in other eukaryotic cells.

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RNA polymerases stall and/or prematurely terminate nearby both early and late promoters on polyomavirus DNA

Cited by 46 publications

References 54 publications

Role of the mammalian transcription factors IIF, IIS, and IIX during elongation by RNA polymerase II.

Role of the mammalian transcription factors IIF, IIS, and IIX during elongation by RNA polymerase II.

Functional analysis of a stable transcription arrest site in the first intron of the murine adenosine deaminase gene.

Transcription elongation in the human c-myc gene is governed by overall transcription initiation levels in Xenopus oocytes.

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