Positive and Negative Functional Interactions Between Promoter Elements from Different Classes of RNA Polymerase III-transcribed Genes

Overview

Journal EMBO J

Specialties Biotechnology
Molecular Biology

Date 1990 Apr 1

PMID 2323333

Citations 11

Authors

H D Parry

I W Mattaj

Affiliations

Soon will be listed here.

Abstract

Consensus tRNA gene promoter elements, A and B boxes, were introduced into the coding sequence of a Xenopus U6 gene. Combinations in which A and B boxes were coupled to wild-type or mutant U6 promoters were made. In this way information about both the functions of individual promoter elements and functional relationships between different classes of RNA polymerase III promoter element were obtained. Mutants in which the U6 PSE was non-functional were rescued by the presence of a B box, indicating a degree of functional relationship between these two elements. Moreover, the B box acted to increase the transcriptional activity and competitive strength of the wild-type U6 promoter. In contrast, no evidence was obtained to suggest that a tRNA A box can interact productively with U6 promoter elements in the absence of a B box. Data obtained suggest that the U6 PSE functions as an 'adaptor', being necessary to enable the basal U6 promoter to respond to upstream enhancement. Certain combinations of U6 and tRNA promoter elements are shown to be mutually antagonistic by a mechanism which is likely to involve blockage of transcription initiation. In summary, the U6 and tRNA promoters are shown to consist of functionally related, but distinct, promoter elements whose interactions shed new light on their normal roles in transcription.

Citing Articles

Selection of retroviral reverse transcription primer is coordinated with tRNA biogenesis.

Kelly N, Palmer M, Morrow C J Virol. 2003; 77(16):8695-701.

PMID: 12885888 PMC: 167244. DOI: 10.1128/jvi.77.16.8695-8701.2003.

Cloning and characterization of the beta subunit of human proximal sequence element-binding transcription factor and its involvement in transcription of small nuclear RNA genes by RNA polymerases II and III.

Bai L, Wang Z, Yoon J, Roeder R Mol Cell Biol. 1996; 16(10):5419-26.

PMID: 8816454 PMC: 231541. DOI: 10.1128/MCB.16.10.5419.

Cloning of two proximal sequence element-binding transcription factor subunits (gamma and delta) that are required for transcription of small nuclear RNA genes by RNA polymerases II and III and interact with the TATA-binding protein.

Yoon J, Roeder R Mol Cell Biol. 1996; 16(1):1-9.

PMID: 8524284 PMC: 230972. DOI: 10.1128/MCB.16.1.1.

Upstream basal promoter element important for exclusive RNA polymerase III transcription of the EBER 2 gene.

Howe J, Shu M Mol Cell Biol. 1993; 13(5):2655-65.

PMID: 8386314 PMC: 359634. DOI: 10.1128/mcb.13.5.2655-2665.1993.

Proximal sequence element-binding transcription factor (PTF) is a multisubunit complex required for transcription of both RNA polymerase II- and RNA polymerase III-dependent small nuclear RNA genes.

Yoon J, Murphy S, Bai L, Wang Z, Roeder R Mol Cell Biol. 1995; 15(4):2019-27.

PMID: 7891697 PMC: 230429. DOI: 10.1128/MCB.15.4.2019.

References

Ciliberto G, Palla F, Tebb G, Mattaj I, Philipson L . Properties of a U1 RNA enhancer-like sequence. Nucleic Acids Res. 1987; 15(6):2403-16. PMC: 340659. DOI: 10.1093/nar/15.6.2403. View

BARK C, Weller P, Zabielski J, Janson L, Pettersson U . A distant enhancer element is required for polymerase III transcription of a U6 RNA gene. Nature. 1987; 328(6128):356-9. DOI: 10.1038/328356a0. View

Kunkel G, Pederson T . Transcription of a human U6 small nuclear RNA gene in vivo withstands deletion of intragenic sequences but not of an upstream TATATA box. Nucleic Acids Res. 1989; 17(18):7371-9. PMC: 334816. DOI: 10.1093/nar/17.18.7371. View

Ciliberto G, Castagnoli L, Cortese R . Transcription by RNA polymerase III. Curr Top Dev Biol. 1983; 18:59-88. DOI: 10.1016/s0070-2153(08)60579-7. View

Pieler T, Hamm J, Roeder R . The 5S gene internal control region is composed of three distinct sequence elements, organized as two functional domains with variable spacing. Cell. 1987; 48(1):91-100. DOI: 10.1016/0092-8674(87)90359-x. View

Larson D, Bradford-Wilcox J, Young L, Sprague K . A short 5' flanking region containing conserved sequences is required for silkworm alanine tRNA gene activity. Proc Natl Acad Sci U S A. 1983; 80(11):3416-20. PMC: 394054. DOI: 10.1073/pnas.80.11.3416. View

Tanaka M, Grossniklaus U, Herr W, Hernandez N . Activation of the U2 snRNA promoter by the octamer motif defines a new class of RNA polymerase II enhancer elements. Genes Dev. 1988; 2(12B):1764-78. DOI: 10.1101/gad.2.12b.1764. View

Sinha N, Biernat J, McManus J, Koster H . Polymer support oligonucleotide synthesis XVIII: use of beta-cyanoethyl-N,N-dialkylamino-/N-morpholino phosphoramidite of deoxynucleosides for the synthesis of DNA fragments simplifying deprotection and isolation of the final product. Nucleic Acids Res. 1984; 12(11):4539-57. PMC: 318857. DOI: 10.1093/nar/12.11.4539. View

Howe J, Shu M . Epstein-Barr virus small RNA (EBER) genes: unique transcription units that combine RNA polymerase II and III promoter elements. Cell. 1989; 57(5):825-34. DOI: 10.1016/0092-8674(89)90797-6. View

10.

Ciliberto G, Castagnoli L, Melton D, Cortese R . Promoter of a eukaryotic tRNAPro gene is composed of three noncontiguous regions. Proc Natl Acad Sci U S A. 1982; 79(4):1195-9. PMC: 345928. DOI: 10.1073/pnas.79.4.1195. View

11.

Carbon P, Murgo S, Ebel J, Krol A, Tebb G, Mattaj L . A common octamer motif binding protein is involved in the transcription of U6 snRNA by RNA polymerase III and U2 snRNA by RNA polymerase II. Cell. 1987; 51(1):71-9. DOI: 10.1016/0092-8674(87)90011-0. View

12.

Parry H, Tebb G, Mattaj I . The Xenopus U2 gene PSE is a single, compact, element required for transcription initiation and 3' end formation. Nucleic Acids Res. 1989; 17(10):3633-44. PMC: 317845. DOI: 10.1093/nar/17.10.3633. View

13.

Geiduschek E, Tocchini-Valentini G . Transcription by RNA polymerase III. Annu Rev Biochem. 1988; 57:873-914. DOI: 10.1146/annurev.bi.57.070188.004301. View

14.

Wilson E, Larson D, Young L, Sprague K . A large region controls tRNA gene transcription. J Mol Biol. 1985; 183(2):153-63. DOI: 10.1016/0022-2836(85)90209-8. View

15.

Fairall L, Rhodes D, Klug A . Mapping of the sites of protection on a 5 S RNA gene by the Xenopus transcription factor IIIA. A model for the interaction. J Mol Biol. 1986; 192(3):577-91. DOI: 10.1016/0022-2836(86)90278-0. View

16.

Engelke D, Ng S, Shastry B, Roeder R . Specific interaction of a purified transcription factor with an internal control region of 5S RNA genes. Cell. 1980; 19(3):717-28. DOI: 10.1016/s0092-8674(80)80048-1. View

17.

Bogenhagen D, Sakonju S, Brown D . A control region in the center of the 5S RNA gene directs specific initiation of transcription: II. The 3' border of the region. Cell. 1980; 19(1):27-35. DOI: 10.1016/0092-8674(80)90385-2. View

18.

Trendelenburg M, Mathis D, Oudet P . Transcription units of chicken ovalbumin gene observed after injection of cloned complete genes into Xenopus oocyte nuclei. Proc Natl Acad Sci U S A. 1980; 77(10):5984-8. PMC: 350197. DOI: 10.1073/pnas.77.10.5984. View

19.

Guilfoyle R, Weinmann R . Control region for adenovirus VA RNA transcription. Proc Natl Acad Sci U S A. 1981; 78(6):3378-82. PMC: 319571. DOI: 10.1073/pnas.78.6.3378. View

20.

Mattaj I, De Robertis E . Nuclear segregation of U2 snRNA requires binding of specific snRNP proteins. Cell. 1985; 40(1):111-8. DOI: 10.1016/0092-8674(85)90314-9. View