Skip to main content
The EMBO Journal logoLink to The EMBO Journal
. 1989 Mar;8(3):851–861. doi: 10.1002/j.1460-2075.1989.tb03446.x

Function of the mammalian La protein: evidence for its action in transcription termination by RNA polymerase III.

E Gottlieb 1, J A Steitz 1
PMCID: PMC400884  PMID: 2470590

Abstract

We have tested the hypothesis that the mammalian La protein, which appears to be required for accurate and efficient RNA polymerase III transcription, is a transcription termination factor. Our data suggest that 3' foreshortened transcripts generated in La's absence are components of a novel transcription intermediate containing a paused polymerase. These transcripts are produced by fractionated transcription complexes, are synthesized with kinetics different from full-length transcripts, and are chasable to completion from the stalled transcription complexes. Together, these findings argue that termination by RNA polymerase III requires auxilliary factor(s) and implicate La as such a factor. Since La appears to facilitate transcript completion and release and also binds the resulting RNA product, it may be a regulator of RNA polymerase III transcription.

Full text

PDF
854

Images in this article

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Ackerman S., Bunick D., Zandomeni R., Weinmann R. RNA polymerase II ternary transcription complexes generated in vitro. Nucleic Acids Res. 1983 Sep 10;11(17):6041–6064. doi: 10.1093/nar/11.17.6041. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Allison D. S., Hall B. D. Effects of alterations in the 3' flanking sequence on in vivo and in vitro expression of the yeast SUP4-o tRNATyr gene. EMBO J. 1985 Oct;4(10):2657–2664. doi: 10.1002/j.1460-2075.1985.tb03984.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bieker J. J., Martin P. L., Roeder R. G. Formation of a rate-limiting intermediate in 5S RNA gene transcription. Cell. 1985 Jan;40(1):119–127. doi: 10.1016/0092-8674(85)90315-0. [DOI] [PubMed] [Google Scholar]
  4. Birkenmeier E. H., Brown D. D., Jordan E. A nuclear extract of Xenopus laevis oocytes that accurately transcribes 5S RNA genes. Cell. 1978 Nov;15(3):1077–1086. doi: 10.1016/0092-8674(78)90291-x. [DOI] [PubMed] [Google Scholar]
  5. Bogenhagen D. F., Brown D. D. Nucleotide sequences in Xenopus 5S DNA required for transcription termination. Cell. 1981 Apr;24(1):261–270. doi: 10.1016/0092-8674(81)90522-5. [DOI] [PubMed] [Google Scholar]
  6. Bogenhagen D. F., Sakonju S., Brown D. 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 Jan;19(1):27–35. doi: 10.1016/0092-8674(80)90385-2. [DOI] [PubMed] [Google Scholar]
  7. Bogenhagen D. F., Wormington W. M., Brown D. D. Stable transcription complexes of Xenopus 5S RNA genes: a means to maintain the differentiated state. Cell. 1982 Feb;28(2):413–421. doi: 10.1016/0092-8674(82)90359-2. [DOI] [PubMed] [Google Scholar]
  8. Brennan C. A., Dombroski A. J., Platt T. Transcription termination factor rho is an RNA-DNA helicase. Cell. 1987 Mar 27;48(6):945–952. doi: 10.1016/0092-8674(87)90703-3. [DOI] [PubMed] [Google Scholar]
  9. Camier S., Gabrielsen O., Baker R., Sentenac A. A split binding site for transcription factor tau on the tRNA3Glu gene. EMBO J. 1985 Feb;4(2):491–500. doi: 10.1002/j.1460-2075.1985.tb03655.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Carbon P., Murgo S., Ebel J. P., Krol A., Tebb G., Mattaj L. W. 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 Oct 9;51(1):71–79. doi: 10.1016/0092-8674(87)90011-0. [DOI] [PubMed] [Google Scholar]
  11. Carey M. F., Gerrard S. P., Cozzarelli N. R. Analysis of RNA polymerase III transcription complexes by gel filtration. J Biol Chem. 1986 Mar 25;261(9):4309–4317. [PubMed] [Google Scholar]
  12. Chen C. Y., Galluppi G. R., Richardson J. P. Transcription termination at lambda tR1 is mediated by interaction of rho with specific single-stranded domains near the 3' end of cro mRNA. Cell. 1986 Sep 26;46(7):1023–1028. doi: 10.1016/0092-8674(86)90701-4. [DOI] [PubMed] [Google Scholar]
  13. Ciliberto G., Dathan N., Frank R., Philipson L., Mattaj I. W. Formation of the 3' end on U snRNAs requires at least three sequence elements. EMBO J. 1986 Nov;5(11):2931–2937. doi: 10.1002/j.1460-2075.1986.tb04589.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Cozzarelli N. R., Gerrard S. P., Schlissel M., Brown D. D., Bogenhagen D. F. Purified RNA polymerase III accurately and efficiently terminates transcription of 5S RNA genes. Cell. 1983 Oct;34(3):829–835. doi: 10.1016/0092-8674(83)90540-8. [DOI] [PubMed] [Google Scholar]
  15. Das G., Henning D., Wright D., Reddy R. Upstream regulatory elements are necessary and sufficient for transcription of a U6 RNA gene by RNA polymerase III. EMBO J. 1988 Feb;7(2):503–512. doi: 10.1002/j.1460-2075.1988.tb02838.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. DeFranco D., Burke K. B., Hayashi S., Tener G. M., Miller R. C., Jr, Söll D. Genes for tRNALys5 from Drosophila melanogaster. Nucleic Acids Res. 1982 Oct 11;10(19):5799–5808. doi: 10.1093/nar/10.19.5799. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Engelke D. R., Ng S. Y., Shastry B. S., Roeder R. G. Specific interaction of a purified transcription factor with an internal control region of 5S RNA genes. Cell. 1980 Mar;19(3):717–728. doi: 10.1016/s0092-8674(80)80048-1. [DOI] [PubMed] [Google Scholar]
  18. Francoeur A. M., Chan E. K., Garrels J. I., Mathews M. B. Characterization and purification of lupus antigen La, and RNA-binding protein. Mol Cell Biol. 1985 Mar;5(3):586–590. doi: 10.1128/mcb.5.3.586. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Francoeur A. M., Mathews M. B. Interaction between VA RNA and the lupus antigen La: formation of a ribonucleoprotein particle in vitro. Proc Natl Acad Sci U S A. 1982 Nov;79(22):6772–6776. doi: 10.1073/pnas.79.22.6772. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Fuhrman S. A., Engelke D. R., Geiduschek E. P. HeLa cell RNA polymerase III transcription factors. Functional characterization of a fraction identified by its activity in a second template rescue assay. J Biol Chem. 1984 Feb 10;259(3):1934–1943. [PubMed] [Google Scholar]
  21. Geiduschek E. P., Tocchini-Valentini G. P. Transcription by RNA polymerase III. Annu Rev Biochem. 1988;57:873–914. doi: 10.1146/annurev.bi.57.070188.004301. [DOI] [PubMed] [Google Scholar]
  22. Ginsberg A. M., King B. O., Roeder R. G. Xenopus 5S gene transcription factor, TFIIIA: characterization of a cDNA clone and measurement of RNA levels throughout development. Cell. 1984 Dec;39(3 Pt 2):479–489. doi: 10.1016/0092-8674(84)90455-0. [DOI] [PubMed] [Google Scholar]
  23. Glickman J. N., Howe J. G., Steitz J. A. Structural analyses of EBER1 and EBER2 ribonucleoprotein particles present in Epstein-Barr virus-infected cells. J Virol. 1988 Mar;62(3):902–911. doi: 10.1128/jvi.62.3.902-911.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Gottlieb E., Steitz J. A. The RNA binding protein La influences both the accuracy and the efficiency of RNA polymerase III transcription in vitro. EMBO J. 1989 Mar;8(3):841–850. doi: 10.1002/j.1460-2075.1989.tb03445.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Grayhack E. J., Yang X. J., Lau L. F., Roberts J. W. Phage lambda gene Q antiterminator recognizes RNA polymerase near the promoter and accelerates it through a pause site. Cell. 1985 Aug;42(1):259–269. doi: 10.1016/s0092-8674(85)80121-5. [DOI] [PubMed] [Google Scholar]
  26. Grummt I., Kuhn A., Bartsch I., Rosenbauer H. A transcription terminator located upstream of the mouse rDNA initiation site affects rRNA synthesis. Cell. 1986 Dec 26;47(6):901–911. doi: 10.1016/0092-8674(86)90805-6. [DOI] [PubMed] [Google Scholar]
  27. Habets W. J., den Brok J. H., Boerbooms A. M., van de Putte L. B., van Venrooij W. J. Characterization of the SS-B (La) antigen in adenovirus-infected and uninfected HeLa cells. EMBO J. 1983;2(10):1625–1631. doi: 10.1002/j.1460-2075.1983.tb01636.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Henderson S., Sollner-Webb B. A transcriptional terminator is a novel element of the promoter of the mouse ribosomal RNA gene. Cell. 1986 Dec 26;47(6):891–900. doi: 10.1016/0092-8674(86)90804-4. [DOI] [PubMed] [Google Scholar]
  29. Hendrick J. P., Wolin S. L., Rinke J., Lerner M. R., Steitz J. A. Ro small cytoplasmic ribonucleoproteins are a subclass of La ribonucleoproteins: further characterization of the Ro and La small ribonucleoproteins from uninfected mammalian cells. Mol Cell Biol. 1981 Dec;1(12):1138–1149. doi: 10.1128/mcb.1.12.1138. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Hernandez N., Weiner A. M. Formation of the 3' end of U1 snRNA requires compatible snRNA promoter elements. Cell. 1986 Oct 24;47(2):249–258. doi: 10.1016/0092-8674(86)90447-2. [DOI] [PubMed] [Google Scholar]
  31. Hoch S. O., Billings P. B. Characterization of the La (SS-B) antigen from several mammalian sources. J Immunol. 1984 Sep;133(3):1397–1403. [PubMed] [Google Scholar]
  32. Honda B. M., Roeder R. G. Association of a 5S gene transcription factor with 5S RNA and altered levels of the factor during cell differentiation. Cell. 1980 Nov;22(1 Pt 1):119–126. doi: 10.1016/0092-8674(80)90160-9. [DOI] [PubMed] [Google Scholar]
  33. Jahn D., Wingender E., Seifart K. H. Transcription complexes for various class III genes differ in parameters of formation and stability towards salt. J Mol Biol. 1987 Jan 20;193(2):303–313. doi: 10.1016/0022-2836(87)90221-x. [DOI] [PubMed] [Google Scholar]
  34. Jat P., Arrand J. R. In vitro transcription of two Epstein-Barr virus specified small RNA molecules. Nucleic Acids Res. 1982 Jun 11;10(11):3407–3425. doi: 10.1093/nar/10.11.3407. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Kassavetis G. A., Zentner P. G., Geiduschek E. P. Transcription at bacteriophage T4 variant late promoters. An application of a newly devised promoter-mapping method involving RNA chain retraction. J Biol Chem. 1986 Oct 25;261(30):14256–14265. [PubMed] [Google Scholar]
  36. Klekamp M. S., Weil P. A. Partial purification and characterization of the Saccharomyces cerevisiae transcription factor TFIIIB. J Biol Chem. 1986 Feb 25;261(6):2819–2827. [PubMed] [Google Scholar]
  37. Klemenz R., Stillman D. J., Geiduschek E. P. Specific interactions of Saccharomyces cerevisiae proteins with a promoter region of eukaryotic tRNA genes. Proc Natl Acad Sci U S A. 1982 Oct;79(20):6191–6195. doi: 10.1073/pnas.79.20.6191. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Koo H. S., Wu H. M., Crothers D. M. DNA bending at adenine . thymine tracts. Nature. 1986 Apr 10;320(6062):501–506. doi: 10.1038/320501a0. [DOI] [PubMed] [Google Scholar]
  39. Koski R. A., Allison D. S., Worthington M., Hall B. D. An in vitro RNA polymerase III system from S. cerevisiae: effects of deletions and point mutations upon SUP4 gene transcription. Nucleic Acids Res. 1982 Dec 20;10(24):8127–8143. doi: 10.1093/nar/10.24.8127. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Lassar A. B., Martin P. L., Roeder R. G. Transcription of class III genes: formation of preinitiation complexes. Science. 1983 Nov 18;222(4625):740–748. doi: 10.1126/science.6356356. [DOI] [PubMed] [Google Scholar]
  41. Maderious A., Chen-Kiang S. Pausing and premature termination of human RNA polymerase II during transcription of adenovirus in vivo and in vitro. Proc Natl Acad Sci U S A. 1984 Oct;81(19):5931–5935. doi: 10.1073/pnas.81.19.5931. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Martin F. H., Tinoco I., Jr DNA-RNA hybrid duplexes containing oligo(dA:rU) sequences are exceptionally unstable and may facilitate termination of transcription. Nucleic Acids Res. 1980 May 24;8(10):2295–2299. doi: 10.1093/nar/8.10.2295. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Mathews M. B., Francoeur A. M. La antigen recognizes and binds to the 3'-oligouridylate tail of a small RNA. Mol Cell Biol. 1984 Jun;4(6):1134–1140. doi: 10.1128/mcb.4.6.1134. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Matter L., Schopfer K., Wilhelm J. A., Nyffenegger T., Parisot R. F., De Robertis E. M. Molecular characterization of ribonucleoprotein antigens bound by antinuclear antibodies. A diagnostic evaluation. Arthritis Rheum. 1982 Nov;25(11):1278–1283. doi: 10.1002/art.1780251102. [DOI] [PubMed] [Google Scholar]
  45. McStay B., Reeder R. H. A termination site for Xenopus RNA polymerase I also acts as an element of an adjacent promoter. Cell. 1986 Dec 26;47(6):913–920. doi: 10.1016/0092-8674(86)90806-8. [DOI] [PubMed] [Google Scholar]
  46. Mimori T., Hinterberger M., Pettersson I., Steitz J. A. Autoantibodies to the U2 small nuclear ribonucleoprotein in a patient with scleroderma-polymyositis overlap syndrome. J Biol Chem. 1984 Jan 10;259(1):560–565. [PubMed] [Google Scholar]
  47. Murphy S., Di Liegro C., Melli M. The in vitro transcription of the 7SK RNA gene by RNA polymerase III is dependent only on the presence of an upstream promoter. Cell. 1987 Oct 9;51(1):81–87. doi: 10.1016/0092-8674(87)90012-2. [DOI] [PubMed] [Google Scholar]
  48. Pelham H. R., Brown D. D. A specific transcription factor that can bind either the 5S RNA gene or 5S RNA. Proc Natl Acad Sci U S A. 1980 Jul;77(7):4170–4174. doi: 10.1073/pnas.77.7.4170. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Pizer L. I., Deng J. S., Stenberg R. M., Tan E. M. Characterization of a phosphoprotein associated with the SS-B/La nuclear antigen in adenovirus-infected and uninfected KB cells. Mol Cell Biol. 1983 Jul;3(7):1235–1245. doi: 10.1128/mcb.3.7.1235. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Platt T. Transcription termination and the regulation of gene expression. Annu Rev Biochem. 1986;55:339–372. doi: 10.1146/annurev.bi.55.070186.002011. [DOI] [PubMed] [Google Scholar]
  51. Rinke J., Steitz J. A. Precursor molecules of both human 5S ribosomal RNA and transfer RNAs are bound by a cellular protein reactive with anti-La lupus antibodies. Cell. 1982 May;29(1):149–159. doi: 10.1016/0092-8674(82)90099-x. [DOI] [PubMed] [Google Scholar]
  52. Rosa M. D., Gottlieb E., Lerner M. R., Steitz J. A. Striking similarities are exhibited by two small Epstein-Barr virus-encoded ribonucleic acids and the adenovirus-associated ribonucleic acids VAI and VAII. Mol Cell Biol. 1981 Sep;1(9):785–796. doi: 10.1128/mcb.1.9.785. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Ruet A., Camier S., Smagowicz W., Sentenac A., Fromageot P. Isolation of a class C transcription factor which forms a stable complex with tRNA genes. EMBO J. 1984 Feb;3(2):343–350. doi: 10.1002/j.1460-2075.1984.tb01809.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Sakonju S., Bogenhagen D. F., Brown D. D. A control region in the center of the 5S RNA gene directs specific initiation of transcription: I. The 5' border of the region. Cell. 1980 Jan;19(1):13–25. doi: 10.1016/0092-8674(80)90384-0. [DOI] [PubMed] [Google Scholar]
  55. Sakonju S., Brown D. D., Engelke D., Ng S. Y., Shastry B. S., Roeder R. G. The binding of a transcription factor to deletion mutants of a 5S ribosomal RNA gene. Cell. 1981 Mar;23(3):665–669. doi: 10.1016/0092-8674(81)90429-3. [DOI] [PubMed] [Google Scholar]
  56. Schaack J., Sharp S., Dingermann T., Söll D. Transcription of eukaryotic tRNA genes in vitro. II. Formation of stable complexes. J Biol Chem. 1983 Feb 25;258(4):2447–2453. [PubMed] [Google Scholar]
  57. Segall J., Matsui T., Roeder R. G. Multiple factors are required for the accurate transcription of purified genes by RNA polymerase III. J Biol Chem. 1980 Dec 25;255(24):11986–11991. [PubMed] [Google Scholar]
  58. Setzer D. R., Brown D. D. Formation and stability of the 5 S RNA transcription complex. J Biol Chem. 1985 Feb 25;260(4):2483–2492. [PubMed] [Google Scholar]
  59. Sharp S., Dingermann T., Schaack J., DeFranco D., Söll D. Transcription of eukaryotic tRNA genes in vitro. I. Analysis of control regions using a competition assay. J Biol Chem. 1983 Feb 25;258(4):2440–2446. [PubMed] [Google Scholar]
  60. Shastry B. S., Ng S. Y., Roeder R. G. Multiple factors involved in the transcription of class III genes in Xenopus laevis. J Biol Chem. 1982 Nov 10;257(21):12979–12986. [PubMed] [Google Scholar]
  61. Smith P. R., Williams D. G., Venables P. J., Maini R. N. Monoclonal antibodies to the Sjögren's syndrome associated antigen SS-B (La). J Immunol Methods. 1985 Feb 28;77(1):63–76. doi: 10.1016/0022-1759(85)90184-x. [DOI] [PubMed] [Google Scholar]
  62. Stefano J. E. Purified lupus antigen La recognizes an oligouridylate stretch common to the 3' termini of RNA polymerase III transcripts. Cell. 1984 Jan;36(1):145–154. doi: 10.1016/0092-8674(84)90083-7. [DOI] [PubMed] [Google Scholar]
  63. Steitz J. A., Wolin S. L., Rinke J., Pettersson I., Mount S. M., Lerner E. A., Hinterberger M., Gottlieb E. Small ribonucleoproteins from eukaryotes: structures and roles in RNA biogenesis. Cold Spring Harb Symp Quant Biol. 1983;47(Pt 2):893–900. doi: 10.1101/sqb.1983.047.01.103. [DOI] [PubMed] [Google Scholar]
  64. Stillman D. J., Better M., Geiduschek E. P. Electron-microscopic examination of the binding of a large RNA polymerase III transcription factor to a tRNA gene. J Mol Biol. 1985 Sep 20;185(2):451–455. doi: 10.1016/0022-2836(85)90417-6. [DOI] [PubMed] [Google Scholar]
  65. Stillman D. J., Geiduschek E. P. Differential binding of a S. cerevisiae RNA polymerase III transcription factor to two promoter segments of a tRNA gene. EMBO J. 1984 Apr;3(4):847–853. doi: 10.1002/j.1460-2075.1984.tb01895.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Stillman D. J., Sivertsen A. L., Zentner P. G., Geiduschek E. P. Correlations between transcription of a yeast tRNA gene and transcription factor-DNA interactions. J Biol Chem. 1984 Jun 25;259(12):7955–7962. [PubMed] [Google Scholar]
  67. Straney D. C., Crothers D. M. Intermediates in transcription initiation from the E. coli lac UV5 promoter. Cell. 1985 Dec;43(2 Pt 1):449–459. doi: 10.1016/0092-8674(85)90175-8. [DOI] [PubMed] [Google Scholar]
  68. Thoen C. O., Mills K., Hopkins M. P. Enzyme-linked protein A: an enzyme-linked immunosorbent assay reagent for detecting antibodies in tuberculous exotic animals. Am J Vet Res. 1980 May;41(5):833–835. [PubMed] [Google Scholar]
  69. Tora L., Financsek I., Hidvégi E. J. Characterization of the L1NH repeat family of Novikoff hepatoma. J Mol Biol. 1987 Sep 5;197(1):1–9. doi: 10.1016/0022-2836(87)90604-8. [DOI] [PubMed] [Google Scholar]
  70. Towbin H., Staehelin T., Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4350–4354. doi: 10.1073/pnas.76.9.4350. [DOI] [PMC free article] [PubMed] [Google Scholar]
  71. Van Dyke M. W., Roeder R. G. Multiple proteins bind to VA RNA genes of adenovirus type 2. Mol Cell Biol. 1987 Mar;7(3):1021–1031. doi: 10.1128/mcb.7.3.1021. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. Watson J. B., Chandler D. W., Gralla J. D. Specific termination of in vitro transcription by calf thymus RNA polymerase III. Nucleic Acids Res. 1984 Jul 11;12(13):5369–5384. doi: 10.1093/nar/12.13.5369. [DOI] [PMC free article] [PubMed] [Google Scholar]
  73. Weil P. A., Segall J., Harris B., Ng S. Y., Roeder R. G. Faithful transcription of eukaryotic genes by RNA polymerase III in systems reconstituted with purified DNA templates. J Biol Chem. 1979 Jul 10;254(13):6163–6173. [PubMed] [Google Scholar]
  74. Wilson E. T., Larson D., Young L. S., Sprague K. U. A large region controls tRNA gene transcription. J Mol Biol. 1985 May 25;183(2):153–163. doi: 10.1016/0022-2836(85)90209-8. [DOI] [PubMed] [Google Scholar]
  75. Wingender E., Jahn D., Seifart K. H. Association of RNA polymerase III with transcription factors in the absence of DNA. J Biol Chem. 1986 Jan 25;261(3):1409–1413. [PubMed] [Google Scholar]
  76. Wingender E., Shi X. P., Houpert A., Seifart K. H. Isolation of a transcription complex for ribosomal 5S RNA. EMBO J. 1984 Aug;3(8):1761–1768. doi: 10.1002/j.1460-2075.1984.tb02043.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  77. Wu G. J., Railey J. F., Cannon R. E. Defining the functional domains in the control region of the adenovirus type 2 specific VARNA1 gene. J Mol Biol. 1987 Apr 5;194(3):423–442. doi: 10.1016/0022-2836(87)90672-3. [DOI] [PubMed] [Google Scholar]
  78. Yen T. S., Webster R. E. Bacteriophage f1 gene II and X proteins. Isolation and characterization of the products of two overlapping genes. J Biol Chem. 1981 Nov 10;256(21):11259–11265. [PubMed] [Google Scholar]
  79. Yoshinaga S. K., Boulanger P. A., Berk A. J. Resolution of human transcription factor TFIIIC into two functional components. Proc Natl Acad Sci U S A. 1987 Jun;84(11):3585–3589. doi: 10.1073/pnas.84.11.3585. [DOI] [PMC free article] [PubMed] [Google Scholar]
  80. de Vegvar H. E., Lund E., Dahlberg J. E. 3' end formation of U1 snRNA precursors is coupled to transcription from snRNA promoters. Cell. 1986 Oct 24;47(2):259–266. doi: 10.1016/0092-8674(86)90448-4. [DOI] [PubMed] [Google Scholar]
  81. von Hippel P. H., Bear D. G., Morgan W. D., McSwiggen J. A. Protein-nucleic acid interactions in transcription: a molecular analysis. Annu Rev Biochem. 1984;53:389–446. doi: 10.1146/annurev.bi.53.070184.002133. [DOI] [PubMed] [Google Scholar]

Articles from The EMBO Journal are provided here courtesy of Nature Publishing Group

RESOURCES