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PMID: 1588962 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

The promoter for the procyclic acidic repetitive protein (PARP) genes of Trypanosoma brucei shares features with RNA polymerase I promoters.

Molecular and cellular biology ·Vol. 12 ·No. 6 ·1992-06-00 ·Pages 2644-52

Brown SD, Huang J, Van der Ploeg LH

Abstract

All eukaryotic protein-coding genes are believed to be transcribed by RNA polymerase (Pol) II. An exception may exist in the protozoan parasite Trypanosoma brucei, in which the genes encoding the variant surface glycoprotein (VSG) and procyclic acidic repetitive protein (PARP) are transcribed by an RNA polymerase that is resistant to the Pol II inhibitor alpha-amanitin. The PARP and VSG genes were proposed to be transcribed by Pol I (C. Shea, M. G.-S. Lee, and L. H. T. Van der Ploeg, Cell 50:603-612, 1987; G. Rudenko, M. G.-S. Lee, and L. H. T. Van der Ploeg, Nucleic Acids Res. 20:303-306, 1992), a suggestion that has been substantiated by the finding that trypanosomes can transcribe protein-coding genes by Pol I (G. Rudenko, H.-M. Chung, V. P. Pham, and L. H. T. Van der Ploeg, EMBO J. 10:3387-3397, 1991). We analyzed the sequence elements of the PARP promoter by linker scanning mutagenesis and compared the PARP promoter with Pol I, Pol II, and Pol III promoters. The PARP promoter appeared to be of limited complexity and contained at least two critical regions. The first was located adjacent to the transcription initiation site (nucleotides [nt] -69 to +12) and contained three discrete domains in which linker scanning mutants affected the transcriptional efficiency: at nt -69 to -56, -37 to -11, and -11 to +12. The second region was located between nt -140 and -131, and a third region may be located between nt -228 and -205. The nucleotide sequences of these elements, and their relative positioning with respect to the transcription initiation site did not resemble those of either Pol II or Pol III promoter elements, but rather reflected the organization of Pol I promoters in (i) similarity in the positioning of essential domains in the PARP promoter and Pol I promoter, (ii) strong sequence homology between the PARP core promoter element (nt -37 to -11) and identically positioned nucleotide sequences in the trypanosome rRNA and VSG gene promoters, and (iii) moderate effects on promoter activity of mutations around the transcription initiation site.

Related Genes
MeSH Terms
Base Sequence DNA Mutational Analysis Gene Expression Regulation Membrane Glycoproteins Molecular Sequence Data Promoter Regions, Genetic Protozoan Proteins/genetics RNA Polymerase I/metabolism Restriction Mapping Transcription, Genetic Variant Surface Glycoproteins, Trypanosoma/genetics
Chemicals
Membrane Glycoproteins Protozoan Proteins Variant Surface Glycoproteins, Trypanosoma procyclic acidic repetitive protein, Trypanosoma RNA Polymerase I
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Brown S D
Department of Pharmacology, Columbia University, New York, New York 10032.
Huang J
Van der Ploeg L H
References (56)
56 references, click to expand
  1. Requirement of a polypyrimidine tract for trans-splicing in trypanosomes: discriminating the PARP promoter from the immediately adjacent 3' splice acceptor site.
    EMBO J. 1991 Dec;10(12):3877-85 PMID: 1935907
  2. Transcription by RNA polymerase III.
    Annu Rev Biochem. 1988;57:873-914 PMID: 3052292
  3. Anatomy of the parp gene promoter of Trypanosoma brucei.
    EMBO J. 1991 Nov;10(11):3379-86 PMID: 1840521
  4. Homologous recombination and stable transfection in the parasitic protozoan Trypanosoma brucei.
    Science. 1990 Dec 14;250(4987):1583-7 PMID: 2177225
  5. Inhibition of protein synthesis results in super-induction of procyclin (PARP) RNA levels.
    Mol Biochem Parasitol. 1991 Jan;44(1):133-9 PMID: 2011148
  6. The PARP and VSG genes of Trypanosoma brucei do not resemble RNA polymerase II transcription units in sensitivity to Sarkosyl in nuclear run-on assays.
    Nucleic Acids Res. 1992 Jan 25;20(2):303-6 PMID: 1371345
  7. Characterization of VSG gene expression site promoters and promoter-associated DNA rearrangement events.
    Mol Cell Biol. 1991 May;11(5):2467-80 PMID: 1708090
  8. Trypanosoma brucei: constitutive activity of the VSG and procyclin gene promoters.
    EMBO J. 1990 Oct;9(10):3145-51 PMID: 1698609
  9. Alpha-amanitin-resistant transcription units in trypanosomes: a comparison of promoter sequences for a VSG gene expression site and for the ribosomal RNA genes.
    Nucleic Acids Res. 1991 Oct 11;19(19):5153-8 PMID: 1923801
  10. News from the nucleolus: rRNA gene expression.
    Trends Biochem Sci. 1991 Feb;16(2):58-62 PMID: 1858134
  11. Trans splicing in trypanosomes--archaism or adaptation?
    Trends Genet. 1989 Jul;5(7):204-8 PMID: 2675423
  12. Procyclin gene expression and loss of the variant surface glycoprotein during differentiation of Trypanosoma brucei.
    J Cell Biol. 1989 Feb;108(2):737-46 PMID: 2645304
  13. Trypanosoma brucei: posttranscriptional control of the variable surface glycoprotein gene expression site.
    Mol Cell Biol. 1989 Sep;9(9):4018-21 PMID: 2779574
  14. In trypanosomes the homolog of the largest subunit of RNA polymerase II is encoded by two genes and has a highly unusual C-terminal domain structure.
    Cell. 1989 Mar 10;56(5):815-27 PMID: 2924350
  15. Trypanosoma brucei contains two RNA polymerase II largest subunit genes with an altered C-terminal domain.
    Cell. 1989 Feb 24;56(4):585-97 PMID: 2917367
  16. Alpha-amanitin-insensitive transcription of variant surface glycoprotein genes provides further evidence for discontinuous transcription in trypanosomes.
    Nucleic Acids Res. 1984 Dec 21;12(24):9457-72 PMID: 6514580
  17. Developmental regulation of a novel repetitive protein of Trypanosoma brucei.
    Mol Cell Biol. 1987 Aug;7(8):2838-44 PMID: 3670296
  18. Expression of a polypeptide containing a dipeptide repeat is confined to the insect stage of Trypanosoma brucei.
    Nature. 1987 Jan 15-21;325(6101):272-4 PMID: 3808022
  19. Three small RNAs within the 10 kb trypanosome rRNA transcription unit are analogous to domain VII of other eukaryotic 28S rRNAs.
    Nucleic Acids Res. 1986 Dec 9;14(23):9471-89 PMID: 3797245
  20. A simple phase-extraction assay for chloramphenicol acyltransferase activity.
    Gene. 1988 Jul 30;67(2):271-7 PMID: 3169576
  21. Transcription of cloned eukaryotic ribosomal RNA genes.
    Annu Rev Biochem. 1986;55:801-30 PMID: 3527052
  22. Discontinuous transcription and antigenic variation in trypanosomes.
    Annu Rev Biochem. 1986;55:701-32 PMID: 2874767
  23. A complex control region of the mouse rRNA gene directs accurate initiation by RNA polymerase I.
    Mol Cell Biol. 1985 Mar;5(3):554-62 PMID: 3990683
  24. Polymorphism in the procyclic acidic repetitive protein gene family of Trypanosoma brucei.
    Mol Cell Biol. 1988 Oct;8(10):4055-62 PMID: 3185541
  25. Evidence for trans splicing in trypanosomes.
    Cell. 1986 Nov 21;47(4):527-35 PMID: 3022935
  26. Presence of a limited number of essential nucleotides in the promoter region of mouse ribosomal RNA gene.
    Nucleic Acids Res. 1985 May 24;13(10):3515-32 PMID: 2989774
  27. Inhibition of in vivo and in vitro transcription by monoclonal antibodies prepared against wheat germ RNA polymerase II that react with the heptapeptide repeat of eukaryotic RNA polymerase II.
    J Biol Chem. 1989 Jul 5;264(19):11511-20 PMID: 2472398
  28. Procyclin: an unusual immunodominant glycoprotein surface antigen from the procyclic stage of African trypanosomes.
    Mol Biochem Parasitol. 1988 Dec;31(3):203-16 PMID: 2464763
  29. VSG gene 118 is transcribed from a cotransposed pol I-like promoter.
    Cell. 1987 Aug 14;50(4):603-12 PMID: 2440585
  30. Linker scanning of the yeast RNA polymerase I promoter.
    Nucleic Acids Res. 1989 Dec 11;17(23):9661-78 PMID: 2690005
  31. Two distant and precisely positioned domains promote transcription of Xenopus laevis rRNA genes: analysis with linker-scanning mutants.
    Mol Cell Biol. 1986 Dec;6(12):4585-93 PMID: 3796610
  32. Two distinct promoter elements in the human rRNA gene identified by linker scanning mutagenesis.
    Mol Cell Biol. 1986 Jan;6(1):227-35 PMID: 3785147
  33. Primer-independent abortive initiation by wheat-germ RNA polymerase B (II).
    Eur J Biochem. 1985 Jun 3;149(2):337-43 PMID: 3888625
  34. Half helical turn spacing changes convert a frog into a mouse rDNA promoter: a distant upstream domain determines the helix face of the initiation site.
    Genes Dev. 1990 Jan;4(1):52-62 PMID: 2155160
  35. The promoter for a variant surface glycoprotein gene expression site in Trypanosoma brucei.
    EMBO J. 1990 Sep;9(9):2791-801 PMID: 1697265
  36. Procyclic acidic repetitive protein (PARP) genes located in an unusually small alpha-amanitin-resistant transcription unit: PARP promoter activity assayed by transient DNA transfection of Trypanosoma brucei.
    Mol Cell Biol. 1990 Jul;10(7):3492-504 PMID: 1694012
  37. Trans splicing of nuclear pre-mRNAs.
    Cell. 1990 Jun 29;61(7):1157-60 PMID: 2142018
  38. RNA polymerase B (II) and general transcription factors.
    Annu Rev Biochem. 1990;59:711-54 PMID: 2197989
  39. Transcription of the procyclic acidic repetitive protein genes of Trypanosoma brucei.
    Mol Cell Biol. 1990 Jun;10(6):3036-47 PMID: 2342468
  40. Excision of an intact intron as a novel lariat structure during pre-mRNA splicing in vitro.
    Cell. 1984 Aug;38(1):317-31 PMID: 6088074
  41. Ribosomal RNA transcription in vitro is species specific.
    Nature. 1982 Mar 11;296(5853):173-4 PMID: 7063022
  42. RNA splicing is required to make the messenger RNA for a variant surface antigen in trypanosomes.
    Nucleic Acids Res. 1982 Jun 25;10(12):3591-604 PMID: 6287414
  43. Transcriptional control signals of a eukaryotic protein-coding gene.
    Science. 1982 Jul 23;217(4557):316-24 PMID: 6283634
  44. Transcripts coding for variant surface glycoproteins of Trypanosoma brucei have a short, identical exon at their 5' end.
    Gene. 1982 Dec;20(2):281-9 PMID: 7166234
  45. Cultivation and in vitro cloning or procyclic culture forms of Trypanosoma brucei in a semi-defined medium. Short communication.
    Acta Trop. 1979 Sep;36(3):289-92 PMID: 43092
  46. Sizing and mapping of early adenovirus mRNAs by gel electrophoresis of S1 endonuclease-digested hybrids.
    Cell. 1977 Nov;12(3):721-32 PMID: 922889
  47. Control of antigenic variation in African trypanosomes.
    New Biol. 1991 Apr;3(4):324-30 PMID: 2065016
  48. Structure of the core promoter of human and mouse ribosomal RNA gene. Asymmetry of species-specific transcription.
    J Mol Biol. 1991 Mar 5;218(1):55-67 PMID: 2002507
  49. Participation of the TATA factor in transcription of the yeast U6 gene by RNA polymerase C.
    Science. 1991 Jan 25;251(4992):424-6 PMID: 1989075
  50. rRNA synthesis in the nucleolus.
    Trends Genet. 1990 Dec;6(12):390-5 PMID: 2087780
  51. Analysis of clustered point mutations in the human ribosomal RNA gene promoter by transient expression in vivo.
    Proc Natl Acad Sci U S A. 1988 Feb;85(3):669-73 PMID: 3422449
  52. Minimal exon sequence requirements for efficient in vitro splicing of mono-intronic nuclear pre-mRNA.
    J Biol Chem. 1987 Aug 15;262(23):11284-91 PMID: 3649340
  53. An RNA processing activity that debranches RNA lariats.
    Science. 1985 Jul 12;229(4709):135-40 PMID: 2990042
  54. Characterization of the RNA polymerases of Trypanosoma brucei: trypanosomal mRNAs are composed of transcripts derived from both RNA polymerase II and III.
    EMBO J. 1989 Nov;8(11):3383-9 PMID: 2583103
  55. Alpha-amanitin resistant transcription of protein coding genes in insect and bloodstream form Trypanosoma brucei.
    EMBO J. 1989 Dec 20;8(13):4259-63 PMID: 2591373
  56. RNA polymerase I can mediate expression of CAT and neo protein-coding genes in Trypanosoma brucei.
    EMBO J. 1991 Nov;10(11):3387-97 PMID: 1915299
Article Info
Journal
Molecular and cellular biology
Abbr.
Mol Cell Biol
ISSN
0270-7306
Published
1992-06-00
Pages
2644-52
Language
English
Region
United States
NLM ID
8109087
PMCID
PMC364458
Subset
IM
Grants
NIAID NIH HHS · AI 21784 · United States
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