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. 1995 Jun;59(2):223–240. doi: 10.1128/mr.59.2.223-240.1995

Control of gene expression in trypanosomes.

L Vanhamme 1, E Pays 1
PMCID: PMC239361  PMID: 7603410

Abstract

Trypanosomes are protozoan agents of major parasitic diseases such as Chagas' disease in South America and sleeping sickness of humans and nagana disease of cattle in Africa. They are transmitted to mammalian hosts by specific insect vectors. Their life cycle consists of a succession of differentiation and growth phases requiring regulated gene expression to adapt to the changing extracellular environment. Typical of such stage-specific expression is that of the major surface antigens of Trypanosoma brucei, procyclin in the procyclic (insect) form and the variant surface glycoprotein (VSG) in the bloodstream (mammalian) form. In trypanosomes, the regulation of gene expression is effected mainly at posttranscriptional levels, since primary transcription of most of the genes occurs in long polycistronic units and is constitutive. The transcripts are processed by transsplicing and polyadenylation under the influence of intergenic polypyrimidine tracts. These events show some developmental regulation. Untranslated sequences of the mRNAs seem to play a prominent role in the stage-specific control of individual gene expression, through a modulation of mRNA abundance. The VSG and procyclin transcription units exhibit particular features that are probably related to the need for a high level of expression. The promoters and RNA polymerase driving the expression of these units resemble those of the ribosomal genes. Their mutually exclusive expression is ensured by controls operating at several levels, including RNA elongation. Antigenic variation in the bloodstream is achieved through DNA rearrangements or alternative activation of the telomeric VSG gene expression sites. Recent discoveries, such as the existence of a novel nucleotide in telomeric DNA and the generation of point mutations in VSG genes, have shed new light on the mechanisms and consequences of antigenic variation.

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Selected References

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  1. Abeliovich H., Tzfati Y., Shlomai J. A trypanosomal CCHC-type zinc finger protein which binds the conserved universal sequence of kinetoplast DNA minicircles: isolation and analysis of the complete cDNA from Crithidia fasciculata. Mol Cell Biol. 1993 Dec;13(12):7766–7773. doi: 10.1128/mcb.13.12.7766. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Affranchino J. L., González S. A., Pays E. Isolation of a mitotic-like cyclin homologue from the protozoan Trypanosoma brucei. Gene. 1993 Sep 30;132(1):75–82. doi: 10.1016/0378-1119(93)90516-6. [DOI] [PubMed] [Google Scholar]
  3. Agabian N. Trans splicing of nuclear pre-mRNAs. Cell. 1990 Jun 29;61(7):1157–1160. doi: 10.1016/0092-8674(90)90674-4. [DOI] [PubMed] [Google Scholar]
  4. Agami R., Aly R., Halman S., Shapira M. Functional analysis of cis-acting DNA elements required for expression of the SL RNA gene in the parasitic protozoan Leishmania amazonensis. Nucleic Acids Res. 1994 Jun 11;22(11):1959–1965. doi: 10.1093/nar/22.11.1959. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Agur Z., Abiri D., Van der Ploeg L. H. Ordered appearance of antigenic variants of African trypanosomes explained in a mathematical model based on a stochastic switch process and immune-selection against putative switch intermediates. Proc Natl Acad Sci U S A. 1989 Dec;86(23):9626–9630. doi: 10.1073/pnas.86.23.9626. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Alarcon C. M., Son H. J., Hall T., Donelson J. E. A monocistronic transcript for a trypanosome variant surface glycoprotein. Mol Cell Biol. 1994 Aug;14(8):5579–5591. doi: 10.1128/mcb.14.8.5579. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Alexandre S., Guyaux M., Murphy N. B., Coquelet H., Pays A., Steinert M., Pays E. Putative genes of a variant-specific antigen gene transcription unit in Trypanosoma brucei. Mol Cell Biol. 1988 Jun;8(6):2367–2378. doi: 10.1128/mcb.8.6.2367. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Alexandre S., Paindavoine P., Tebabi P., Pays A., Halleux S., Steinert M., Pays E. Differential expression of a family of putative adenylate/guanylate cyclase genes in Trypanosoma brucei. Mol Biochem Parasitol. 1990 Dec;43(2):279–288. doi: 10.1016/0166-6851(90)90152-c. [DOI] [PubMed] [Google Scholar]
  9. Aly R., Argaman M., Halman S., Shapira M. A regulatory role for the 5' and 3' untranslated regions in differential expression of hsp83 in Leishmania. Nucleic Acids Res. 1994 Aug 11;22(15):2922–2929. doi: 10.1093/nar/22.15.2922. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Argaman M., Aly R., Shapira M. Expression of heat shock protein 83 in Leishmania is regulated post-transcriptionally. Mol Biochem Parasitol. 1994 Mar;64(1):95–110. doi: 10.1016/0166-6851(94)90138-4. [DOI] [PubMed] [Google Scholar]
  11. Aslund L., Carlsson L., Henriksson J., Rydåker M., Toro G. C., Galanti N., Pettersson U. A gene family encoding heterogeneous histone H1 proteins in Trypanosoma cruzi. Mol Biochem Parasitol. 1994 Jun;65(2):317–330. doi: 10.1016/0166-6851(94)90082-5. [DOI] [PubMed] [Google Scholar]
  12. Baltz T., Giroud C., Bringaud F., Eisen H., Jacquemot C., Roth C. W. Exposed epitopes on a Trypanosoma equiperdum variant surface glycoprotein altered by point mutations. EMBO J. 1991 Jul;10(7):1653–1659. doi: 10.1002/j.1460-2075.1991.tb07688.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Barbet A. F., Kamper S. M. The importance of mosaic genes to trypanosome survival. Parasitol Today. 1993 Feb;9(2):63–66. doi: 10.1016/0169-4758(93)90039-i. [DOI] [PubMed] [Google Scholar]
  14. Barry J. D., Graham S. V., Matthews K. R., Shiels P. G., Shonekan O. A. Stage-specific mechanisms for activation and expression of variant surface glycoprotein genes in Trypanosoma brucei. Biochem Soc Trans. 1990 Oct;18(5):708–710. doi: 10.1042/bst0180708. [DOI] [PubMed] [Google Scholar]
  15. Bass K. E., Wang C. C. Transient inhibition of protein synthesis accompanies differentiation of Trypanosoma brucei from bloodstream to procyclic forms. Mol Biochem Parasitol. 1992 Nov;56(1):129–140. doi: 10.1016/0166-6851(92)90160-l. [DOI] [PubMed] [Google Scholar]
  16. Bayne R. A., Kilbride E. A., Lainson F. A., Tetley L., Barry J. D. A major surface antigen of procyclic stage Trypanosoma congolense. Mol Biochem Parasitol. 1993 Oct;61(2):295–310. doi: 10.1016/0166-6851(93)90075-9. [DOI] [PubMed] [Google Scholar]
  17. Ben Amar M. F., Pays A., Tebabi P., Dero B., Seebeck T., Steinert M., Pays E. Structure and transcription of the actin gene of Trypanosoma brucei. Mol Cell Biol. 1988 May;8(5):2166–2176. doi: 10.1128/mcb.8.5.2166. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Benne R. RNA editing in trypanosomes. Eur J Biochem. 1994 Apr 1;221(1):9–23. doi: 10.1111/j.1432-1033.1994.tb18710.x. [DOI] [PubMed] [Google Scholar]
  19. Berberof M., Pays A., Pays E. A similar gene is shared by both the variant surface glycoprotein and procyclin gene transcription units of Trypanosoma brucei. Mol Cell Biol. 1991 Mar;11(3):1473–1479. doi: 10.1128/mcb.11.3.1473. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Bernards A., van Harten-Loosbroek N., Borst P. Modification of telomeric DNA in Trypanosoma brucei; a role in antigenic variation? Nucleic Acids Res. 1984 May 25;12(10):4153–4170. doi: 10.1093/nar/12.10.4153. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Blum M. L., Down J. A., Gurnett A. M., Carrington M., Turner M. J., Wiley D. C. A structural motif in the variant surface glycoproteins of Trypanosoma brucei. Nature. 1993 Apr 15;362(6421):603–609. doi: 10.1038/362603a0. [DOI] [PubMed] [Google Scholar]
  22. Borst P., Gommers-Ampt J. H., Ligtenberg M. J., Rudenko G., Kieft R., Taylor M. C., Blundell P. A., van Leeuwen F. Control of antigenic variation in African trypanosomes. Cold Spring Harb Symp Quant Biol. 1993;58:105–114. doi: 10.1101/sqb.1993.058.01.014. [DOI] [PubMed] [Google Scholar]
  23. Bringaud F., Baltz T. Differential regulation of two distinct families of glucose transporter genes in Trypanosoma brucei. Mol Cell Biol. 1993 Feb;13(2):1146–1154. doi: 10.1128/mcb.13.2.1146. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Brown L., Hines J. C., Ray D. S. The Crithidia fasciculata CRK gene encodes a novel cdc2-related protein containing large inserts between highly conserved domains. Nucleic Acids Res. 1992 Oct 25;20(20):5451–5456. doi: 10.1093/nar/20.20.5451. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Brown S. D., Huang J., Van der Ploeg L. H. The promoter for the procyclic acidic repetitive protein (PARP) genes of Trypanosoma brucei shares features with RNA polymerase I promoters. Mol Cell Biol. 1992 Jun;12(6):2644–2652. doi: 10.1128/mcb.12.6.2644. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Brown S. D., Van der Ploeg L. H. Single-stranded DNA-protein binding in the procyclic acidic repetitive protein (PARP) promoter of Trypanosoma brucei. Mol Biochem Parasitol. 1994 May;65(1):109–122. doi: 10.1016/0166-6851(94)90120-1. [DOI] [PubMed] [Google Scholar]
  27. Bruzik J. P., Maniatis T. Spliced leader RNAs from lower eukaryotes are trans-spliced in mammalian cells. Nature. 1992 Dec 17;360(6405):692–695. doi: 10.1038/360692a0. [DOI] [PubMed] [Google Scholar]
  28. Bruzik J. P., Steitz J. A. Spliced leader RNA sequences can substitute for the essential 5' end of U1 RNA during splicing in a mammalian in vitro system. Cell. 1990 Sep 7;62(5):889–899. doi: 10.1016/0092-8674(90)90264-f. [DOI] [PubMed] [Google Scholar]
  29. Carrington M., Miller N., Blum M., Roditi I., Wiley D., Turner M. Variant specific glycoprotein of Trypanosoma brucei consists of two domains each having an independently conserved pattern of cysteine residues. J Mol Biol. 1991 Oct 5;221(3):823–835. doi: 10.1016/0022-2836(91)80178-w. [DOI] [PubMed] [Google Scholar]
  30. Chapman A. B., Agabian N. Trypanosoma brucei RNA polymerase II is phosphorylated in the absence of carboxyl-terminal domain heptapeptide repeats. J Biol Chem. 1994 Feb 18;269(7):4754–4760. [PubMed] [Google Scholar]
  31. Chung H. M., Lee M. G., Dietrich P., Huang J., Van der Ploeg L. H. Disruption of largest subunit RNA polymerase II genes in Trypanosoma brucei. Mol Cell Biol. 1993 Jun;13(6):3734–3743. doi: 10.1128/mcb.13.6.3734. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Chung H. M., Lee M. G., Van der Ploeg L. H. RNA polymerase I-mediated protein-coding gene expression in Trypanosoma brucei. Parasitol Today. 1992 Dec;8(12):414–418. doi: 10.1016/0169-4758(92)90194-7. [DOI] [PubMed] [Google Scholar]
  33. Clayton C. E., Fueri J. P., Itzhaki J. E., Bellofatto V., Sherman D. R., Wisdom G. S., Vijayasarathy S., Mowatt M. R. Transcription of the procyclic acidic repetitive protein genes of Trypanosoma brucei. Mol Cell Biol. 1990 Jun;10(6):3036–3047. doi: 10.1128/mcb.10.6.3036. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Clayton C. E. Structure and regulated expression of genes encoding fructose biphosphate aldolase in Trypanosoma brucei. EMBO J. 1985 Nov;4(11):2997–3003. doi: 10.1002/j.1460-2075.1985.tb04035.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Clayton C. Developmental regulation of nuclear gene expression in Trypanosoma brucei. Prog Nucleic Acid Res Mol Biol. 1992;43:37–66. doi: 10.1016/s0079-6603(08)61043-0. [DOI] [PubMed] [Google Scholar]
  36. Coquelet H., Steinert M., Pays E. Ultraviolet irradiation inhibits RNA decay and modifies ribosomal RNA processing in Trypanosoma brucei. Mol Biochem Parasitol. 1991 Jan;44(1):33–42. doi: 10.1016/0166-6851(91)90218-u. [DOI] [PubMed] [Google Scholar]
  37. Coquelet H., Tebabi P., Pays A., Steinert M., Pays E. Trypanosoma brucei: enrichment by UV of intergenic transcripts from the variable surface glycoprotein gene expression site. Mol Cell Biol. 1989 Sep;9(9):4022–4025. doi: 10.1128/mcb.9.9.4022. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Cornelissen A. W., Backes S., Evers R., Grondal E. J., Jess W., Köck J. Transcription analysis in Trypanosoma brucei. Biochem Soc Trans. 1990 Oct;18(5):710–714. doi: 10.1042/bst0180710. [DOI] [PubMed] [Google Scholar]
  39. Cross G. A. Cellular and genetic aspects of antigenic variation in trypanosomes. Annu Rev Immunol. 1990;8:83–110. doi: 10.1146/annurev.iy.08.040190.000503. [DOI] [PubMed] [Google Scholar]
  40. Crozatier M., Van der Ploeg L. H., Johnson P. J., Gommers-Ampt J., Borst P. Structure of a telomeric expression site for variant specific surface antigens in Trypanosoma brucei. Mol Biochem Parasitol. 1990 Aug;42(1):1–12. doi: 10.1016/0166-6851(90)90107-w. [DOI] [PubMed] [Google Scholar]
  41. Cully D. F., Ip H. S., Cross G. A. Coordinate transcription of variant surface glycoprotein genes and an expression site associated gene family in Trypanosoma brucei. Cell. 1985 Aug;42(1):173–182. doi: 10.1016/s0092-8674(85)80113-6. [DOI] [PubMed] [Google Scholar]
  42. Curotto de Lafaille M. A., Laban A., Wirth D. F. Gene expression in Leishmania: analysis of essential 5' DNA sequences. Proc Natl Acad Sci U S A. 1992 Apr 1;89(7):2703–2707. doi: 10.1073/pnas.89.7.2703. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Daï Do Thi C., Aerts D., Steinert M., Pays E. High homology between variant surface glycoprotein gene expression sites of Trypanosoma brucei and Trypanosoma gambiense. Mol Biochem Parasitol. 1991 Oct;48(2):199–210. doi: 10.1016/0166-6851(91)90115-m. [DOI] [PubMed] [Google Scholar]
  44. De Lange T., Borst P. Genomic environment of the expression-linked extra copies of genes for surface antigens of Trypanosoma brucei resembles the end of a chromosome. Nature. 1982 Sep 30;299(5882):451–453. doi: 10.1038/299451a0. [DOI] [PubMed] [Google Scholar]
  45. Dietrich P., Soares M. B., Affonso M. H., Floeter-Winter L. M. The Trypanosoma cruzi ribosomal RNA-encoding gene: analysis of promoter and upstream intergenic spacer sequences. Gene. 1993 Mar 15;125(1):103–107. doi: 10.1016/0378-1119(93)90753-p. [DOI] [PubMed] [Google Scholar]
  46. Dorn P. L., Aman R. A., Boothroyd J. C. Inhibition of protein synthesis results in super-induction of procyclin (PARP) RNA levels. Mol Biochem Parasitol. 1991 Jan;44(1):133–139. doi: 10.1016/0166-6851(91)90229-y. [DOI] [PubMed] [Google Scholar]
  47. Ehlers B., Czichos J., Overath P. RNA turnover in Trypanosoma brucei. Mol Cell Biol. 1987 Mar;7(3):1242–1249. doi: 10.1128/mcb.7.3.1242. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Eid J., Sollner-Webb B. Stable integrative transformation of Trypanosoma brucei that occurs exclusively by homologous recombination. Proc Natl Acad Sci U S A. 1991 Mar 15;88(6):2118–2121. doi: 10.1073/pnas.88.6.2118. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Erondu N. E., Donelson J. E. Differential expression of two mRNAs from a single gene encoding an HMG1-like DNA binding protein of African trypanosomes. Mol Biochem Parasitol. 1992 Mar;51(1):111–118. doi: 10.1016/0166-6851(92)90206-y. [DOI] [PubMed] [Google Scholar]
  50. Evers R., Cornelissen A. W. The Trypanosoma brucei protein phosphatase gene: polycistronic transcription with the RNA polymerase II largest subunit gene. Nucleic Acids Res. 1990 Sep 11;18(17):5089–5095. doi: 10.1093/nar/18.17.5089. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Evers R., Hammer A., Köck J., Jess W., Borst P., Mémet S., Cornelissen A. W. Trypanosoma brucei contains two RNA polymerase II largest subunit genes with an altered C-terminal domain. Cell. 1989 Feb 24;56(4):585–597. doi: 10.1016/0092-8674(89)90581-3. [DOI] [PubMed] [Google Scholar]
  52. Fantoni A., Dare A. O., Tschudi C. RNA polymerase III-mediated transcription of the trypanosome U2 small nuclear RNA gene is controlled by both intragenic and extragenic regulatory elements. Mol Cell Biol. 1994 Mar;14(3):2021–2028. doi: 10.1128/mcb.14.3.2021. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Fasel N. J., Robyr D. C., Mauel J., Glaser T. A. Identification of a histone H1-like gene expressed in Leishmania major. Mol Biochem Parasitol. 1993 Dec;62(2):321–323. doi: 10.1016/0166-6851(93)90123-f. [DOI] [PubMed] [Google Scholar]
  54. Florent I. C., Raibaud A., Eisen H. A family of genes related to a new expression site-associated gene in Trypanosoma equiperdum. Mol Cell Biol. 1991 Apr;11(4):2180–2188. doi: 10.1128/mcb.11.4.2180. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Frasch A. C., Borst P., Van den Burg J. Rapid evolution of genes coding for variant surface glycoproteins in trypanosomes. Gene. 1982 Feb;17(2):197–211. doi: 10.1016/0378-1119(82)90073-7. [DOI] [PubMed] [Google Scholar]
  56. Gale M., Jr, Carter V., Parsons M. Translational control mediates the developmental regulation of the Trypanosoma brucei Nrk protein kinase. J Biol Chem. 1994 Dec 16;269(50):31659–31665. [PubMed] [Google Scholar]
  57. García-Salcedo J. A., Oliver J. L., Stock R. P., González A. Molecular characterization and transcription of the histone H2B gene from the protozoan parasite Trypanosoma cruzi. Mol Microbiol. 1994 Sep;13(6):1033–1043. doi: 10.1111/j.1365-2958.1994.tb00494.x. [DOI] [PubMed] [Google Scholar]
  58. Genske J. E., Cairns B. R., Stack S. P., Landfear S. M. Structure and regulation of histone H2B mRNAs from Leishmania enriettii. Mol Cell Biol. 1991 Jan;11(1):240–249. doi: 10.1128/mcb.11.1.240. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Gibbs C. P., Cross G. A. Cloning and transcriptional analysis of a variant surface glycoprotein gene expression site in Trypanosoma brucei. Mol Biochem Parasitol. 1988 Apr;28(3):197–206. doi: 10.1016/0166-6851(88)90004-7. [DOI] [PubMed] [Google Scholar]
  60. Gibson W. C., Swinkels B. W., Borst P. Post-transcriptional control of the differential expression of phosphoglycerate kinase genes in Trypanosoma brucei. J Mol Biol. 1988 May 20;201(2):315–325. doi: 10.1016/0022-2836(88)90140-4. [DOI] [PubMed] [Google Scholar]
  61. Glass D. J., Polvere R. I., Van der Ploeg L. H. Conserved sequences and transcription of the hsp70 gene family in Trypanosoma brucei. Mol Cell Biol. 1986 Dec;6(12):4657–4666. doi: 10.1128/mcb.6.12.4657. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Gommers-Ampt J. H., Teixeira A. J., van de Werken G., van Dijk W. J., Borst P. The identification of hydroxymethyluracil in DNA of Trypanosoma brucei. Nucleic Acids Res. 1993 May 11;21(9):2039–2043. doi: 10.1093/nar/21.9.2039. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Gommers-Ampt J. H., Van Leeuwen F., de Beer A. L., Vliegenthart J. F., Dizdaroglu M., Kowalak J. A., Crain P. F., Borst P. beta-D-glucosyl-hydroxymethyluracil: a novel modified base present in the DNA of the parasitic protozoan T. brucei. Cell. 1993 Dec 17;75(6):1129–1136. doi: 10.1016/0092-8674(93)90322-h. [DOI] [PubMed] [Google Scholar]
  64. Gommers-Ampt J., Lutgerink J., Borst P. A novel DNA nucleotide in Trypanosoma brucei only present in the mammalian phase of the life-cycle. Nucleic Acids Res. 1991 Apr 25;19(8):1745–1751. doi: 10.1093/nar/19.8.1745. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Gottesdiener K. M. A new VSG expression site-associated gene (ESAG) in the promoter region of Trypanosoma brucei encodes a protein with 10 potential transmembrane domains. Mol Biochem Parasitol. 1994 Jan;63(1):143–151. doi: 10.1016/0166-6851(94)90017-5. [DOI] [PubMed] [Google Scholar]
  66. Gottesdiener K. M., Goriparthi L., Masucci J. P., Van der Ploeg L. H. A proposed mechanism for promoter-associated DNA rearrangement events at a variant surface glycoprotein gene expression site. Mol Cell Biol. 1992 Oct;12(10):4784–4795. doi: 10.1128/mcb.12.10.4784. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Gottesdiener K., Chung H. M., Brown S. D., Lee M. G., Van der Ploeg L. H. Characterization of VSG gene expression site promoters and promoter-associated DNA rearrangement events. Mol Cell Biol. 1991 May;11(5):2467–2480. doi: 10.1128/mcb.11.5.2467. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. Graham S. V., Barry J. D. Expression site-associated genes transcribed independently of variant surface glycoprotein genes in Trypanosoma brucei. Mol Biochem Parasitol. 1991 Jul;47(1):31–41. doi: 10.1016/0166-6851(91)90145-v. [DOI] [PubMed] [Google Scholar]
  69. Graham S. V., Matthews K. R., Barry J. D. Trypanosoma brucei: unusual expression-site-associated gene homologies in a metacyclic VSG gene expression site. Exp Parasitol. 1993 Feb;76(1):96–99. doi: 10.1006/expr.1993.1011. [DOI] [PubMed] [Google Scholar]
  70. Graham S. V., Matthews K. R., Shiels P. G., Barry J. D. Distinct, developmental stage-specific activation mechanisms of trypanosome VSG genes. Parasitology. 1990 Dec;101(Pt 3):361–367. doi: 10.1017/s0031182000060558. [DOI] [PubMed] [Google Scholar]
  71. Grondal E. J., Evers R., Kosubek K., Cornelissen A. W. 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):3383–3389. doi: 10.1002/j.1460-2075.1989.tb08502.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. Hasan G., Turner M. J., Cordingley J. S. Ribosomal RNA genes of Trypanosoma brucei: mapping the regions specifying the six small ribosomal RNAs. Gene. 1984 Jan;27(1):75–86. doi: 10.1016/0378-1119(84)90240-3. [DOI] [PubMed] [Google Scholar]
  73. Hecker H., Betschart B., Bender K., Burri M., Schlimme W. The chromatin of trypanosomes. Int J Parasitol. 1994 Sep;24(6):809–819. doi: 10.1016/0020-7519(94)90007-8. [DOI] [PubMed] [Google Scholar]
  74. Hehl A., Roditi I. The regulation of procyclin expression in Trypanosoma bruceli: making or breaking the rules? Parasitol Today. 1994 Nov;10(11):442–445. doi: 10.1016/0169-4758(94)90180-5. [DOI] [PubMed] [Google Scholar]
  75. Hehl A., Vassella E., Braun R., Roditi I. A conserved stem-loop structure in the 3' untranslated region of procyclin mRNAs regulates expression in Trypanosoma brucei. Proc Natl Acad Sci U S A. 1994 Jan 4;91(1):370–374. doi: 10.1073/pnas.91.1.370. [DOI] [PMC free article] [PubMed] [Google Scholar]
  76. Hobbs M. R., Boothroyd J. C. An expression-site-associated gene family of trypanosomes is expressed in vivo and shows homology to a variant surface glycoprotein gene. Mol Biochem Parasitol. 1990 Nov;43(1):1–16. doi: 10.1016/0166-6851(90)90125-6. [DOI] [PubMed] [Google Scholar]
  77. Huang J., Van der Ploeg L. H. 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):3877–3885. doi: 10.1002/j.1460-2075.1991.tb04957.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  78. Huang J., van der Ploeg L. H. Maturation of polycistronic pre-mRNA in Trypanosoma brucei: analysis of trans splicing and poly(A) addition at nascent RNA transcripts from the hsp70 locus. Mol Cell Biol. 1991 Jun;11(6):3180–3190. doi: 10.1128/mcb.11.6.3180. [DOI] [PMC free article] [PubMed] [Google Scholar]
  79. Hug M., Carruthers V. B., Hartmann C., Sherman D. S., Cross G. A., Clayton C. A possible role for the 3'-untranslated region in developmental regulation in Trypanosoma brucei. Mol Biochem Parasitol. 1993 Sep;61(1):87–95. doi: 10.1016/0166-6851(93)90161-p. [DOI] [PubMed] [Google Scholar]
  80. Hug M., Hotz H. R., Hartmann C., Clayton C. Hierarchies of RNA-processing signals in a trypanosome surface antigen mRNA precursor. Mol Cell Biol. 1994 Nov;14(11):7428–7435. doi: 10.1128/mcb.14.11.7428. [DOI] [PMC free article] [PubMed] [Google Scholar]
  81. Janz L., Clayton C. The PARP and rRNA promoters of Trypanosoma brucei are composed of dissimilar sequence elements that are functionally interchangeable. Mol Cell Biol. 1994 Sep;14(9):5804–5811. doi: 10.1128/mcb.14.9.5804. [DOI] [PMC free article] [PubMed] [Google Scholar]
  82. Janz L., Hug M., Clayton C. Factors that bind to RNA polymerase I promoter sequences of Trypanosoma brucei. Mol Biochem Parasitol. 1994 May;65(1):99–108. doi: 10.1016/0166-6851(94)90119-8. [DOI] [PubMed] [Google Scholar]
  83. Jefferies D., Tebabi P., Le Ray D., Pays E. The ble resistance gene as a new selectable marker for Trypanosoma brucei: fly transmission of stable procyclic transformants to produce antibiotic resistant bloodstream forms. Nucleic Acids Res. 1993 Jan 25;21(2):191–195. doi: 10.1093/nar/21.2.191. [DOI] [PMC free article] [PubMed] [Google Scholar]
  84. Jefferies D., Tebabi P., Pays E. Transient activity assays of the Trypanosoma brucei variant surface glycoprotein gene promoter: control of gene expression at the posttranscriptional level. Mol Cell Biol. 1991 Jan;11(1):338–343. doi: 10.1128/mcb.11.1.338. [DOI] [PMC free article] [PubMed] [Google Scholar]
  85. Jess W., Hammer A., Cornelissen A. W. Complete sequence of the gene encoding the largest subunit of RNA polymerase I of Trypanosoma brucei. FEBS Lett. 1989 May 22;249(1):123–128. doi: 10.1016/0014-5793(89)80029-8. [DOI] [PubMed] [Google Scholar]
  86. Kamper S. M., Barbet A. F. Surface epitope variation via mosaic gene formation is potential key to long-term survival of Trypanosoma brucei. Mol Biochem Parasitol. 1992 Jul;53(1-2):33–44. doi: 10.1016/0166-6851(92)90004-4. [DOI] [PubMed] [Google Scholar]
  87. Kapotas N., Bellofatto V. Differential response to RNA trans-splicing signals within the phosphoglycerate kinase gene cluster in Trypanosoma brucei. Nucleic Acids Res. 1993 Aug 25;21(17):4067–4072. doi: 10.1093/nar/21.17.4067. [DOI] [PMC free article] [PubMed] [Google Scholar]
  88. Koenig-Martin E., Yamage M., Roditi I. A procyclin-associated gene in Trypanosoma brucei encodes a polypeptide related to ESAG 6 and 7 proteins. Mol Biochem Parasitol. 1992 Oct;55(1-2):135–145. doi: 10.1016/0166-6851(92)90134-6. [DOI] [PubMed] [Google Scholar]
  89. Kooter J. M., Borst P. 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):9457–9472. doi: 10.1093/nar/12.24.9457. [DOI] [PMC free article] [PubMed] [Google Scholar]
  90. Kooter J. M., van der Spek H. J., Wagter R., d'Oliveira C. E., van der Hoeven F., Johnson P. J., Borst P. The anatomy and transcription of a telomeric expression site for variant-specific surface antigens in T. brucei. Cell. 1987 Oct 23;51(2):261–272. doi: 10.1016/0092-8674(87)90153-x. [DOI] [PubMed] [Google Scholar]
  91. Köck J., Evers R., Cornelissen A. W. Structure and sequence of the gene for the largest subunit of trypanosomal RNA polymerase III. Nucleic Acids Res. 1988 Sep 26;16(18):8753–8772. doi: 10.1093/nar/16.18.8753. [DOI] [PMC free article] [PubMed] [Google Scholar]
  92. König E., Delius H., Carrington M., Williams R. O., Roditi I. Duplication and transcription of procyclin genes in Trypanosoma brucei. Nucleic Acids Res. 1989 Nov 11;17(21):8727–8739. doi: 10.1093/nar/17.21.8727. [DOI] [PMC free article] [PubMed] [Google Scholar]
  93. Laird P. W. Trans splicing in trypanosomes--archaism or adaptation? Trends Genet. 1989 Jul;5(7):204–208. doi: 10.1016/0168-9525(89)90082-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  94. Laurent M., Pays E., Magnus E., Van Meirvenne N., Matthyssens G., Williams R. O., Steinert M. DNA rearrangements linked to expression of a predominant surface antigen gene of trypanosomes. Nature. 1983 Mar 17;302(5905):263–266. doi: 10.1038/302263a0. [DOI] [PubMed] [Google Scholar]
  95. Laurent M., Pays E., Van der Werf A., Aerts D., Magnus E., Van Meirvenne N., Steinert M. Translocation alters the activation rate of a trypanosome surface antigen gene. Nucleic Acids Res. 1984 Nov 26;12(22):8319–8328. doi: 10.1093/nar/12.22.8319. [DOI] [PMC free article] [PubMed] [Google Scholar]
  96. Layden R. E., Eisen H. Alternate trans splicing in Trypanosoma equiperdum: implications for splice site selection. Mol Cell Biol. 1988 Mar;8(3):1352–1360. doi: 10.1128/mcb.8.3.1352. [DOI] [PMC free article] [PubMed] [Google Scholar]
  97. LeBowitz J. H., Smith H. Q., Rusche L., Beverley S. M. Coupling of poly(A) site selection and trans-splicing in Leishmania. Genes Dev. 1993 Jun;7(6):996–1007. doi: 10.1101/gad.7.6.996. [DOI] [PubMed] [Google Scholar]
  98. Lee M. G., Polvere R. I., Van der Ploeg L. H. Evidence for segmental gene conversion between a cognate hsp 70 gene and the temperature-sensitively transcribed hsp70 genes of Trypanosoma brucei. Mol Biochem Parasitol. 1990 Jun;41(2):213–220. doi: 10.1016/0166-6851(90)90184-n. [DOI] [PubMed] [Google Scholar]
  99. Lee M. G., Van der Ploeg L. H. Homologous recombination and stable transfection in the parasitic protozoan Trypanosoma brucei. Science. 1990 Dec 14;250(4987):1583–1587. doi: 10.1126/science.2177225. [DOI] [PubMed] [Google Scholar]
  100. Lee M. G., Van der Ploeg L. H. Transcription of the heat shock 70 locus in Trypanosoma brucei. Mol Biochem Parasitol. 1990 Jun;41(2):221–231. doi: 10.1016/0166-6851(90)90185-o. [DOI] [PubMed] [Google Scholar]
  101. Lenardo M. J., Esser K. M., Moon A. M., Van der Ploeg L. H., Donelson J. E. Metacyclic variant surface glycoprotein genes of Trypanosoma brucei subsp. rhodesiense are activated in situ, and their expression is transcriptionally regulated. Mol Cell Biol. 1986 Jun;6(6):1991–1997. doi: 10.1128/mcb.6.6.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  102. Ligtenberg M. J., Bitter W., Kieft R., Steverding D., Janssen H., Calafat J., Borst P. Reconstitution of a surface transferrin binding complex in insect form Trypanosoma brucei. EMBO J. 1994 Jun 1;13(11):2565–2573. doi: 10.1002/j.1460-2075.1994.tb06546.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  103. Lips S., Revelard P., Pays E. Identification of a new expression site-associated gene in the complete 30.5 kb sequence from the AnTat 1.3A variant surface protein gene expression site of Trypanosoma brucei. Mol Biochem Parasitol. 1993 Nov;62(1):135–137. doi: 10.1016/0166-6851(93)90189-5. [DOI] [PubMed] [Google Scholar]
  104. Liu A. Y., Van der Ploeg L. H., Rijsewijk F. A., Borst P. The transposition unit of variant surface glycoprotein gene 118 of Trypanosoma brucei. Presence of repeated elements at its border and absence of promoter-associated sequences. J Mol Biol. 1983 Jun 15;167(1):57–75. doi: 10.1016/s0022-2836(83)80034-5. [DOI] [PubMed] [Google Scholar]
  105. Lodes M. J., Smiley B. L., Stadnyk A. W., Bennett J. L., Myler P. J., Stuart K. Expression of a retroposon-like sequence upstream of the putative Trypanosoma brucei variant surface glycoprotein gene expression site promoter. Mol Cell Biol. 1993 Nov;13(11):7036–7044. doi: 10.1128/mcb.13.11.7036. [DOI] [PMC free article] [PubMed] [Google Scholar]
  106. Lu Y., Alarcon C. M., Hall T., Reddy L. V., Donelson J. E. A strand bias occurs in point mutations associated with variant surface glycoprotein gene conversion in Trypanosoma rhodesiense. Mol Cell Biol. 1994 Jun;14(6):3971–3980. doi: 10.1128/mcb.14.6.3971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  107. Lu Y., Hall T., Gay L. S., Donelson J. E. Point mutations are associated with a gene duplication leading to the bloodstream reexpression of a trypanosome metacyclic VSG. Cell. 1993 Feb 12;72(3):397–406. doi: 10.1016/0092-8674(93)90116-8. [DOI] [PubMed] [Google Scholar]
  108. Martínez-Calvillo S., Hernández R. Trypanosoma cruzi ribosomal DNA: mapping of a putative distal promoter. Gene. 1994 May 16;142(2):243–247. doi: 10.1016/0378-1119(94)90268-2. [DOI] [PubMed] [Google Scholar]
  109. Matthews K. R., Gull K. Cycles within cycles: the interplay between differentiation and cell division in Trypanosoma brucei. Parasitol Today. 1994 Dec;10(12):473–476. doi: 10.1016/0169-4758(94)90159-7. [DOI] [PubMed] [Google Scholar]
  110. Matthews K. R., Gull K. Evidence for an interplay between cell cycle progression and the initiation of differentiation between life cycle forms of African trypanosomes. J Cell Biol. 1994 Jun;125(5):1147–1156. doi: 10.1083/jcb.125.5.1147. [DOI] [PMC free article] [PubMed] [Google Scholar]
  111. Matthews K. R., Tschudi C., Ullu E. A common pyrimidine-rich motif governs trans-splicing and polyadenylation of tubulin polycistronic pre-mRNA in trypanosomes. Genes Dev. 1994 Feb 15;8(4):491–501. doi: 10.1101/gad.8.4.491. [DOI] [PubMed] [Google Scholar]
  112. Morris D. R., Kakegawa T., Kaspar R. L., White M. W. Polypyrimidine tracts and their binding proteins: regulatory sites for posttranscriptional modulation of gene expression. Biochemistry. 1993 Mar 30;32(12):2931–2937. doi: 10.1021/bi00063a001. [DOI] [PubMed] [Google Scholar]
  113. Mottram J. C., Bell S. D., Nelson R. G., Barry J. D. tRNAs of Trypanosoma brucei. Unusual gene organization and mitochondrial importation. J Biol Chem. 1991 Sep 25;266(27):18313–18317. [PubMed] [Google Scholar]
  114. Mottram J. C., Kinnaird J. H., Shiels B. R., Tait A., Barry J. D. A novel CDC2-related protein kinase from Leishmania mexicana, LmmCRK1, is post-translationally regulated during the life cycle. J Biol Chem. 1993 Oct 5;268(28):21044–21052. [PubMed] [Google Scholar]
  115. Mottram J. C. cdc2-related protein kinases and cell cycle control in trypanosomatids. Parasitol Today. 1994 Jul;10(7):253–257. doi: 10.1016/0169-4758(94)90136-8. [DOI] [PubMed] [Google Scholar]
  116. Mottram J., Perry K. L., Lizardi P. M., Lührmann R., Agabian N., Nelson R. G. Isolation and sequence of four small nuclear U RNA genes of Trypanosoma brucei subsp. brucei: identification of the U2, U4, and U6 RNA analogs. Mol Cell Biol. 1989 Mar;9(3):1212–1223. doi: 10.1128/mcb.9.3.1212. [DOI] [PMC free article] [PubMed] [Google Scholar]
  117. Muhich M. L., Boothroyd J. C. Synthesis of trypanosome hsp70 mRNA is resistant to disruption of trans-splicing by heat shock. J Biol Chem. 1989 May 5;264(13):7107–7110. [PubMed] [Google Scholar]
  118. Musters W., Knol J., Maas P., Dekker A. F., van Heerikhuizen H., Planta R. J. Linker scanning of the yeast RNA polymerase I promoter. Nucleic Acids Res. 1989 Dec 11;17(23):9661–9678. doi: 10.1093/nar/17.23.9661. [DOI] [PMC free article] [PubMed] [Google Scholar]
  119. Myler P. J., Aline R. F., Jr, Scholler J. K., Stuart K. D. Changes in telomere length associated with antigenic variation in Trypanosoma brucei. Mol Biochem Parasitol. 1988 Jun;29(2-3):243–250. doi: 10.1016/0166-6851(88)90079-5. [DOI] [PubMed] [Google Scholar]
  120. Nakaar V., Dare A. O., Hong D., Ullu E., Tschudi C. Upstream tRNA genes are essential for expression of small nuclear and cytoplasmic RNA genes in trypanosomes. Mol Cell Biol. 1994 Oct;14(10):6736–6742. doi: 10.1128/mcb.14.10.6736. [DOI] [PMC free article] [PubMed] [Google Scholar]
  121. Nilsen T. W. Trans-splicing of nematode premessenger RNA. Annu Rev Microbiol. 1993;47:413–440. doi: 10.1146/annurev.mi.47.100193.002213. [DOI] [PubMed] [Google Scholar]
  122. Norton P. A. Polypyrimidine tract sequences direct selection of alternative branch sites and influence protein binding. Nucleic Acids Res. 1994 Sep 25;22(19):3854–3860. doi: 10.1093/nar/22.19.3854. [DOI] [PMC free article] [PubMed] [Google Scholar]
  123. O'Brien T., Hardin S., Greenleaf A., Lis J. T. Phosphorylation of RNA polymerase II C-terminal domain and transcriptional elongation. Nature. 1994 Jul 7;370(6484):75–77. doi: 10.1038/370075a0. [DOI] [PubMed] [Google Scholar]
  124. Overath P., Chaudhri M., Steverding D., Ziegelbauer K. Invariant surface proteins in bloodstream forms of Trypanosoma brucei. Parasitol Today. 1994 Feb;10(2):53–58. doi: 10.1016/0169-4758(94)90393-x. [DOI] [PubMed] [Google Scholar]
  125. Paindavoine P., Rolin S., Van Assel S., Geuskens M., Jauniaux J. C., Dinsart C., Huet G., Pays E. A gene from the variant surface glycoprotein expression site encodes one of several transmembrane adenylate cyclases located on the flagellum of Trypanosoma brucei. Mol Cell Biol. 1992 Mar;12(3):1218–1225. doi: 10.1128/mcb.12.3.1218. [DOI] [PMC free article] [PubMed] [Google Scholar]
  126. Patnaik P. K., Fang X., Cross G. A. The region encompassing the procyclic acidic repetitive protein (PARP) gene promoter plays a role in plasmid DNA replication in Trypanosoma brucei. Nucleic Acids Res. 1994 Oct 11;22(20):4111–4118. doi: 10.1093/nar/22.20.4111. [DOI] [PMC free article] [PubMed] [Google Scholar]
  127. Patnaik P. K., Kulkarni S. K., Cross G. A. Autonomously replicating single-copy episomes in Trypanosoma brucei show unusual stability. EMBO J. 1993 Jun;12(6):2529–2538. doi: 10.1002/j.1460-2075.1993.tb05908.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  128. Pays E., Coquelet H., Pays A., Tebabi P., Steinert M. Trypanosoma brucei: posttranscriptional control of the variable surface glycoprotein gene expression site. Mol Cell Biol. 1989 Sep;9(9):4018–4021. doi: 10.1128/mcb.9.9.4018. [DOI] [PMC free article] [PubMed] [Google Scholar]
  129. Pays E., Coquelet H., Tebabi P., Pays A., Jefferies D., Steinert M., Koenig E., Williams R. O., Roditi I. Trypanosoma brucei: constitutive activity of the VSG and procyclin gene promoters. EMBO J. 1990 Oct;9(10):3145–3151. doi: 10.1002/j.1460-2075.1990.tb07512.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  130. Pays E., Delauw M. F., Laurent M., Steinert M. Possible DNA modification in GC dinucleotides of Trypanosoma brucei telomeric sequences; relationship with antigen gene transcription. Nucleic Acids Res. 1984 Jul 11;12(13):5235–5247. doi: 10.1093/nar/12.13.5235. [DOI] [PMC free article] [PubMed] [Google Scholar]
  131. Pays E. Gene conversion in trypanosome antigenic variation. Prog Nucleic Acid Res Mol Biol. 1985;32:1–26. doi: 10.1016/s0079-6603(08)60344-x. [DOI] [PubMed] [Google Scholar]
  132. Pays E., Hanocq-Quertier J., Hanocq F., Van Assel S., Nolan D., Rolin S. Abrupt RNA changes precede the first cell division during the differentiation of Trypanosoma brucei bloodstream forms into procyclic forms in vitro. Mol Biochem Parasitol. 1993 Sep;61(1):107–114. doi: 10.1016/0166-6851(93)90163-r. [DOI] [PubMed] [Google Scholar]
  133. Pays E., Houard S., Pays A., Van Assel S., Dupont F., Aerts D., Huet-Duvillier G., Gomés V., Richet C., Degand P. Trypanosoma brucei: the extent of conversion in antigen genes may be related to the DNA coding specificity. Cell. 1985 Oct;42(3):821–829. doi: 10.1016/0092-8674(85)90278-8. [DOI] [PubMed] [Google Scholar]
  134. Pays E., Laurent M., Delinte K., Van Meirvenne N., Steinert M. Differential size variations between transcriptionally active and inactive telomeres of Trypanosoma brucei. Nucleic Acids Res. 1983 Dec 10;11(23):8137–8147. doi: 10.1093/nar/11.23.8137. [DOI] [PMC free article] [PubMed] [Google Scholar]
  135. Pays E. Pseudogenes, chimaeric genes and the timing of antigen variation in African trypanosomes. Trends Genet. 1989 Dec;5(12):389–391. doi: 10.1016/0168-9525(89)90181-9. [DOI] [PubMed] [Google Scholar]
  136. Pays E., Tebabi P., Pays A., Coquelet H., Revelard P., Salmon D., Steinert M. The genes and transcripts of an antigen gene expression site from T. brucei. Cell. 1989 Jun 2;57(5):835–845. doi: 10.1016/0092-8674(89)90798-8. [DOI] [PubMed] [Google Scholar]
  137. Pays E., Vanhamme L., Berberof M. Genetic controls for the expression of surface antigens in African trypanosomes. Annu Rev Microbiol. 1994;48:25–52. doi: 10.1146/annurev.mi.48.100194.000325. [DOI] [PubMed] [Google Scholar]
  138. Pellé R., Murphy N. B. Stage-specific differential polyadenylation of mini-exon derived RNA in African trypanosomes. Mol Biochem Parasitol. 1993 Jun;59(2):277–286. doi: 10.1016/0166-6851(93)90225-m. [DOI] [PubMed] [Google Scholar]
  139. Priest J. W., Hajduk S. L. Developmental regulation of Trypanosoma brucei cytochrome c reductase during bloodstream to procyclic differentiation. Mol Biochem Parasitol. 1994 Jun;65(2):291–304. doi: 10.1016/0166-6851(94)90080-9. [DOI] [PubMed] [Google Scholar]
  140. Puerta C., Martin J., Alonso C., López M. C. Isolation and characterization of the gene encoding histone H2A from Trypanosoma cruzi. Mol Biochem Parasitol. 1994 Mar;64(1):1–10. doi: 10.1016/0166-6851(94)90129-5. [DOI] [PubMed] [Google Scholar]
  141. Revelard P., Lips S., Pays E. A gene from the VSG expression site of Trypanosoma brucei encodes a protein with both leucine-rich repeats and a putative zinc finger. Nucleic Acids Res. 1990 Dec 25;18(24):7299–7303. doi: 10.1093/nar/18.24.7299. [DOI] [PMC free article] [PubMed] [Google Scholar]
  142. Revelard P., Lips S., Pays E. Alternative splicing within and between alleles of the ATPase gene 1 locus of Trypanosoma brucei. Mol Biochem Parasitol. 1993 Nov;62(1):93–101. doi: 10.1016/0166-6851(93)90181-v. [DOI] [PubMed] [Google Scholar]
  143. Roditi I., Pearson T. W. The procyclin coat of African trypanosomes (or the not-so-naked trypanosome). Parasitol Today. 1990 Mar;6(3):79–82. doi: 10.1016/0169-4758(90)90216-q. [DOI] [PubMed] [Google Scholar]
  144. Roditi I., Schwarz H., Pearson T. W., Beecroft R. P., Liu M. K., Richardson J. P., Bühring H. J., Pleiss J., Bülow R., Williams R. O. Procyclin gene expression and loss of the variant surface glycoprotein during differentiation of Trypanosoma brucei. J Cell Biol. 1989 Feb;108(2):737–746. doi: 10.1083/jcb.108.2.737. [DOI] [PMC free article] [PubMed] [Google Scholar]
  145. Rolin S., Paindavoine P., Hanocq-Quertier J., Hanocq F., Claes Y., Le Ray D., Overath P., Pays E. Transient adenylate cyclase activation accompanies differentiation of Trypanosoma brucei from bloodstream to procyclic forms. Mol Biochem Parasitol. 1993 Sep;61(1):115–125. doi: 10.1016/0166-6851(93)90164-s. [DOI] [PubMed] [Google Scholar]
  146. Ross D. T., Raibaud A., Florent I. C., Sather S., Gross M. K., Storm D. R., Eisen H. The trypanosome VSG expression site encodes adenylate cyclase and a leucine-rich putative regulatory gene. EMBO J. 1991 Aug;10(8):2047–2053. doi: 10.1002/j.1460-2075.1991.tb07735.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  147. Rudenko G., Bishop D., Gottesdiener K., Van der Ploeg L. H. Alpha-amanitin resistant transcription of protein coding genes in insect and bloodstream form Trypanosoma brucei. EMBO J. 1989 Dec 20;8(13):4259–4263. doi: 10.1002/j.1460-2075.1989.tb08611.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  148. Rudenko G., Blundell P. A., Taylor M. C., Kieft R., Borst P. VSG gene expression site control in insect form Trypanosoma brucei. EMBO J. 1994 Nov 15;13(22):5470–5482. doi: 10.1002/j.1460-2075.1994.tb06882.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  149. Rudenko G., Chung H. M., Pham V. P., Van der Ploeg L. H. RNA polymerase I can mediate expression of CAT and neo protein-coding genes in Trypanosoma brucei. EMBO J. 1991 Nov;10(11):3387–3397. doi: 10.1002/j.1460-2075.1991.tb04903.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  150. Rudenko G., Le Blancq S., Smith J., Lee M. G., Rattray A., Van der Ploeg L. H. 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):3492–3504. doi: 10.1128/mcb.10.7.3492. [DOI] [PMC free article] [PubMed] [Google Scholar]
  151. Rudenko G., Lee M. G., Van der Ploeg L. H. 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):303–306. doi: 10.1093/nar/20.2.303. [DOI] [PMC free article] [PubMed] [Google Scholar]
  152. Saito R. M., Elgort M. G., Campbell D. A. A conserved upstream element is essential for transcription of the Leishmania tarentolae mini-exon gene. EMBO J. 1994 Nov 15;13(22):5460–5469. doi: 10.1002/j.1460-2075.1994.tb06881.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  153. Salmon D., Geuskens M., Hanocq F., Hanocq-Quertier J., Nolan D., Ruben L., Pays E. A novel heterodimeric transferrin receptor encoded by a pair of VSG expression site-associated genes in T. brucei. Cell. 1994 Jul 15;78(1):75–86. doi: 10.1016/0092-8674(94)90574-6. [DOI] [PubMed] [Google Scholar]
  154. Sandell L. L., Zakian V. A. Telomeric position effect in yeast. Trends Cell Biol. 1992 Jan;2(1):10–14. doi: 10.1016/0962-8924(92)90138-d. [DOI] [PubMed] [Google Scholar]
  155. Schell D., Evers R., Preis D., Ziegelbauer K., Kiefer H., Lottspeich F., Cornelissen A. W., Overath P. A transferrin-binding protein of Trypanosoma brucei is encoded by one of the genes in the variant surface glycoprotein gene expression site. EMBO J. 1991 May;10(5):1061–1066. doi: 10.1002/j.1460-2075.1991.tb08045.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  156. Schlimme W., Burri M., Bender K., Betschart B., Hecker H. Trypanosoma brucei brucei: differences in the nuclear chromatin of bloodstream forms and procyclic culture forms. Parasitology. 1993 Sep;107(Pt 3):237–247. doi: 10.1017/s003118200007921x. [DOI] [PubMed] [Google Scholar]
  157. Schürch N., Hehl A., Vassella E., Braun R., Roditi I. Accurate polyadenylation of procyclin mRNAs in Trypanosoma brucei is determined by pyrimidine-rich elements in the intergenic regions. Mol Cell Biol. 1994 Jun;14(6):3668–3675. doi: 10.1128/mcb.14.6.3668. [DOI] [PMC free article] [PubMed] [Google Scholar]
  158. Sherman D. R., Janz L., Hug M., Clayton C. Anatomy of the parp gene promoter of Trypanosoma brucei. EMBO J. 1991 Nov;10(11):3379–3386. doi: 10.1002/j.1460-2075.1991.tb04902.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  159. Smiley B. L., Stadnyk A. W., Myler P. J., Stuart K. The trypanosome leucine repeat gene in the variant surface glycoprotein expression site encodes a putative metal-binding domain and a region resembling protein-binding domains of yeast, Drosophila, and mammalian proteins. Mol Cell Biol. 1990 Dec;10(12):6436–6444. doi: 10.1128/mcb.10.12.6436. [DOI] [PMC free article] [PubMed] [Google Scholar]
  160. Smith J. L., Chapman A. B., Agabian N. Trypanosoma vivax: evidence for only one RNA polymerase II largest subunit gene in a trypanosome which undergoes antigenic variation. Exp Parasitol. 1993 May;76(3):242–246. doi: 10.1006/expr.1993.1029. [DOI] [PubMed] [Google Scholar]
  161. Smith J. L., Levin J. R., Ingles C. J., Agabian N. 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):815–827. doi: 10.1016/0092-8674(89)90686-7. [DOI] [PubMed] [Google Scholar]
  162. Sollner-Webb B., Tower J. Transcription of cloned eukaryotic ribosomal RNA genes. Annu Rev Biochem. 1986;55:801–830. doi: 10.1146/annurev.bi.55.070186.004101. [DOI] [PubMed] [Google Scholar]
  163. Soto M., Requena J. M., Gomez L. C., Navarrete I., Alonso C. Molecular characterization of a Leishmania donovani infantum antigen identified as histone H2A. Eur J Biochem. 1992 Apr 1;205(1):211–216. doi: 10.1111/j.1432-1033.1992.tb16770.x. [DOI] [PubMed] [Google Scholar]
  164. Spieth J., Brooke G., Kuersten S., Lea K., Blumenthal T. Operons in C. elegans: polycistronic mRNA precursors are processed by trans-splicing of SL2 to downstream coding regions. Cell. 1993 May 7;73(3):521–532. doi: 10.1016/0092-8674(93)90139-h. [DOI] [PubMed] [Google Scholar]
  165. Steverding D., Stierhof Y. D., Chaudhri M., Ligtenberg M., Schell D., Beck-Sickinger A. G., Overath P. ESAG 6 and 7 products of Trypanosoma brucei form a transferrin binding protein complex. Eur J Cell Biol. 1994 Jun;64(1):78–87. [PubMed] [Google Scholar]
  166. Thon G., Baltz T., Giroud C., Eisen H. Trypanosome variable surface glycoproteins: composite genes and order of expression. Genes Dev. 1990 Aug;4(8):1374–1383. doi: 10.1101/gad.4.8.1374. [DOI] [PubMed] [Google Scholar]
  167. Tommerup H., Dousmanis A., de Lange T. Unusual chromatin in human telomeres. Mol Cell Biol. 1994 Sep;14(9):5777–5785. doi: 10.1128/mcb.14.9.5777. [DOI] [PMC free article] [PubMed] [Google Scholar]
  168. Torri A. F., Bertrand K. I., Hajduk S. L. Protein stability regulates the expression of cytochrome c during the developmental cycle of Trypanosoma brucei. Mol Biochem Parasitol. 1993 Feb;57(2):305–315. doi: 10.1016/0166-6851(93)90206-d. [DOI] [PubMed] [Google Scholar]
  169. Torri A. F., Hajduk S. L. Posttranscriptional regulation of cytochrome c expression during the developmental cycle of Trypanosoma brucei. Mol Cell Biol. 1988 Nov;8(11):4625–4633. doi: 10.1128/mcb.8.11.4625. [DOI] [PMC free article] [PubMed] [Google Scholar]
  170. Turner C. M., Barry J. D. High frequency of antigenic variation in Trypanosoma brucei rhodesiense infections. Parasitology. 1989 Aug;99(Pt 1):67–75. doi: 10.1017/s0031182000061035. [DOI] [PubMed] [Google Scholar]
  171. Tzfati Y., Abeliovich H., Kapeller I., Shlomai J. A single-stranded DNA-binding protein from Crithidia fasciculata recognizes the nucleotide sequence at the origin of replication of kinetoplast DNA minicircles. Proc Natl Acad Sci U S A. 1992 Aug 1;89(15):6891–6895. doi: 10.1073/pnas.89.15.6891. [DOI] [PMC free article] [PubMed] [Google Scholar]
  172. Ullu E., Matthews K. R., Tschudi C. Temporal order of RNA-processing reactions in trypanosomes: rapid trans splicing precedes polyadenylation of newly synthesized tubulin transcripts. Mol Cell Biol. 1993 Jan;13(1):720–725. doi: 10.1128/mcb.13.1.720. [DOI] [PMC free article] [PubMed] [Google Scholar]
  173. Van der Ploeg L. H., Giannini S. H., Cantor C. R. Heat shock genes: regulatory role for differentiation in parasitic protozoa. Science. 1985 Jun 21;228(4706):1443–1446. doi: 10.1126/science.4012301. [DOI] [PubMed] [Google Scholar]
  174. Van der Ploeg L. H., Gottesdiener K., Lee M. G. Antigenic variation in African trypanosomes. Trends Genet. 1992 Dec;8(12):452–457. doi: 10.1016/0168-9525(92)90330-7. [DOI] [PubMed] [Google Scholar]
  175. Van der Werf A., Van Assel S., Aerts D., Steinert M., Pays E. Telomere interactions may condition the programming of antigen expression in Trypanosoma brucei. EMBO J. 1990 Apr;9(4):1035–1040. doi: 10.1002/j.1460-2075.1990.tb08207.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  176. Vassella E., Braun R., Roditi I. Control of polyadenylation and alternative splicing of transcripts from adjacent genes in a procyclin expression site: a dual role for polypyrimidine tracts in trypanosomes? Nucleic Acids Res. 1994 Apr 25;22(8):1359–1364. doi: 10.1093/nar/22.8.1359. [DOI] [PMC free article] [PubMed] [Google Scholar]
  177. Vickerman K. Developmental cycles and biology of pathogenic trypanosomes. Br Med Bull. 1985 Apr;41(2):105–114. doi: 10.1093/oxfordjournals.bmb.a072036. [DOI] [PubMed] [Google Scholar]
  178. Vickerman K., Tetley L., Hendry K. A., Turner C. M. Biology of African trypanosomes in the tsetse fly. Biol Cell. 1988;64(2):109–119. doi: 10.1016/0248-4900(88)90070-6. [DOI] [PubMed] [Google Scholar]
  179. Watkins K. P., Dungan J. M., Agabian N. Identification of a small RNA that interacts with the 5' splice site of the Trypanosoma brucei spliced leader RNA in vivo. Cell. 1994 Jan 14;76(1):171–182. doi: 10.1016/0092-8674(94)90181-3. [DOI] [PubMed] [Google Scholar]
  180. Webb J. R., McMaster W. R. Leishmania major HEXBP deletion mutants generated by double targeted gene replacement. Mol Biochem Parasitol. 1994 Feb;63(2):231–242. doi: 10.1016/0166-6851(94)90059-0. [DOI] [PubMed] [Google Scholar]
  181. Webb J. R., McMaster W. R. Molecular cloning and expression of a Leishmania major gene encoding a single-stranded DNA-binding protein containing nine "CCHC" zinc finger motifs. J Biol Chem. 1993 Jul 5;268(19):13994–14002. [PubMed] [Google Scholar]
  182. White T. C., Rudenko G., Borst P. 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):9471–9489. doi: 10.1093/nar/14.23.9471. [DOI] [PMC free article] [PubMed] [Google Scholar]
  183. Wong A. K., Curotto de Lafaille M. A., Wirth D. F. Identification of a cis-acting gene regulatory element from the lemdr1 locus of Leishmania enriettii. J Biol Chem. 1994 Oct 21;269(42):26497–26502. [PubMed] [Google Scholar]
  184. Wong S., Morales T. H., Neigel J. E., Campbell D. A. Genomic and transcriptional linkage of the genes for calmodulin, EF-hand 5 protein, and ubiquitin extension protein 52 in Trypanosoma brucei. Mol Cell Biol. 1993 Jan;13(1):207–216. doi: 10.1128/mcb.13.1.207. [DOI] [PMC free article] [PubMed] [Google Scholar]
  185. Xu G. L., Wieland B., Bindereif A. trans-spliceosomal U6 RNAs of Crithidia fasciculata and Leptomonas seymouri: deviation from the conserved ACAGAG sequence and potential base pairing with spliced leader RNA. Mol Cell Biol. 1994 Jul;14(7):4565–4570. doi: 10.1128/mcb.14.7.4565. [DOI] [PMC free article] [PubMed] [Google Scholar]
  186. Ziegelbauer K., Overath P. Organization of two invariant surface glycoproteins in the surface coat of Trypanosoma brucei. Infect Immun. 1993 Nov;61(11):4540–4545. doi: 10.1128/iai.61.11.4540-4545.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  187. Ziegelbauer K., Quinten M., Schwarz H., Pearson T. W., Overath P. Synchronous differentiation of Trypanosoma brucei from bloodstream to procyclic forms in vitro. Eur J Biochem. 1990 Sep 11;192(2):373–378. doi: 10.1111/j.1432-1033.1990.tb19237.x. [DOI] [PubMed] [Google Scholar]
  188. Ziegelbauer K., Stahl B., Karas M., Stierhof Y. D., Overath P. Proteolytic release of cell surface proteins during differentiation of Trypanosoma brucei. Biochemistry. 1993 Apr 13;32(14):3737–3742. doi: 10.1021/bi00065a028. [DOI] [PubMed] [Google Scholar]
  189. Zomerdijk J. C., Kieft R., Borst P. A ribosomal RNA gene promoter at the telomere of a mini-chromosome in Trypanosoma brucei. Nucleic Acids Res. 1992 Jun 11;20(11):2725–2734. doi: 10.1093/nar/20.11.2725. [DOI] [PMC free article] [PubMed] [Google Scholar]
  190. Zomerdijk J. C., Kieft R., Borst P. Efficient production of functional mRNA mediated by RNA polymerase I in Trypanosoma brucei. Nature. 1991 Oct 24;353(6346):772–775. doi: 10.1038/353772a0. [DOI] [PubMed] [Google Scholar]
  191. Zomerdijk J. C., Kieft R., Duyndam M., Shiels P. G., Borst P. Antigenic variation in Trypanosoma brucei: a telomeric expression site for variant-specific surface glycoprotein genes with novel features. Nucleic Acids Res. 1991 Apr 11;19(7):1359–1368. doi: 10.1093/nar/19.7.1359. [DOI] [PMC free article] [PubMed] [Google Scholar]
  192. Zomerdijk J. C., Kieft R., Shiels P. G., Borst P. 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):5153–5158. doi: 10.1093/nar/19.19.5153. [DOI] [PMC free article] [PubMed] [Google Scholar]
  193. Zomerdijk J. C., Ouellette M., ten Asbroek A. L., Kieft R., Bommer A. M., Clayton C. E., Borst P. The promoter for a variant surface glycoprotein gene expression site in Trypanosoma brucei. EMBO J. 1990 Sep;9(9):2791–2801. doi: 10.1002/j.1460-2075.1990.tb07467.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  194. ten Asbroek A. L., Mol C. A., Kieft R., Borst P. Stable transformation of Trypanosoma brucei. Mol Biochem Parasitol. 1993 May;59(1):133–142. doi: 10.1016/0166-6851(93)90014-o. [DOI] [PubMed] [Google Scholar]
  195. ten Asbroek A. L., Ouellette M., Borst P. Targeted insertion of the neomycin phosphotransferase gene into the tubulin gene cluster of Trypanosoma brucei. Nature. 1990 Nov 8;348(6297):174–175. doi: 10.1038/348174a0. [DOI] [PubMed] [Google Scholar]

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