Unravelling the procyclin coat of Trypanosoma brucei

Molecular and Biochemical Parasitology

Volumn 91, Issue 1, 1998, Pages

  Roditi, I ^a   Furger, A ^a   Ruepp, S ^a   Schurch N ^a   Butikofer P ^a  

^a UNIVERSITY OF BERN   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

COAT PROTEIN; PROCYCLIN; UNCLASSIFIED DRUG; VARIANT SURFACE GLYCOPROTEIN;

ANIMAL CELL; GENE EXPRESSION REGULATION; GENE LOCUS; GENETIC ORGANIZATION; LIFE CYCLE; NONHUMAN; PRIORITY JOURNAL; REVIEW; TRANSCRIPTION REGULATION; TRYPANOSOMA BRUCEI; TSETSE FLY;

TRYPANOSOMA BRUCEI;

EID: 0032029253     PISSN: 01666851     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0166-6851(97)00195-3     Document Type: Article

References (79)

1. [1] Koch R. Remarks on trypanosome diseases. Brit Med J 1904;ii:1445-1449.
2. [2] Bruce D, Hamerton AE, Bateman HR, Mackie FP. The development of Trypanosoma gambiense in Glossina palpalis. Proc R Soc London 1909;B81:405-14.
3. [3] Bruce D, Hamerton AE, Bateman HR, Mackie FP. The development of trypanosomes in tsetse flies. Proc R Soc London 1910;B82:368-88.
4. [4] Vickerman K. On the surface coat and flagellar adhesion in trypanosomes. J Cell Sci 1969;5:163-93.
5. [5] Richardson JP, Jenni L, Beecroft RP, Pearson TW. Procyclic tsetse fly midgut forms and culture forms of African trypanosomes share stage- and species-specific surface antigens identified by monoclonal antibodies. J Immunol 1986;136:2259-64.
6. [6] Roditi I, Carrington M, Turner M. Expression of a polypeptide containing a dipeptide repeat is confined to the insect stage of Trypanosoma brucei. Nature 1987;325:272-4.
7. [7] Mowatt MR, Clayton CE. Developmental regulation of a novel repetitive protein of Trypanosoma brucei. Mol Cell Biol 1987;7:2833-44.
8. [8] Richardson JP, Beecroft RP, Tolson DL, Liu MK, Pearson TW. Procyclin: an unusual immunodominant glycoprotein surface antigen from the procyclic stage of African trypanosomes. Mol Biochem Parasitol 1988;31:203-16.
9. [9] Roditi I, Pearson TW. The procyclin coat of African trypanosomes. Parasitol Today 1990;6:79-82.
10. [10] Cross GAM. Antigenic variation in trypanosomes: secrets surface slowly. Bioessays 1996;18:283-91.
11. [11] Roditi I, Schwarz H, Pearson TW, Beecroft RP, Liu MK, Richardson JP, Bühring H-J, Pleiss J, Bülow R, Williams RO, Overath P. Procyclin gene expression and loss of the variant surface glycoprotein during differentiation of Trypanosoma brucei. J Cell Biol 1989;108:737-46.
12. [12] Ziegelbauer K, Quinten M, Schwarz H, Pearson TW, Overath P. Synchronous differentiation of Trypanosoma bruceii from bloodstream to procyclic forms in vitro. Eur J Biochem 1990;192:373-80.
13. [13] Matthews KR, Gull K. Cycles within cycles: the interplay between differentiation and cell division in Trypanosoma brucei. Parasitol Today 1994;10:473-6.
14. [14] Vanhamme L, Pays E. Control of gene expression in trypanosomes. Microbiol Rev 1995;59:223-40.
15. [15] Roditi, I. The VSG-Procyclin Switch. Parasitol Today 1996;12:47-49.
16. [16] Borst P, Bitter W, Blundell P, et al. Control of VSG gene expression sites in Trypanosoma brucei. Mol Biochem Parasitol. 1998;91:67-76.
17. [17] Cross G, Wirtz L, Navarro M. Regulation of vsg expression site transcription and switching in Trypanosoma brucei. Mol Biochem Parasitol 1998;91:77-91.
18. [18] Barry JD, Graham SV, Fotheriingham M, Graham VS, Kobryn K, Wymer B. VSG gene control and infectivity strategy of metacyclic stage Trypanosoma brucei. Mol Biochem Parasitol 1998;91:91-105.
19. [19] Vanhamme et al., this issue.
20. [20] Koenig E, Delius H, Carrington M, Williams RO, Roditi I. Duplication and transcription of procyclin genes in Trypanosoma brucei. Nucleic Acids Res 1989;17:8727-39.
21. [21] Ruepp S, Furger A, Kurath U, Kunz Renggli C, Hemphill A, Brun R, Roditi I. Survival of Trypanosoma brucei in the tsetse fly is enhanced by the expression of specific forms of procyclin. J Cell Biol 1997;137:1369-79.
22. [22] Mowatt MR, Clayton CE. Polymorphisms in the procyclic acidic repetitive protein (PARP) gene family of Trypanosoma brucei. Mol Cell Biol 1988;8:4055-62.
23. [23] Kooter JM, Borst P. α-amanitin-insensitive transcription of variant surface glycoprotein genes provides further evidence for discontinous transcription in trypanosomes. Nucleic Acids Res 1984;12:9457-72.
24. [24] Rudenko G, Bishop D, Gottesdiener K, van der Ploeg LHT. Alpha-amanitin resistant transcription of protein coding genes in insect and bloodstream form Trypanosoma brucei. EMBO J 1989;8:4259-63.
25. [25] Rudenko G, LeBlanq S, Smith J, Lee MGS, Rattray A, van der Ploeg LHT. Procyclic acidic repetitive protein genes (PARP) genes located in an unusually small α-amanitin-resistant transcription unit: PARP promoter activity assayed by transient DNA transfection of Trypanosoma brucei. Mol Cell Biol 1990;10:3492-504.
26. [26] Sherman DR, Janz L, Hug M, Clayton C. Anatomy of the parp gene promoter of Trypanosoma brucei. EMBO J 1991;10:3379-86.
27. [27] Brown SD, Huang J, van der Ploeg LHT. The promoter for the procyclic acidic repetitive protein (PARP) genes of Trypanosoma brucei shares features with RNA polymerase I promoters. Mol Cell Biol 1992;12:2644-52.
28. [28] 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;14:5804-11.
29. [29] Vanhamme L, Pays A, Tebabi P, Alexandre S, Pays E. Specific binding of proteins to the noncoding strand of a crucial element of the variant surface glycoprotein, procyclin and ribosomal promotors of Trypanosoma brucei. Mol Cell Biol 1995;15:5598-606.
30. [30] Rudenko G, Lee MG-S, van der Ploeg LHT. 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;20:303-6.
31. [31] Grondal EJM, Evers R, Kosubek K, Cornelissen AWCA. Characterisation of the RNA polymerases of Trypanosoma brucei trypanosomal RNAs are composed of transcripts derived from both RNA polymerase II and III. EMBO J 1989;8:3383-9.
32. [32] Sharp PA. TATA-binding protein is a classless factor. Cell 1992;68:819-21.
33. [33] Koenig-Martin E, Yamage M, Roditi I. A procyclin-associated gene in Trypanosoma brucei encodes a polypeptide related to ESAG 6 and 7. Mol Biochem Parasitol 1992;55:135-46.
34. [34] Huang J, van der Ploeg LHT. 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;10:3877-85.
35. [35] Metzenberg S, Agabian N. Human and fungal 3′ splice sites are used by Trypanosoma brucei for trans splicing. Mol Biochem Parasitol 1996;83:11-23.
36. [36] Graham SV, Jefferies D, Barry JD. A promotor directing alpha-amanitin-sensitive transcription of GARP, the major surface antigen of insect stage Trypanosoma congolense. Nucleic Acid Res 1996;24:272-81.
37. [37] Matthews KR, Tschudi C, Ullu E. A common pyrimidine-rich motif governs trans-splicing and polyadenylation of tubulin polycistronic pre-mRNA in trypanosomes. Genes Dev 1994;8:491-501.
38. [38] 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;14:3668-75.
39. [39] 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;22:1359-64.
40. [40] 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;14:7428-35.
41. [41] Furger A, Schürch N, Kurath U, Roditi I. Elements in the 3′ untranslated region of procyclin mRNA regulate expression in insect forms of Trypanosoma brucei by modulating RNA stability and translation. Mol Cell Biol 1997;17:4372-80.
42. [42] Berberof M, Pays A, Lips S, Tebabi P, Pays E. Characterization of a transcriptional terminator the of the procyclin PARP A unit of Trypanosoma brucei. Mol Cell Biol 1996;16:914-24.
43. [43] Ligtenberg MJ, 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;13:2565-73.
44. [44] 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 Trypanosoma brucei. Cell 1994;78:75-86.
45. [45] Chaudhri M, Steverding D, Kittelberger D, Tjia S, Overath P. Expression of a glycosylphosphatidylinositol-anchored Trypanosoma brucei transferrin-binding protein complex in insect cells. Proc Natl Acad Sci USA 1994;91:6443-7.
46. [46] Koenig-Martin E. Ph.D. thesis. University of Tübingen, Germany, 1992.
47. [47] Berberof M, Pays A, Pays E. A similar gene is shared by both variant surface glycoprotein and procyclin gene transcription units of Trypanosoma brucei. Mol Cell Biol 1991;11:1473-9.
48. [48] Schneider A, Hemphill A, Wyler T, Seebeck T. Large microtubule-associated protein of T. brucei has tandemly repeated, near-identical sequences. Science 1988;241:459-62.
49. [49] Pays E, Coquelet H, Tebabi P, Pays A, Jefferies D, Steinert M, Koenig E, Williams RO, Roditi I. Trypanosoma brucei: constitutive activity of the VSG and procyclin promoters. EMBO J 1990;9:3145-51.
50. [50] Vanhamme L, Berberof M, Le Ray D, Pays E. Stimuli of differentiation regulate RNA elongation in the transcription units for the major stage-specific antigens of Trypanosoma brucei. Nucleic Acids Res 1995;23:1862-9.
51. [51] Ürményi TP, van der Ploeg. PARP promoter-mediated activation of a VSG expression site promoter in insect form Trypanosoma brucei. Nucleic Acids Res 1995;23:1010-8.
52. [52] Jefferies D, Tebabi P, Pays E. Transient activity assays of the Trypanosoma brucei VSG gene promoter: control of gene expression at the post-transcriptional level. Mol Cell Biol 1991;11:338-43.
53. [53] 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 USA 1994;91:370-4.
54. [54] Clayton C, Hotz H-R. Post-transcriptional control of PARP gene expression. Mol Biochem Parasitol 1996;77:1-6.
55. [55] Schürch N, Furger A, Kurath U, Roditi I. Contributions of the procyclin 3′ untranslated region and coding region to the regulation of expression in bloodstream forms of Trypanosoma brucei. Mol Biochem Parasitol 1997;89:109-21.
56. [56] Hans-Rudolf H, Biebinger S, Flaspohler J, Clayton C. PARP gene expression: control at many levels. Mol Biochem Parasitol 1998;91:131-43.
57. [57] Bayne RAL, Kilbride EA, Lainson FA, Tetley L, Barry JD. A major surface antigen of procyclic stage Trypanosoma congolense. Mol Biochem Parasitol 1993;61:295-310.
58. [58] Hehl A, Roditi I. The regulation of procyclin expression in Trypanosoma brucei: Making or breaking the rules? Parasitol Today 1994;10:442-5.
59. [59] Dorn PL, Aman RA, Boothroyd JC. Inhibition of protein synthesis results in super-induction of procyclin (PARP) RNA levels. Mol Biochem Parasitol 1991;44:133-9.
60. [60] Graham SV, Barry JD. Polysomal, procyclin mRNAs accumulate in bloodstream forms of monomorphic and pleomorphic trypanosomes treated with protein synthesis inhibitors. Mol Biochem Parasitol 1996;80:179-91.
61. [61] Evans JS, Levine BA, Trayer IP, Dorman CJ, Higgins CF. Sequence-imposed structural restraints in the Ton B protein of E. coli. FEBS Lett 1986;208:211-6.
62. 2+ release channel (ryanodine receptor) of rabbit cardiac muscle sarcoplasmic reticulum. J Biol Chem 1990;265:13472-83.
63. [63] Lafrenière RG, Carrel L, Willard HF. A novel transmembrane transporter encoded by the XPCT gene in Xq13.2. Hum Mol Genet 1994;3:1133-9.
64. [64] Geertman R, McMahon A, Sabban E. Cloning and characterisation of cDNAs for novel proteins with glutamic acid-proline dipeptide tandem repeats. Biochim Biophys Acta 1996;1306:147-52.
65. [65] Latif F, Tory K, Gnarra J, Yao M, Duh F-M, Orcutt ML, et al. Identification of the von Hippel-Lindau disease tumor suppressor gene. Science 1993;260:1317-20.
66. [66] Ferguson MAF, Murray P, Rutherford H, McConville MJ. A simple purification of procyclic acidic repetitive protein and demonstration of a sialylated glycosyl-phosphatidylinositol membrane anchor. Biochem J 1993;291:51-5.
67. [67] Bütikofer P, Ruepp S, Boschung M, Roditi I. 'GPEET' procyclin is the major surface glycoprotein of Trypanosoma brucei brucei procyclic culture forms. Biochem J 1997;326:415-23.
68. [68] Treumann A, Zitzmann N, Hülsmeier A, Prescott AR, Almond A, Sheelah J, Ferguson MAJ. Structural characterisation of two forms of procyclic acidic repetitive protein expressed by procyclic forms of Trypanosoma brucei. J Mol Biol 1997;269:529-47.
69. [69] Pontes de Carvalho LC, Tomlinson S, Vandekerckhove F, Bienen EJ, Clarkson AB, Jiang M-S, Hart GW, Nussenzweig V. Characterization of a novel trans-sialidase of Trypanosoma brucei procyclic trypomastigotes and identification of procyclin as the main sialic acid acceptor. J Exp Med 1993;177:465-74.
70. [70] Engstler M, Reuter G, Schauer R. The developmentally regulated trans-sialidase from Trypanosoma brucei sialylates the procyclic acidic repetitive protein. Mol Biochem Parasitol 1993;61:1-13.
71. [71] Clayton CE, Mowatt MR. The procyclic acid repetitive proteins of Trypanosoma brucei: purification and post-translational modification. J Biol Chem 1989;264:15088-93.
72. [72] Maudlin I, Welburn SC. Maturation of trypanosome infections in tsetse. Exp Parasitol 1994;79:202-5.
73. [73] Maudlin I, Welburn SC. The role of lectins and trypanosome genotype in the maturation of midgut infections in Glossina morsitans. Trop Med Parasitol 1988;39:56-8.
74. [74] Welburn S, Dale C, Ellis D, Beecroft R, Pearson TW. Apoptosis in procyclic Trypanosoma brucei rhodesiense in vitro. Cell Death Differ 1996;3:229-36.
75. [75] Ten Asbroek ALMA, Ouellette M, Borst P. Targeted insertion of the neomycin phosphotransferase gene into the tubulin gene cluster of Trypanosoma brucei. Nature 1990;348:174-5.
76. [76] Beecroft RP, Roditi I, Pearson TW. Identification and characterization of a major surface glycoprotein from procyclic stage Trypanosoma congolense. Mol Biochem Parasitol 1993;61:285-94.
77. [77] Hehl A, Pearson TW, Barry JD, Braun R, Roditi I. Expression of GARP, a major surface glycoprotein of Trypanosoma congolense, on the surface of Trypanosoma brucei: characterisation and use as a surface marker. Mol Biochem Parasitol 1995;70:45-58.
78. [78] Majiwa PAO, Masake RA, Nantulya VM, Hamers R, Matthyssens G. Trypanosoma (Nannomonas) congolense: identification of two karyotypic groups. EMBO J 1985;4:3307-13.
79. [79] Garside LH, Gibson WC. Molecular characterisation of trypanosome species and subgroups with subgenus Nannomonas. Parasitology 1995;111:301-12.