© The Rockefeller University Press,
0021-9525/1997//1369 $5.00
The Journal of Cell Biology, Volume 137, Number 6,
, 1997 1369-1379
Survival of Trypanosoma brucei in the Tsetse Fly Is Enhanced by the Expression of Specific Forms of Procyclin
Stefan Ruepp*,
André Furger*,
Ursula Kurath*,
Christina Kunz Renggli
,
Andrew Hemphill
,
Reto Brun
, and
Isabel Roditi*
* Institut für Allgemeine Mikrobiologie, Universität Bern, CH-3012 Bern, Switzerland;
Schweizerisches Tropeninstitut, CH-4051 Basel, Switzerland; and
Institut für Parasitologie, Universität Bern, CH-3012 Bern, Switzerland
African trypanosomes are not passively transmitted, but they undergo several rounds of differentiation and proliferation within their intermediate host, the tsetse fly. At each stage, the survival and successful replication of the parasites improve their chances of continuing the life cycle, but little is known about specific molecules that contribute to these processes. Procyclins are the major surface glycoproteins of the insect forms of Trypanosoma brucei. Six genes encode proteins with extensive glutamic acid–proline dipeptide repeats (EP in the single-letter amino acid code), and two genes encode proteins with an internal pentapeptide repeat (GPEET). To study the function of procyclins, we have generated mutants that have no EP genes and only one copy of GPEET. This last gene could not be replaced by EP procyclins, and could only be deleted once a second GPEET copy was introduced into another locus. The EP knockouts are morphologically indistinguishable from the parental strain, but their ability to establish a heavy infection in the insect midgut is severely compromised; this phenotype can be reversed by the reintroduction of a single, highly expressed EP gene. These results suggest that the two types of procyclin have different roles, and that the EP form, while not required in culture, is important for survival in the fly.
Abbreviations used in this paper: UTR, untranslated region; VSG, variant surface glycoproteins.
Please address all correspondence to I. Roditi, Institut für Allgemeine Mikrobiologie, Universität Bern, Baltzerstrasse 4, CH-3012 Bern, Switzerland. Tel.: (41) 31-631-4647. Fax: (41) 31-631-4684. e-mail: roditi{at}imb.unibe.ch

CiteULike
Complore
Connotea
Del.icio.us
Digg
Facebook
Reddit
Technorati
Twitter What's this?
This article has been cited by other articles:
-
Haenni, S., Studer, E., Burkard, G. S., Roditi, I.
(2009). Bidirectional silencing of RNA polymerase I transcription by a strand switch region in Trypanosoma brucei. Nucleic Acids Res
37: 5007-5018
[Abstract]
[Full Text]
-
Signorell, A., Jelk, J., Rauch, M., Butikofer, P.
(2008). Phosphatidylethanolamine Is the Precursor of the Ethanolamine Phosphoglycerol Moiety Bound to Eukaryotic Elongation Factor 1A. J. Biol. Chem.
283: 20320-20329
[Abstract]
[Full Text]
-
Utz, S., Roditi, I., Kunz Renggli, C., Almeida, I. C., Acosta-Serrano, A., Butikofer, P.
(2006). Trypanosoma congolense Procyclins: Unmasking Cryptic Major Surface Glycoproteins in Procyclic Forms.. Eukaryot Cell
5: 1430-1440
[Abstract]
[Full Text]
-
Domenicali Pfister, D., Burkard, G., Morand, S., Renggli, C. K., Roditi, I., Vassella, E.
(2006). A Mitogen-Activated Protein Kinase Controls Differentiation of Bloodstream Forms of Trypanosoma brucei.. Eukaryot Cell
5: 1126-1135
[Abstract]
[Full Text]
-
Hong, Y., Nagamune, K., Morita, Y. S., Nakatani, F., Ashida, H., Maeda, Y., Kinoshita, T.
(2006). Removal or Maintenance of Inositol-linked Acyl Chain in Glycosylphosphatidylinositol Is Critical in Trypanosome Life Cycle. J. Biol. Chem.
281: 11595-11602
[Abstract]
[Full Text]
-
Vassella, E., Probst, M., Schneider, A., Studer, E., Renggli, C. K., Roditi, I.
(2004). Expression of a Major Surface Protein of Trypanosoma brucei Insect Forms Is Controlled by the Activity of Mitochondrial Enzymes. Mol. Biol. Cell
15: 3986-3993
[Abstract]
[Full Text]
-
Leal, S., Acosta-Serrano, A., Morris, J., Cross, G. A. M.
(2004). Transposon Mutagenesis of Trypanosoma brucei Identifies Glycosylation Mutants Resistant to Concanavalin A. J. Biol. Chem.
279: 28979-28988
[Abstract]
[Full Text]
-
Nagamune, K., Acosta-Serrano, A., Uemura, H., Brun, R., Kunz-Renggli, C., Maeda, Y., Ferguson, M. A.J., Kinoshita, T.
(2004). Surface Sialic Acids Taken from the Host Allow Trypanosome Survival in Tsetse Fly Vectors. JEM
199: 1445-1450
[Abstract]
[Full Text]
-
Sheader, K., te Vruchte, D., Rudenko, G.
(2004). Bloodstream Form-specific Up-regulation of Silent VSG Expression Sites and Procyclin in Trypanosoma brucei after Inhibition of DNA Synthesis or DNA Damage. J. Biol. Chem.
279: 13363-13374
[Abstract]
[Full Text]
-
Acosta-Serrano, A., O'Rear, J., Quellhorst, G., Lee, S. H., Hwa, K.-Y., Krag, S. S., Englund, P. T.
(2004). Defects in the N-Linked Oligosaccharide Biosynthetic Pathway in a Trypanosoma brucei Glycosylation Mutant. Eukaryot Cell
3: 255-263
[Abstract]
[Full Text]
-
Schlaeppi, A.-C., Malherbe, T., Butikofer, P.
(2003). Coordinate Expression of GPEET Procyclin and Its Membrane-associated Kinase in Trypanosoma brucei Procyclic Forms. J. Biol. Chem.
278: 49980-49987
[Abstract]
[Full Text]
-
Gunzl, A., Bruderer, T., Laufer, G., Schimanski, B., Tu, L.-C., Chung, H.-M., Lee, P.-T., Lee, M. G.-S.
(2003). RNA Polymerase I Transcribes Procyclin Genes and Variant Surface Glycoprotein Gene Expression Sites in Trypanosoma brucei. Eukaryot Cell
2: 542-551
[Abstract]
[Full Text]
-
Vassella, E., Butikofer, P., Engstler, M., Jelk, J., Roditi, I.
(2003). Procyclin Null Mutants of Trypanosoma brucei Express Free Glycosylphosphatidylinositols on Their Surface. Mol. Biol. Cell
14: 1308-1318
[Abstract]
[Full Text]
-
Lillico, S., Field, M. C., Blundell, P., Coombs, G. H., Mottram, J. C.
(2003). Essential Roles for GPI-anchored Proteins in African Trypanosomes Revealed Using Mutants Deficient in GPI8. Mol. Biol. Cell
14: 1182-1194
[Abstract]
[Full Text]
-
Muller, I. B., Domenicali-Pfister, D., Roditi, I., Vassella, E.
(2002). Stage-specific Requirement of a Mitogen-activated Protein Kinase by Trypanosoma brucei. Mol. Biol. Cell
13: 3787-3799
[Abstract]
[Full Text]
-
BUTIKOFER, P., MALHERBE, T., BOSCHUNG, M., RODITI, I.
(2001). GPI-anchored proteins: now you see 'em, now you don't. FASEB J.
15: 545-548
[Abstract]
[Full Text]
-
Acosta-Serrano, A., Vassella, E., Liniger, M., Renggli, C. K., Brun, R., Roditi, I., Englund, P. T.
(2001). The surface coat of procyclic Trypanosoma brucei: Programmed expression and proteolytic cleavage of procyclin in the tsetse fly. Proc. Natl. Acad. Sci. USA
10.1073/pnas.041611698v1
[Abstract]
[Full Text]
-
Ferguson, M. A. J.
(2000). Glycosylphosphatidylinositol biosynthesis validated as a drug target for African sleeping sickness. Proc. Natl. Acad. Sci. USA
97: 10673-10675
[Full Text]
-
Nagamune, K., Nozaki, T., Maeda, Y., Ohishi, K., Fukuma, T., Hara, T., Schwarz, R. T., Sütterlin, C., Brun, R., Riezman, H., Kinoshita, T.
(2000). Critical roles of glycosylphosphatidylinositol for Trypanosoma brucei. Proc. Natl. Acad. Sci. USA
10.1073/pnas.180230697v1
[Abstract]
[Full Text]
-
Vassella, E., Den Abbeele, J. V., Bütikofer, P., Renggli, C. K., Furger, A., Brun, R., Roditi, I.
(2000). A major surface glycoprotein of Trypanosoma brucei is expressed transiently during development and can be regulated post-transcriptionally by glycerol or hypoxia. Genes Dev.
14: 615-626
[Abstract]
[Full Text]
-
Acosta-Serrano, A., Cole, R. N., Mehlert, A., Lee, M. G.-S., Ferguson, M. A. J., Englund, P. T.
(1999). The Procyclin Repertoire of Trypanosoma brucei. IDENTIFICATION AND STRUCTURAL CHARACTERIZATION OF THE GLU-PRO-RICH POLYPEPTIDES. J. Biol. Chem.
274: 29763-29771
[Abstract]
[Full Text]
-
Butikofer, P, Vassella, E, Ruepp, S, Boschung, M, Civenni, G, Seebeck, T, Hemphill, A, Mookherjee, N, Pearson, T., Roditi, I
(1999). Phosphorylation of a major GPI-anchored surface protein of Trypanosoma brucei during transport to the plasma membrane. J. Cell Sci.
112: 1785-1795
[Abstract]
-
Acosta-Serrano, A., Vassella, E., Liniger, M., Renggli, C. K., Brun, R., Roditi, I., Englund, P. T.
(2001). The surface coat of procyclic Trypanosoma brucei: Programmed expression and proteolytic cleavage of procyclin in the tsetse fly. Proc. Natl. Acad. Sci. USA
98: 1513-1518
[Abstract]
[Full Text]
-
Nagamune, K., Nozaki, T., Maeda, Y., Ohishi, K., Fukuma, T., Hara, T., Schwarz, R. T., Sutterlin, C., Brun, R., Riezman, H., Kinoshita, T.
(2000). Critical roles of glycosylphosphatidylinositol for Trypanosoma brucei. Proc. Natl. Acad. Sci. USA
97: 10336-10341
[Abstract]
[Full Text]