Social Motility of African Trypanosomes Is a Property of a Distinct Life-Cycle Stage That Occurs Early in Tsetse Fly Transmission

PLoS Pathogens

Volumn 10, Issue 10, 2014, Pages

  Imhof, Simon ^a   Knüsel, Sebastian ^a,b   Gunasekera, Kapila ^a   Vu, Xuan Lan ^a   Roditi, Isabel ^a  

^a UNIVERSITY OF BERN   (Switzerland)

^b BOSTON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENYLATE CYCLASE; HEXOKINASE; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE KINASE 1; GPEET PROTEIN, TRYPANOSOMA BRUCEI; MEMBRANE PROTEIN; PROTOZOAL PROTEIN;

ARTICLE; CELL DIFFERENTIATION; DOWN REGULATION; GENE EXPRESSION; GLOSSINIDAE; IMMUNOFLUORESCENCE; ISOTOPE LABELING; LIFE CYCLE STAGE; MASS SPECTROMETRY; MICROBIAL COLONIZATION; NONHUMAN; NORTHERN BLOTTING; PARASITE MIGRATION; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SALIVARY GLAND; TRYPANOSOMA; UPREGULATION; AFRICAN TRYPANOSOMIASIS; ANIMAL; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PARASITOLOGY; PHYSIOLOGY; TRANSMISSION; TRYPANOSOMA BRUCEI BRUCEI;

GLOSSINA (GENUS);

ANIMALS; GENE EXPRESSION REGULATION; LIFE CYCLE STAGES; MEMBRANE GLYCOPROTEINS; PROTOZOAN PROTEINS; SALIVARY GLANDS; TRYPANOSOMA BRUCEI BRUCEI; TRYPANOSOMIASIS, AFRICAN; TSETSE FLIES;

EID: 84908333490     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1004493     Document Type: Article

References (47)

1. Schwede A, Carrington M, (2010) Bloodstream form Trypanosome plasma membrane proteins: antigenic variation and invariant antigens. Parasitology 137: 2029–2039.
2. Reuner B, Vassella E, Yutzy B, Boshart M, (1997) Cell density triggers slender to stumpy differentiation of Trypanosoma brucei bloodstream forms in culture. Molecular and biochemical parasitology 90: 269–280.
3. Vassella E, Reuner B, Yutzy B, Boshart M, (1997) Differentiation of African trypanosomes is controlled by a density sensing mechanism which signals cell cycle arrest via the cAMP pathway. Journal of cell science 110 (Pt 21): 2661–2671.
4. Vassella E, Den Abbeele JV, Butikofer P, Renggli CK, Furger A, et al. (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.
5. Gibson W, Bailey M, (2003) The development of Trypanosoma brucei within the tsetse fly midgut observed using green fluorescent trypanosomes. Kinetoplastid Biol Dis 2: 1.
6. Vassella E, Oberle M, Urwyler S, Renggli CK, Studer E, et al. (2009) Major surface glycoproteins of insect forms of Trypanosoma brucei are not essential for cyclical transmission by tsetse. PLoS One 4: e4493.
7. Knüsel S, Roditi I, (2013) Insights into the regulation of GPEET procyclin during differentiation from early to late procyclic forms of Trypanosoma brucei. Molecular and biochemical parasitology 191: 66–74.
8. Roditi I, Furger A, Ruepp S, Schurch N, Butikofer P, (1998) Unravelling the procyclin coat of Trypanosoma brucei. Molecular and biochemical parasitology 91: 117–130.
9. Morris JC, Wang Z, Drew ME, Englund PT, (2002) Glycolysis modulates trypanosome glycoprotein expression as revealed by an RNAi library. The EMBO journal 21: 4429–4438.
10. Vassella E, Probst M, Schneider A, Studer E, Renggli CK, et al. (2004) Expression of a major surface protein of Trypanosoma brucei insect forms is controlled by the activity of mitochondrial enzymes. Molecular biology of the cell 15: 3986–3993.
11. Oberle M, Balmer O, Brun R, Roditi I, (2010) Bottlenecks and the maintenance of minor genotypes during the life cycle of Trypanosoma brucei. PLoS pathogens 6: e1001023.
12. Shapiro JA, (1998) Thinking about bacterial populations as multicellular organisms. Annual review of microbiology 52: 81–104.
13. Fraser GM, Hughes C, (1999) Swarming motility. Current opinion in microbiology 2: 630–635.
14. Harshey RM, (2003) Bacterial motility on a surface: many ways to a common goal. Annual review of microbiology 57: 249–273.
15. Bassler BL, Losick R, (2006) Bacterially speaking. Cell 125: 237–246.
16. Blankenship JR, Mitchell AP, (2006) How to build a biofilm: a fungal perspective. Current opinion in microbiology 9: 588–594.
17. Firtel RA, Meili R, (2000) Dictyostelium: a model for regulated cell movement during morphogenesis. Current opinion in genetics & development 10: 421–427.
18. Shaulsky G, Kessin RH, (2007) The cold war of the social amoebae. Current biology: CB 17: R684–692.
19. Lopez MA, Nguyen HT, Oberholzer M, Hill KL, (2011) Social parasites. Current opinion in microbiology 14: 642–648.
20. Oberholzer M, Lopez MA, McLelland BT, Hill KL, (2010) Social motility in African trypanosomes. PLoS Pathog 6: e1000739.
21. Freire ER, Vashisht AA, Malvezzi AM, Zuberek J, Langousis G, et al. (2014) eIF4F-like complexes formed by cap-binding homolog TbEIF4E5 with TbEIF4G1 or TbEIF4G2 are implicated in post-transcriptional regulation in Trypanosoma brucei. RNA
22. Vassella E, Probst M, Schneider A, Studer E, Renggli CK, et al. (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.
23. Schumann Burkard G, Kaser S, de Araujo PR, Schimanski B, Naguleswaran A, et al. (2013) Nucleolar proteins regulate stage-specific gene expression and ribosomal RNA maturation in Trypanosoma brucei. Molecular microbiology 88: 827–840.
24. Urwyler S, Vassella E, Van Den Abbeele J, Renggli CK, Blundell P, et al. (2005) Expression of procyclin mRNAs during cyclical transmission of Trypanosoma brucei. PLoS Pathog 1: e22.
25. Morand S, Renggli CK, Roditi I, Vassella E, (2012) MAP kinase kinase 1 (MKK1) is essential for transmission of Trypanosoma brucei by Glossina morsitans. Mol Biochem Parasitol 186: 73–76.
26. Fragoso CM, Schumann Burkard G, Oberle M, Renggli CK, Hilzinger K, et al. (2009) PSSA-2, a membrane-spanning phosphoprotein of Trypanosoma brucei, is required for efficient maturation of infection. PLoS One 4: e7074.
27. Nudleman E, Wall D, Kaiser D, (2005) Cell-to-cell transfer of bacterial outer membrane lipoproteins. Science 309: 125–127.
28. Vassella E, Butikofer P, Engstler M, Jelk J, Roditi I, (2003) Procyclin null mutants of Trypanosoma brucei express free glycosylphosphatidylinositols on their surface. Molecular biology of the cell 14: 1308–1318.
29. Emmer BT, Daniels MD, Taylor JM, Epting CL, Engman DM, (2010) Calflagin inhibition prolongs host survival and suppresses parasitemia in Trypanosoma brucei infection. Eukaryot Cell 9: 934–942.
30. Kolev NG, Ramey-Butler K, Cross GA, Ullu E, Tschudi C, (2012) Developmental progression to infectivity in Trypanosoma brucei triggered by an RNA-binding protein. Science 338: 1352–1353.
31. Rotureau B, Subota I, Buisson J, Bastin P, (2012) A new asymmetric division contributes to the continuous production of infective trypanosomes in the tsetse fly. Development 139: 1842–1850.
32. Acosta-Serrano A, Vassella E, Liniger M, Kunz Renggli C, Brun R, et al. (2001) The surface coat of procyclic Trypanosoma brucei: programmed expression and proteolytic cleavage of procyclin in the tsetse fly. Proc Natl Acad Sci U S A 98: 1513–1518.
33. Schlaeppi AC, Malherbe T, Bütikofer P, (2003) Coordinate expression of GPEET procyclin and its membrane-associated kinase in Trypanosoma brucei procyclic forms. The Journal of biological chemistry 278: 49980–49987.
34. Bütikofer P, Vassella E, Boschung M, Renggli CK, Brun R, et al. (2002) Glycosylphosphatidylinositol-anchored surface molecules of Trypanosoma congolense insect forms are developmentally regulated in the tsetse fly. Molecular and biochemical parasitology 119: 7–16.
35. Utz S, Roditi I, Kunz Renggli C, Almeida IC, Acosta-Serrano A, et al. (2006) Trypanosoma congolense procyclins: unmasking cryptic major surface glycoproteins in procyclic forms. Eukaryotic cell 5: 1430–1440.
36. Van Den Abbeele J, Claes Y, van Bockstaele D, Le Ray D, Coosemans M, (1999) Trypanosoma brucei spp. development in the tsetse fly: characterization of the post-mesocyclic stages in the foregut and proboscis. Parasitology 118 (Pt 5): 469–478.
37. Stevens JR, Mathieu-Daude F, McNamara JJ, Mizen VH, Nzila A, (1994) Mixed populations of Trypanosoma brucei in wild Glossina palpalis palpalis. Tropical medicine and parasitology: official organ of Deutsche Tropenmedizinische Gesellschaft and of Deutsche Gesellschaft fur Technische Zusammenarbeit 45: 313–318.
38. MacLeod A, Turner CM, Tait A, (1999) A high level of mixed Trypanosoma brucei infections in tsetse flies detected by three hypervariable minisatellites. Molecular and biochemical parasitology 102: 237–248.
39. Delauw MF, Pays E, Steinert M, Aerts D, Van Meirvenne N, et al. (1985) Inactivation and reactivation of a variant-specific antigen gene in cyclically transmitted Trypanosoma brucei. EMBO J 4: 989–993.
40. Le Ray D, Barry JD, Easton C, Vickerman K, (1977) First tsetse fly transmission of the “AnTat” serodeme of Trypanosoma brucei. Ann Soc Belg Med Trop 57: 369–381.
41. Brun R, Schonenberger (1979) Cultivation and in vitro cloning or procyclic culture forms of Trypanosoma brucei in a semi-defined medium. Short communication. Acta Trop 36: 289–292.
42. Ruepp S, Furger A, Kurath U, Renggli CK, Hemphill A, et al. (1997) Survival of Trypanosoma brucei in the tsetse fly is enhanced by the expression of specific forms of procyclin. J Cell Biol 137: 1369–1379.
43. Chomczynski P, Sacchi N, (1987) Single-step RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anan Biochem 162: 156–159.
44. Brun R, Schonenberger M, (1981) Stimulating effect of citrate and cis-Aconitate on the transformation of Trypanosoma brucei bloodstream forms to procyclic forms in vitro. Z Parasitenkd 66: 17–24.
45. Richardson JP, Beecroft RP, Tolson DL, Liu MK, Pearson TW, (1988) Procyclin: an unusual immunodominant glycoprotein surface antigen from the procyclic stage of African trypanosomes. Mol Biochem Parasitol 31: 203–216.
46. Gunasekera K, Wüthrich D, Braga-Lagache S, Heller M, Ochsenreiter T, (2012) Proteome remodelling during development from blood to insect-form Trypanosoma brucei quantified by SILAC and mass spectrometry. BMC Genomics 13: 556.
47. Flück C, Salomone JY, Kurath U, Roditi I, (2003) Cycloheximide-mediated accumulation of transcripts from a procyclin expression site depends on the intergenic region. Mol Biochem Parasitol 127: 93–97.