Extracellular Vesicles from Trypanosoma brucei Mediate Virulence Factor Transfer and Cause Host Anemia

Cell

Volumn 164, Issue 1-2, 2016, Pages 246-257

  Szempruch, Anthony J ^a   Sykes, Steven E ^a   Kieft, Rudo ^a   Dennison, Lauren ^a   Becker, Allison C ^a   Gartrell, Anzio ^a   Martin, William J ^b   Nakayasu, Ernesto S ^c   Almeida, Igor C ^d   Hajduk, Stephen L ^a   Harrington, John M ^a  

^a University of Georgia ^*  (United States)

^b UNIVERSITY OF GEORGIA   (United States)

^c PACIFIC NORTHWEST NATIONAL LABORATORY   (United States)

^d UNIVERSITY OF TEXAS AT EL PASO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENYLATE CYCLASE; GLYCEROL KINASE; GLYCOSYLPHOSPHATIDYLINOSITOL DIACYLGLYCEROL LYASE; NANOTUBE; VARIANT SURFACE GLYCOPROTEIN; VIRULENCE FACTOR; MEMBRANE PROTEIN; OCTADECYL RHODAMINE B CHLORIDE; PROTEOME; PROTOZOAL PROTEIN; RHODAMINE; SERUM RESISTANCE ASSOCIATED PROTEIN, TRYPANOSOMA BRUCEI;

AFRICAN TRYPANOSOMIASIS; ANEMIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL COMMUNICATION; CELL ORGANELLE; COCULTURE; CONTROLLED STUDY; ENDOCYTOSIS; ERYTHROCYTE CLEARANCE; ERYTHROCYTE GHOST; ERYTHROCYTE MEMBRANE; ERYTHROCYTE PARAMETERS; ERYTHROCYTE VOLUME; EX VIVO STUDY; EXOSOME; FEMALE; FLOW CYTOMETRY; HOST CELL; HOST PATHOGEN INTERACTION; HUMAN; HUMAN CELL; INNATE IMMUNITY; INTERNALIZATION; LIPID BILAYER; LIPID COMPOSITION; LIPID MEMBRANE; LIPID TRANSPORT; MOUSE; NONHUMAN; PARASITE VIRULENCE; PRIORITY JOURNAL; PROTEIN TRANSPORT; QUORUM SENSING; SURFACE PROPERTY; TRYPANOSOMA BRUCEI; WESTERN BLOTTING; ANIMAL; CYTOLOGY; ERYTHROCYTE; FLAGELLUM; IMMUNE EVASION; IMMUNOLOGY; METABOLISM; PARASITOLOGY; PATHOGENICITY; PATHOLOGY; TRYPANOSOMA BRUCEI RHODESIENSE;

ANEMIA; ANIMALS; ERYTHROCYTES; EXTRACELLULAR VESICLES; FLAGELLA; HUMANS; IMMUNE EVASION; MEMBRANE GLYCOPROTEINS; MICE; PROTEOME; PROTOZOAN PROTEINS; RHODAMINES; TRYPANOSOMA BRUCEI RHODESIENSE; TRYPANOSOMIASIS, AFRICAN; VIRULENCE FACTORS;

EID: 84954285538     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2015.11.051     Document Type: Article

References (46)

1. B. Babudieri, and N. Tomasini Fine struttura dei trypanosomi Parassitologia 4 1962 89 95
2. E. Bayer-Santos, C. Aguilar-Bonavides, S.P. Rodrigues, E.M. Cordero, A.F. Marques, A. Varela-Ramirez, H. Choi, N. Yoshida, J.F. da Silveira, and I.C. Almeida Proteomic analysis of Trypanosoma cruzi secretome: characterization of two populations of extracellular vesicles and soluble proteins J. Proteome Res. 12 2013 883 897
3. R. Broadhead, H.R. Dawe, H. Farr, S. Griffiths, S.R. Hart, N. Portman, M.K. Shaw, M.L. Ginger, S.J. Gaskell, P.G. McKean, and K. Gull Flagellar motility is required for the viability of the bloodstream trypanosome Nature 440 2006 224 227
4. C. De Greef, and R. Hamers The serum resistance-associated (SRA) gene of Trypanosoma brucei rhodesiense encodes a variant surface glycoprotein-like protein Mol. Biochem. Parasitol. 68 1994 277 284
5. G.P. Dubey, and S. Ben-Yehuda Intercellular nanotubes mediate bacterial communication Cell 144 2011 590 600
6. D.S. Ellis, W.E. Ormerod, and W.H. Lumsden Filaments of Trypanosoma brucei: some notes on differences in origin and structure in two strains of Trypanosoma (Trypanozoon) brucei rhodesiense Acta Trop. 33 1976 151 168
7. B.T. Emmer, M.D. Daniels, J.M. Taylor, C.L. Epting, and D.M. Engman Calflagin inhibition prolongs host survival and suppresses parasitemia in Trypanosoma brucei infection Eukaryot. Cell 9 2010 934 942
8. A.G. Evans, H.M. Davey, A. Cookson, H. Currinn, G. Cooke-Fox, P.J. Stanczyk, and D.E. Whitworth Predatory activity of Myxococcus xanthus outer-membrane vesicles and properties of their hydrolase cargo Microbiology 158 2012 2742 2752
9. B. Fevrier, D. Vilette, F. Archer, D. Loew, W. Faigle, M. Vidal, H. Laude, and G. Raposo Cells release prions in association with exosomes Proc. Natl. Acad. Sci. USA 101 2004 9683 9688
10. U. Frevert, and E. Reinwald Formation of filopodia in Trypanosoma congolense by crosslinking the variant surface antigen J. Ultrastruct. Mol. Struct. Res. 99 1988 124 136
11. W. Gibson, L. Peacock, V. Ferris, K. Fischer, J. Livingstone, J. Thomas, and M. Bailey Genetic recombination between human and animal parasites creates novel strains of human pathogen PLoS Negl. Trop. Dis. 9 2015 e0003665
12. M.L. Güther, M.D. Urbaniak, A. Tavendale, A. Prescott, and M.A. Ferguson High-confidence glycosome proteome for procyclic form Trypanosoma brucei by epitope-tag organelle enrichment and SILAC proteomics J. Proteome Res. 13 2014 2796 2806
13. W.J. Herbert, and W.H. Lumsden Trypanosoma brucei: a rapid "matching" method for estimating the host's parasitemia Exp. Parasitol. 40 1976 427 431
14. B.C. Jensen, G. Ramasamy, E.J. Vasconcelos, N.T. Ingolia, P.J. Myler, and M. Parsons Extensive stage-regulation of translation revealed by ribosome profiling of Trypanosoma brucei BMC Genomics 15 2014 911
15. J.R. Kremer, D.N. Mastronarde, and J.R. McIntosh Computer visualization of three-dimensional image data using IMOD J. Struct. Biol. 116 1996 71 76
16. S. Magez, A. Schwegmann, R. Atkinson, F. Claes, M. Drennan, P. De Baetselier, and F. Brombacher The role of B-cells and IgM antibodies in parasitemia, anemia, and VSG switching in Trypanosoma brucei-infected mice PLoS Pathog. 4 2008 e1000122
17. P.Y. Mantel, A.N. Hoang, I. Goldowitz, D. Potashnikova, B. Hamza, I. Vorobjev, I. Ghiran, M. Toner, D. Irimia, A.R. Ivanov, and et al. Malaria-infected erythrocyte-derived microvesicles mediate cellular communication within the parasite population and with the host immune system Cell Host Microbe 13 2013 521 534
18. A. Marcilla, L. Martin-Jaular, M. Trelis, A. de Menezes-Neto, A. Osuna, D. Bernal, C. Fernandez-Becerra, I.C. Almeida, and H.A. Del Portillo Extracellular vesicles in parasitic diseases J. Extracell. Vesicles 3 2014 25040
19. B.M. Mony, P. MacGregor, A. Ivens, F. Rojas, A. Cowton, J. Young, D. Horn, and K. Matthews Genome-wide dissection of the quorum sensing signalling pathway in Trypanosoma brucei Nature 505 2014 681 685
20. J. Naessens Bovine trypanotolerance: A natural ability to prevent severe anaemia and haemophagocytic syndrome? Int. J. Parasitol. 36 2006 521 528
21. M. Oberholzer, M.A. Lopez, B.T. McLelland, and K.L. Hill Social motility in african trypanosomes PLoS Pathog. 6 2010 e1000739
22. M. Oberholzer, G. Langousis, H.T. Nguyen, E.A. Saada, M.M. Shimogawa, Z.O. Jonsson, S.M. Nguyen, J.A. Wohlschlegel, and K.L. Hill Independent analysis of the flagellum surface and matrix proteomes provides insight into flagellum signaling in mammalian-infectious Trypanosoma brucei Mol. Cell. Proteomics 10 2011 M111.010538
23. M.W. Oli, L.F. Cotlin, A.M. Shiflett, and S.L. Hajduk Serum resistance-associated protein blocks lysosomal targeting of trypanosome lytic factor in Trypanosoma brucei Eukaryot. Cell 5 2006 132 139
24. A.K. Panigrahi, Y. Ogata, A. Zíková, A. Anupama, R.A. Dalley, N. Acestor, P.J. Myler, and K.D. Stuart A comprehensive analysis of Trypanosoma brucei mitochondrial proteome Proteomics 9 2009 434 450
25. W.R. Proto, E. Castanys-Munoz, A. Black, L. Tetley, C.X. Moss, L. Juliano, G.H. Coombs, and J.C. Mottram Trypanosoma brucei metacaspase 4 is a pseudopeptidase and a virulence factor J. Biol. Chem. 286 2011 39914 39925
26. N. Regev-Rudzki, D.W. Wilson, T.G. Carvalho, X. Sisquella, B.M. Coleman, M. Rug, D. Bursac, F. Angrisano, M. Gee, A.F. Hill, and et al. Cell-cell communication between malaria-infected red blood cells via exosome-like vesicles Cell 153 2013 1120 1133
27. J.P. Remis, D. Wei, A. Gorur, M. Zemla, J. Haraga, S. Allen, H.E. Witkowska, J.W. Costerton, J.E. Berleman, and M. Auer Bacterial social networks: structure and composition of Myxococcus xanthus outer membrane vesicle chains Environ. Microbiol. 16 2014 598 610
28. M.R. Rifkin, and F.R. Landsberger Trypanosome variant surface glycoprotein transfer to target membranes: a model for the pathogenesis of trypanosomiasis Proc. Natl. Acad. Sci. USA 87 1990 801 805
29. D. Salmon, G. Vanwalleghem, Y. Morias, J. Denoeud, C. Krumbholz, F. Lhommé, S. Bachmaier, M. Kador, J. Gossmann, F.B. Dias, and et al. Adenylate cyclases of Trypanosoma brucei inhibit the innate immune response of the host Science 337 2012 463 466
30. E. Schepilewsky Fadenförmige Anhängsel bei den Trypanosomen. Zentralblatt fur Bakteriologie, Parasitenkunde Infektionskrankheiten und Hygiene 65 1912 79 83
31. J.S. Schorey, Y. Cheng, P.P. Singh, and V.L. Smith Exosomes and other extracellular vesicles in host-pathogen interactions EMBO Rep. 16 2015 24 43
32. J.M. Silverman, J. Clos, C.C. de'Oliveira, O. Shirvani, Y. Fang, C. Wang, L.J. Foster, and N.E. Reiner An exosome-based secretion pathway is responsible for protein export from Leishmania and communication with macrophages J. Cell Sci. 123 2010 842 852
33. N.A. Stephens, and S.L. Hajduk Endosomal localization of the serum resistance-associated protein in African trypanosomes confers human infectivity Eukaryot. Cell 10 2011 1023 1033
34. B. Stijlemans, J. Cnops, P. Naniima, A. Vaast, V. Bockstal, P. De Baetselier, and S. Magez Development of a pHrodo-based assay for the assessment of in vitro and in vivo erythrophagocytosis during experimental trypanosomosis PLoS Negl. Trop. Dis. 9 2015 e0003561
35. S. Sykes, A. Szempruch, and S. Hajduk The krebs cycle enzyme α-ketoglutarate decarboxylase is an essential glycosomal protein in bloodstream African trypanosomes Eukaryot. Cell 14 2015 206 215
36. P. Truc, P. Büscher, G. Cuny, M.I. Gonzatti, J. Jannin, P. Joshi, P. Juyal, Z.R. Lun, R. Mattioli, E. Pays, and et al. Atypical human infections by animal trypanosomes PLoS Negl. Trop. Dis. 7 2013 e2256
37. O. Twu, N. de Miguel, G. Lustig, G.C. Stevens, A.A. Vashisht, J.A. Wohlschlegel, and P.J. Johnson Trichomonas vaginalis exosomes deliver cargo to host cells and mediate hostτparasite interactions PLoS Pathog. 9 2013 e1003482
38. L. Vanhamme, F. Paturiaux-Hanocq, P. Poelvoorde, D.P. Nolan, L. Lins, J. Van Den Abbeele, A. Pays, P. Tebabi, H. Van Xong, A. Jacquet, and et al. Apolipoprotein L-I is the trypanosome lytic factor of human serum Nature 422 2003 83 87
39. K. Vickerman, and A.G. Luckins Localization of variable antigens in the surface coat of Trypanosoma brucei using ferritin conjugated antibody Nature 224 1969 1125 1126
40. M. Vidal, and D. Hoekstra In vitro fusion of reticulocyte endocytic vesicles with liposomes J. Biol. Chem. 270 1995 17823 17829
41. H. Webb, N. Carnall, L. Vanhamme, S. Rolin, J. Van Den Abbeele, S. Welburn, E. Pays, and M. Carrington The GPI-phospholipase C of Trypanosoma brucei is nonessential but influences parasitemia in mice J. Cell Biol. 139 1997 103 114
42. C.R. Wood, and J.L. Rosenbaum Ciliary ectosomes: transmissions from the cell's antenna Trends Cell Biol. 25 2015 276 285
43. K.A. Wright, W.H. Lumsden, and H. Hales The formation of filopodium-like processes by Trypanosoma (Trypanozoon) brucei J. Cell Sci. 6 1970 285 297
44. H.V. Xong, L. Vanhamme, M. Chamekh, C.E. Chimfwembe, J. Van Den Abbeele, A. Pays, N. Van Meirvenne, R. Hamers, P. De Baetselier, and E. Pays A VSG expression site-associated gene confers resistance to human serum in Trypanosoma rhodesiense Cell 95 1998 839 846
45. M. Yáñez-Mó, P.R. Siljander, Z. Andreu, A.B. Zavec, F.E. Borràs, E.I. Buzas, K. Buzas, E. Casal, F. Cappello, J. Carvalho, and et al. Biological properties of extracellular vesicles and their physiological functions J. Extracell. Vesicles 4 2015 27066
46. A. Zomer, C. Maynard, F.J. Verweij, A. Kamermans, R. Schäfer, E. Beerling, R.M. Schiffelers, E. de Wit, J. Berenguer, S.I. Ellenbroek, and et al. In Vivo imaging reveals extracellular vesicle-mediated phenocopying of metastatic behavior Cell 161 2015 1046 1057