Carbohydrate-binding agents act as potent trypanocidals that elicit modifications in VSG glycosylation and reduced virulence in Trypanosoma brucei

Molecular Microbiology

Volumn 90, Issue 4, 2013, Pages 665-679

  Castillo Acosta, Víctor M ^a   Vidal, Antonio E ^a   Ruiz Pérez, Luis M ^a   Van Damme, Els J M ^b   Igarashi, Yasuhiro ^c   Balzarini, Jan ^d   González Pacanowska, Dolores ^a  

^a INSTITUTO DE PARASITOLOGÍA Y BIOMEDICINA LÓPEZ NEYRA   (Spain)

^b GHENT UNIVERSITY   (Belgium)

^c TOYAMA PREFECTURAL UNIVERSITY   (Japan)

^d REGA INSTITUTE FOR MEDICAL RESEARCH   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

ANTITRYPANOSOMAL AGENT; CARBOHYDRATE BINDING AGENT; CYANOVIRIN N; DAFFODIL LECTIN; GLYCOPROTEIN; HELLEBORINE LECTIN; HIPPEASTRUM HYBRID AGGLUTININ; MANNOSE OLIGOSACCHARIDE; SNOWDROP LECTIN; STINGING NETTLE LECTIN; UNCLASSIFIED DRUG; VARIANT SURFACE GLYCOPROTEIN;

AFRICAN TRYPANOSOMIASIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIPROTOZOAL ACTIVITY; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; CYTOLYSIS; DRUG DESIGN; DRUG EXPOSURE; DRUG POTENCY; ENDOCYTOSIS; FEMALE; GENE; GENE EXPRESSION; GENE REARRANGEMENT; GROWTH INHIBITION; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PARASITE VIRULENCE; PRIORITY JOURNAL; PROTEIN GLYCOSYLATION; TBSTT3B GENE; TRYPANOSOMA BRUCEI;

HIPPEASTRUM; TRYPANOSOMA BRUCEI;

ANIMALS; CELL CYCLE; CELL LINE; DISEASE MODELS, ANIMAL; ENDOCYTOSIS; GLYCOSYLATION; HUMANS; LILIACEAE; MANNOSE-BINDING LECTINS; MANNOSYLTRANSFERASES; MICE; MICE, INBRED C57BL; TRYPANOCIDAL AGENTS; TRYPANOSOMA BRUCEI BRUCEI; TRYPANOSOMIASIS, AFRICAN; VARIANT SURFACE GLYCOPROTEINS, TRYPANOSOMA; VIRULENCE;

EID: 84887403734     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12359     Document Type: Article

References (45)

1. Allen, C.L., Goulding, D., and Field, M.C. (2003) Clathrin-mediated endocytosis is essential in Trypanosoma brucei. EMBO J 22: 4991-5002.
2. Atrih, A., Richardson, J.M., Prescott, A.R., and Ferguson, M.A. (2005) Trypanosoma brucei glycoproteins contain novel giant poly-N-acetyllactosamine carbohydrate chains. J Biol Chem 280: 865-871.
3. Balzarini, J. (2007) Targeting the glycans of glycoproteins: a novel paradigm for antiviral therapy. Nat Rev Microbiol 5: 583-597.
4. Balzarini, J., Schols, D., Neyts, J., Van Damme, E., Peumans, W., and De Clercq, E. (1991) Alpha-(1-3)- and alpha-(1-6)-D-mannose-specific plant lectins are markedly inhibitory to human immunodeficiency virus and cytomegalovirus infections in vitro. Antimicrob Agents Chemother 35: 410-416.
5. Balzarini, J., Neyts, J., Schols, D., Hosoya, M., Van Damme, E., Peumans, W., and De Clercq, E. (1992) The mannose-specific plant lectins from Cymbidium hybrid and Epipactis helleborine and the (N-acetylglucosamine)n-specific plant lectin from Urtica dioica are potent and selective inhibitors of human immunodeficiency virus and cytomegalovirus replication in vitro. Antiviral Res 18: 191-207.
6. Balzarini, J., Van Laethem, K., Daelemans, D., Hatse, S., Bugatti, A., Rusnati, M., etal. (2007) Pradimicin A, a carbohydrate-binding nonpeptidic lead compound for treatment of infections with viruses with highly glycosylated envelopes, such as human immunodeficiency virus. J Virol 81: 362-373.
7. Baral, T.N., Magez, S., Stijlemans, B., Conrath, K., Vanhollebeke, B., Pays, E., etal. (2006) Experimental therapy of African trypanosomiasis with a nanobody-conjugated human trypanolytic factor. Nat Med 12: 580-584.
8. Blum, M.L., Down, J.A., Gurnett, A.M., Carrington, M., Turner, M.J., and Wiley, D.C. (1993) A structural motif in the variant surface glycoproteins of Trypanosoma brucei. Nature 362: 603-609.
9. Boyd, M.R., Gustafson, K.R., McMahon, J.B., Shoemaker, R.H., O'Keefe, B.R., Mori, T., etal. (1997) Discovery of cyanovirin-N, a novel human immunodeficiency virus-inactivating protein that binds viral surface envelope glycoprotein gp120: potential applications to microbicide development. Antimicrob Agents Chemother 41: 1521-1530.
10. Brickman, M.J., Cook, J.M., and Balber, A.E. (1995) Low temperature reversibly inhibits transport from tubular endosomes to a perinuclear, acidic compartment in African trypanosomes. J Cell Sci 108 (Part 11): 3611-3621.
11. Cardoso de Almeida, M.L., and Turner, M.J. (1983) The membrane form of variant surface glycoproteins of Trypanosoma brucei. Nature 302: 349-352.
12. Castillo-Acosta, V.M., Aguilar-Pereyra, F., Bart, J.M., Navarro, M., Ruiz-Perez, L.M., Vidal, A.E., and Gonzalez-Pacanowska, D. (2012) Increased uracil insertion in DNA is cytotoxic and increases the frequency of mutation, double strand break formation and VSG switching in Trypanosoma brucei. DNA Repair (Amst) 11: 986-995.
13. Cross, G.A. (1984) Release and purification of Trypanosoma brucei variant surface glycoprotein. J Cell Biochem 24: 79-90.
14. Denton, H., Fyffe, S., and Smith, T.K. (2010) GDP-mannose pyrophosphorylase is essential in the bloodstream form of Trypanosoma brucei. Biochem J 425: 603-614.
15. Engstler, M., Thilo, L., Weise, F., Grunfelder, C.G., Schwarz, H., Boshart, M., and Overath, P. (2004) Kinetics of endocytosis and recycling of the GPI-anchored variant surface glycoprotein in Trypanosoma brucei. J Cell Sci 117: 1105-1115.
16. Engstler, M., Pfohl, T., Herminghaus, S., Boshart, M., Wiegertjes, G., Heddergott, N., and Overath, P. (2007) Hydrodynamic flow-mediated protein sorting on the cell surface of trypanosomes. Cell 131: 505-515.
17. Field, M.C., and Carrington, M. (2009) The trypanosome flagellar pocket. Nat Rev Microbiol 7: 775-786.
18. Hall, B., Allen, C.L., Goulding, D., and Field, M.C. (2004) Both of the Rab5 subfamily small GTPases of Trypanosoma brucei are essential and required for endocytosis. Mol Biochem Parasitol 138: 67-77.
19. Hall, B.S., Smith, E., Langer, W., Jacobs, L.A., Goulding, D., and Field, M.C. (2005) Developmental variation in Rab11-dependent trafficking in Trypanosoma brucei. Eukaryot Cell 4: 971-980.
20. Hammarton, T.C. (2007) Cell cycle regulation in Trypanosoma brucei. Mol Biochem Parasitol 153: 1-8.
21. Izquierdo, L., Schulz, B.L., Rodrigues, J.A., Guther, M.L., Procter, J.B., Barton, G.J., etal. (2009) Distinct donor and acceptor specificities of Trypanosoma brucei oligosaccharyltransferases. EMBO J 28: 2650-2661.
22. Jones, D.C., Mehlert, A., Guther, M.L., and Ferguson, M.A. (2005) Deletion of the glucosidase II gene in Trypanosoma brucei reveals novel N-glycosylation mechanisms in the biosynthesis of variant surface glycoprotein. J Biol Chem 280: 35929-35942.
23. Kaku, H., Van Damme, E.J., Peumans, W.J., and Goldstein, I.J. (1990) Carbohydrate-binding specificity of the daffodil (Narcissus pseudonarcissus) and amaryllis (Hippeastrum hybr.) bulb lectins. Arch Biochem Biophys 279: 298-304.
24. Landeira, D., Bart, J.M., Van Tyne, D., and Navarro, M. (2009) Cohesin regulates VSG monoallelic expression in trypanosomes. J Cell Biol 186: 243-254.
25. Lillico, S., Field, M.C., Blundell, P., Coombs, G.H., and 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.
26. Manthri, S., Guther, M.L., Izquierdo, L., Acosta-Serrano, A., and Ferguson, M.A. (2008) Deletion of the TbALG3 gene demonstrates site-specific N-glycosylation and N-glycan processing in Trypanosoma brucei. Glycobiology 18: 367-383.
27. Morrison, L.J., Marcello, L., and McCulloch, R. (2009) Antigenic variation in the African trypanosome: molecular mechanisms and phenotypic complexity. Cell Microbiol 11: 1724-1734.
28. Naismith, J.H., and Field, R.A. (1996) Structural basis of trimannoside recognition by concanavalin A. J Biol Chem 271: 972-976.
29. O'Beirne, C., Lowry, C.M., and Voorheis, H.P. (1998) Both IgM and IgG anti-VSG antibodies initiate a cycle of aggregation-disaggregation of bloodstream forms of Trypanosoma brucei without damage to the parasite. Mol Biochem Parasitol 91: 165-193.
30. Overath, P., and Engstler, M. (2004) Endocytosis, membrane recycling and sorting of GPI-anchored proteins: Trypanosoma brucei as a model system. Mol Microbiol 53: 735-744.
31. Pal, A., Hall, B.S., Jeffries, T.R., and Field, M.C. (2003) Rab5 and Rab11 mediate transferrin and anti-variant surface glycoprotein antibody recycling in Trypanosoma brucei. Biochem J 374: 443-451.
32. Pearson, T.W., Beecroft, R.P., Welburn, S.C., Ruepp, S., Roditi, I., Hwa, K.Y., etal. (2000) The major cell surface glycoprotein procyclin is a receptor for induction of a novel form of cell death in African trypanosomes in vitro. Mol Biochem Parasitol 111: 333-349.
33. Perez-Moreno, G., Sealey-Cardona, M., Rodrigues-Poveda, C., Gelb, M.H., Ruiz-Perez, L.M., Castillo-Acosta, V., etal. (2012) Endogenous sterol biosynthesis is important for mitochondrial function and cell morphology in procyclic forms of Trypanosoma brucei. Int J Parasitol 42: 975-989.
34. Peumans, W.J., de Ley, M., and Broekaert, W.F. (1984) An unusual lectin from stinging nettle (Urtica dioica) rhizomes. FEBS Lett 177: 99-103.
35. Pfaffl, M.W. (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29: e45.
36. Russo, D.C., Williams, D.J., and Grab, D.J. (1994) Mechanisms for the elimination of potentially lytic complement-fixing variable surface glycoprotein antibody-complexes in Trypanosoma brucei. Parasitol Res 80: 487-492.
37. Schwartz, K.J., Peck, R.F., and Bangs, J.D. (2013) Intracellular trafficking and glycobiology of TbPDI2, a stage-specific protein disulfide isomerase in Trypanosoma brucei. Eukaryot Cell 12: 132-141.
38. Stijlemans, B., Conrath, K., Cortez-Retamozo, V., Van Xong, H., Wyns, L., Senter, P., etal. (2004) Efficient targeting of conserved cryptic epitopes of infectious agents by single domain antibodies. African trypanosomes as paradigm. J Biol Chem 279: 1256-1261.
39. Stijlemans, B., Caljon, G., Natesan, S.K., Saerens, D., Conrath, K., Perez-Morga, D., etal. (2011) High affinity nanobodies against the Trypanosome brucei VSG are potent trypanolytic agents that block endocytosis. PLoS Pathog 7: e1002072.
40. Stokes, M.J., Guther, M.L., Turnock, D.C., Prescott, A.R., Martin, K.L., Alphey, M.S., and Ferguson, M.A. (2008) The synthesis of UDP-N-acetylglucosamine is essential for bloodstream form Trypanosoma brucei in vitro and in vivo and UDP-N-acetylglucosamine starvation reveals a hierarchy in parasite protein glycosylation. J Biol Chem 283: 16147-16161.
41. Van Damme, E.J.M., Allen, A.K., and Peumans, W.J. (1987) Isolation and characterization of a lectin with exclusive specificity toward mannose from snowdrop (Galanthus nivalis) bulbs. FEBS Lett 215: 140-144.
42. Van Damme, E.J.M., Allen, A.K., and Peumans, W.J. (1988) Related mannose-specific lectins from different species of the family Amaryllidaceae. Plant Physiol 73: 51-57.
43. Wirtz, E., Leal, S., Ochatt, C., and Cross, G.A. (1999) A tightly regulated inducible expression system for conditional gene knock-outs and dominant-negative genetics in Trypanosoma brucei. Mol Biochem Parasitol 99: 89-101.
44. Ziegelbauer, K., and Overath, P. (1992) Identification of invariant surface glycoproteins in the bloodstream stage of Trypanosoma brucei. J Biol Chem 267: 10791-10796.
45. Zitzmann, N., Mehlert, A., Carrouee, S., Rudd, P.M., and Ferguson, M.A. (2000) Protein structure controls the processing of the N-linked oligosaccharides and glycosylphosphatidylinositol glycans of variant surface glycoproteins expressed in bloodstream form Trypanosoma brucei. Glycobiology 10: 243-249.