The Protein Journal

, Volume 38, Issue 1, pp 50–57 | Cite as

Trans-sialidase Protein as a Potential Serological Marker for African Trypanosomiasis

  • Ana Filipa Teixeira
  • João Gomes Pereira
  • Sónia Pestana-Ascensão
  • Marcelo Sousa SilvaEmail author


Trypanosoma brucei is the etiological agent of African trypanosomiasis responsible for human and animal infections. T. brucei is transmitted by infected tsetse flies. There is no vaccine for the disease and drugs available for treatment are inefficient and high toxicity. In this context, it is a priority to find antigenic targets suitable for the development of new diagnostic tools, drugs and vaccines. In this work, we report that mice infected with T. b. brucei produce antibodies against trans-sialidase recombinant protein (TS). In addition, we also demonstrate that bloodstream T. b. brucei express messenger RNA related to the TS gene. Collectively, our data strongly suggest that bloodstream forms of T. b. brucei also express the TS gene, that to date was described only in the procyclic forms of the T. b. brucei. In conclusion, these results highlight the importance of TS protein as a possible antigen target during infection caused by T. b. brucei.


Trans-sialidase Trypanosoma brucei African trypanosomiasis Antigenic targets Serological markers 



Thanks to Global Health and Tropical Medicine (GHTM-UID/multi/04413/2013) by support and the Programa Ciências Sem Fronteiras, Capes—Brazil (Grant No. 019/2013). We are also grateful to Paulo Fanado for editing this manuscript.

Author Contributions

Conceived and designed the experiments: AFT and MSS; Performed the experiments: AFT, JGP, and SPA; Analysed the data: AFT, JGP, SPA, and MSS; Wrote the paper: AFT and MSS. All authors read and approved the final version of the manuscript.

Compliance with Ethical Standards

Conflict of interest

The authors declare no conflict of interest.

Ethics Approval

Murine model was performed in accordance with existing legislation in Portugal and in accordance of the Ethical Committee at Institute of Hygiene and Tropical Medicine, Lisbon—Portugal.


  1. 1.
    Matthews KR, Ellis JR, Paterou A (2004) Molecular regulation of the life cycle of African trypanosomes. Trends Parasitol 20(1):40–47Google Scholar
  2. 2.
    Cardoso de Almeida ML, Turner MJ (1983) The membrane form of variant surface glycoproteins of Trypanosoma brucei. Nature 302(5906):349–352Google Scholar
  3. 3.
    Ponte-Sucre A (2016) An overview of Trypanosoma brucei infections: an intense host-parasite interaction. Front Microbiol 7(2126):1–12Google Scholar
  4. 4.
    Montagna GN, Donelson JE, Frasch AC (2006) Procyclic Trypanosoma brucei expresses separate sialidase and trans-sialidase enzymes on its surface membrane. J Biol Chem 281(45):33949–33958Google Scholar
  5. 5.
    Montagna G, Cremona ML, Paris G, Amaya MF, Buschiazzo A, Alzari PM, Frasch AC (2002) The trans-sialidase from the African trypanosome Trypanosoma brucei. Eur J Biochem 269(12):2941–2950Google Scholar
  6. 6.
    Engstler M, Reuter G, Schauer R (1993) The developmentally regulated trans-sialidase from Trypanosoma brucei sialylates the procyclic acidic repetitive protein. Mol Biochem Parasitol 61(1):1–13Google Scholar
  7. 7.
    Pontes de Carvalho, LC, Tomlinson S, Vandekerckhove F, Bienen EJ, Clarkson AB, Jiang MS, Hart GW, Nussenzweig V (1993) Characterization of a novel trans-sialidase of Trypanosoma brucei procyclic trypomastigotes and identification of procyclin as the main sialic acid acceptor. J Exp Med 177(2):465–474Google Scholar
  8. 8.
    Schenkman S, Jiang MS, Hart GW, Nussenzweig V (1991) A novel cell surface trans-sialidase of Trypanosoma cruzi generates a stage-specific epitope required for invasion of mammalian cells. Cell 65(7):1117–1125Google Scholar
  9. 9.
    Schankman S, Eichinger D (1993) Trypanosoma cruzi trans-sialidase and cell invasion. Parasitol Today 9(6):218–222Google Scholar
  10. 10.
    Egima CM, Briones MR, Freitas Júnior LH, Schenkman RP, Uemura H, Schenkman S (1996) Organizaton of trans-sialidase genes in Trypanosoma cruzi. Mol Biochem Parasitol 77(2):115–125Google Scholar
  11. 11.
    Rubin-de-Celis SS, Uemura H, Yoshida N, Schenkman S (2006) Expression of trypomastigote trans-sialidase in metacyclic forms of Trypanosoma cruzi increases parasite escape from its parasitophorous vacuole. Cell Microbiol 8(12):1888–1898Google Scholar
  12. 12.
    Perreira-Chioccola VL, Fragata-Filho AA, Levy AM, Rodrigues MM, Schenkman S (2003) Enzyme-linked immunoassay using recombinant trans-sialidase of Trypanosoma cruzi can be employed for monitoring of patients with Chagas’ disease after drug treatment. Clin Diagn Lab Immunol 10(5):826–830Google Scholar
  13. 13.
    Ribeirão M, Pereira-Chioccola VL, Rénia L, Filho AF, Schenkman S, Rodrigues MM (2000) Chagasic patients develop a type 1 immune response to Trypanosoma cruzi trans-sialidase. Parasite Immunol 22(1):49–53Google Scholar
  14. 14.
    Costa F, Franchin G, Pereira-Chioccola VL, Ribeirão M, Schenkman S, Rodrigues MM (1998) Immunization with a plasmid DNA containing the gene of trans-sialidase reduces Trypanosoma cruzi infection in mice. Vaccine 16(8):768–774Google Scholar
  15. 15.
    Schauer R, Kamerling JP (2011) The chemistry and biology of trypanosomal trans-sialidases: virulence factor in Chagas disease and sleeping sickness. Chembiochem 12(15):2246–2264Google Scholar
  16. 16.
    Engstler M, Schauer R, Brun R (1995) Distribution of developmentally regulated trans-sialidases in the Kinetoplastida and characterization of a shed trans-sialidase activity from procyclic Trypanosoma congolense. Acta Trop 59(2):117–129Google Scholar
  17. 17.
    Tiralongo E, Martensen I, Grötzinger J, Tiralongo J, Schauer R (2003) Trans-sialidase-like sequences from Trypanosoma congolense conserve most of the critical active site residues found in other trans-sialidases. Biol Chem 384(8):1203–1213Google Scholar
  18. 18.
    Tiralongo E, Schrader S, Lange H, Lemke H, Tiralongo J, Schauer R (2003) Two trans-sialidase forms with different sialic acid transfer and sialidase activities from Trypanosoma congolense. J Biol Chem 278(26):23301–23310Google Scholar
  19. 19.
    Ammar Z, Plazolles N, Baltz T, Coustou V (2013) Identification of trans-sialidases as a common mediator of endothelial cell activation by African trypanosomes. PloS Pathog 9(10):e1003710. Google Scholar
  20. 20.
    Silva MS, Prazeres DM, Lança A, Atouguia J, Monteiro GA (2009) Trans-sialidase from Trypanosoma brucei as a potential target for DNA vaccine development against African trypanosomiasis. Parasitol Res 105(5):1223–1229Google Scholar
  21. 21.
    World Health Organization (2007) Report of a WHO informal consultation on sustainable control of human African trypanosomiasis. Geneva, SwitzerlandGoogle Scholar
  22. 22.
    Giordani F, Morrison LJ, Rowan TG, Koning DE, Barrett HP, M. P (2016) The animal trypanosomiasis and their chemotherapy: a review. Parasitology 143(14):1862–1889Google Scholar
  23. 23.
    Lejon V, Jacobs J, Simarro PP (2013) Elimination of sleeping sickness hindered by difficult diagnosis. Bull World Health Organ 91(10):718Google Scholar
  24. 24.
    Nakatani F, Morita YS, Ashida H, Nagamune K, Maeda Y, Kinoshita T (2011) Identification of a second catalytically active trans-sialidase in Trypanosoma brucei. Biochem Biophys Res Commun 415(2):421–425Google Scholar
  25. 25.
    Tribulatti MV, Mucci J, Van Rooijen N, Leguizamón MS, Campetella O (2005) The trans-sialidase from Trypanosoma cruzi induces thrombocytopenia during acute Chagas’disease by reducing the platelet sialic acid contents. Infect Immun 74(1):201–207Google Scholar
  26. 26.
    Nagamune K, Acosta-Serrano A, Uemura H, Brun R, Kunz-Renggli C, Maeda Y, Ferguson MA, Kinoshita T (2004) Surface sialic acids taken from the host allow trypanosome survival in tsetse fly vectors. J Exp Med 199(10):1445–1450Google Scholar
  27. 27.
    Jennings FW (1993) Combination chemotherapy of CNS trypanosomiasis. Acta Trop 54:205–213Google Scholar
  28. 28.
    Lança AS, de Sousa KP, Atouguia J, Prazeres DM, Monteiro GA, Silva MS (2011) Trypanosoma brucei: immunisation with plasmid DNA encoding invariant surface glycoprotein gene is able to induce partial protection in experimental African trypanosomiasis. Exp Parasitol 127(1):18–24Google Scholar
  29. 29.
    de Sousa KP, Atouguia J, Silva MS (2010) Partial biochemical characterization of a metalloproteinase from the bloodstream forms of Trypanosoma brucei brucei parasites. Protein J 29(4):283–289Google Scholar
  30. 30.
    Retamal CA, Thiebaut P, Alves EW (1999) Protein purification from polyacrylamide gels by sonication extraction. Anal Biochem 268:15–20Google Scholar
  31. 31.
    Lanham SM, Godfrey DG (1970) Isolation of salivarian trypanosomes from man and other mammals using DEAE-cellulose. Exp Parasitol 28(3):521–534Google Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Global Health and Tropical Medicine, Institute of Hygiene and Tropical MedicineUniversidade Nova de LisboaLisbonPortugal
  2. 2.Immunoparasitology Laboratory, Department of Clinical and Toxicological AnalysisFederal University of Rio Grande do NorteNatalBrazil
  3. 3.Programa de Pós-graduação em Bioquímica, Centro de BiociênciasFederal University of Rio Grande do NorteNatalBrazil
  4. 4.Programa de Pós-graduação em Ciências Farmacêuticas, Centro de Ciências da SaúdeFederal University of Rio Grande do NorteNatalBrazil

Personalised recommendations