Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Opinion
  • Published:

The trypanolytic factor of human serum

Nature Reviews Microbiology volume 4, pages 477–486 (2006)Cite this article

Abstract

African trypanosomes (the prototype of which is Trypanosoma brucei brucei) are protozoan parasites that infect a wide range of mammals. Human blood, unlike the blood of other mammals, has efficient trypanolytic activity, and this needs to be counteracted by these parasites. Resistance to this activity has arisen in two subspecies of Trypanosoma brucei — Trypanosoma brucei rhodesiense and Trypanosoma brucei gambiense — allowing these parasites to infect humans, and this results in sleeping sickness in East Africa and West Africa, respectively. Study of the mechanism by which T. b. rhodesiense escapes lysis by human serum led to the identification of an ionic-pore-forming apolipoprotein — known as apolipoprotein L1 — that is associated with high-density-lipoprotein particles in human blood. In this Opinion article, we argue that apolipoprotein L1 is the factor that is responsible for the trypanolytic activity of human serum.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Life cycle of Trypanosoma brucei.
Figure 2: Antigenic variation and resistance to human serum of Trypanosoma brucei rhodesiense.
Figure 3: Models of the three domains of apolipoprotein L1 (APOL1).
Figure 4: Phenotype of trypanosome lysis by human serum or by recombinant apolipoprotein L1 (APOL1).
Figure 5: Model of the mechanism of trypanolysis by apolipoprotein L1 (APOL1).

Similar content being viewed by others

References

  1. Blum, M. L. et al. A structural motif in the variant surface glycoproteins of Trypanosoma brucei. Nature 362, 603–609 (1993).

    CAS  PubMed  Google Scholar 

  2. Cross, G. A. M. Antigenic variation in trypanosomes. Proc. R. Soc. Lond. B 202, 55–72 (1978).

    CAS  PubMed  Google Scholar 

  3. Barry, J. D. The relative significance of mechanisms of antigenic variation in African trypanosomes. Parasitol. Today 13, 212–218 (1997).

    CAS  PubMed  Google Scholar 

  4. Borst, P. Antigenic variation and allelic exclusion. Cell 109, 5–8 (2002).

    CAS  PubMed  Google Scholar 

  5. Pays, E., Vanhamme, L. & Pérez-Morga, D. Antigenic variation in Trypanosoma brucei: facts, challenges and mysteries. Curr. Opin. Microbiol. 7, 369–374 (2004).

    CAS  PubMed  Google Scholar 

  6. Laveran, A. & Mesnil, F. in Trypanosomes et Trypanosomiases 126–183 (Libraires de l'Académie de Médecine, Paris, 1912) (in French).

    Google Scholar 

  7. Seed, J. R., Sechelski, J. B. & Loomis, M. R. A survey for a trypanocidal factor in primate sera. J. Protozool. 37, 393–400 (1990).

    CAS  PubMed  Google Scholar 

  8. Poelvoorde, P., Vanhamme, L., Van Den Abbeele, J., Switzer, W. M. & Pays, E. Distribution of apolipoprotein L-I and trypanosome lytic activity among primate sera. Mol. Biochem. Parasitol. 134, 155–157 (2004).

    CAS  PubMed  Google Scholar 

  9. Lugli, E. B., Pouliot, M., Portela, M. P., Loomis, M. R. & Raper, J. Characterization of primate trypanosome lytic factors. Mol. Biochem. Parasitol. 138, 9–20 (2004).

    CAS  PubMed  Google Scholar 

  10. Rifkin, M. R. Identification of the trypanocidal factor in normal human serum: high density lipoprotein. Proc. Natl Acad. Sci. USA 75, 3450–3454 (1978).

    CAS  PubMed  PubMed Central  Google Scholar 

  11. Rifkin, M. R. Role of phospholipids in the cytotoxic action of high density lipoprotein on trypanosomes. J. Lipid Res. 32, 639–647 (1991).

    CAS  PubMed  Google Scholar 

  12. Hajduk, S. L. et al. Lysis of Trypanosoma brucei by a toxic subspecies of human high-density lipoprotein. J. Biol. Chem. 264, 5210–5217 (1989).

    CAS  PubMed  Google Scholar 

  13. Gillett, M. P. & Owen, J. S. Trypanosoma brucei brucei: differences in the trypanocidal activity of human plasma and its relationship to the level of high density lipoproteins. Trans. R. Soc. Trop. Med. Hyg. 85, 612–616 (1991).

    CAS  PubMed  Google Scholar 

  14. Gillett, M. P. & Owen, J. S. Comparison of the cytolytic effects in vitro on Trypanosoma brucei brucei of plasma, high density lipoproteins, and apolipoprotein A-I from hosts both susceptible (cattle and sheep) and resistant (human and baboon) to infection. J. Lipid Res. 33, 513–523 (1992).

    CAS  PubMed  Google Scholar 

  15. Lorenz, P., Owen, J. S. & Hassall, D. G. Human serum resistant Trypanosoma brucei rhodesiense accumulates similar amounts of fluorescently-labelled trypanolytic human HDL3 particles as human serum sensitive T. b. brucei. Mol. Biochem. Parasitol. 74, 113–118 (1995).

    CAS  PubMed  Google Scholar 

  16. Hager, K. M. et al. Endocytosis of a cytotoxic human high density lipoprotein results in disruption of acidic intracellular vesicles and subsequent killing of African trypanosomes. J. Cell Biol. 126, 155–167 (1994).

    CAS  PubMed  Google Scholar 

  17. Lorenz, P., Barth, P. E., Rudin, W. & Betschart, B. Importance of acidic intracellular compartments in the lysis of Trypanosoma brucei brucei by normal human serum. Trans. R. Soc. Trop. Med. Hyg. 88, 487–488 (1994).

    CAS  PubMed  Google Scholar 

  18. Ortiz-Ordonez, J. C., Sechelski, J. B. & Seed, J. R. Mechanism of lysis of Trypanosoma brucei gambiense by human serum. J. Parasitol. 80, 924–930 (1994).

    CAS  PubMed  Google Scholar 

  19. Hager, K. M. & Hajduk, S. L. Mechanism of resistance of African trypanosomes to cytotoxic human HDL. Nature 385, 823–826 (1997).

    CAS  PubMed  Google Scholar 

  20. Shimamura, M., Hager, K. M. & Hajduk, S. L. The lysosomal targeting and intracellular metabolism of trypanosome lytic factor by Trypanosoma brucei brucei. Mol. Biochem. Parasitol. 115, 227–237 (2001).

    CAS  PubMed  Google Scholar 

  21. Vanhamme, L. & Pays, E. The trypanosome lytic factor of human serum and the molecular basis of sleeping sickness. Int. J. Parasitol. 34, 887–898 (2004).

    CAS  PubMed  Google Scholar 

  22. Garcia-Salcedo, J. A. et al. A differential role for actin during the life cycle of Trypanosoma brucei. EMBO J. 23, 780–789 (2004).

    CAS  PubMed Central  PubMed  Google Scholar 

  23. Green, H. P., del Pilar Molina Portela, M., St Jean, E. N., Lugli, E. B. & Raper, J. Evidence for a Trypanosoma brucei lipoprotein scavenger receptor. J. Biol. Chem. 278, 422–427 (2003).

    CAS  PubMed  Google Scholar 

  24. Smith, A. B, Esko, J. D. & Hajduk, S. L. Killing of trypanosomes by the human haptoglobin-related protein. Science 268, 284–286 (1995).

    CAS  PubMed  Google Scholar 

  25. Raper, J., Nussenzweig, V. & Tomlinson, S. The main lytic factor of Trypanosoma brucei brucei in normal human serum is not high density lipoprotein. J. Exp. Med. 183, 1023–1029 (1996).

    CAS  PubMed  Google Scholar 

  26. Tomlinson, S., Muranjan, M., Nussenzweig, V. & Raper, J. Haptoglobin-related protein and apolipoprotein AI are components of the two trypanolytic factors in human serum. Mol. Biochem. Parasitol. 86, 117–120 (1997).

    CAS  PubMed  Google Scholar 

  27. Muranjan, M., Nussenzweig, V. & Tomlinson, S. Characterization of the human serum trypanosome toxin, haptoglobin-related protein. J. Biol. Chem. 273, 3884–3887 (1998).

    CAS  PubMed  Google Scholar 

  28. Rifkin, M. R. Trypanosoma brucei: cytotoxicity of host high-density lipoprotein is not mediated by apolipoprotein A-I. Exp. Parasitol. 72, 216–218 (1991).

    CAS  PubMed  Google Scholar 

  29. Owen, J. S., Gillett, M. P. & Hughes, T. E. Transgenic mice expressing human apolipoprotein A-I have sera with modest trypanolytic activity in vitro but remain susceptible to infection by Trypanosoma brucei brucei. J. Lipid Res. 33, 1639–1646 (1992).

    CAS  PubMed  Google Scholar 

  30. Tomlinson, S. et al. High-density-lipoprotein-independent killing of Trypanosoma brucei by human serum. Mol. Biochem. Parasitol. 70, 131–138 (1995).

    CAS  PubMed  Google Scholar 

  31. Smith, A. B. & Hajduk, S. L. Identification of haptoglobin as a natural inhibitor of trypanocidal activity in human serum. Proc. Natl Acad. Sci. USA 92, 10262–10266 (1995).

    CAS  PubMed  PubMed Central  Google Scholar 

  32. Raper, J., Nussenzweig, V. & Tomlinson, S. Lack of correlation between haptoglobin concentration and trypanolytic activity of normal human serum. Mol. Biochem. Parasitol. 76, 337–338 (1996).

    CAS  PubMed  Google Scholar 

  33. Raper, J., Fung, R., Ghiso, J., Nussenzweig, V. & Tomlinson, S. Characterization of a novel trypanosome lytic factor from human serum. Infect. Immun. 67, 1910–1916 (1999).

    CAS  PubMed Central  PubMed  Google Scholar 

  34. Barker, C., Barbour, K. W., Berger, F. G. & Hajduk, S. L. Activity of human trypanosome lytic factor in mice. Mol. Biochem. Parasitol. 117, 129–136 (2001).

    CAS  PubMed  Google Scholar 

  35. McEvoy, S. M. & Maeda, N. Complex events in the evolution of the haptoglobin gene cluster in primates. J. Biol. Chem. 263, 15740–15747 (1988).

    CAS  PubMed  Google Scholar 

  36. Drain, J., Bishop, J. R. & Hajduk, S. L. Haptoglobin-related protein mediates trypanosome lytic factor binding to trypanosomes. J. Biol. Chem. 276, 30254–30260 (2001).

    CAS  PubMed  Google Scholar 

  37. Bishop, J. R., Shimamura, M. & Hajduk, S. L. Insight into the mechanism of trypanosome lytic factor-1 killing of Trypanosoma brucei brucei. Mol. Biochem. Parasitol. 118, 33–40 (2001).

    CAS  PubMed  Google Scholar 

  38. Molina Portela, M. P., Raper, J. & Tomlinson, S. An investigation into the mechanism of trypanosome lysis by human serum factors. Mol. Biochem. Parasitol. 110, 273–282 (2000).

    CAS  PubMed  Google Scholar 

  39. Van Meirvenne, N., Magnus, E. & Janssens, P. G. The effect of normal human serum on trypanosomes of distinct antigenic type (ETat 1 to 12) isolated from a strain of Trypanosoma brucei rhodesiense. Ann. Soc. Belg. Med. Trop. 56, 55–63 (1976).

    CAS  PubMed  Google Scholar 

  40. Xong, H. V. et al. A VSG expression site-associated gene confers resistance to human serum in Trypanosoma rhodesiense. Cell 95, 839–846 (1998).

    CAS  PubMed  Google Scholar 

  41. Pays, E., Lips, S., Nolan, D., Vanhamme, L. & Pérez-Morga, D. The VSG expression sites of Trypanosoma brucei: multipurpose tools for the adaptation of the parasite to mammalian hosts. Mol. Biochem. Parasitol. 114, 1–16 (2001).

    CAS  PubMed  Google Scholar 

  42. De Greef, C., Imberechts, H., Matthyssens, G., Van Meirvenne, N. & Hamers, R. A gene expressed only in serum-resistant variants of Trypanosoma brucei rhodesiense. Mol. Biochem. Parasitol. 36, 169–176 (1989).

    CAS  PubMed  Google Scholar 

  43. De Greef, C. & Hamers, R. The serum resistance-associated (SRA) gene of Trypanosoma brucei rhodesiense encodes a variant surface glycoprotein-like protein. Mol. Biochem. Parasitol. 68, 277–284 (1994).

    CAS  PubMed  Google Scholar 

  44. Campillo, N. & Carrington, M. The origin of the serum resistance associated (SRA) gene and a model of the structure of the SRA polypeptide from Trypanosoma brucei rhodesiense. Mol. Biochem. Parasitol. 127, 79–84 (2003).

    CAS  PubMed  Google Scholar 

  45. Vanhamme, L. et al. The Trypanosoma brucei reference strain TREU927/4 contains T. b. rhodesiense-specific SRA sequences, but displays a distinct phenotype of relative resistance to human serum. Mol. Biochem. Parasitol. 135, 39–47 (2004).

    CAS  PubMed  Google Scholar 

  46. Milner, J. D. & Hajduk, S. L. Expression and localization of serum resistance associated protein in Trypanosoma brucei rhodesiense. Mol. Biochem. Parasitol. 104, 271–283 (1999).

    CAS  PubMed  Google Scholar 

  47. Welburn, S. C. et al. Identification of human-infective trypanosomes in animal reservoir of sleeping sickness in Uganda by means of serum-resistance-associated (SRA) gene. Lancet 358, 2017–2019 (2001).

    CAS  PubMed  Google Scholar 

  48. Gibson, W., Backhouse, T. & Griffiths, A. The human serum resistance associated gene is ubiquitous and conserved in Trypanosoma brucei rhodesiense throughout East Africa. Infect. Genet. Evol. 1, 207–214 (2002).

    CAS  PubMed  Google Scholar 

  49. Radwanska, M. et al. The serum resistance-associated gene as a diagnostic tool for the detection of Trypanosoma brucei rhodesiense. Am. J. Trop. Med. Hyg. 67, 684–690 (2002).

    CAS  PubMed  Google Scholar 

  50. Gibson, W. & Ferris, V. Conservation of the genomic location of the human serum resistance associated gene in Trypanosoma brucei rhodesiense. Mol. Biochem. Parasitol. 130, 159–162 (2003).

    CAS  PubMed  Google Scholar 

  51. Gibson, W. C. The SRA gene: the key to understanding the nature of Trypanosoma brucei rhodesiense. Parasitology 131, 143–150 (2005).

    CAS  PubMed  Google Scholar 

  52. Vanhamme, L. et al. Differential RNA elongation controls the variant surface glycoprotein gene expression sites of Trypanosoma brucei. Mol. Microbiol. 36, 328–340 (2000).

    CAS  PubMed  Google Scholar 

  53. De Greef, C., Chimfwembe, E., Kihang' a Wabacha, J., Bajyana Songa, E. & Hamers, R. Only the serum-resistant bloodstream forms of Trypanosoma brucei rhodesiense express the serum resistance associated (SRA) protein. Ann. Soc. Belg. Med. Trop. 72 (Suppl. 1), 13–21 (1992).

    PubMed  Google Scholar 

  54. Vanhamme, L. et al. Apolipoprotein L-I is the trypanosome lytic factor of human serum. Nature 422, 83–87 (2003).

    CAS  PubMed  Google Scholar 

  55. Triggs, V. P. & Bangs, J. D. Glycosylphosphatidylinositol-dependent protein trafficking in bloodstream stage Trypanosoma brucei. Eukaryot. Cell 2, 76–83 (2003).

    CAS  PubMed Central  PubMed  Google Scholar 

  56. Wang, J., Böhme, U. & Cross, G. A. M. Structural features affecting variant surface glycoprotein expression in Trypanosoma brucei. Mol. Biochem. Parasitol. 128, 135–145 (2003).

    CAS  PubMed  Google Scholar 

  57. Duchateau, P. N. et al. Apolipoprotein L, a new human high density lipoprotein apolipoprotein expressed by the pancreas. Identification, cloning, characterization, and plasma distribution of apolipoprotein L. J. Biol. Chem. 272, 25576–25582 (1997).

    CAS  PubMed  Google Scholar 

  58. Mikkelsen, T. S. et al. Initial sequence of the chimpanzee genome and comparison with the human genome. Nature 437, 69–87 (2005).

    CAS  Google Scholar 

  59. Oli, M. W., Cotlin, L. F., Shiflett, A. M. & Hajduk, S. L. Serum resistance-associated protein blocks lysosomal targeting of trypanosome lytic factor in Trypanosoma brucei. Eukaryot. Cell 5, 132–139 (2006).

    CAS  PubMed Central  PubMed  Google Scholar 

  60. Moore, D. R. et al. Developmentally regulated sensitivity of Trypanosoma brucei brucei to the cytotoxic effects of human high-density lipoprotein. Exp. Parasitol. 81, 216–226 (1995).

    CAS  PubMed  Google Scholar 

  61. Brun, R. & Jenni, L. Human serum resistance of metacyclic forms of Trypanosoma brucei brucei, T. brucei rhodesiense and T. brucei gambiense. Parasitol. Res. 73, 218–223 (1987).

    CAS  PubMed  Google Scholar 

  62. Duchateau, P. N. et al. Plasma apolipoprotein L concentrations correlate with plasma triglycerides and cholesterol levels in normolipidemic, hyperlipidemic, and diabetic subjects. J. Lipid Res. 41, 1231–1236 (2000).

    CAS  PubMed  Google Scholar 

  63. Mimmack, M. L. et al. Gene expression analysis in schizophrenia: reproducible up-regulation of several members of the apolipoprotein L family located in a high-susceptibility locus for schizophrenia on chromosome 22. Proc. Natl Acad. Sci. USA 99, 4680–4685 (2002).

    CAS  PubMed  PubMed Central  Google Scholar 

  64. Pérez-Morga, D. et al. Apolipoprotein L-I promotes trypanosome lysis by forming pores in lysosomal membranes. Science 309, 469–472 (2005).

    PubMed  Google Scholar 

  65. Raper, J., Molina Portela, M. P., Lugli, E., Frevert, U. & Tomlinson, S. Trypanosome lytic factors: novel mediators of innate immunity. Curr. Opin. Microbiol. 4, 402–408 (2001).

    CAS  PubMed  Google Scholar 

  66. Nolan, D. P. & Voorheis, H. P. Factors that determine the plasma-membrane potential in bloodstream forms of Trypanosoma brucei. Eur. J. Biochem. 267, 4615–4623 (2000).

    CAS  PubMed  Google Scholar 

  67. Rifkin, M. R. Trypanosoma brucei: biochemical and morphological studies of cytotoxicity caused by normal human serum. Exp. Parasitol. 58, 81–93 (1984).

    CAS  PubMed  Google Scholar 

  68. Cardoso de Almeida, M. L., Geuskens, M. & Pays, E. Cell lysis induces redistribution of the GPI-anchored variant surface glycoprotein on both faces of the plasma membrane of Trypanosoma brucei. J. Cell Sci. 112, 4461–4473 (1999).

    PubMed  Google Scholar 

  69. del Pilar Molina-Portela, M., Lugli, E. B., Recio-Pinto, E. & Raper, J. Trypanosome lytic factor, a subclass of high-density lipoprotein, forms cation-selective pores in membranes. Mol. Biochem. Parasitol. 144, 218–226 (2005).

    CAS  Google Scholar 

  70. Shiflett, A. M., Bishop, J. R., Pahwa, A. K. & Hajduk, S. L. Human HDLs are platforms for the assembly of multi-component innate immune complexes. J. Biol. Chem. 280, 32578–32585 (2005).

    CAS  PubMed  Google Scholar 

  71. McGwire, B. S., Olson, C. L., Tack, B. F. & Engman, D. M. Killing of African trypanosomes by antimicrobial peptides. J. Infect. Dis. 188, 146–152 (2003).

    PubMed  Google Scholar 

  72. Baral, T. N. et al. Experimental therapy of African trypanosomiasis with a nanobody-conjugated human trypanolytic factor. Nature Med. 12, 580–584 (2006).

    CAS  PubMed  Google Scholar 

  73. Hatada, S. et al. No trypanosome lytic activity in the sera of mice producing human haptoglobin-related protein. Mol. Biochem. Parasitol. 119, 291–294 (2002).

    CAS  PubMed  Google Scholar 

  74. Stijlemans, B. et al. Efficient targeting of conserved cryptic epitopes of infectious agents by single domain antibodies. African trypanosomes as paradigm. J. Biol. Chem. 279, 1256–1261 (2004).

    CAS  PubMed  Google Scholar 

  75. Monajemi, H., Fontijn, R. D., Pannekoek, H. & Horrevoets, A. J. The apolipoprotein L gene cluster has emerged recently in evolution and is expressed in human vascular tissue. Genomics 79, 539–546 (2002).

    CAS  PubMed  Google Scholar 

  76. Page, N. M., Butlin, D. J., Lomthaisong, K. & Lowry, P. J. The human apolipoprotein L gene cluster: identification, classification, and sites of distribution. Genomics 74, 71–78 (2001).

    CAS  PubMed  Google Scholar 

  77. Duchateau, P. N., Pullinger, C. R., Cho, M. H., Eng, C. & Kane, J. P. Apolipoprotein L gene family: tissue-specific expression, splicing, promoter regions; discovery of a new gene. J. Lipid Res. 42, 620–630 (2001).

    CAS  PubMed  Google Scholar 

  78. Horrevoets, A. J. et al. Vascular endothelial genes that are responsive to tumor necrosis factor-α in vitro are expressed in atherosclerotic lesions, including inhibitor of apoptosis protein-1, stannin, and two novel genes. Blood 93, 3418–3431 (1999).

    CAS  PubMed  Google Scholar 

  79. Liu, Z., Lu, H., Jiang, Z., Pastuszyn, A. & Hu, C. A. Apolipoprotein L6, a novel proapoptotic Bcl-2 homology 3-only protein, induces mitochondria-mediated apoptosis in cancer cells. Mol. Cancer Res. 3, 21–31 (2005).

    CAS  PubMed  Google Scholar 

  80. Lazebnik, Y. Why do regulators of apoptosis look like bacterial toxins? Curr. Biol. 11, R767–R768 (2001).

    CAS  PubMed  Google Scholar 

  81. Concha, M. I. et al. Apolipoproteins A-I and A-II are potentially important effectors of innate immunity in the teleost fish Cyprinus carpio. Eur. J. Biochem. 271, 2984–2990 (2004).

    CAS  PubMed  Google Scholar 

  82. Sorensen, O., Bratt, T., Johnsen, A. H., Madsen, M. T. & Borregaard, N. The human antibacterial cathelicidin, hCAP-18, is bound to lipoproteins in plasma. J. Biol. Chem. 274, 22445–22451 (1999).

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This paper is dedicated to the memory of M. Steinert. This work was supported by the Fonds National de la Recherche Scientifique (FNRS), the United Nations Children's Fund, United Nations Development Programme, World Bank, and World Health Organization Special Programme for Research and Training in Tropical Diseases (TDR), and the Interuniversity Attraction Poles Programme (Belgian Science Policy).

Author information

Authors and Affiliations

  1. Laboratory of Molecular Parasitology, Institute of Molecular Biology and Medicine (IBMM), Université Libre de Bruxelles, 12 rue des Professeurs Jeener et Brachet, Gosselies, B-6041, Belgium

    Etienne Pays, Benoit Vanhollebeke, Luc Vanhamme, Françoise Paturiaux-Hanocq & David Pérez-Morga

  2. Department of Biochemistry, Trinity College, Dublin, 2, Ireland

    Derek P. Nolan

Authors
  1. Etienne Pays
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Benoit Vanhollebeke
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Luc Vanhamme
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Françoise Paturiaux-Hanocq
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Derek P. Nolan
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. David Pérez-Morga
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Etienne Pays.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Related links

Related links

DATABASES

Entrez Genome Project

T. brucei

FURTHER INFORMATION

Etienne Pays's laboratory

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pays, E., Vanhollebeke, B., Vanhamme, L. et al. The trypanolytic factor of human serum. Nat Rev Microbiol 4, 477–486 (2006). https://doi.org/10.1038/nrmicro1428

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1038/nrmicro1428

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing