The trypanolytic factor of human serum

Nature Reviews Microbiology

Volumn 4, Issue 6, 2006, Pages 477-486

  Pays, Etienne ^a   Vanhollebeke, Benoit ^a   Vanhamme, Luc ^a   Paturiaux Hanocq, Fraņoise ^a   Nolan, Derek P ^b   Pérez Morga, David ^a  

^a UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^b TRINITY COLLEGE DUBLIN   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

APOLIPOPROTEIN; APOLIPOPROTEIN L1; HIGH DENSITY LIPOPROTEIN; UNCLASSIFIED DRUG;

AFRICA; AFRICAN TRYPANOSOMIASIS; ARTICLE; CELL DEATH; ENDOCYTOSIS; HUMAN; INNATE IMMUNITY; LIFE CYCLE; LYSIS; LYSOSOME; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN INTERACTION; SERUM; TRYPANOSOMA; TRYPANOSOMA BRUCEI; TRYPANOSOMA RHODESIENSE;

ANIMALS; ANTIGENS, NEOPLASM; APOLIPOPROTEINS; BLOOD PROTEINS; HAPTOGLOBINS; HUMANS; IMMUNE SERA; LIPOPROTEINS, HDL; TRYPANOSOMA BRUCEI GAMBIENSE; TRYPANOSOMA BRUCEI RHODESIENSE; TRYPANOSOMIASIS, AFRICAN;

MAMMALIA; PROTOZOA; TRYPANOSOMA; TRYPANOSOMA BRUCEI; TRYPANOSOMA BRUCEI BRUCEI; TRYPANOSOMA BRUCEI GAMBIENSE; TRYPANOSOMA BRUCEI RHODESIENSE;

EID: 33646832920     PISSN: 17401526     EISSN: None     Source Type: Journal    
DOI: 10.1038/nrmicro1428     Document Type: Article

References (82)

1. Blum, M. L. et al. A structural motif in the variant surface glycoproteins of Trypanosoma brucei. Nature 362, 603-609 (1993).
2. Cross, G. A. M. Antigenic variation in trypanosomes. Proc. R. Soc. Lond. B 202, 55-72 (1978).
3. Barry, J. D. The relative significance of mechanisms of antigenic variation in African trypanosomes. Parasitol. Today 13, 212-218 (1997).
4. Borst, P. Antigenic variation and allelic exclusion. Cell 109, 5-8 (2002).
5. Pays, E., Vanhamme, L. & Pérez-Morga, D. Antigenic variation in Trypanosoma brucei: Facts, challenges and mysteries. Curr. Opin. Microbiol. 7, 369-374 (2004).
6. Laveran, A. & Mesnil, F. in Trypanosomes et Trypanosomiases 126-183 (Libraires de l'Académie de Médecine, Paris, 1912) (in French).
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).
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).
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).
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).
11. Rifkin, M. R. Role of phospholipids in the cytotoxic action of high density lipoprotein on trypanosomes. J. Lipid Res. 32, 639-647 (1991).
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).
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).
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).
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).
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).
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).
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).
19. Hager, K. M. & Hajduk, S. L. Mechanism of resistance of African trypanosomes to cytotoxic human HDL. Nature 385, 823-826 (1997).
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).
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).
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).
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).
24. Smith, A. B, Esko, J. D. & Hajduk, S. L. Killing of trypanosomes by the human haptoglobin-related protein. Science 268, 284-286 (1995).
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).
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).
27. Muranjan, M., Nussenzweig, V. & Tomlinson, S. Characterization of the human serum trypanosome toxin, haptoglobin-related protein. J. Biol. Chem. 273, 3884-3887 (1998).
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).
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).
30. Tomlinson, S. et al. High-density-lipoprotein-independent killing of Trypanosoma brucei by human serum. Mol. Biochem. Parasitol. 70, 131-138 (1995).
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).
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).
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).
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).
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).
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).
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).
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).
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).
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).
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).
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).
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).
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).
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).
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).
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).
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).
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).
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).
51. Gibson, W. C. The SRA gene: The key to understanding the nature of Trypanosoma brucei rhodesiense. Parasitology 131, 143-150 (2005).
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).
53. De Greef, C., Chimfwembe, E., Kihang'a Wabacha, J., Bajyana Songa, E. & Harriers, 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).
54. Vanhamme, L. et al. Apolipoprotein L-I is the trypanosome lytic factor of human serum. Nature 422, 83-87 (2003).
55. Triggs, V. P. & Bangs, J. D. Glycosylphosphatidylinositol-dependent protein trafficking in bloodstream stage Trypanosoma brucei. Eukaryot. Cell 2, 76-83 (2003).
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).
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).
58. Mikkelsen, T. S. et al. Initial sequence of the chimpanzee genome and comparison with the human genome. Nature 437, 69-87 (2005).
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).
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).
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).
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).
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).
64. Pérez-Morga, D. et al. Apolipoprotein L-I promotes trypanosome lysis by forming pores in lysosomal membranes. Science 309, 469-472 (2005).
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).
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).
67. Rifkin, M. R. Trypanosoma brucei: Biochemical and morphological studies of cytotoxicity caused by normal human serum. Exp. Parasitol. 58, 81-93 (1984).
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).
69. del Filar 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).
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).
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).
72. Baral, T. N. et al. Experimental therapy of African trypanosomiasis with a nanobody-conjugated human trypanolytic factor. Nature Med. 12, 580-584 (2006).
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).
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).
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).
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).
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).
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).
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).
80. Lazebnik, Y. Why do regulators of apoptosis look like bacterial toxins? Curr. Biol. 11, R767-R768 (2001).
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).
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).