A Primate APOL1 Variant That Kills Trypanosoma brucei gambiense

PLoS Neglected Tropical Diseases

Volumn 10, Issue 8, 2016, Pages

  Cooper, Anneli ^a   Capewell, Paul ^a   Clucas, Caroline ^a   Veitch, Nicola ^a   Weir, William ^a   Thomson, Russell ^b   Raper, Jayne ^b   MacLeod, Annette ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

^b NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; APOLIPOPROTEIN; RECOMBINANT APOLIPOPROTEIN L1; UNCLASSIFIED DRUG; RECOMBINANT PROTEIN;

ADULT; AFRICAN TRYPANOSOMIASIS; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; CYTOLYSIS; DOSE RESPONSE; IC50; IMMUNOFLUORESCENCE TEST; IN VITRO STUDY; MALE; MOLECULAR CLONING; NONHUMAN; PAPIO PAPIO; POLYACRYLAMIDE GEL ELECTROPHORESIS; POLYMERASE CHAIN REACTION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PURIFICATION; TRYPANOSOMA BRUCEI GAMBIENSE; TRYPANOSOMA BRUCEI RHODESIENSE; WESTERN BLOTTING; AFRICA; ANIMAL; CHEMISTRY; DRUG EFFECTS; GENETIC VARIATION; GENETICS; HUMAN; ISOLATION AND PURIFICATION; METABOLISM; PARASITOLOGY; TRYPANOSOMIASIS, AFRICAN;

AFRICA, EASTERN; AFRICA, WESTERN; ANIMALS; APOLIPOPROTEINS; GENETIC VARIATION; HUMANS; PAPIO PAPIO; RECOMBINANT PROTEINS; TRYPANOSOMA BRUCEI GAMBIENSE; TRYPANOSOMA BRUCEI RHODESIENSE; TRYPANOSOMIASIS, AFRICAN;

EID: 84988695807     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0004903     Document Type: Article

References (95)

1. Food and Agriculture Organization. On target against poverty: the Programme Against African Trypanosomiasis (PAAT) 1997–2007. Rome; 2008.
2. Kennedy PG, Clinical features, diagnosis, and treatment of human African trypanosomiasis (sleeping sickness). Lancet Neurol. 2013;12: 186–194. doi: 10.1016/S1474-4422(12)70296-X23260189
3. Brun R, Blum J, Chappuis F, Burri C, Human African trypanosomiasis. Lancet. Elsevier; 2010;375: 148–159. doi: 10.1016/S0140-6736(09)60829-119833383
4. Simarro PP, Cecchi G, Franco JR, Paone M, Diarra A, Ruiz-Postigo JA, et al. Estimating and mapping the population at risk of sleeping sickness. Ndung’u JM, editor. PLOS Negl Trop Dis. Public Library of Science; 2012;6: e1859. doi: 10.1371/journal.pntd.000185923145192
5. Barrett MP, Vincent IM, Burchmore RJS, Kazibwe AJN, Matovu E, Drug resistance in human African trypanosomiasis. Future Microbiol. Future Medicine Ltd London, UK; 2011;6: 1037–1047. doi: 10.2217/fmb.11.8821958143
6. Delespaux V, Geysen D, Van den Bossche P, Geerts S, Molecular tools for the rapid detection of drug resistance in animal trypanosomes. Trends in Parasitology. Elsevier; 2008;24: 236–242. doi: 10.1016/j.pt.2008.02.00618420457
7. Simarro PP, Franco J, Diarra A, Postigo JAR, Jannin J, Update on field use of the available drugs for the chemotherapy of human African trypanosomiasis. Parasitology. Cambridge University Press; 2012;139: 842–846. doi: 10.1017/S003118201200016922309684
8. Priotto G, Kasparian S, Mutombo W, Ngouama D, Ghorashian S, Arnold U, et al. Nifurtimox-eflornithine combination therapy for second-stage African Trypanosoma brucei gambiense trypanosomiasis: a multicentre, randomised, phase III, non-inferiority trial. Lancet. Elsevier; 2009;374: 56–64. doi: 10.1016/S0140-6736(09)61117-X19559476
9. Stich A, Ponte-Sucre A, Holzgrabe U, Do we need new drugs against human African trypanosomiasis?Lancet Infect Dis. Elsevier; 2013;13: 733–734. doi: 10.1016/S1473-3099(13)70191-923969207
10. Nare B, Wring S, Bacchi C, Beaudet B, Bowling T, Brun R, et al. Discovery of novel orally bioavailable oxaborole 6-carboxamides that demonstrate cure in a murine model of late-stage central nervous system african trypanosomiasis. Antimicrob Agents Chemother. American Society for Microbiology; 2010;54: 4379–4388. doi: 10.1128/AAC.00498-1020660666
11. Brun R, Don R, Jacobs RT, Wang MZ, Barrett MP, Development of novel drugs for human African trypanosomiasis. Future Microbiol. Future Medicine Ltd London, UK; 2011;6: 677–691. doi: 10.2217/fmb.11.4421707314
12. Barry JD, McCulloch R, Antigenic variation in trypanosomes: enhanced phenotypic variation in a eukaryotic parasite. Adv Parasitol. 2001;49: 1–70. 11461029
13. Mugnier MR, Cross GAM, Papavasiliou FN, The in vivo dynamics of antigenic variation in Trypanosoma brucei. Science. American Association for the Advancement of Science; 2015;347: 1470–1473. doi: 10.1126/science.aaa450225814582
14. Thomson R, Molina-Portela P, Mott H, Carrington M, Raper J, Hydrodynamic gene delivery of baboon trypanosome lytic factor eliminates both animal and human-infective African trypanosomes. Proc Natl Acad Sci USA. National Acad Sciences; 2009;106: 19509–19514. doi: 10.1073/pnas.090566910619858474
15. Lukeš J, Raper J, Prophylactic antiparasitic transgenesis for human parasitic disease?Mol Ther. Nature Publishing Group; 2010;18: 1745–1747. doi: 10.1038/mt.2010.19320885434
16. Hajduk SL, Hager KM, Esko JD, Human high density lipoprotein killing of African trypanosomes. Annu Rev Microbiol. Annual Reviews 4139 El Camino Way, P.O. Box 10139, Palo Alto, CA 94303–0139, USA; 1994;48: 139–162. doi: 10.1146/annurev.mi.48.100194.0010357826003
17. Laveran A, Mesnil F, Trypanosomes and Trypanosomiases. Paris: Masson et Cie; 1912.
18. Rifkin MR, Identification of the trypanocidal factor in normal human serum: high density lipoprotein. Proc Natl Acad Sci USA. National Academy of Sciences; 1978;75: 3450–3454. 210461
19. Hajduk SL, Moore DR, Vasudevacharya J, Siqueira H, Torri AF, Tytler EM, et al. Lysis of Trypanosoma brucei by a toxic subspecies of human high density lipoprotein. Journal of Biological Chemistry. 1989;264: 5210–5217. 2494183
20. Raper J, Portela MP, Lugli E, Frevert U, Tomlinson S, Trypanosome lytic factors: novel mediators of human innate immunity. Curr Opin Microbiol. 2001;4: 402–408. 11495802
21. Tomlinson S, Jansen AM, Koudinov A, Ghiso JA, Choi-Miura NH, Rifkin MR, et al. High-density-lipoprotein-independent killing of Trypanosoma brucei by human serum. Molecular and Biochemical Parasitology. 1995;70: 131–138. 7637693
22. Vanhollebeke B, Nielsen MJ, Watanabe Y, Truc P, Vanhamme L, Nakajima K, et al. Distinct roles of haptoglobin-related protein and apolipoprotein L-I in trypanolysis by human serum. Proc Natl Acad Sci USA. National Acad Sciences; 2007;104: 4118–4123. doi: 10.1073/pnas.060990210417360487
23. Widener J, Nielsen MJ, Shiflett A, Moestrup SK, Hajduk S, Hemoglobin is a co-factor of human trypanosome lytic factor. PLOS Pathog. Public Library of Science; 2007;3: 1250–1261. doi: 10.1371/journal.ppat.003012917845074
24. Drain J, Bishop JR, Hajduk SL, Haptoglobin-related protein mediates trypanosome lytic factor binding to trypanosomes. Journal of Biological Chemistry. American Society for Biochemistry and Molecular Biology; 2001;276: 30254–30260. doi: 10.1074/jbc.M01019820011352898
25. Hager KM, Pierce MA, Moore DR, Tytler EM, Esko JD, Hajduk SL, Endocytosis of a cytotoxic human high density lipoprotein results in disruption of acidic intracellular vesicles and subsequent killing of African trypanosomes. J Cell Biol. The Rockefeller University Press; 1994;126: 155–167. 8027174
26. 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. The Rockefeller University Press; 1996;183: 1023–1029. 8642243
27. Vanhamme L, Paturiaux-Hanocq F, Poelvoorde P, Nolan DP, Lins L, Van Den Abbeele J, et al. Apolipoprotein L-I is the trypanosome lytic factor of human serum. Nature. Nature Publishing Group; 2003;422: 83–87. doi: 10.1038/nature0146112621437
28. Molina-Portela MP, Samanovic M, Raper J, Distinct roles of apolipoprotein components within the trypanosome lytic factor complex revealed in a novel transgenic mouse model. J Exp Med. 2008;205: 1721–1728. doi: 10.1084/jem.2007146318606856
29. Vanhollebeke B, Pays E, The function of apolipoproteins L. Cell Mol Life Sci. 2006;63: 1937–1944. doi: 10.1007/s00018-006-6091-x16847577
30. Harrington JM, Howell S, Hajduk SL, Membrane permeabilization by trypanosome lytic factor, a cytolytic human high density lipoprotein. Journal of Biological Chemistry. American Society for Biochemistry and Molecular Biology; 2009;284: 13505–13512. doi: 10.1074/jbc.M90015120019324878
31. Molina-Portela MDP, Lugli EB, Recio-Pinto E, Raper J, Trypanosome lytic factor, a subclass of high-density lipoprotein, forms cation-selective pores in membranes. Molecular and Biochemical Parasitology. 2005;144: 218–226. doi: 10.1016/j.molbiopara.2005.08.01816202458
32. Pérez-Morga D, Vanhollebeke B, Paturiaux-Hanocq F, Nolan DP, Lins L, Homblé F, et al. Apolipoprotein L-I promotes trypanosome lysis by forming pores in lysosomal membranes. Science. American Association for the Advancement of Science; 2005;309: 469–472. doi: 10.1126/science.111456616020735
33. Vanwalleghem G, Fontaine F, Lecordier L, Tebabi P, Klewe K, Nolan DP, et al. Coupling of lysosomal and mitochondrial membrane permeabilization in trypanolysis by APOL1. Nat Commun. Nature Publishing Group; 2015;6: 8078. doi: 10.1038/ncomms907826307671
34. Thomson R, Finkelstein A, Human trypanolytic factor APOL1 forms pH-gated cation-selective channels in planar lipid bilayers: relevance to trypanosome lysis. Proc Natl Acad Sci USA. National Acad Sciences; 2015;112: 2894–2899. doi: 10.1073/pnas.142195311225730870
35. Van Xong H, Vanhamme L, Chamekh M, Chimfwembe CE, Van Den Abbeele J, Pays A, et al. A VSG Expression Site–Associated Gene Confers Resistance to Human Serum in Trypanosoma rhodesiense. Cell. 1998;95: 839–846. doi: 10.1016/S0092-8674(00)81706-79865701
36. De Greef C, Imberechts H, Matthyssens G, Van Meirvenne N, Hamers R, A gene expressed only in serum-resistant variants of Trypanosoma brucei rhodesiense. Molecular and Biochemical Parasitology. 1989;36: 169–176. 2528066
37. Lecordier L, Vanhollebeke B, Poelvoorde P, Tebabi P, Paturiaux-Hanocq F, Andris F, Mansfield JM, et al. C-terminal mutants of apolipoprotein L-I efficiently kill both Trypanosoma brucei brucei and Trypanosoma brucei rhodesiense. PLOS Pathog. Public Library of Science; 2009;5: e1000685. doi: 10.1371/journal.ppat.100068519997494
38. Stephens NA, Hajduk SL, Endosomal localization of the serum resistance-associated protein in African trypanosomes confers human infectivity. Eukaryotic Cell. 2011;10: 1023–1033. doi: 10.1128/EC.05112-1121705681
39. Bart J-M, Cordon-Obras C, Vidal I, Reed J, Perez-Pastrana E, Cuevas L, et al. Localization of serum resistance-associated protein in Trypanosoma brucei rhodesiense and transgenic Trypanosoma brucei brucei. Cell Microbiol. 2015;: n/a–n/a. doi: 10.1111/cmi.12454
40. Pays E, Vanhollebeke B, Uzureau P, Lecordier L, Pérez-Morga D, The molecular arms race between African trypanosomes and humans. Nature Reviews Microbiology. Nature Publishing Group; 2014;12: 575–584. doi: 10.1038/nrmicro329824975321
41. Gibson WC, de C Marshall TF, Godfrey DG, Numerical analysis of enzyme polymorphism: a new approach to the epidemiology and taxonomy of trypanosomes of the subgenus Trypanozoon. Adv Parasitol. 1980;18: 175–246. 7001872
42. Mehlitz D, Zillmann U, Scott CM, Godfrey DG, Epidemiological studies on the animal reservoir of Gambiense sleeping sickness. Part III. Characterization of trypanozoon stocks by isoenzymes and sensitivity to human serum. Tropenmed Parasitol. 1982;33: 113–118. 6287687
43. Tait A, Babiker EA, Le Ray D, Enzyme variation in Trypanosoma brucei spp. I. Evidence for the sub-speciation of Trypanosoma brucei gambiense. Parasitology. 1984;89 (Pt 2): 311–326. 6504561
44. Gibson WC, Will the real Trypanosoma b. gambiense please stand up. Parasitol Today (Regul Ed). 1986;2: 255–257.
45. Weir W, Capewell P, Foth B, Clucas C, Pountain A, Steketee P, et al. Population genomics reveals the origin and asexual evolution of human infective trypanosomes. Elife. eLife Sciences Publications Limited; 2016;5: pdb.ip71. doi: 10.7554/eLife.11473
46. Simarro PP, Cecchi G, Paone M, Franco JR, Diarra A, Ruiz JA, et al. The Atlas of human African trypanosomiasis: a contribution to global mapping of neglected tropical diseases. Int J Health Geogr. BioMed Central Ltd; 2010;9: 57. doi: 10.1186/1476-072X-9-5721040555
47. Zillmann U, Mehlitz D, Sachs R, Identity of Trypanozoon stocks isolated from man and a domestic dog in Liberia. Tropenmed Parasitol. 1984;35: 105–108. 6464184
48. Capewell P, Veitch NJ, Turner CMR, Raper J, Berriman M, Hajduk SL, Büscher P, et al. Differences between Trypanosoma brucei gambiense groups 1 and 2 in their resistance to killing by trypanolytic factor 1. PLOS Negl Trop Dis. Public Library of Science; 2011;5: e1287. doi: 10.1371/journal.pntd.000128721909441
49. Kieft R, Capewell P, Turner CMR, Veitch NJ, MacLeod A, Hajduk S, Mechanism of Trypanosoma brucei gambiense (group 1) resistance to human trypanosome lytic factor. Proc Natl Acad Sci USA. National Acad Sciences; 2010;107: 16137–16141. doi: 10.1073/pnas.100707410720805508
50. DeJesus E, Kieft R, Albright B, Stephens NA, Hajduk SL, Hill KL, A single amino acid substitution in the group 1 Trypanosoma brucei gambiense haptoglobin-hemoglobin receptor abolishes TLF-1 binding. PLOS Pathog. Public Library of Science; 2013;9: e1003317. doi: 10.1371/journal.ppat.100331723637606
51. Capewell P, Clucas C, DeJesus E, Kieft R, Hajduk S, Veitch N, Alsford S, et al. The TgsGP Gene Is Essential for Resistance to Human Serum in Trypanosoma brucei gambiense. PLOS Pathog. Public Library of Science; 2013;9: e1003686. doi: 10.1371/journal.ppat.100368624098129
52. Uzureau P, Uzureau S, Lecordier L, Fontaine F, Tebabi P, Homblé F, et al. Mechanism of Trypanosoma brucei gambiense resistance to human serum. Nature. Nature Publishing Group; 2013;501: 430–434. doi: 10.1038/nature1251623965626
53. Alsford S, Currier RB, Guerra-Assunção JA, Clark TG, Horn D, Beverley SM, Cathepsin-L can resist lysis by human serum in Trypanosoma brucei brucei. PLOS Pathog. Public Library of Science; 2014;10: e1004130. doi: 10.1371/journal.ppat.100413024830321
54. Balmer O, Beadell JS, Gibson W, Caccone A, Solano P, Phylogeography and taxonomy of Trypanosoma brucei. PLoS Negl Trop Dis. 2011;5: e961. doi: 10.1371/journal.pntd.000096121347445
55. Radwanska M, Chamekh M, Vanhamme L, Claes F, Magez S, Magnus E, et al. The serum resistance-associated gene as a diagnostic tool for the detection of Trypanosoma brucei rhodesiense. Am J Trop Med Hyg. 2002;67: 684–690. 12518862
56. Gibson W, Nemetschke L, Ndung'u J, Conserved sequence of the TgsGP gene in Group 1 Trypanosoma brucei gambiense. Infect Genet Evol. 2010;10: 453–458. doi: 10.1016/j.meegid.2010.03.00520302972
57. Radwanska M, Claes F, Magez S, Magnus E, Pérez-Morga D, Pays E, et al. Novel primer sequences for polymerase chain reaction-based detection of Trypanosoma brucei gambiense. Am J Trop Med Hyg. 2002;67: 289–295. 12408669
58. Lugli EB, Pouliot M, Portela MDPM, Loomis MR, Raper J, Characterization of primate trypanosome lytic factors. Molecular and Biochemical Parasitology. 2004;138: 9–20. doi: 10.1016/j.molbiopara.2004.07.00415500911
59. Poelvoorde P, Vanhamme L, Van Den Abbeele J, Switzer WM, Pays E, Distribution of apolipoprotein L-I and trypanosome lytic activity among primate sera. Molecular and Biochemical Parasitology. 2004;134: 155–157. 14747153
60. Kumar S, Hedges SB, A molecular timescale for vertebrate evolution. Nature. Nature Publishing Group; 1998;392: 917–920. doi: 10.1038/319279582070
61. Seed JR, Sechelski JB, Loomis MR, A survey for a trypanocidal factor in primate sera. J Protozool. 1990;37: 393–400. 2120433
62. Thomson R, Genovese G, Canon C, Kovacsics D, Higgins MK, Carrington M, et al. Evolution of the primate trypanolytic factor APOL1. Proc Natl Acad Sci USA. National Acad Sciences; 2014;111: E2130–9. doi: 10.1073/pnas.140069911124808134
63. Genovese G, Friedman DJ, Ross MD, Lecordier L, Uzureau P, Freedman BI, et al. Association of trypanolytic ApoL1 variants with kidney disease in African Americans. Science. American Association for the Advancement of Science; 2010;329: 841–845. doi: 10.1126/science.119303220647424
64. Kageruka P, Mangus E, Bajyana Songa E, Nantulya V, Jochems M, Hamers R, et al. Infectivity of Trypanosoma (Trypanozoon) brucei gambiense for baboons (Papio hamadryas, Papio papio). Ann Soc Belg Med Trop. 1991;71: 39–46. 2042999
65. Geigy R, Kauffmann M, Sleeping sickness survey in the Serengeti area (Tanzania) 1971. I. Examination of large mammals for trypanosomes. Acta Trop. 1973;30: 12–23. 4144952
66. Tait A, Barry JD, Wink R, Sanderson A, Crowe JS, Enzyme variation in T. brucei ssp. II. Evidence for T. b. rhodesiense being a set of variants of T. b. brucei. Parasitology. 1985;90 (Pt 1): 89–100. 3856830
67. Felgner P, Brinkmann U, Zillmann U, Mehlitz D, Abu-Ishira S, Epidemiological studies on the animal reservoir of gambiense sleeping sickness. Part II. Parasitological and immunodiagnostic examination of the human population. Tropenmed Parasitol. 1981;32: 134–140. 6285560
68. O'Connell KM, Hutner SH, Fromentin H, Frank O, Baker H, Cryoprotectants for Crithidia fasciculata stored at -20 C, with notes on Trypanosoma gambiense and T. conorhini. J Protozool. 1968;15: 719–724. 5719068
69. Barnes DA, Mottram J, Selkirk M, Agabian N, Two variant surface glycoprotein genes distinguish between different substrains of Trypanosoma brucei gambiense. Molecular and Biochemical Parasitology. 1989;34: 135–146. 2469013
70. Holzmuller P, Biron DG, Courtois P, Koffi M, Bras-Gonçalves R, Daulouède S, et al. Virulence and pathogenicity patterns of Trypanosoma brucei gambiense field isolates in experimentally infected mouse: differences in host immune response modulation by secretome and proteomics. Microbes Infect. 2008;10: 79–86. doi: 10.1016/j.micinf.2007.10.00818068387
71. Hirumi H, Hirumi K, Continuous cultivation of Trypanosoma brucei blood stream forms in a medium containing a low concentration of serum protein without feeder cell layers. J Parasitol. 1989;75: 985–989. 2614608
72. Turner CMR, McLellan S, Lindergard LAG, Bisoni L, Tait A, MacLeod A, Human infectivity trait in Trypanosoma brucei: stability, heritability and relationship to sra expression. Parasitology. 2004;129: 445–454. 15521633
73. MacLeod A, Tweedie A, McLellan S, Taylor S, Cooper A, Sweeney L, et al. Allelic segregation and independent assortment in T. brucei crosses: Proof that the genetic system is Mendelian and involves meiosis. Molecular and Biochemical Parasitology. 2005;143: 12–19. doi: 10.1016/j.molbiopara.2005.04.00915941603
74. Duchateau PN, Movsesyan I, Yamashita S, Sakai N, Hirano K, Schoenhaus SA, et al. Plasma apolipoprotein L concentrations correlate with plasma triglycerides and cholesterol levels in normolipidemic, hyperlipidemic, and diabetic subjects. J Lipid Res. 2000;41: 1231–1236. 10946010
75. Weckerle A, Snipes JA, Cheng D, Gebre AK, Reisz JA, Murea M, et al. Characterization of circulating APOL1 protein complexes in African Americans. J Lipid Res. American Society for Biochemistry and Molecular Biology; 2016;57: 120–130. doi: 10.1194/jlr.M06345326586272
76. Bruggeman LA, O'Toole JF, Ross MD, Madhavan SM, Smurzynski M, Wu K, et al. Plasma apolipoprotein L1 levels do not correlate with CKD. J Am Soc Nephrol. American Society of Nephrology; 2014;25: 634–644. doi: 10.1681/ASN.201307070024231663
77. Pays E, Vanhollebeke B, Vanhamme L, Paturiaux-Hanocq F, Nolan DP, Pérez-Morga D, The trypanolytic factor of human serum. Nature Reviews Microbiology. Nature Publishing Group; 2006;4: 477–486. doi: 10.1038/nrmicro142816710327
78. Vanhollebeke B, De Muylder G, Nielsen MJ, Pays A, Tebabi P, Dieu M, et al. A haptoglobin-hemoglobin receptor conveys innate immunity to Trypanosoma brucei in humans. Science. American Association for the Advancement of Science; 2008;320: 677–681. doi: 10.1126/science.115629618451305
79. Higgins MK, Tkachenko O, Brown A, Reed J, Raper J, Carrington M, Structure of the trypanosome haptoglobin-hemoglobin receptor and implications for nutrient uptake and innate immunity. Proc Natl Acad Sci USA. National Acad Sciences; 2013;110: 1905–1910. doi: 10.1073/pnas.121494311023319650
80. Bullard W, Kieft R, Capewell P, Veitch NJ, MacLeod A, Hajduk SL, Haptoglobin-hemoglobin receptor independent killing of African trypanosomes by human serum and trypanosome lytic factors. Virulence. Taylor & Francis; 2012;3: 72–76. doi: 10.4161/viru.3.1.1829522286709
81. Green HP, Del Pilar Molina Portela M, St Jean EN, Lugli EB, Raper J, Evidence for a Trypanosoma brucei lipoprotein scavenger receptor. Journal of Biological Chemistry. American Society for Biochemistry and Molecular Biology; 2003;278: 422–427. doi: 10.1074/jbc.M20721520012401813
82. Raper J, Fung R, Ghiso J, Nussenzweig V, Tomlinson S, Characterization of a novel trypanosome lytic factor from human serum. Infect Immun. American Society for Microbiology; 1999;67: 1910–1916. 10085035
83. Vanhollebeke B, Pays E, The trypanolytic factor of human serum: many ways to enter the parasite, a single way to kill. Molecular Microbiology. Blackwell Publishing Ltd; 2010;76: 806–814. doi: 10.1111/j.1365-2958.2010.07156.x20398209
84. Alexander DL, Schwartz KJ, Balber AE, Bangs JD, Developmentally regulated trafficking of the lysosomal membrane protein p67 in Trypanosoma brucei. J Cell Sci. 2002;115: 3253–3263. 12140257
85. Kelley RJ, Alexander DL, Cowan C, Balber AE, Bangs JD, Molecular cloning of p67, a lysosomal membrane glycoprotein from Trypanosoma brucei. Molecular and Biochemical Parasitology. 1999;98: 17–28. 10029306
86. Marcello L, Menon S, Ward P, Wilkes JM, Jones NG, Carrington M, et al. VSGdb: a database for trypanosome variant surface glycoproteins, a large and diverse family of coiled coil proteins. BMC Bioinformatics. BioMed Central; 2007;8: 143. doi: 10.1186/1471-2105-8-14317474977
87. Gibson W, Ferris V, Conservation of the genomic location of the human serum resistance associated gene in Trypanosoma brucei rhodesiense. Molecular and Biochemical Parasitology. 2003;130: 159–162. 12946855
88. Berberof M, Pérez-Morga D, Pays E, A receptor-like flagellar pocket glycoprotein specific to Trypanosoma brucei gambiense. Molecular and Biochemical Parasitology. 2001;113: 127–138. 11254961
89. Kopp JB, Nelson GW, Sampath K, Johnson RC, Genovese G, An P, et al. APOL1 genetic variants in focal segmental glomerulosclerosis and HIV-associated nephropathy. J Am Soc Nephrol. American Society of Nephrology; 2011;22: 2129–2137. doi: 10.1681/ASN.201104038821997394
90. Kasembeli AN, Duarte R, Ramsay M, Mosiane P, Dickens C, Dix-Peek T, et al. APOL1 Risk Variants Are Strongly Associated with HIV-Associated Nephropathy in Black South Africans. J Am Soc Nephrol. American Society of Nephrology; 2015;: ASN.2014050469. doi: 10.1681/ASN.2014050469
91. Freedman BI, Langefeld CD, Andringa KK, Croker JA, Williams AH, Garner NE, et al. End-stage renal disease in African Americans with lupus nephritis is associated with APOL1. Arthritis Rheumatol. 2014;66: 390–396. doi: 10.1002/art.3822024504811
92. Larsen CP, Beggs ML, Saeed M, Walker PD, Apolipoprotein L1 risk variants associate with systemic lupus erythematosus-associated collapsing glomerulopathy. J Am Soc Nephrol. American Society of Nephrology; 2013;24: 722–725. doi: 10.1681/ASN.201212118023520206
93. Baral TN, Magez S, Stijlemans B, Conrath K, Vanhollebeke B, Pays E, et al. Experimental therapy of African trypanosomiasis with a nanobody-conjugated human trypanolytic factor. Nat Med. 2006;12: 580–584. doi: 10.1038/nm139516604085
94. Simarro PP, Cecchi G, Franco JR, Paone M, Diarra A, Ruiz Postigo JA, et al. Mapping the capacities of fixed health facilities to cover people at risk of gambiense human African trypanosomiasis. Int J Health Geogr. BioMed Central; 2014;13: 4. doi: 10.1186/1476-072X-13-424517513
95. Zinner D, Wertheimer J, Liedigk R, Groeneveld LF, Roos C, Baboon phylogeny as inferred from complete mitochondrial genomes. Am J Phys Anthropol. Wiley Subscription Services, Inc., A Wiley Company; 2013;150: 133–140. doi: 10.1002/ajpa.2218523180628