Trypanosoma brucei gambiense adaptation to different Mammalian Sera is associated with VSG expression site plasticity

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  Cordon Obras, Carlos ^a   Cano, Jorge ^b   González Pacanowska, Dolores ^a   Benito, Agustin ^b   Navarro, Miguel ^a   Bart, Jean Mathieu ^a,b  

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

^b Red de Investigación de Centros de Enfermedades Tropicales RICET Madrid   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; PROTEIN ANTIBODY; PROTEIN VARIANT; TRANSFERRIN; TRANSFERRIN RECEPTOR; UNCLASSIFIED DRUG; VARIANT SURFACE GLYCOPROTEIN ANTIBODY;

ADAPTATION; ANTIBODY SPECIFICITY; ARTICLE; CONTROLLED STUDY; CULTURE TECHNIQUE; DNA POLYMORPHISM; ESAG3 GENE; ESAG6 GENE; ESAG7 GENE; FAUNA; GENE; GENE EXPRESSION; GENE SEQUENCE; GENETIC ASSOCIATION; GENETIC TRANSCRIPTION; GENOTYPE; GOAT; HOST PARASITE INTERACTION; IN VITRO STUDY; MOLECULAR BIOLOGY; MOLECULAR MODEL; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PROTEIN EXPRESSION; PROTEIN TRANSPORT; SERUM; SWINE; TRYPANOSOMA; VSG GENE;

ADAPTATION, PHYSIOLOGICAL; ANALYSIS OF VARIANCE; ANIMALS; DISEASE RESERVOIRS; DNA PRIMERS; DNA, COMPLEMENTARY; FLUORESCENT ANTIBODY TECHNIQUE; GENETIC VARIATION; GENOTYPE; GLYCOPROTEINS; GOATS; HUMANS; MAMMALS; MEMBRANE GLYCOPROTEINS; PROTOZOAN PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SERUM; SPECIES SPECIFICITY; SWINE; TRANSFERRIN; TRYPANOSOMA BRUCEI GAMBIENSE;

EID: 84893518004     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0085072     Document Type: Article

References (76)

1. Hoare CA (1972) The trypanosomes of mammals.Oxford: Blackwell Scientific Publications.
2. Blum JA, Neumayr AL, Hatz CF (2012) Human African trypanosomiasis in endemic populations and travellers. Eur J Clin Microbiol Infect Dis, 31: 905-13. PubMed: 21901632.
3. Gibson WC (1986) Will the real Trypanosoma b. gambiense please stand up. Parasitol Today 2: 255-257. doi: 10.1016/0169-4758(86)90011-6. PubMed: 15462856.
4. Kuzoe FAS, Schofield CJ (2004) Strategic review of traps and targets for tsetse and African Trypanosomiasis control. Report of Special Programme for Research and Training in Tropical Disease (TDR) TDR/IDE/TRY/05.1.
5. Checchi F, Filipe JA, Barrett MP, Chandramohan D (2008) The natural progression of gambiense sleeping sickness: what is the evidence? PLoS Negl Trop. Drosophila Inf Service 2: e303.
6. Barrett MP, Burchmore RJ, Stich A, Lazzari JO, Frasch AC et al. (2003) The trypanosomiases. Lancet 362: 1469-1480. doi:10.1016/S0140-6736(03)14694-6. PubMed: 14602444. (Pubitemid 37352887)
7. Simarro PP, Franco JR, Ndongo P, Nguema E, Louis FJ et al. (2006) The elimination of Trypanosoma brucei gambiense sleeping sickness in the focus of Luba, Bioko Island, Equatorial Guinea. Trop Med Int Health 11: 636-646. doi:10.1111/j.1365-3156.2006.01624.x. PubMed: 16640616.
8. Louis FJ, Simarro PP, Lucas P (2002) Sleeping sickness: one hundred years of control strategy evolution. Bull Soc Pathol Exot 95: 331-336. PubMed: 12696370. (Pubitemid 36369095)
9. Robays J, Bilengue MM, Van der Stuyft P, Boelaert M (2004) The effectiveness of active population screening and treatment for sleeping sickness control in the Democratic Republic of Congo. Trop Med Int Health 9: 542-550. doi:10.1111/j.1365-3156.2004.01240.x. PubMed: 15117297. (Pubitemid 38657278)
10. Lutumba P, Robays J, Miaka mia Bilenge C, Mesu VK, Molisho D et al. (2005) Trypanosomiasis control, Democratic Republic of Congo, 1993-2003. Emerg Infect Dis 11: 1382-1388. doi:10.3201/eid1109.041020. PubMed: 16229766. (Pubitemid 41209131)
11. Simarro PP, Jannin J, Cattand P (2008) Eliminating human African trypanosomiasis: where do we stand and what comes next? PLoS Med 5: e55. doi:10.1371/journal.pmed.0050055. PubMed: 18303943.
12. Cordon-Obras C, Berzosa P, Ndong-Mabale N, Bobuakasi L, Buatiche JN et al. (2009) Trypanosoma brucei gambiense in domestic livestock of Kogo and Mbini foci (Equatorial Guinea). Trop Med Int Health 14: 535-541. doi:10.1111/j.1365- 3156.2009.02271.x. PubMed: 19320872.
13. Herder S, Simo G, Nkinin S, Njiokou F (2002) Identification of trypanosomes in wild animals from southern Cameroon using the polymerase chain reaction (PCR). Parasite 9: 345-349. PubMed: 12514949. (Pubitemid 135697689)
14. Njiokou F, Laveissière C, Simo G, Nkinin S, Grébaut P et al. (2006) Wild fauna as a probable animal reservoir for Trypanosoma brucei gambiense in Cameroon. Infect Genet Evol 6: 147-153. doi:10.1016/j.meegid.2005. 04.003. PubMed: 16236560. (Pubitemid 43285821)
15. Simo G, Asonganyi T, Nkinin SW, Njiokou F, Herder S (2006) High prevalence of Trypanosoma brucei gambiense group 1 in pigs from the Fontem sleeping sickness focus in Cameroon. Vet Parasitol 139: 57-66. doi:10.1016/j.vetpar.2006.02.026. PubMed: 16567049. (Pubitemid 43775773)
16. Jamonneau V, Ravel S, Koffi M, Kaba D, Zeze DG et al. (2004) Mixed infections of trypanosomes in tsetse and pigs and their epidemiological significance in a sleeping sickness focus of Cote d'Ivoire. Parasitology 129: 693-702. doi:10.1017/S0031182004005876. PubMed: 15648692. (Pubitemid 39657761)
17. Simo G, Cuny G, Demonchy R, Herder S (2008) Trypanosoma brucei gambiense : Study of population genetic structure of Central African stocks using amplified fragment length polymorphism (AFLP). Exp Parasitol 118: 172-180. doi:10.1016/j.exppara.2007.07.010. PubMed: 17850792. (Pubitemid 350309296)
18. Penchenier L, Alhadji D, Bahébégué S, Simo G, Laveissière C et al. (2005) Spontaneous cure of domestic pigs experimentally infected by Trypanosoma brucei gambiense. Implications for the control of sleeping sickness. Vet Parasitol 133: 7-11. doi:10.1016/j.vetpar. 2005.04.034. PubMed: 16076528. (Pubitemid 41242966)
19. Gerrits H, Mussmann R, Bitter W, Kieft R, Borst P (2002) The physiological significance of transferrin receptor variations in Trypanosoma brucei. Mol Biochem Parasitol 119: 237-247. doi: 10.1016/S0166-6851(01)00417-0. PubMed: 11814575. (Pubitemid 34114062)
20. Mussmann R, Engstler M, Gerrits H, Kieft R, Toaldo CB et al. (2004) Factors affecting the level and localization of the transferrin receptor in Trypanosoma brucei. J Biol Chem 279: 40690-40698. doi:10.1074/jbc.M404697200. PubMed: 15263009. (Pubitemid 39287664)
21. Horn D, McCulloch R (2010) Molecular mechanisms underlying the control of antigenic variation in African trypanosomes. Curr Opin Microbiol 13: 700-705. doi:10.1016/j.mib.2010.08.009. PubMed: 20884281.
22. Pays E, Lips S, Nolan D, Vanhamme L, Pérez-Morga D (2001) The VSG expression sites of Trypanosoma brucei: multipurpose tools for the adaptation of the parasite to mammalian hosts. Mol Biochem Parasitol 114: 1-16. doi:10.1016/S0166-6851(01)00242-0. PubMed: 11356509. (Pubitemid 32453210)
23. Horn D (2004) The molecular control of antigenic variation in Trypanosoma brucei. Curr Mol Med 4: 563-576. doi:10.2174/1566524043360078. PubMed: 15357208.
24. Navarro M, Gull K (2001) A pol I transcriptional body associated with VSG mono-allelic expression in Trypanosoma brucei. Nature 414: 759-763. doi:10.1038/414759a. PubMed: 11742402. (Pubitemid 34000774)
25. Landeira D, Bart JM, Van Tyne D, Navarro M (2009) Cohesin regulates VSG monoallelic expression in trypanosomes. J Cell Biol 186: 243-254. doi:10.1083/jcb.200902119. PubMed: 19635842.
26. Navarro M, Cross GA (1998) In situ analysis of a variant surface glycoprotein expression-site promoter region in Trypanosoma brucei. Mol Biochem Parasitol 94: 53-66. doi:10.1016/S0166-6851(98)00049-8. PubMed: 9719510. (Pubitemid 28345148)
27. Berriman M, Hall N, Sheader K, Bringaud F, Tiwari B et al. (2002) The architecture of variant surface glycoprotein gene expression sites in Trypanosoma brucei. Mol Biochem Parasitol 122: 131-140. doi:10.1016/S0166- 6851(02)00092-0. PubMed: 12106867. (Pubitemid 34775082)
28. Steverding D, Stierhof YD, Chaudhri M, Ligtenberg M, Schell D et al. (1994) ESAG 6 and 7 products of Trypanosoma brucei form a transferrin binding protein complex. Eur J Cell Biol 64: 78-87. PubMed: 7957316. (Pubitemid 24205986)
29. Ligtenberg MJ, Bitter W, Kieft R, Steverding D, Janssen H et al. (1994) Reconstitution of a surface transferrin binding complex in insect form Trypanosoma brucei. EMBO J 13: 2565-2573. PubMed: 8013456. (Pubitemid 24188389)
30. Schell D, Evers R, Preis D, Ziegelbauer K, Kiefer H et al. (1991) A transferrin-binding protein of Trypanosoma brucei is encoded by one of the genes in the variant surface glycoprotein gene expression site. EMBO J 10: 1061-1066. PubMed: 1845367. (Pubitemid 21905566)
31. Salmon D, Hanocq-Quertier J, Paturiaux-Hanocq F, Pays A, Tebabi P et al. (1997) Characterization of the ligand-binding site of the transferrin receptor in Trypanosoma brucei demonstrates a structural relationship with the N-terminal domain of the variant surface glycoprotein. EMBO J 16: 7272-7278. doi:10.1093/emboj/16.24.7272. PubMed: 9405356. (Pubitemid 28010487)
32. Steverding D (2000) The transferrin receptor of Trypanosoma brucei. Parasitol Int 48: 191-198. doi:10.1016/S1383-5769(99)00018-5. PubMed: 11227758.
33. Bitter W, Gerrits H, Kieft R, Borst P (1998) The role of transferrin-receptor variation in the host range of Trypanosoma brucei. Nature 391: 499-502: 499-502. doi:10.1038/35166. PubMed: 9461219.
34. van Luenen HG, Kieft R, Mussmann R, Engstler M, ter Riet B et al. (2005) Trypanosomes change their transferrin receptor expression to allow effective uptake of host transferrin. Mol Microbiol 58: 151-165. doi:10.1111/j.1365-2958. 2005.04831.x. PubMed: 16164555. MMI4831 . PII;Available: . doi:10.1111/j.1365- 2958.2005.04831.x
35. Isobe T, Holmes EC, Rudenko G (2003) The transferrin receptor genes of Trypanosoma equiperdum are less diverse in their transferrin binding site than those of the broad-host range Trypanosoma brucei. J Mol Evol 56: 377-386. doi:10.1007/s00239-002-2408-z. PubMed: 12664158. (Pubitemid 36390769)
36. Young R, Taylor JE, Kurioka A, Becker M, Louis EJ et al. (2008) Isolation and analysis of the genetic diversity of repertoires of VSG expression site containing telomeres from Trypanosoma brucei gambiense, T. b. brucei and T. equiperdum. BMC Genomics 9: 385
37. Njiokou F, Sima FO, Njitchouang GR, Nimpaye H, Cuny G et al. (2005) Importance of domestic animal reservoir of Trypanosoma brucei gambiense in Cameroon. 28th Meeting ISCTRC Addis Ababa, Ethiopia .
38. Xong HV, Vanhamme L, Chamekh M, Chimfwembe CE, Van Den AJ et al. (1998) A VSG expression site-associated gene confers resistance to human serum in Trypanosoma rhodesiense. Cell 95: 839-846. doi:10.1016/S0092-8674(00)81706-7. PubMed: 9865701. (Pubitemid 29014463)
39. Capewell P, Veitch NJ, Turner CM, Raper J, Berriman M et al. (2011) Differences between Trypanosoma brucei gambiense Groups 1 and 2 in Their Resistance to Killing by Trypanolytic Factor 1. PLoS Negl Trop. Drosophila Inf Service 5: e1287.
40. Vanhamme L (2010) The human trypanolytic factor: a drug shaped naturally. Infect Disord Drug Targets 10: 266-282. doi:10.2174/187152610791591566. PubMed: 20429865.
41. De Greef C, Imberechts H, Matthyssens G, Van MN, Hamers R (1989) A gene expressed only in serum-resistant variants of Trypanosoma brucei rhodesiense. Mol Biochem Parasitol 36: 169-176. doi:10.1016/0166-6851(89)90189-8. PubMed: 2528066. (Pubitemid 19212840)
42. De Greef C, Chimfwembe E, Kihang'a WJ, Bajyana SE, Hamers R (1992) 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. PubMed: 1417165.
43. Borst P, Rudenko G, Taylor MC, Blundell PA, Van Leeuwen F et al. (1996) Antigenic variation in trypanosomes. Arch Med Res 27: 379-388. PubMed: 8854399. (Pubitemid 26316148)
44. Diffley P, Scott JO, Mama K, Tsen TN (1987) The rate of proliferation among African trypanosomes is a stable trait that is directly related to virulence. Am J Trop Med Hyg 36: 533-540. PubMed: 3578651. (Pubitemid 17099467)
45. Biebinger S, Helfert S, Steverding D, Ansorge I, Clayton C (2003) Impaired dimerization and trafficking of ESAG6 lacking a glycosyl- phosphatidylinositol anchor. Mol Biochem Parasitol 132: 93-96: 93-6. PubMed: 14599669. S0166685103002172 . PII.
46. Ansorge I, Steverding D, Melville S, Hartmann C, Clayton C (1999) Transcription of 'inactive' expression sites in African trypanosomes leads to expression of multiple transferrin receptor RNAs in bloodstream forms. Mol Biochem Parasitol 101: 81-94. doi:10.1016/S0166-6851(99)00060-2. PubMed: 10413045. (Pubitemid 29257843)
47. Engstler M, Thilo L, Weise F, Grünfelder CG, Schwarz H et al. (2004) Kinetics of endocytosis and recycling of the GPI-anchored variant surface glycoprotein in Trypanosoma brucei. J Cell Sci 117: 1105-1115. doi:10.1242/jcs.00938. PubMed: 14996937. 117/7/1105 . PII.
48. Schell D, Borowy NK, Overath P (1991) Transferrin is a growth factor for the bloodstream form of Trypanosoma brucei. Parasitol Res 77: 558-560. doi:10.1007/BF00931012. PubMed: 1792224.
49. Steverding D (1998) Bloodstream forms of Trypanosoma brucei require only small amounts of iron for growth. Parasitol Res 84: 59-62. PubMed: 9491428.
50. Hobbs MR, Boothroyd JC (1990) An expression-site-associated gene family of trypanosomes is expressed in vivo and shows homology to a variant surface glycoprotein gene. Mol Biochem Parasitol 43: 1-16. doi:10.1016/0166-6851(90) 90125-6. PubMed: 2290439. 0166-6851(90)90125-6 . PII.
51. Salmon D, Geuskens M, Hanocq F, Hanocq-Quertier J, Nolan D et al. (1994) A novel heterodimeric transferrin receptor encoded by a pair of VSG expression site-associated genes in T. brucei. Cell 78: 75-86. doi:10.1016/0092-8674(94) 90574-6. PubMed: 8033214.0092-8674(94)90574-6 . PII.
52. Uzureau P, Uzureau S, Lecordier L, Fontaine F, Tebabi P et al. (2013) Mechanism of Trypanosoma brucei gambiense resistance to human serum. Nature 501: 430-434. doi:10.1038/nature12516. PubMed: 23965626. nature12516 . PII;Available: . doi:10.1038/nature12516
53. Berberof M, Pérez-Morga D, Pays E (2001) A receptor-like flagellar pocket glycoprotein specific to Trypanosoma brucei gambiense. Mol Biochem Parasitol 113: 127-138. doi:10.1016/S0166-6851(01)00208-0. PubMed: 11254961. (Pubitemid 32209289)
54. Felu C, Pasture J, Pays E, Pérez-Morga D (2007) Diagnostic potential of a conserved genomic rearrangement in the Trypanosoma brucei gambiense -specific TGSGP locus. Am J Trop Med Hyg 76: 922-929. PubMed: 17488917. (Pubitemid 351627681)
55. Kieft R, Capewell P, Turner CM, Veitch NJ, MacLeod A et al. (2010) Mechanism of Trypanosoma brucei gambiense (group 1) resistance to human trypanosome lytic factor. Proc Natl Acad Sci U S A 107: 16137-16141. doi:10.1073/pnas.1007074107. PubMed: 20805508.
56. Vanhollebeke B, De Muylder G, Nielsen MJ, Pays A, Tebabi P et al. (2008) A haptoglobin-hemoglobin receptor conveys innate immunity to Trypanosoma brucei in humans. Science 320: 677-681. doi:10.1126/science.1156296. PubMed: 18451305. 320/5876/677 . PII;Available: . doi:10.1126/science.1156296
57. Hertz-Fowler C, Figueiredo LM, Quail MA, Becker M, Jackson A et al. (2008) Telomeric expression sites are highly conserved in Trypanosoma brucei. PLOS ONE 3: e3527. doi:10.1371/journal.pone.0003527. PubMed: 18953401.
58. Jackson AP, Sanders M, Berry A, McQuillan J, Aslett MA et al. (2010) The genome sequence of Trypanosoma brucei gambiense, causative agent of chronic human african trypanosomiasis. PLoS Negl Trop. Drosophila Inf Service 4: e658.
59. Berriman M, Ghedin E, Hertz-Fowler C, Blandin G, Renauld H et al. (2005) The genome of the African trypanosome Trypanosoma brucei. Science 309: 416-422. doi:10.1126/science.1112642. PubMed: 16020726. (Pubitemid 40994676)
60. Pays E, Coquelet H, Tebabi P, Pays A, Jefferies D et al. (1990) Trypanosoma brucei: constitutive activity of the VSG and procyclin gene promoters. EMBO J 9: 3145-3151. PubMed: 1698609.
61. Kooter JM, Winter AJ, de Oliveira C, Wagter R, Borst P (1988) Boundaries of telomere conversion in Trypanosoma brucei. Gene 69: 1-11. doi:10.1016/0378-1119(88)90372-1. PubMed: 3224817.
62. Faulkner SD, Oli MW, Kieft R, Cotlin L, Widener J et al. (2006) In vitro generation of human high-density-lipoprotein-resistant Trypanosoma brucei brucei. Eukaryot Cell 5: 1276-1286. doi:10.1128/EC.00116-06. PubMed: 16896212.
63. Thatcher LF, Gardiner DM, Kazan K, Manners J (2011) A Highly Conserved Effector in Fusarium oxysporum is Required for Full Virulence on Arabidopsis. Mol Plant Microbe Interact.
64. Williams B, Kabbage M, Kim HJ, Britt R, Dickman MB (2011) Tipping the balance: Sclerotinia sclerotiorum secreted oxalic acid suppresses host defenses by manipulating the host redox environment. PLoS Pathog 7: e1002107. PubMed: 21738471.
65. Wiley M, Teygong C, Phelps E, Radke J, Blader IJ (2011) Serum response factor regulates immediate early host gene expression in Toxoplasma gondii-infected host cells. PLOS ONE 6: e18335. doi:10.1371/journal.pone. 0018335. PubMed: 21479245.
66. Tarlovsky Y, Fabian M, Solomaha E, Honsa E, Olson JS et al. (2010) A Bacillus anthracis S-layer homology protein that binds heme and mediates heme delivery to IsdC. J Bacteriol 192: 3503-3511. doi:10.1128/JB.00054-10. PubMed: 20435727.
67. Salmon D, Vanwalleghem G, Morias Y, Denoeud J, Krumbholz C et al. (2012) Adenylate cyclases of Trypanosoma brucei inhibit the innate immune response of the host. Science 337: 463-466. doi:10.1126/science.1222753. PubMed: 22700656. science.1222753 . PII;Available: . doi:10.1126/science.1222753
68. Simarro PP, Diarra A, Ruiz Postigo JA, Franco JR, Jannin JG (2011) The human African trypanosomiasis control and surveillance programme of the World Health Organization 2000-2009: the way forward. PLoS Negl Trop. Drosophila Inf Service 5: e1007.
69. Turner CM, McLellan S, Lindergard LA, Bisoni L, Tait A et al. (2004) Human infectivity trait in Trypanosoma brucei: stability, heritability and relationship to sra expression. Parasitology 129: 445-454. doi:10.1017/ S0031182004005906. PubMed: 15521633. (Pubitemid 39371874)
70. Hirumi H, Hirumi K (1994) Axenic culture of African trypanosome bloodstream forms. Parasitol Today 10: 80-84. doi:10.1016/0169-4758(94)90402-2. PubMed: 15275508. (Pubitemid 24052922)
71. Enyaru JC, Allingham R, Bromidge T, Kanmogne GD, Carasco JF (1993) The isolation and genetic heterogeneity of Trypanosoma brucei gambiense from north-west Uganda. Acta Trop 54: 31-39. doi:10.1016/0001-706X(93)90066-K. PubMed: 8103626.
72. Dukes P, Gibson WC, Gashumba JK, Hudson KM, Bromidge TJ et al. (1992) Absence of the LiTat 1.3 (CATT antigen) gene in Trypanosoma brucei gambiense stocks from Cameroon. Acta Trop 51: 123-134. doi:10.1016/0001-706X(92)90054-2. PubMed: 1354930.
73. Cross GA (1984) Release and purification of Trypanosoma brucei variant surface glycoprotein. J Cell Biochem 24: 79-90. doi:10.1002/jcb.240240107. PubMed: 6725422.
74. Aline RF Jr., Stuart K (1989) Trypanosoma brucei: conserved sequence organization 3' to telomeric variant surface glycoprotein genes. Exp Parasitol 68: 57-66. doi:10.1016/0014-4894(89)90008-8. PubMed: 2645163.
75. Castillo-Acosta VM, Vidal AE, Ruiz-Pérez LM, Van Damme EJ, Igarashi Y et al. (2013) Carbohydrate-binding agents act as potent trypanocidals that elicit modifications in VSG glycosylation and reduced virulence in Trypanosoma brucei. Mol Microbiol, 90: 665-79. doi:10.1111/mmi.12359. PubMed: 23926900.
76. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29: e45. doi:10.1093/nar/29.9.e45. PubMed: 11328886.