Trypanosome genetics: Populations, phenotypes and diversity

Veterinary Parasitology

Volumn 181, Issue 1, 2011, Pages 61-68

  Tait, Andy ^a,b   Morrison, Liam J ^a,b   Duffy, Craig W ^a,b   Cooper, Anneli ^a,b   Turner, C Mike R ^a   Macleod, Annette ^a,b  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

^b Henry Wellcome Institute of Comparative Medical Sciences   (United Kingdom)

Author keywords

Genetics; Pathogenesis; Populations; Trypanosomes

Indexed keywords

ARTICLE; BLOOD BRAIN BARRIER; GENE LOCUS; GENETIC VARIABILITY; HOST PARASITE INTERACTION; IMMUNE RESPONSE; LABORATORY TEST; MOLECULAR EPIDEMIOLOGY; NONHUMAN; PARASITE TRANSMISSION; PARASITE VIRULENCE; PHENOTYPE; POPULATION GENETICS; PROTOZOAL GENETICS; TRYPANOSOMA; TRYPANOSOMA BRUCEI;

ANIMALS; GENETIC VARIATION; MOLECULAR EPIDEMIOLOGY; PHENOTYPE; TRYPANOSOMA BRUCEI BRUCEI; TRYPANOSOMIASIS, AFRICAN; TSETSE FLIES; VIRULENCE;

TRYPANOSOMA BRUCEI;

EID: 84860389392     PISSN: 03044017     EISSN: 18732550     Source Type: Journal    
DOI: 10.1016/j.vetpar.2011.04.024     Document Type: Article

References (72)

1. Agbo E.E.C., Majiwa P.A.O., Claassen H.J.H.M., Tepas M.F.W. Molecular variation of Trypanosoma brucei subspecies as revealed by AFLP fingerprinting. Parasitology 2002, 124:249-358.
2. Balloux F., Lehmann L., de Meeus T. The population genetics of clonal and partially clonal diploids. Genetics 2003, 164:1635-1644.
3. Balmer O., Stearns S.C., Schotzau A., Brun R. Intraspecific competition between co-infecting parasite strains enhances host survival in African trypanosomes. Ecology 2009, 90:3367-3378.
4. Bengaly Z., Sidibe I., Boly H., Sawadogo L., Desquesnes M. Comparative pathogenicity of three genetically distinct Trypanosoma congolense-types in inbred Balb/c mice. Vet. Parasitol. 2002, 105:111-118.
5. Bengaly Z., Sidibe I., Ganaba R., Desquesnes M., Boly H., Sawadogo L. Comparative pathogenicity of three genetically distinct types of Trypanosoma congolense in cattle: clinical observations and haematological changes. Vet. Parasitol. 2002, 108:1-19.
6. Biteau N., Bringaud F., Gibson W., Truc P., Baltz T. Characterization of Trypanozoon isolates using a repeated coding sequence and microsatellite markers. Mol. Biochem. Parasitol. 2000, 105:187-202.
7. Burkard G., Fragoso C.M., Roditi I. Highly efficient stable transformation of bloodstream forms of Trypanosoma brucei. Mol. Biochem. Parasitol. 2007, 153:220-223.
8. Charlier C., Coppieters W., Rollin F., Desmecht D., Agerholm J., Cambisano S., Carta N., Dardano E., Dive S., Fasquelle M., Frennet C.J., Hanset C., Hubin R., Jorgensen X., Karim C., Kent L., Harvey M., Pearce K.B., Simon R., Tama P., Nie N., Vandeputte H., Lien S., Longeri S., Fredholm M., Harvey M.R., Georges J.M. Highly effective SNP-based association mapping and management of recessive defects in livestock. Nat. Genet. 2008, 40:449-454.
9. Cooper A., Tait A., Sweeney L., Tweedie A., Morrison L., Turner C.M.R., MacLeod A. Genetic analysis of the human infective trypanosome Trypanosoma brucei gambiense: chromosomal segregation, crossing over, and the construction of a genetic map. Genome Biol. 2008, 9:R103.
10. Courtin D., Berthier D., Thevenon S., Dayo G.-K., Garcia A., Bucheton B. Host genetics in African trypanosomiasis. Infect. Gen. Evol. 2008, 8:229-238.
11. Coustou V., Guegan F., Plazolles N., Baltz T. Complete in vitro life cycle of Trypanosoma congolense: development of genetic tools. PLoS Negl. Trop. Dis. 2010, 4:e618.
12. Delespaux V., de Koning H.P. Drugs and drug resistance in African trypanosomiasis. Drug Res. Updates 2007, 10:30-50.
13. Duffy C.W., Morrison L.J., Black A., Pinchbeck G.L., Christley R.M., Schoenefeld A., Tait A., Turner C.M.R., MacLeod A. Trypanosoma vivax displays a clonal population structure. Int. J. Parasitol. 2009, 39:1475-1483.
14. Fasogbon A.I., Knowles G., Gardiner P.R. A comparison of the isoenzymes of Trypanosoma (duttonella) vivax isolates from East and West Africa. Int. J. Parasitol. 1990, 20:389-394.
15. Fevre E.M., Wissmann B.V., Welburn S.C., Lutumba P. The burden of Human African Trypanosomiasis. PLoS Negl. Trop. Dis. 2008, 2:e333.
16. Garcia A., Courtin D., Solano P., Koffi M., Jamonneau V. Human African trypanosomiasis: connecting parasite and host genetics. Trends Parasitol. 2006, 22:405-409.
17. Gardiner P.R. Recent studies of the biology of Trypanosoma vivax. Adv. Parasitol. 1989, 28:229-317.
18. Gashumba J.K., Baker R.D., Godfrey D.G. Trypanosoma congolense: the distribution of enzymic variants in East and West Africa. Parasitology 1988, 96:475-486.
19. Gibson W.C., Marshall T.F., de C., Godfrey D.G. 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.
20. Gibson W.C. Will the real Trypansoma b. gambiense please stand up. Parasitol. Today 1986, 2:255-257.
21. Gibson W.C., Bailey M. Genetic exchange in Trypanosoma brucei: evidence for meiosis from analysis of a cross between drug-resistant transformants. Mol. Biochem. Parasitol. 1994, 64:241-252.
22. Gibson W.C. The significance of genetic exchange in trypanosmes. Parasitol. Today 1995, 11:465-468.
23. Gibson W.C., Stevens J. Genetic exchange in the Trypanosomatidae. Adv. Parasitol. 1999, 43:1-45.
24. Gibson W., Peacock L., Ferris V., Williams K., Bailey M. The use of yellow fluorescent hybrids to indicate mating in Trypanosoma brucei. Parasites Vectors 2008, 1:4.
25. Grab D.J., Nikolskaia O., Kim Y.V., Lonsdale-Eccles J.D., Ito S., Hara T., Fukuma T., Nykrko E., Jim K.J., Stins M.F., Delannoy M.J., Kim K.S. African trypanosome interactions with an in vitro model of the human blood-brain barrier. J. Parasitol. 2004, 90:970-979.
26. Hanotte O., Ronin Y., Agaba M., Nilsson P., Gelhaus A., horstmann R., Sugimoto Y., Kemp S., Gibson J., Korol A., Soller M., Teale A. Mapping of quantitative trait loci controlling trypanotolerance in a cross of tolerant West African N'Dama and susceptible East African Boran cattle. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:7443-7448.
27. Hide G., Tilley A. Use of mobile genetic elements as tools for molecular epidemiology. Int. J. Parasitol. 2001, 31:599-602.
28. Hill E.W., O'Gorman G.M., Agaba M., Gibson J.P., Hanotte O., Kemp S.J., Naessens J., Coussens P.M., Machugh D.E. Understanding bovine trypanosomiasis and trypanotolerance: the promise of functional genomics. Vet. Immunol. Immunopathol. 2005, 105:247-258.
29. Hoare C.A. The Trypanosomes of Mammals A Zoological Monograph 1972, Blackwell Scientific Publications, Oxford.
30. Holzmuller P., Biron D.G., Courtois P., Koffi M., Bras-Goncalves R., de Dauloue S., Solano P., Cuny G., Vincendeau P., Jamonneau V. 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.
31. Iraqi F., Clapcott S.J., Kumari P., Haley C.S., Kemp S.J., Teale A.J. Fine mapping of trypanosomiasis resistance loci in murine advanced intercross lines. Mamm. Genome 2000, 11:645-648.
32. Jamonneau V., Garcia A., Frezil J.L., N'guessan P., N'dri L., Sanon R., Laveissiere C., Truc P. Clinical and biological evolution of human trypanosomiasis in Cote d'Ivoire. Ann. Trop. Med. Parasitol. 2000, 94:831-835.
33. Jamonneau V., Barnabe C., Koffi M., Sane B., Cuny G., Solano P. Identification of Trypanosoma brucei circulating in a sleeping sickness focus in Cote d'Ivoire: assessment of genotype selection by the isolation method. Infect. Genet. Evol. 2003, 3:143-149.
34. Jamonneau V., Ravel S., Garcia A., Koffi M., Truc P., Laveissiere C., Herder S., Grebaut P., Cuny G., Solano P. Characterization of Trypanosoma brucei s.l. infecting asymptomatic sleeping-sickness patients in Cote d'Ivoire: a new genetic group? Ann. Trop. Med. Parasitol. 2004, 98:329-337.
35. Jenni L., Marti S., Schweizer J., Betschart B., LePage R.W.F., Wells J.M., Tait A., Pays E., Paindavoine P., Steinert M. Hybrid formation between African trypanosomes during cyclical transmission. Nature 1986, 322:173-175.
36. Karlsson E.K., Baranowska I., Wade C.M., Salmon Hillbertz N.H., Zody M.C., Anderson N., Biagi T.M., Patterson N., Pielberg G.R., Kulbokas E.J., 3rd, Comstock K.E., Keller E.T., Mesirov J.P., von Euler H., Kampe O., Hedhammar A., Lander E.S., Andersson G., Andersson L., Lindblad-Toh K. Efficient mapping of Mendelian traits in dogs through genome-wide association. Nat. Genet. 2007, 39:1321-1328.
37. Kemp S.J., Iraqi F., Darvasi A., Soller M., Teale A.J. Localization of genes controlling resistance to trypanosomiasis in mice. Nat. Genet. 1997, 16:194-196.
38. Koffi M., Solano P., Barnabé C., de Meeûs T., Bucheton B., Cuny G., Jamonneau V. Genetic characterisation of Trypanosoma brucei s.l. using microsatellite typing: new perspectives for the molecular epidemiology of human african trypanosomosis. Infect. Genet. Evol. 2007, 7:675-684.
39. Koffi M., De Meeûs T., Bucheton B., Solano P., Camara M., Kaba D., Cuny G., Ayala F.J., Jamonneau V. Population genetics of Trypanosoma brucei gambiense, the agent of sleeping sickness in Western Africa. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:209-214.
40. MacLean L., Chisi J.E., Odiit M., Gibson W.C., Ferris V., Picozzi K., Sternberg J.M. Severity of human african trypanosomiasis in East Africa is associated with geographic location, parasite genotype, and host inflammatory cytokine response profile. Infect. Immun. 2004, 72:7040-7044.
41. MacLean L., Odiit M., MacLeod A., Morrison L., Sweeney L., Cooper A., Kennedy P.G., Sternberg J.M. Spatially and genetically distinct African trypanosome virulence variants defined by host interferon-gamma response. J. Infect. Dis. 2007, 196:1620-1628.
42. MacLeod A., Tweedie A., Welburn S.C., Maudlin I., Turner C.M., Tait A. Minisatellite marker analysis of Trypanosoma brucei: reconciliation of clonal, panmictic, and epidemic population genetic structures. Proc. Natl. Acad. Sci. U.S.A. 2000, 97:13442-13447.
43. MacLeod A., Tweedie A., McLellan S., Hope M., Taylor S., Cooper A., Sweeney L., Turner C.M.R., Tait A. Allelic segregation and independent assortment in T. brucei crosses: proof that the genetic system is Mendelian and involves meiosis. Mol. Biochem. Parasitol. 2005, 143:12-19.
44. MacLeod A., Tweedie A., McLellan S., Taylor S., Hall N., Berriman M., El-Sayed N.M., Hope M., Michael C., Turner R., Tait C.M.R.A. The genetic map and comparative analysis with the physical map of Trypanosoma brucei. Nucleic Acids Res. 2005, 33:6688-6693.
45. MacLeod A., Turner M., Tait A. The system of genetic exchange in Trypanosoma brucei and other Trypanosomatids. Trypanosomes After the Genome 2007, 71-91. Horizon Bioscience. D. Barry, R. McCulloch, J. Mottram, A. Acosta-Serrano (Eds.).
46. Majiwa P.A.O., Hamers R., Vanmmeirvenne N., Matthyssens G. Evidence for genetic diversity in Trypanosoma congolense. Parasitology 1986, 93:291-304.
47. Masiga D.K., Tait A., Turner C.M.R. The use of the amplified fragment length polymorphism (AFLP) technique in parasite genetics. Parasitol. Today 2000, 16:350-353.
48. Masumu J., Geysen D., Vansnick N.E., Geerts S., Van den Bossche P. A modified AFLP for Trypanosoma congolense isolate characterisation. J. Biotechnol. 2006, 125:22-26.
49. Masumu J., Marcotty T., Geysen D., Geerts S., Vercruysse J., Dorny P., Van den Bossche P. Comparison of the virulence of Trypanosoma congolense strains isolated from cattle in a trypanosomiasis endemic area of eastern Zambia. Int. J. Parasitol. 2006, 36:497-501.
50. Masumu J., Marcotty T., Ndeledje N., Kubi C., Geerts S., Vercruysse J., Dorny P., Van den Bossche P. Comparison of the transmissibility of Trypanosoma congolense strains, isolated in a trypanosomiasis endemic area of eastern Zambia, by Glossina morsitans morsitans. Parasitology 2006, 133:331-334.
51. Matovu E., Seebeck T., Enaru J.C.K., Kaminsky R. Drug resistance in Trypanosoma brucei spp., the causative agents of sleeping sickness in man and nagana in cattle. Microbes. Infect. 2001, 3:763-770.
52. Maynard Smith J., Smith N.H., O'Rourke M., Spratt B.G. How clonal are bacteria?. Proc. Natl. Acad. Sci. U.S.A. 1993, 90:4384-4388.
53. McNamara J.J., Bailey J.W., Smith D.H., Wakhooli S., Godfrey D.G. Isolation of Trypanosoma brucei gambiense from northern Uganda: evaluation of the kit for in vitro isolation (KIVI) in an epidemic focus. Trans. R. Soc. Trop. Med. Hyg. 1995, 89:388-389.
54. Morrison L.J., Tait A., McCormack G., Sweeney L., Black A., Truc P., Likeufack A.C.L., Turner C.M., Macleod A. Trypanosoma brucei gambiense type 1 populations from human patients are clonal and display geographical genetic differentiation. Infect. Genet. Evol. 2008, 8:847-854.
55. Morrison L.J., Tweedie A., Black A., Pinchbeck G., Christley R., Schoenefeld A., Hertz-Fowler C., MacLeod A., Turner C.M.R., Tait A. Discovery of mating in the major African livestock pathogen Trypanosoma congolense. PLoS One 2009, 4:e5564.
56. Morrison L.J., McLellan S., Sweeney L., Chi Chan C., MacLeod A., Turner C.M.R., Tait A. Role for parasite genetic diversity in differential host responses to Trypanosoma brucei infection. Infect. Immun. 2009, 78:1096-1108.
57. Morrison L.J., Tait A., McLellan S., Sweeney L., Turner C.M.R., MacLeod A. A major genetic locus in Trypanosoma brucei is a determinant of host pathology. PLoS Negl. Dis. 2010, 3:e557.
58. Ngo H., Tschudi C., Gull K., Ullu E. Double stranded RNA induces mRNA degradation in Trypanosoma brucei. Proc. Natl. Acad. Sci. U.S.A. 1998, 95:14687-14692.
59. Nikolskaia O.V., Lima A.P.C.A., Kim Y.V., Lonsdale-Eccles J.D., Fukuma T., Scharfstein J., Grab D.J. Blood-brain barrier traversal by African trypanosomes requires calcium signaling induced by parasite cysteine protease. J. Clin. Invest. 2006, 116:2739-2747.
60. Peacock L., Ferris V., Bailey M., Gibson W. Intraclonal mating occurs during tsetse transmission of Trypanosoma brucei. Parasites Vectors 2009, 2:43.
61. Schurko A.M., Logsdon J.M.J. Using a meiosis detection toolkit to investigate ancient asexual " scandals" and the evolution of sex. Bioessays 2008, 30:579-589.
62. Schweizer J., Tait A., Jenni L. The timing and frequency of hybrid formation in African trypanosomes during cyclical transmission. Parasitol. Res. 1988, 75:98-101.
63. Simo G., Cuny G., Demonchy R., Herder S. Trypanosoma brucei gambiense: study of population genetic structure of central African stocks using amplified fragment length polymorphism (AFLP). Exp. Parasitol. 2007, 118:172-180.
64. Tibayrenc M., Kjellberg F., Ayala F.J. A clonal theory of parasitic protozoa: the population structures of entamoeba, giardia, leishmania, naegleria, plasmodium, trichomonas, and trypanosoma and their medical and taxonomical consequences. Proc. Natl. Acad. Sci. U.S.A. 1990, 87:2414-2418.
65. Tait A. Evidence for diploidy and mating in trypanosomes. Nature 1980, 287:536-538.
66. Tait A., Buchanan N., Hide G., Turner C.M.R. Self-fertilisation in Trypanosoma brucei. Mol. Biochem. Parasitol. 1996, 76:31-42.
67. Tait A., Masiga D., Ouma J., MacLeod A., Sasse J., Melville M., Lindegard G., McIntosh A., Turner C.M.R. The genetic analysis of complex phenotypes in T. brucei. Phil. Trans. Roy. Soc. B 2002, 367:89-99.
68. Tait A., MacLeod A., Tweedie A., Masiga D., Turner C.M.R. Genetic exchange in T. brucei: evidence for mating prior to metacyclic stage development. Mol. Biochem. Parasitol. 2007, 151:133-136.
69. Tilley A., Welburn S.C., Fevre E.M., Feil E.J., Hide G. Trypanosoma brucei: Trypanosome strain typing using PCR analysis of mobile genetic elements (MGE-PCR). Exp. Parasitol. 2003, 104:26-32.
70. Turner C.M.R., Sternberg J., Buchanan N., Smith E., Hide G., et al. Evidence that the mechanism of gene exchange in Trypanosoma brucei involves meiosis and syngamy. Parasitology 1990, 101:377-386.
71. Welburn S.C., Maudlin I., Milligan P.J.M. Trypanozoon: infectivity to humans is linked to reduced transmissibility in tsetse. I. Comparison of human serum-resistant and human serum-sensitive field isolates. Exp. Parasitol. 1995, 81:404-408.
72. Young C.J., Godfrey D.G. Enzyme polymorphism and the distribution of Trypanosoma congolense isolates. Ann. Trop. Med. Parasitol. 1983, 77:467-481.