Genetic Recombination between Human and Animal Parasites Creates Novel Strains of Human Pathogen

PLoS Neglected Tropical Diseases

Volumn 9, Issue 3, 2015, Pages

  Gibson, Wendy ^a   Peacock, Lori ^a   Ferris, Vanessa ^a   Fischer, Katrin ^a   Livingstone, Jennifer ^a   Thomas, James ^a   Bailey, Mick ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AFRICAN TRYPANOSOMIASIS; ARTICLE; GENETIC RECOMBINATION; GENETIC VARIABILITY; GENOTYPE; HUMAN; INHERITANCE; MOUSE; NEW SPECIES; NONHUMAN; PARASITE SURVIVAL; PARASITEMIA; POLYMERASE CHAIN REACTION; PULSED FIELD GEL ELECTROPHORESIS; REPRODUCTION; TRYPANOSOMA BRUCEI BRUCEI; TRYPANOSOMA BRUCEI RHODESIENSE; VIRULENCE; AFRICA; ANIMAL; CROSS BREEDING; FLUORESCENCE; GENETIC VARIATION; GENETICS; HORIZONTAL GENE TRANSFER; PARASITOLOGY; SPECIES DIFFERENCE; TRYPANOSOMIASIS, AFRICAN;

MEMBRANE PROTEIN; PROTOZOAL PROTEIN; SERUM RESISTANCE ASSOCIATED PROTEIN, TRYPANOSOMA BRUCEI;

AFRICA, EASTERN; ANIMALS; CROSSES, GENETIC; FLUORESCENCE; GENE TRANSFER, HORIZONTAL; GENETIC VARIATION; HUMANS; MEMBRANE GLYCOPROTEINS; PROTOZOAN PROTEINS; RECOMBINATION, GENETIC; SPECIES SPECIFICITY; TRYPANOSOMA BRUCEI RHODESIENSE; TRYPANOSOMIASIS, AFRICAN;

EID: 84928820643     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0003665     Document Type: Article

References (56)

1. Gibson W, Will the real Trypanosoma brucei rhodesiense please step forward? Trends Parasitol. 2002; 18: 486–490. 12473364
2. Xong VH, 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. 9865701
3. 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
4. Njiru ZK, Mikosza ASJ, Armstrong T, Enyaru JC, Ndung'u JM, Thompson ARC, Loop-Mediated Isothermal Amplification (LAMP) Method for Rapid Detection of Trypanosoma brucei rhodesiense. PLoS NTD. 2008; 2: e147.
5. Gibson W, Species-specific probes for the identification of the African tsetse-transmitted trypanosomes. Parasitology. 2009; 136: 1501–1507. doi: 10.1017/S0031182009006179 19490726
6. Balmer O, Beadell JS, Gibson W, Caccone A, Phylogeography and taxonomy of Trypanosoma brucei. PLoS NTD. 2011; 5: e961.
7. Sistrom M, Evans B, Bjornson R, Gibson W, Balmer O, Mäser P, et al. Comparative genomics reveals multiple genetic backgrounds of human pathogenicity in the Trypanosoma brucei complex. Genome Biol Evol. 2014; 6: 2811–2819. doi: 10.1093/gbe/evu222 25287146
8. Goodhead I, Capewell P, Bailey JW, Beament T, Chance M, Kay S, et al. Whole-genome sequencing of Trypanosoma brucei reveals introgression between subspecies that is associated with virulence. MBio. 2013; 4: e00197–00213. doi: 10.1128/mBio.00197-13 23963174
9. Jenni L, Marti S, Schweizer J, Betschart B, Lepage RWF, Wells JM, et al. Hybrid formation between African trypanosomes during cyclical transmission. Nature. 1986; 322: 173–175. 3724860
10. Peacock L, Ferris V, Sharma R, Sunter J, Bailey M, Carrington M, et al. Identification of the meiotic life cycle stage of Trypanosoma brucei in the tsetse fly. Proc Natl Acad Sci U S A. 2011; 108: 3671–3676. doi: 10.1073/pnas.1019423108 21321215
11. Peacock L, Bailey M, Carrington M, Gibson W, Meiosis and haploid gametes in the pathogen Trypanosoma brucei. Curr Biol. 2014; 24: 1–6. doi: 10.1016/j.cub.2013.11.017 24332542
12. Gibson WC, Analysis of a genetic cross between Trypanosoma brucei rhodesiense and T. b. brucei. Parasitology. 1989; 99: 391–402. 2575239
13. Gibson W, Garside L, Bailey M, Trisomy and chromosome size changes in hybrid trypanosomes from a genetic cross between Trypanosoma brucei rhodesiense and T. b. brucei. Mol Biochem Parasitol. 1992; 52: 189–200.
14. Gibson W, Winters K, Mizen G, Kearns J, Bailey M, Intraclonal mating in Trypanosoma brucei is associated with out-crossing. Microbiology. 1997; 143: 909–920. 9084175
15. Gibson WC, Mizen VH, Heritability of the trait for human infectivity in genetic crosses of Trypanosoma brucei ssp. Trans Roy Soc Trop Med Hyg. 1997; 91: 236–237. 9196780
16. Gibson W, Ferris V, Conservation of the genomic location of the human serum resistance associated gene in Trypanosoma brucei rhodesiense. Mol Biochem Parasitol. 2003; 130: 159–162. 12946855
17. Turner CMR, Melville SE, Tait A, A proposal for karyotype nomenclature in Trypanosoma brucei. Parasitol Today. 1997; 13: 5–6. 15275158
18. Becker M, Aitcheson N, Byles E, Wickstead B, Louis E, Rudenko G, Isolation of the repertoire of VSG expression site containing telomeres of Trypanosoma brucei 427 using transformation-associated recombination in yeast. Genome Res. 2004; 14: 2319–2329. 15520294
19. McCulloch R, Horn D, What has DNA sequencing revealed about the VSG expression sites of African trypanosomes? Trends Parasitol. 2009; 25: 359–363. doi: 10.1016/j.pt.2009.05.007 19632154
20. Hertz-Fowler C, Figueiredo LM, Quail MA, Becker M, Jackson A, Bason N, et al. Telomeric expression sites are highly conserved in Trypanosoma brucei. PLoS One. 2008; 3: e3527. doi: 10.1371/journal.pone.0003527 18953401
21. Young R, Taylor JE, Kurioka A, Becker M, Louis EJ, Rudenko G, 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. 2008; 9: 385. doi: 10.1186/1471-2164-9-385 18700033
22. Steverding D, Stierhof YD, Chaudhri M, Ligtenberg M, Schell D, Becksickinger AG, et al. ESAG 6 and ESAG 7 products of Trypanosoma brucei form a transferrin-binding protein complex. Eu J Cell Biol. 1994; 64: 78–87.
23. Bitter W, Gerrits H, Kieft R, Borst P, The role of transferrin-receptor variation in the host range of Trypanosoma brucei. Nature. 1998; 391: 499–502. 9461219
24. Gerrits H, Mussmann R, Bitter W, Kieft R, Borst P, The physiological significance of transferrin receptor variations in Trypanosoma brucei. Mol Biochem Parasitol. 2002; 119: 237–247. 11814575
25. Graham SV, Terry S, Barry JD, A structural and transcription pattern for variant surface glycoprotein gene expression sites used in metacyclic stage Trypanosoma brucei. Mol Biochem Parasitol. 1999; 103: 141–154. 10551359
26. Gibson WC, Marshall TFdC, 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
27. 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. 2002; 1: 207–214. 12798017
28. Stevens JR, Lanham SM, Allingham R, Gashumba JK, A simplified method for identifying subspecies and strain groups in Trypanozoon by isoenzymes. Ann Trop Med Parasit. 1992; 86: 9–28. 1616401
29. Gibson WC, Fase-Fowler F, Borst P, Further analysis of intraspecific variation in Trypanosoma brucei using restriction site polymorphisms in the maxi-circle of kinetoplast DNA. Mol Biochem Parasitol. 1985; 15: 21–36. 2985985
30. Peacock L, Ferris V, Bailey M, Gibson W, Fly transmission and mating of Trypanosoma brucei brucei strain 427. Mol Biochem Parasitol. 2008; 160: 100–106. doi: 10.1016/j.molbiopara.2008.04.009 18524395
31. Bingle LEH, Eastlake JL, Bailey M, Gibson WC, A novel GFP approach for the analysis of genetic exchange in trypanosomes allowing the in situ detection of mating events. Microbiology. 2001; 147: 3231–3240. 11739755
32. Campbell RE, Tour O, Palmer AE, Steinbach PA, Baird GS, Zacharias DA, et al. A monomeric red fluorescent protein. Proc Natl Acad Sci U S A. 2002; 99: 7877–7882. 12060735
33. Gibson W, Peacock L, Ferris V, Williams K, Bailey M, The use of yellow fluorescent hybrids to indicate mating in Trypanosoma brucei. Parasit Vector. 2008; 1: 4.
34. Cunningham I, New culture medium for maintenance of tsetse tissues and growth of trypanosomatids. J Protozoo. 1977; 24: 325–329. 881656
35. Peacock L, Ferris V, Bailey M, Gibson W, Mating compatibility in the parasitic protist Trypanosoma brucei. Parasit Vector. 2014; 7: 78. doi: 10.1186/1756-3305-7-78 24559099
36. Peacock L, Ferris V, Bailey M, Gibson W, Intraclonal mating occurs during tsetse transmission of Trypanosoma brucei. Parasit Vector. 2009; 2: 43. doi: 10.1186/1756-3305-2-43 19772562
37. Macleod ET, Maudlin I, Darby AC, Welburn SC, Antioxidants promote establishment of trypanosome infections in tsetse. Parasitology. 2007; 134: 827–831. 17306056
38. Hirumi H, Hirumi K, Continuous cultivation of Trypanosoma brucei bloodstream forms in a medium containing a low concentration of serum protein without feeder cell layers. J Parasitol. 1989; 75: 985–989. 2614608
39. MacLeod A, Tweedie A, McLellan S, Taylor S, Cooper A, Sweeney L, et al. Allelic segregation and independent assortment in Trypanosoma brucei crosses: Proof that the genetic system is Mendelian and involves meiosis. Mol Biochem Parasitol. 2005; 143: 12–19. 15941603
40. Van der Ploeg LHT, Schwartz DC, Cantor CR, Borst P, Antigenic variation in Trypanosoma brucei analysed by electrophoretic separation of chromosome-sized DNA molecules. Cell. 1984; 37: 77–84. 6202420
41. Gibson WC, Osinga KA, Michels PAM, Borst P, Trypanosomes of subgenus Trypanozoon are diploid for housekeeping genes. Mol Biochem Parasitol. 1985; 16: 231–242. 3840571
42. Tait A, Barry JD, Wink R, Sanderson A, Crowe JS, Enzyme variation in Trypanosoma brucei spp. II. Evidence for T. b. rhodesiense being a set of variants of T. b. brucei. Parasitology. 1985; 90: 89–100. 3856830
43. Gibson WC, Wellde BT, Characterisation of Trypanozoon stocks from the South Nyanza sleeping sickness focus in Western Kenya. Trans Roy Soc Trop Med Hyg. 1985; 79: 671–676. 4095748
44. Komba EK, Kibona SN, Ambwene AK, Stevens JR, Gibson WC, Genetic diversity among Trypanosoma brucei rhodesiense isolates from Tanzania. Parasitology. 1997; 115: 571–579. 9488868
45. MacLean L, Chisi JE, Odiit M, Gibson WC, Ferris V, Picozzi K, et al. Severity of Human African Trypanosomiasis in East Africa is associated with geographic location, parasite genotype and host-inflammatory cytokine response profile. Infection and Immunity. 2004; 72: 7040–7044. 15557627
46. Godfrey DG, Baker RD, Rickman LR, Mehlitz D, The distribution, relationships and identification of enzymic variants within the subgenus Trypanozoon. Adv Parasitol. 1990; 29: 1–74. 2181826
47. Stevens JR, Godfrey DG, Numerical taxonomy of Trypanozoon based on polymorphisms in a reduced range of enzymes. Parasitology. 1992; 104: 75–86. 1614742
48. Coleman PG, Welburn SC, Are fitness costs associated with resistance to human serum in Trypanosoma brucei rhodesiense? Trends Parasitol. 2004; 20: 311–315. 15193561
49. Barry JD, Graham SV, Fotheringham M, Graham VS, Kobryn K, Wymer B, VSG gene control and infectivity strategy of metacyclic stage Trypanosoma brucei. Mol Biochem Parasitol. 1998; 91: 93–105. 9574928
50. De Greef C, Hamers R, The serum resistance associated (SRA) gene of Trypanosoma brucei rhodesiense encodes a VSG-like protein. Mol Biochem Parasitol. 1994; 68: 277–284. 7739673
51. 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. 2003; 127: 79–84. 12615339
52. Vanhamme L, Paturiaux-Hanocq F, Poelvoorde P, Nolan D, Lins L, Van den Abbeele J, et al. Apolipoprotein L-1 is the trypanosome lytic factor of human serum. Nature. 2003; 422: 83–87. 12621437
53. Poelvoorde P, Vanhamme L, Van den Abbeele J, Switzer WM, Pays E, Distribution of apolipoprotein L-I and trypanosome lytic activity among primate sera. Mol Biochem Parasitol. 2004; 134: 155–157. 14747153
54. 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 U S A. 2009; 106: 19509–19514. doi: 10.1073/pnas.0905669106 19858474
55. Brun R, Jenni L, Human serum resistance of metacyclic forms of Trypanosoma brucei brucei, T. brucei rhodesiense and T. brucei gambiense. Parasitol Res. 1987; 73: 218–223. 3588581
56. Gibson W, 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. 7935602