Species-Specific Adaptations of Trypanosome Morphology and Motility to the Mammalian Host

PLoS Pathogens

Volumn 12, Issue 2, 2016, Pages

  Bargul, Joel L ^a,b,c   Jung, Jamin ^a   McOdimba, Francis A ^c   Omogo, Collins O ^c   Adung’a, Vincent O ^c,d   Krüger, Timothy ^a   Masiga, Daniel K ^c   Engstler, Markus ^a  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b JOMO KENYATTA UNIVERSITY OF AGRICULTURE AND TECHNOLOGY   (Kenya)

^c INTERNATIONAL CENTRE OF INSECT PHYSIOLOGY AND ECOLOGY ICIPE   (Kenya)

^d EGERTON UNIVERSITY   (Kenya)

Author keywords

[No Author keywords available]

Indexed keywords

BEHAVIOR; CARDIOVASCULAR SYSTEM; CELL ADHESION; CELL BODY; CELL MOTILITY; CHIRALITY; FLAGELLUM; HUMAN; HUMAN EXPERIMENT; LIVESTOCK; MAMMAL; MICROENVIRONMENT; MORPHOLOGY; OSCILLATION; PARASITE; RIGIDITY; SPECIES; SUBSPECIES; SWIMMING; TRYPANOSOMA; TRYPANOSOMA VIVAX; VELOCITY; VISCOSITY; WAVEFORM; ADAPTATION; AFRICAN TRYPANOSOMIASIS; ANIMAL; BOVINE; CELL MOTION; GLOSSINIDAE; HOST PARASITE INTERACTION; ISOLATION AND PURIFICATION; MOUSE; PARASITOLOGY; PHYSIOLOGY; SPECIES DIFFERENCE; SPRAGUE DAWLEY RAT; TRYPANOSOMA BRUCEI BRUCEI;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; CATTLE; CELL MOVEMENT; FLAGELLA; HOST-PARASITE INTERACTIONS; MAMMALS; MICE; RATS, SPRAGUE-DAWLEY; SPECIES SPECIFICITY; TRYPANOSOMA BRUCEI BRUCEI; TRYPANOSOMA VIVAX; TRYPANOSOMIASIS, AFRICAN; TSETSE FLIES;

EID: 84959457783     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1005448     Document Type: Article

References (54)

1. Hoare CA, The trypanosomes of mammals. A zoological monograph. Oxford, Edinburgh: Blackwell Scientific Publications; 1972.
2. Auty H, Anderson NE, Picozzi K, Lembo T, Mubanga J, Hoare R, et al. Trypanosome diversity in wildlife species from the serengeti and Luangwa Valley ecosystems. PLoS Negl Trop Dis. 2012;6: e1828. doi: 10.1371/journal.pntd.000182823094115
3. Duke HL, On Trypanosoma brucei, T. rhodesiense and T. gambiense and their Ability to Infect Man. Parasitology. 1935;27: 46–67. doi: 10.1017/S0031182000014943
4. Lai D-H, Hashimi H, Lun Z-R, Ayala FJ, Lukeš J, Adaptations of Trypanosoma brucei to gradual loss of kinetoplast DNA: Trypanosoma equiperdum and Trypanosoma evansi are petite mutants of T. brucei. Proc Natl Acad Sci. 2008;105: 1999–2004. doi: 10.1073/pnas.071179910518245376
5. Desquesnes M, Holzmuller P, Lai D-H, Dargantes A, Lun Z-R, Jittaplapong S, Trypanosoma evansi and surra: a review and perspectives on origin, history, distribution, taxonomy, morphology, hosts, and pathogenic effects. BioMed Res Int. 2013;2013: 194176. doi: 10.1155/2013/19417624024184
6. Borst P, Ulbert S, Control of VSG gene expression sites. Mol Biochem Parasitol. 2001;114: 17–27. 11356510
7. McCulloch R, Antigenic variation in African trypanosomes: monitoring progress. Trends Parasitol. 2004;20: 117–121. doi: 10.1016/j.pt.2003.12.00415036032
8. Matthews KR, The developmental cell biology of Trypanosoma brucei. J Cell Sci. 2005;118: 283–290. doi: 10.1242/jcs.0164915654017
9. Engstler M, Thilo L, Weise F, Grünfelder CG, Schwarz H, Boshart M, et al. Kinetics of endocytosis and recycling of the GPI-anchored variant surface glycoprotein in Trypanosoma brucei. J Cell Sci. 2004;117: 1105–1115. doi: 10.1242/jcs.0093814996937
10. Natesan SKA, Peacock L, Matthews K, Gibson W, Field MC, Activation of endocytosis as an adaptation to the mammalian host by trypanosomes. Eukaryot Cell. 2007;6: 2029–2037. doi: 10.1128/EC.00213-0717905918
11. Engstler M, Pfohl T, Herminghaus S, Boshart M, Wiegertjes G, Heddergott N, et al. Hydrodynamic flow-mediated protein sorting on the cell surface of trypanosomes. Cell. 2007;131: 505–515. doi: 10.1016/j.cell.2007.08.04617981118
12. Overath P, Engstler M, Endocytosis, membrane recycling and sorting of GPI-anchored proteins: Trypanosoma brucei as a model system. Mol Microbiol. 2004;53: 735–744. doi: 10.1111/j.1365-2958.2004.04224.x15255888
13. Field MC, Carrington M, Intracellular membrane transport systems in Trypanosoma brucei. Traffic Cph Den. 2004;5: 905–913. doi: 10.1111/j.1600-0854.2004.00234.x
14. Jeffries TR, Morgan GW, Field MC, A developmentally regulated rab11 homologue in Trypanosoma brucei is involved in recycling processes. J Cell Sci. 2001;114: 2617–2626. 11683389
15. Morgan GW, Allen CL, Jeffries TR, Hollinshead M, Field MC, Developmental and morphological regulation of clathrin-mediated endocytosis in Trypanosoma brucei. J Cell Sci. 2001;114: 2605–2615. 11683388
16. Allen CL, Goulding D, Field MC, Clathrin-mediated endocytosis is essential in Trypanosoma brucei. EMBO J. 2003;22: 4991–5002. doi: 10.1093/emboj/cdg48114517238
17. Grünfelder CG, Engstler M, Weise F, Schwarz H, Stierhof Y-D, Boshart M, et al. Accumulation of a GPI-anchored protein at the cell surface requires sorting at multiple intracellular levels. Traffic Cph Den. 2002;3: 547–559.
18. Adung’a VO, Gadelha C, Field MC, Proteomic analysis of clathrin interactions in trypanosomes reveals dynamic evolution of endocytosis. Traffic Cph Den. 2013;14: 440–457. doi: 10.1111/tra.12040
19. Broadhead R, Dawe HR, Farr H, Griffiths S, Hart SR, Portman N, et al. Flagellar motility is required for the viability of the bloodstream trypanosome. Nature. 2006;440: 224–227. doi: 10.1038/nature0454116525475
20. Ralston KS, Lerner AG, Diener DR, Hill KL, Flagellar motility contributes to cytokinesis in Trypanosoma brucei and is modulated by an evolutionarily conserved dynein regulatory system. Eukaryot Cell. 2006;5: 696–711. doi: 10.1128/EC.5.4.696–711.200616607017
21. Griffiths S, Portman N, Taylor PR, Gordon S, Ginger ML, Gull K, RNA interference mutant induction in vivo demonstrates the essential nature of trypanosome flagellar function during mammalian infection. Eukaryot Cell. 2007;6: 1248–1250. doi: 10.1128/EC.00110-0717513568
22. Uppaluri S, Nagler J, Stellamanns E, Heddergott N, Herminghaus S, Engstler M, et al. Impact of microscopic motility on the swimming behavior of parasites: straighter trypanosomes are more directional. PLoS Comput Biol. 2011;7: e1002058. doi: 10.1371/journal.pcbi.100205821698122
23. Weiße S, Heddergott N, Heydt M, Pflästerer D, Maier T, Haraszti T, et al. A quantitative 3D motility analysis of Trypanosoma brucei by use of digital in-line holographic microscopy. PloS One. 2012;7: e37296. doi: 10.1371/journal.pone.003729622629379
24. Heddergott N, Krüger T, Babu SB, Wei A, Stellamanns E, Uppaluri S, et al. Trypanosome motion represents an adaptation to the crowded environment of the vertebrate bloodstream. PLoS Pathog. 2012;8: e1003023. doi: 10.1371/journal.ppat.100302323166495
25. Purcell EM, Life at low Reynolds number. Am J Phys. 1977;45: 3. doi: 10.1119/1.10903
26. Meijering E, Dzyubachyk O, Smal I, conn PM, Chapter nine—Methods for Cell and Particle Tracking. In: Methods in Enzymology. Academic Press; 2012. pp. 183–200. Available: http://www.sciencedirect.com/science/article/pii/B9780123918574000094
27. Shapiro SZ, Naessens J, Liesegang B, Moloo SK, Magondu J, Analysis by flow cytometry of DNA synthesis during the life cycle of African trypanosomes. Acta Trop. 1984;41: 313–323. 6152113
28. Vickerman K, On the surface coat and flagellar adhesion in trypanosomes. J Cell Sci. 1969;5: 163–193. 5353653
29. Walker PJ, Walker JC, Movement of Trypanosomes flagella. JProtozool. 1963;10: 109.
30. Holwill MEJ, The Motion of Strigomonas Oncopelti. J Exp Biol. 1965;42: 125–137.
31. Branche C, Kohl L, Toutirais G, Buisson J, Cosson J, Bastin P, Conserved and specific functions of axoneme components in trypanosome motility. J Cell Sci. 2006;119: 3443–3455. doi: 10.1242/jcs.0307816882690
32. Baron DM, Kabututu ZP, Hill KL, Stuck in reverse: loss of LC1 in Trypanosoma brucei disrupts outer dynein arms and leads to reverse flagellar beat and backward movement. J Cell Sci. 2007;120: 1513–1520. doi: 10.1242/jcs.00484617405810
33. Vickerman K, Developmental cycles and biology of pathogenic trypanosomes. Br Med Bull. 1985;41: 105–114. 3928017
34. Vickerman K, Tetley L, Hendry KA, Turner CM, Biology of African trypanosomes in the tsetse fly. Biol Cell Auspices Eur Cell Biol Organ. 1988;64: 109–119.
35. Krüger T, Engstler M, Flagellar motility in eukaryotic human parasites. Semin Cell Dev Biol. 2015;46: 113–127. doi: 10.1016/j.semcdb.2015.10.03426523344
36. Alizadehrad D, Krüger T, Engstler M, Stark H, Simulating the Complex Cell Design of Trypanosoma brucei and Its Motility. PLoS Comput Biol. 2015;11. doi: 10.1371/journal.pcbi.1003967
37. Chamond N, Cosson A, Blom-Potar MC, Jouvion G, D’Archivio S, Medina M, et al. Trypanosoma vivax infections: pushing ahead with mouse models for the study of Nagana. I. Parasitological, hematological and pathological parameters. PLoS Negl Trop Dis. 2010;4: e792. doi: 10.1371/journal.pntd.000079220706595
38. Clarkson MJ, Awan MA, The immune response of sheep to Trypanosoma vivax. Ann Trop Med Parasitol. 1969;63: 515–527. 4988736
39. Ikede BO, Losos GJ, Hereditary transmission of Trypanosoma vivax in sheep. Br Vet J. 1972;128: i–ii. 5062161
40. van den Ingh TS, Zwart D, Schotman AJ, van Miert AS, Veenendaal GH, The pathology and pathogenesis of Trypanosoma vivax infection in the goat. Res Vet Sci. 1976;21: 264–270. 1025633
41. Gardiner PR, Wilson AJ, Trypanosoma (Duttonefla) vivax. Parasitol Today Pers Ed. 1987;3: 49–52.
42. Abenga JN, A comparative pathology of Trypanosoma brucei infections. Glob Adv Res J Med Med Sci. 2014;3: 390–399.
43. Eyob E, Matios L, Review on camel trypanosomosis (surra) due to Trypanosoma evansi: Epidemiology and host response. Journal of Veterinary Medicine and Animal Health. 2013; 334–43.
44. Losos GJ, Gwamaka G, Histological examination of wild animals naturally infected with pathogenic African trypanosomes. Acta Trop. 1973;30: 57–63. 4144958
45. Losos GJ, Ikede BO, Review of Pathology of Diseases in Domestic and Laboratory Animals Caused by Trypanosoma congolense, T. vivax, T. brucei, T. rhodesiense and T. gambiense. Vet Pathol. 1972;9 (1 Suppl): 1–79.
46. Yorke W, On the variations of the haemolytic complement in experimental trypanosomiasis. Ann Trop Med Parasit. 1911;4: 385.
47. Goodwin LG, Pathological effects of Trypanosoma brucei on small blood vessels in rabbit ear-chambers. Trans R Soc Trop Med Hyg. 1971;65: 82–88. 5092433
48. Goodwin LG, The pathology of African trypanosomiasis. Trans R Soc Trop Med Hyg. 1970;64: 797–817. 5495630
49. Losos GJ, Paris J, Wilson AJ, Dar FK, Distribution of Trypanosoma congolense in tissues of cattle. Trans R Soc Trop Med Hyg. 1973;67: 278.
50. Valli VE, Forsberg CM, Robinson GA, The pathogenesis of Trypanosoma congolense infection in calves. I. Clinical observations and gross pathological changes. Vet Pathol. 1978;15: 608–620. 716157
51. Hemphill A, Ross CA, Flagellum-mediated adhesion of Trypanosoma congolense to bovine aorta endothelial cells. Parasitol Res. 1995;81: 412–420. 7501641
52. 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
53. Leeflang P, Buys J, Blotkamp C, Studies on Trypanosoma vivax: infectivity and serial maintenance of natural bovine isolates in mice. Int J Parasitol. 1976;6: 413–417. 965146
54. Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, et al. Fiji: an open-source platform for biological-image analysis. Nat Methods. 2012;9: 676–682. doi: 10.1038/nmeth.201922743772