The life cycle of Trypanosoma (Nannomonas) congolense in the tsetse fly

详细信息    查看全文

• 作者：Lori Peacock (1) (2)
  Simon Cook (2) (3)
  Vanessa Ferris (1) (2)
  Mick Bailey (2)
  Wendy Gibson (1)
  
• 刊名：Parasites & Vectors
• 出版年：2012
• 出版时间：December 2012
• 年：2012
• 卷：5
• 期：1
• 全文大小：623KB
• 参考文献：1. Stephen LE: / Trypanosomiasis, a veterinary perspective. Pergamon Press, Oxford; 1986.
  2. Hoare CA: / The Trypanosomes of Mammals. Blackwell Scientific Publications, Oxford; 1972.
  3. Stevens JR, Noyes H, Dover GA, Gibson WC: The ancient and divergent origins of the human pathogenic trypanosomes, Trypanosoma brucei and T. cruzi. / Parasitology 1999, 118:107鈥?16. CrossRef
  4. Hamilton PB, Stevens JR, Gaunt MW, Gidley J, Gibson WC: Trypanosomes are monophyletic: evidence from genes for glyceraldehyde phosphate dehydrogenase and small subunit ribosomal RNA. / Int J Parasitol 2004, 34:1393鈥?404. CrossRef
  5. Matthews KR, Gull K: Commitment to differentiation and cell cycle re-entry are coincident but separable events in the transformation of African trypanosomes from their bloodstream to their insect form. / J Cell Sci 1997, 110:2609鈥?618.
  6. Fenn K, Matthews KR: The cell biology of Trypanosoma brucei differentiation. / Curr Opin Microbiol 2007,10(6):539鈥?46. CrossRef
  7. Urwyler S, Studer E, Renggli CK, Roditi I: A family of stage-specific alanine-rich proteins on the surface of epimastigote forms of Trypanosoma brucei. / Mol Micro 2007, 63:218鈥?28. CrossRef
  8. Acosta-Serrano A, Vassella E, Liniger M, Renggli CK, Brun R, Roditi I, Englund PT: The surface coat of procyclic Trypanosoma brucei: Programmed expression and proteolytic cleavage of procyclin in the tsetse fly. / Proc Natl Acad Sci U S A 2001,98(4):1513鈥?518. CrossRef
  9. Roditi I, Carrington M, Turner M: Expression of a polypeptide containing a dipeptide repeat is confined to the insect stage of Trypanosoma brucei. / Nature 1987, 325:272鈥?74. CrossRef
  10. Tetley L, Turner CMR, Barry JD, Crowe JS, Vickerman K: Onset of expression of the variant surface glycoproteins of Trypanosoma brucei in the tsetse fly studied using immunoelectron microscopy. / J Cell Sci 1987, 87:363鈥?72.
  11. Sharma R, Peacock L, Gluenz E, Gull K, Gibson W, Carrington M: Asymmetric cell division as a route to reduction in cell length and change in cell morphology in trypanosomes. / Protist 2008,159(1):137鈥?51. CrossRef
  12. Jenni L, Marti S, Schweizer J, Betschart B, Lepage RWF, Wells JM, Tait A, Paindavoine P, Pays E, Steinert M: Hybrid formation between African trypanosomes during cyclical transmission. / Nature 1986, 322:173鈥?75. CrossRef
  13. Peacock L, Ferris V, Sharma R, Sunter J, Bailey M, Carrington M, Gibson W: Identification of the meiotic life cycle stage of Trypanosoma brucei in the tsetse fly. / Proc Natl Acad Sci U S A 2011,108(9):3671鈥?676. CrossRef
  14. Utz S, Roditi I, Renggli CK, Almeida IC, Acosta-Serrano A, Butikofer P: Trypanosoma congolense procyclins: Unmasking cryptic major surface glycoproteins in procyclic forms. / Euk Cell 2006,5(8):1430鈥?440. CrossRef
  15. Butikofer P, Vassella E, Boschung M, Renggli CK, Brun R, Pearson TW, Roditi I: Glycosylphosphatidylinositol-anchored surface molecules of Trypanosoma congolense insect forms are developmentally regulated in the tsetse fly. / Mol Biochem Parasitol 2002,119(1):7鈥?6. CrossRef
  16. Van den Abbeele J, Claes Y, Van Bockstaele D, Le Ray D: Coosemans M: Trypanosoma brucei spp. development in the tsetse fly: characterization of the post-mesocyclic stages in the foregut and proboscis. / Parasitology 1999, 118:469鈥?78. CrossRef
  17. Lewis EA, Langridge WP: Developmental forms of Trypanosoma brucei in the "saliva" of Glossina pallidipes and G. austeni. / Ann Trop Med Parasit 1947, 41:6鈥?3.
  18. Jefferies D, Helfrich MP, Molyneux DH: Cibarial infections of Trypanosoma vivax and T. congolense in Glossina. / Parasitol Res 1987, 73:289鈥?92. CrossRef
  19. Tetley L, Vickerman K: Differentiation in Trypanosoma brucei: host-parasite cell junctions and their persistence during acquisition of the variable antigen coat. / J Cell Sci 1985, 74:1鈥?9.
  20. Gray MA, Cunningham I, Gardiner PR, Taylor AM, Luckins AG: Cultivation of infective forms of Trypanosoma congolense from trypanosomes in the proboscis of Glossina morsitans. / Parasitology 1981, 82:81鈥?5. CrossRef
  21. Lloyd L, Johnson WB: The trypanosome infections of tsetse flies in northern Nigeria and a new method of estimation. / Bull Entomol Res 1924, 14:265鈥?88.
  22. Thevenaz P, Hecker H: Distribution and attachment of Trypanosoma (Nannomonas) congolense in the proximal part of the proboscis of Glossina morsitans morsitans. / Acta Trop 1980, 37:163鈥?75.
  23. Hirumi H, Hirumi K, Moloo SK, Shaw MK: Trypanosoma brucei brucei: in vitro production of metacyclic forms. / J Protozoo 1992, 39:619鈥?27.
  24. Cunningham I, Honigberg BM: Infectivity reaquisition by Trypanosoma brucei brucei cultivated with tsetse salivary glands. / Science 1977, 197:1279鈥?282. CrossRef
  25. Hirumi H, Hirumi K: In vitro cultivation of Trypanosoma congolense bloodstream forms in the absence of feeder cell layers. / Parasitology 1991, 102:225鈥?36. CrossRef
  26. Gray MA, Ross CA, Taylor AM, Luckins AG: in vitro cultivation of Trypanosoma congolense: the production of infective metacyclic trypanosomes in cultures initiated from cloned stocks. / Acta Trop 1984, 41:343鈥?53.
  27. Ross CA: Trypanosoma congolense: differentiation of metacyclic trypanosomes in culture depends on the concentration of glutamine or proline. / Acta Trop 1987, 44:293鈥?01.
  28. Coustou V, Guegan F, Plazolles N, Baltz T: Complete in vitro life cycle of Trypanosoma congolense: Development of genetic tools. / PLoS NTD 2010,4(3):e618.
  29. Beattie P, Gull K: Cytoskeletal architecture and components involved in the attachment of Trypanosoma congolense epimastigotes. / Parasitology 1997, 115:47鈥?5. CrossRef
  30. Hendry KAK, Vickerman K: The requirement for epimastigote attachment during division and metacyclogenesis in Trypanosoma congolense. / Parasitol Res 1988, 74:403鈥?08. CrossRef
  31. Prain CJ, Ross CA: Trypanosoma congolense: appearance and distribution of variable antigen types during metacyclic differentiation in vitro. / Parasitology 1990, 100:107鈥?13.
  32. Helm JR, Hertz-Fowler C, Aslett M, Berriman M, Sanders M, Quail MA, Soares MB, Bonaldo MF, Sakurai T, Inoue N, / et al.: Analysis of expressed sequence tags from the four main developmental stages of Trypanosoma congolense. / Mol Biochem Parasitol 2009,168(1):34鈥?2. CrossRef
  33. Jackson AP, Berry A, Aslett M, Allison HC, Burton P, Vavrova-Anderson J, Brown R, Browne H, Corton N, Hauser H, / et al.: Antigenic diversity is generated by distinct evolutionary mechanisms in African trypanosome species. / Proc Natl Acad Sci U S A 2012, 109:3416鈥?421. CrossRef
  34. Robertson M: Notes on the life-history of Trypanosoma gambiense, with a brief reference to the cycles of Trypanosoma nanum and Trypanosoma pecorum in Glossina palpalis. / Phil Trans Roy Soc London B 1913, 203:161鈥?84. CrossRef
  35. Gordon RM: Trypanosoma congolense in its passage through the peritrophic membrane of Glossina morsitans. / Trans Roy Soc Trop Med Hyg 1957, 51:296. CrossRef
  36. Kabayo JP: The nature of the nutritional importance of serum-albumin to Glossina morsitans. / J Insect Physiol 1982, 28:917鈥?23. CrossRef
  37. Galun R, Margalit J: Adenine nucleotides as feeding stimulants of tsetse fly Glossina austeni Newst. / Nature 1969, 222:583鈥?84. CrossRef
  38. Peacock L, Ferris V, Bailey M, Gibson W: Multiple effects of the lectin-inhibitory sugars D-glucosamine and N-acetyl-glucosamine on tsetse-trypanosome interactions. / Parasitology 2006, 132:651鈥?58. CrossRef
  39. Macleod ET, Maudlin I, Darby AC, Welburn SC: Antioxidants promote establishment of trypanosome infections in tsetse. / Parasitology 2007, 134:827鈥?31. CrossRef
  40. Young CJ, Godfrey DG: Enzyme polymorphism and the distribution of Trypanosoma congolense isolates. / Ann Trop Med Parasit 1983, 77:467鈥?81.
  41. Peacock L, Ferris V, Bailey M, Gibson W: Dynamics of infection and competition between two strains of Trypanosoma brucei brucei in the tsetse fly observed using fluorescent markers. / Kinetoplastid Biol Dis 2007, 6:4. CrossRef
  42. Godfrey DG: Types of Trypanosoma congolense. I. Morphological differences. / Ann Trop Med Parasit 1960, 54:428鈥?38.
  43. Vickerman K: Developmental cycles and biology of pathogenic trypanosomes. / Brit Med Bull 1985, 41:105鈥?14.
  44. Matthews KR, Sherwin T, Gull K: Mitochondrial genome repositioning during differentiation of the African trypanosome between life cycle forms is microtubule mediated. / J Cell Sci 1995, 108:2231鈥?239.
  45. Hendriks EF, Robinson DR, Hinkins M, Matthews KR: A novel CCCH protein which modulates differentiation of Trypanosoma brucei to its procyclic form. / EMBO J 2001,20(23):6700鈥?711. CrossRef
  46. Hammarton TC, Engstler M, Mottram JC: The Trypanosoma brucei cyclin, CYC2, is required for cell cycle progression through G1 phase and for maintenance of procyclic form cell morphology. / J Biol Chem 2004,279(23):24757鈥?4764. CrossRef
  47. Buxton PA: / The natural history of tsetse flies. Memoir 10 London School of Hygiene and Tropical Medicine. HK Lewis, London; 1955.
  48. Roditi I, Liniger M: Dressed for success: the surface coats of insect-borne protozoan parasites. / Trends Microbiol 2002,10(3):128鈥?34. CrossRef
  49. Oberle M, Balmer O, Brun R, Roditi I: Bottlenecks and the maintenance of minor genotypes during the life cycle of Trypanosoma brucei. / PLoS Path 2010,6(7):e1001023. CrossRef
  50. Adams ER, Hamilton PB, Gibson W: African trypanosomes: celebrating diversity. / Trends Parasitol 2010, 26:324鈥?28. CrossRef
  
• 作者单位：Lori Peacock (1) (2)
  Simon Cook (2) (3)
  Vanessa Ferris (1) (2)
  Mick Bailey (2)
  Wendy Gibson (1)
  
  1. School of Biological Sciences, University of Bristol, Bristol, BS8 1UG, UK
  2. Department of Clinical Veterinary Science, University of Bristol, Langford, Bristol, BS40 7DU, UK
  3. Royal Veterinary College, Hawkshead Lane, North Mymms, Hatfield, Hertfordshire, AL9 7TA, UK
  

文摘

Background The tsetse-transmitted African trypanosomes cause diseases of importance to the health of both humans and livestock. The life cycles of these trypanosomes in the fly were described in the last century, but comparatively few details are available for Trypanosoma (Nannomonas) congolense, despite the fact that it is probably the most prevalent and widespread pathogenic species for livestock in tropical Africa. When the fly takes up bloodstream form trypanosomes, the initial establishment of midgut infection and invasion of the proventriculus is much the same in T. congolense and T. brucei. However, the developmental pathways subsequently diverge, with production of infective metacyclics in the proboscis for T. congolense and in the salivary glands for T. brucei. Whereas events during migration from the proventriculus are understood for T. brucei, knowledge of the corresponding developmental pathway in T. congolense is rudimentary. The recent publication of the genome sequence makes it timely to re-investigate the life cycle of T. congolense. Methods Experimental tsetse flies were fed an initial bloodmeal containing T. congolense strain 1/148 and dissected 2 to 78 days later. Trypanosomes recovered from the midgut, proventriculus, proboscis and cibarium were fixed and stained for digital image analysis. Trypanosomes contained in spit samples from individually caged flies were analysed similarly. Mensural data from individual trypanosomes were subjected to principal components analysis. Results Flies were more susceptible to infection with T. congolense than T. brucei; a high proportion of flies infected with T. congolense established a midgut and subsequent proboscis infection, whereas many T. brucei infections were lost in the migration from foregut to salivary glands. In T. congolense, trypomastigotes ceased division in the proventriculus and became uniform in size. The trypanosomes retained trypomastigote morphology during migration via the foregut to the mouthparts and we confirmed that the trypomastigote-epimastigote transition occurred in the proboscis. We found no equivalent to the asymmetric division stage in T. brucei that mediates transition of proventricular trypomastigotes to epimastigotes. In T. congolense extremely long epimastigotes with remarkably elongated posterior ends were observed in both the proboscis and cibarium; no difference was found in the developmental stages in these two organs. Dividing trypomastigotes and epimastigotes were recovered from the proboscis, some of which were in transition from trypomastigote to epimastigote and vice versa. It remains uncertain whether these morphological transitions are mediated by cell division, since we also found non-dividing cells with a variously positioned, juxta-nuclear kinetoplast. Conclusions We have presented a detailed description of the life cycle of T. congolense in its tsetse fly vector. During development in the fly T. congolense shares a common migratory pathway with its close relative T. brucei, culminating in the production of small metacyclic trypanosomes that can be inoculated with the saliva. Despite this outward similarity in life cycle, the transitional developmental stages in the foregut and mouthparts are remarkably different in the two trypanosome species.