Activation of endocytosis as an adaptation to the mammalian host by trypanosomes

Eukaryotic Cell

Volumn 6, Issue 11, 2007, Pages 2029-2037

  Natesan, Senthil Kumar A ^a   Peacock, Lori ^b   Matthews, Keith ^c   Gibson, Wendy ^b   Field, Mark C ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF BRISTOL   (United Kingdom)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CLATHRIN; PROTOZOAL PROTEIN; RAB PROTEIN; RAB11 PROTEIN;

ADAPTATION; ANIMAL; ARTICLE; CELL CULTURE; CELL DIFFERENTIATION; CYTOLOGY; DOWN REGULATION; ENDOCYTOSIS; FLUORESCENT ANTIBODY TECHNIQUE; GROWTH, DEVELOPMENT AND AGING; KINETICS; LIFE CYCLE; MAMMAL; METABOLISM; PARASITOLOGY; PHYSIOLOGY; REPRODUCIBILITY; TRYPANOSOMA BRUCEI; TSETSE FLY; UPREGULATION;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; CELL DIFFERENTIATION; CELLS, CULTURED; CLATHRIN; DOWN-REGULATION; ENDOCYTOSIS; FLUORESCENT ANTIBODY TECHNIQUE; KINETICS; LIFE CYCLE STAGES; MAMMALS; PROTOZOAN PROTEINS; RAB GTP-BINDING PROTEINS; REPRODUCIBILITY OF RESULTS; TRYPANOSOMA BRUCEI BRUCEI; TSETSE FLIES; UP-REGULATION;

GLOSSINA (GENUS); HEXAPODA; MAMMALIA; TRYPANOSOMA; TRYPANOSOMA BRUCEI;

EID: 36849081968     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.00213-07     Document Type: Article

References (50)

1. Allen, C. L., D. Goulding, and M. C. Field. 2003. Clathrin-mediated endocytosis is essential in Trypanosoma brucei. EMBO J. 22:4991-5002.
2. Bangs, J. D., E. M. Brouch, D. M. Ransom, and J. L. Roggy. 1996. A soluble secretory reporter system in Trypanosoma brucei. Studies on endoplasmic reticulum targeting. J. Biol. Chem. 271:18387-18393.
3. Bangs, J. D., L. Uyetake, M. J. Brickman, A. E. Balber, and J. C. Boothroyd. 1993. Molecular cloning and cellular localization of a BiP homologue in Trypanosoma brucei. Divergent ER retention signals in a lower eukaryote. J. Cell Sci. 105(Pt. 4):1101-1113.
4. Barrett, M. P., R. J. Burchmore, A. Stich, J. O. Lazzari, A. C. Frasch, J. J. Cazzulo, and S. Krishna. 2003. The trypanosomiases. Lancet 362:1469-1480.
5. Barry, J. D. 1979. Capping of variable antigen on Trypanosoma brucei, and its immunological and biological significance. J. Cell Sci. 37:287-302.
6. Barry, J. D., S. L. Hajduk, K. Vickerman, and D. Le Ray. 1979. Detection of multiple variable antigen types in metacyclic populations of Trypanosoma brucei. Trans. R. Soc. Trop. Med. Hyg. 73:205-208.
7. Barry, J. D., and R. McCulloch. 2001. Antigenic variation in trypanosomes: enhanced phenotypic variation in a eukaryotic parasite. Adv. Parasitol. 49: 1-70.
8. Bass, K. E., and C. C. Wang. 1991. The in vitro differentiation of pleomorphic Trypanosoma brucei from bloodstream into procyclic form requires neither intermediary nor short-stumpy stage. Mol. Biochem. Parasitol. 44:261-270.
9. Brun, R., and L. Jenni. 1987. Human serum resistance of metacyclic forms of Trypanosoma brucei brucei, T. brucei rhodesiense and T. brucei gambiense. Parasitol. Res. 73:218-223.
10. Brun, R., and M. Schonenberger. 1979. Cultivation and in vitro cloning or procyclic culture forms of Trypanosoma brucei in a semi-defined medium. Acta Trop. 36:289-292.
11. Buxbaum, L. U., K. G. Milne, K. A. Werbovetz, and P. T. Englund. 1996. Myristate exchange on the Trypanosoma brucei variant surface glycoprotein. Proc. Natl. Acad. Sci. USA 93:1178-1183.
12. Engstler, M., J. D. Bangs, and M. C. Field. 2007. Intracellular transport systems in trypanosomes: function, evolution and virulence, p. 281-317. In J.D. Barry, J. Mottram, R. McCulloch, and A. Acosta-Serrano (ed.), Trypanosomes - after the genome. Horizon Press, Norwich, United Kingdom.
13. Field, H., M. Farjah, A. Pal, K. Gull, and M. C. Field. 1998. Complexity of trypanosomatid endocytosis pathways revealed by Rab4 and Rab5 isoforms in Trypanosoma brucei. J. Biol. Chem. 273:32102-32110.
14. Field, M. C., C. L. Allen, V. Dhir, D. Goulding, B. S. Hall, G. W. Morgan, P. Veazey, and M. Engstler. 2004. New approaches to the microscopic imaging of Trypanosoma brucei. Microsc. Microanal. 10:621-636.
15. Field, M. C., and M. Carrington. 2004. Intracellular membrane transport systems in Trypanosoma brucei. Traffic 5:905-913.
16. Gruszynski, A. E., F. J. van Deursen, M. C. Albareda, A. Best, K. Chaudhary, L. J. Cliffe, L. del Rio, J. D. Dunn, L. Ellis, K. J. Evans, J. M. Figueiredo, N. A. Malmquist, Y. Omosun, J. B. Palenchar, S. Prickett, G. A. Punkosdy, G. van Dooren, Q. Wang, A. K. Menon, K. R. Matthews, and J. D. Bangs. 2006. Regulation of surface coat exchange by differentiating African trypanosomes. Mol. Biochem. Parasitol. 147:211-223.
17. Hall, B., C. L. Allen, D. Goulding, and M. C. Field. 2004. Both of the Rab5 subfamily small GTPases of Trypanosoma brucei are essential and required for endocytosis. Mol. Biochem. Parasitol. 138:67-77.
18. Hall, B. S., A. Pal, D. Goulding, A. Acosta-Serrano, and M. C. Field. 2005. Trypanosoma brucei: TbRAB4 regulates membrane recycling and expression of surface proteins in procyclic forms. Exp. Parasitol. 111:160-171.
19. Hall, B. S., A. Pal, D. Goulding, and M. C. Field. 2004. Rab4 is an essential regulator of lysosomal trafficking in trypanosomes. J. Biol. Chem. 279:45047-45056.
20. Hall, B. S., E. Smith, W. Langer, L. A. Jacobs, D. Goulding, and M. C. Field. 2005. Developmental variation in Rab11-dependent trafficking in Trypanosoma brucei. Eukaryot. Cell 4:971-980.
21. Hendriks, E., F. J. van Deursen, J. Wilson, M. Sarkar, M. Timms, and K. R. Matthews. 2000. Life-cycle differentiation in Trypanosoma brucei: molecules and mutants. Biochem. Soc. Trans. 28:531-536.
22. Hertz-Fowler, C., K. Ersfeld, and K. Gull. 2001. CAP5.5, a life-cycle-regulated, cytoskeleton-associated protein is a member of a novel family of calpain-related proteins in Trypanosoma brucei. Mol. Biochem. Parasitol. 116:25-34.
23. Hirumi, H., and K. Hirumi. 1994. Axenic culture of African trypanosome bloodstream forms. Parasitol. Today 10:80-84.
24. Jeffries, T. R., G. W. Morgan, and M. C. Field. 2001. A developmentally regulated rab11 homologue in Trypanosoma brucei is involved in recycling processes. J. Cell Sci. 114:2617-2626.
25. Kelley, R. J., D. L. Alexander, C. Cowan, A. E. Balber, and J. D. Bangs. 1999. Molecular cloning of p67, a lysosomal membrane glycoprotein from Trypanosoma brucei. Mol. Biochem. Parasitol. 98:17-28.
26. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
27. Lanham, S. M., and D. G. Godfrey. 1970. Isolation of salivarian trypanosomes from man and other mammals using DEAE-cellulose. Exp. Parasitol. 28:521-534.
28. Matthews, K. R., and K. Gull. 1994. Evidence for an interplay between cell cycle progression and the initiation of differentiation between life cycle forms of African trypanosomes. J. Cell Biol. 125:1147-1156.
29. Morgan, G. W., C. L. Allen, T. R. Jeffries, M. Hollinshead, and M. C. Field. 2001. Developmental and morphological regulation of clathrin-mediated endocytosis in Trypanosoma brucei. J. Cell Sci. 114:2605-2615.
30. O'Beirne, C., C. M. Lowry, and H. P. Voorheis. 1998. Both IgM and IgG anti-VSG antibodies initiate a cycle of aggregation-disaggregation of blood-stream forms of Trypanosoma brucei without damage to the parasite. Mol. Biochem. Parasitol. 91:165-193.
31. Pal, A., B. S. Hall, and M. C. Field. 2002. Evidence for a non-LDL-mediated entry route for the trypanocidal drug suramin in Trypanosoma brucei. Mol. Biochem. Parasitol. 122:217-221.
32. Pal, A., B. S. Hall, T. R. Jeffries, and M. C. Field. 2003. Rab5 and Rab11 mediate transferrin and anti-variant surface glycoprotein antibody recycling in Trypanosoma brucei. Biochem. J. 374:443-451.
33. Pal, A., B. S. Hall, D. N. Nesbeth, H. I. Field, and M. C. Field. 2002. Differential endocytic functions of Trypanosoma brucei Rab5 isoforms reveal a glycosylphosphatidylinositol-specific endosomal pathway. J. Biol. Chem. 277:9529-9539.
34. Pays, E., B. Vanhollebeke, L. Vanhamme, F. Paturiaux-Hanocq, D. P. Nolan, and D. Perez-Morga. 2006. The trypanolytic factor of human serum. Nat. Rev. Microbiol. 4:477-486.
35. Peacock, L., V. Ferris, M. Bailey, and W. Gibson. 2006. Multiple effects of the lectin-inhibitory sugars D-glucosamine and N-acetyl-glucosamine on tsetse-trypanosome interactions. Parasitology 132:651-658.
36. Reuner, B., E. Vassella, B. Yutzy, and M. Boshart. 1997. Cell density triggers slender to stumpy differentiation of Trypanosoma brucei bloodstream forms in culture. Mol. Biochem. Parasitol. 90:269-280.
37. Richardson, J. P., R. P. Beecroft, D. L. Tolson, M. K. Liu, and T. W. Pearson. 1988. Procyclin: an unusual immunodominant glycoprotein surface antigen from the procyclic stage of African trypanosomes. Mol. Biochem. Parasitol. 31:203-216.
38. Roditi, I., M. Carrington, and M. Turner. 1987. Expression of a polypeptide containing a dipeptide repeat is confined to the insect stage of Trypanosoma brucei. Nature 325:272-274.
39. Roditi, I., and T. W. Pearson. 1990. The procyclin coat of African trypanosomes (or the not-so-naked trypanosome). Parasitol. Today 6:79-82.
40. Roditi, I., H. Schwarz, T. W. Pearson, R. P. Beecroft, M. K. Liu, J. P. Richardson, H. J. Buhring, J. Pleiss, R. Bulow, R. O. Williams, et al. 1989. Procyclin gene expression and loss of the variant surface glycoprotein during differentiation of Trypanosoma brucei. J. Cell Biol. 108:737-746.
41. Sharma, R., L. Peacock, E. Gluenz, K. Gull, W. Gibson, and M. Carrington. 2007. Asymmetric cell division as a route to reduction in cell length and change in cell morphology in trypanosomes. Protist. doi:10.1016/j.protis.2007.07.004.
42. Sheader, K., S. Vaughan, J. Minchin, K. Hughes, K. Gull, and G. Rudenko. 2005. Variant surface glycoprotein RNA interference triggers a precytokinesis cell cycle arrest in African trypanosomes. Proc. Natl. Acad. Sci. USA 102:8716-8721.
43. Steiger, R. 1973. On the ultrastructure of Trypanosoma (Trypanozoon) brucei in the course of its life cycle and some related aspects. Acta Trop. 30:64-168.
44. Tetley, L., and K. Vickerman. 1985. Differentiation in Trypanosoma brucei: host-parasite cell junctions and their persistence during acquisition of the variable antigen coat. J. Cell Sci. 74:1-19.
45. Turner, C. M., J. D. Barry, and K. Vickerman. 1986. Independent expression of the metacyclic and bloodstream variable antigen repertoires of Trypanosoma brucei rhodesiense. Parasitology 92(Pt. 1):67-73.
46. Urwyler, S., E. Studer, C. K. Renggli, and I. Roditi. 2007. A family of stage-specific alanine-rich proteins on the surface of epimastigote forms of Trypanosoma brucei. Mol. Microbiol. 63:218-228.
47. Van Den Abbeele, J., Y. Claes, D. van Bockstaele, D. Le Ray, and M. Coosemans. 1999. Trypanosoma brucei spp. development in the tsetse fly: characterization of the post-mesocyclic stages in the foregut and proboscis. Parasitology 118(Pt. 5):469-478.
48. Vickerman, K. 1985. Developmental cycles and biology of pathogenic trypanosomes. Br. Med. Bull. 41:105-114.
49. Vickerman, K., L. Tetley, K. A. Hendry, and C. M. Turner. 1988. Biology of African trypanosomes in the tsetse fly. Biol. Cell 64:109-119.
50. Ziegelbauer, K., M. Quinten, H. Schwarz, T. W. Pearson, and P. Overath. 1990. Synchronous differentiation of Trypanosoma brucei from bloodstream to procyclic forms in vitro. Eur. J. Biochem. 192:373-378.