Developmental regulation and extracellular release of a VSG expression-site-associated gene product from Trypanosoma bruceibloodstream forms

Journal of Cell Science

Volumn 123, Issue 19, 2010, Pages 3401-3411

  Barnwell, Eleanor M ^a   Van Deursen, Frederick J ^b   Jeacock, Laura ^a   Smith, Katherine A ^a   Maizels, Rick M ^a   Acosta Serrano, Alvaro ^c   Matthews, Keith ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b CHRISTIE HOSPITAL   (United Kingdom)

^c LIVERPOOL SCHOOL OF TROPICAL MEDICINE   (United Kingdom)

Author keywords

Antigenic variation; ESAG; Secretion; Transmission; Trypanosoma brucei

Indexed keywords

MEMBRANE PROTEIN; MESSENGER RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; ESAG9 GENE; GENE; IMMUNOREGULATION; MOUSE; NONHUMAN; PARASITE IMMUNITY; PARASITE TRANSMISSION; PRIORITY JOURNAL; PROTEIN GLYCOSYLATION; PROTEIN SECRETION; PROTOZOAL GENETICS; TRYPANOSOMA CRUZI; TRYPANOSOMIASIS; VSG GENE;

ANIMALS; BLOOD-BORNE PATHOGENS; CELL LINE; DISEASE MODELS, ANIMAL; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLYCOSYLATION; LIFE CYCLE STAGES; MICE; PROTEIN ENGINEERING; TRANSGENES; TRYPANOSOMA BRUCEI BRUCEI; TRYPANOSOMIASIS, AFRICAN; VARIANT SURFACE GLYCOPROTEINS, TRYPANOSOMA; VIRULENCE;

MAMMALIA; TRYPANOSOMA; TRYPANOSOMA BRUCEI; TRYPANOSOMA CRUZI;

EID: 77956903992     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.068684     Document Type: Article

References (53)

1. Ackermann, M., Stecher, B., Freed, N. E., Songhet, P., Hardt, W. D. and Doebeli, M. (2008). Self-destructive cooperation mediated by phenotypic noise. Nature 454, 987-990.
2. Baida, R. C., Santos, M. R., Carmo, M. S., Yoshida, N., Ferreira, D., Ferreira, A. T., El Sayed, N. M., Andersson, B. and da Silveira, J. F. (2006). Molecular characterization of serine-, alanine-, and proline-rich proteins of Trypanosoma cruzi and their possible role in host cell infection. Infect. Immunol. 74, 1537-1546.
3. Barford, D., Das, A. K. and Egloff, M. P. (1998). The structure and mechanism of protein phosphatases: insights into catalysis and regulation. Annu. Rev. Biophys. Biomol. Struct. 27, 133-164.
4. Barker, A. R., Wickstead, B., Gluenz, E. and Gull, K. (2008). Bioinformatic insights to the ESAG5 and GRESAG5 gene families in kinetoplastid parasites. Mol. Biochem. Parasitol. 162, 112-122.
5. Bartholomeu, D. C., Cerqueira, G. C., Leao, A. C., daRocha, W. D., Pais, F. S., Macedo, C., Djikeng, A., Teixeira, S. M. and El-Sayed, N. M. (2009). Genomic organization and expression profile of the mucin-associated surface protein (masp) family of the human pathogen Trypanosoma cruzi. Nucleic Acids Res. 37, 3407-3417.
6. Bastin, P., Bagherzadeh, Z., Matthews, K. R. and Gull, K. (1996). A novel epitope tag system to study protein targeting and organelle biogenesis in Trypanosoma brucei. Mol. Biochem. Parasitol. 77, 235-239.
7. Beschin, A., Brys, L., Magez, S., Radwanska, M. and De Baetselier, P. (1998). Trypanosoma brucei infection elicits nitric oxide-dependent and nitric oxide-independent suppressive mechanisms. J. Leukoc. Biol. 63, 429-439.
8. Biebinger, S., Wirtz, L. E., Lorenz, P. and Clayton, C. (1997). Vectors for inducible expression of toxic gene products in bloodstream and procyclic Trypanosoma brucei. Mol. Biochem. Parasitol. 85, 99-112.
9. Bitter, W., Gerrits, H., Kieft, R. and Borst, P. (1998). The role of transferrin-receptor variation in the host range of Trypanosoma brucei. Nature 391, 499-502.
10. Borst, P. (2002). Antigenic variation and allelic exclusion. Cell 109, 5-8.
11. Claes, F., Buscher, P., Touratier, L. and Goddeeris, B. M. (2005). Trypanosoma equiperdum: master of disguise or historical mistake? Trends Parasitol. 21, 316-321.
12. Cully, D. F., Ip, H. S. and Cross, G. A. (1985). Coordinate transcription of variant surface glycoprotein genes and an expression site associated gene family in Trypanosoma brucei. Cell 42, 173-182.
13. Dean, S. D., Marchetti, R., Kirk, K. and Matthews, K. (2009). A surface transporter family conveys the trypanosome differentiation signal. Nature 459, 213-217.
14. Diggle, S. P., Griffin, A. S., Campbell, G. S. and West, S. A. (2007). Cooperation and conflict in quorum-sensing bacterial populations. Nature 450, 411-414.
15. Engstler, M. and Boshart, M. (2004). Cold shock and regulation of surface protein trafficking convey sensitization to inducers of stage differentiation in Trypanosoma brucei. Genes Dev. 18, 2798-2811. (Pubitemid 39507772)
16. Engstler, M., Pfohl, P., Herminghaus, S., Boshart, M., Wiegerttjes, G., Heddergott, N. and Overath, P. (2007). Hydrodynamic flow-mediated protein sorting on the cell surface of trypanosomes. Cell 131, 505-515.
17. Florent, I. C., Raibaud, A. and Eisen, H. (1991). A family of genes related to a new expression site-associated gene in Trypanosoma equiperdum. Mol. Cell. Biol. 11, 2180-2188.
18. Gardner, A. and Kummerli, R. (2008). Social evolution: this microbe will self-destruct. Curr. Biol. 18, R1021-R1023.
19. Gomez-Rodriguez, J., Stijlemans, B., De Muylder, G., Korf, H., Brys, L., Berberof, M., Darji, A., Pays, E., De Baetselier, P. and Beschin, A. (2009). Identification of a parasitic immunomodulatory protein triggering the development of suppressive M1 macrophages during African trypanosomiasis. J. Infect. Dis. 200, 1849-1860.
20. Gunzl, A., Bruderer, T., Laufer, G., Schimanski, B., Tu, L. C., Chung, H. M., Lee, P. T. and Lee, M. G. (2003). RNA polymerase I transcribes procyclin genes and variant surface glycoprotein gene expression sites in Trypanosoma brucei. Eukaryotic Cell 2, 542-551.
21. Hertz-Fowler, C., Figueiredo, L. M., Quail, M. A., Becker, M., Jackson, A., Bason, N., Brooks, K., Churcher, C., Fahkro, S., Goodhead, I. et al. (2008). Telomeric expression sites are highly conserved in Trypanosoma brucei. PLoS ONE 3, e3527.
22. Jensen, B. C., Sivam, D., Kifer, C. T., Myler, P. J. and Parsons, M. (2009). Widespread variation in transcript abundance within and across developmental stages of Trypanosoma brucei. BMC Genomics 10, 482.
23. Jones, D. C., Mehlert, A., Guther, M. L. and Ferguson, M. A. (2005). Deletion of the glucosidase II gene in Trypanosoma brucei reveals novel N-glycosylation mechanisms in the biosynthesis of variant surface glycoprotein. J. Biol. Chem. 280, 35929-35942.
24. Kabani, S., Fenn, K., Ross, A., Ivens, A., Smith, T. K., Ghazal, P. and Matthews, K. (2009). Genome-wide expression profiling of in vivo-derived bloodstream parasite stages and dynamic analysis of mRNA alterations during synchronous differentiation in Trypanosoma brucei. BMC Genomics 10, 427.
25. Kooter, J. M., van der Spek, H. J., Wagter, R., d'Oliveira, C. E., van der Hoeven, F., Johnson, P. J. and Borst, P. (1987). The anatomy and transcription of a telomeric expression site for variant-specific surface antigens in T. brucei. Cell 51, 261-272.
26. Kusuda, K., Kobayashi, T., Ikeda, S., Ohnishi, M., Chida, N., Yanagawa, Y., Shineha, R., Nishihira, T., Satomi, S., Hiraga, A. et al. (1998). Mutational analysis of the domain structure of mouse protein phosphatase 2Cbeta. Biochem. J. 332, 243-250.
27. Lai, D. H., Hashimi, H., Lun, Z. R., Ayala, F. J. and Lukes, J. (2008). 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. USA 105, 1999-2004.
28. Lythgoe, K. A., Morrison, L. J., Read, A. F. and Barry, J. D. (2007). Parasite-intrinsic factors can explain ordered progression of trypanosome antigenic variation. Proc. Natl. Acad. Sci. USA 104, 8095-8100.
29. Margos, G., Navarette, S., Butcher, G., Davies, A., Willers, C., Sinden, R. E. and Lachmann, P. J. (2001). Interaction between host complement and mosquito-midgut-stage Plasmodium berghei. Infect. Immunol. 69, 5064-5071.
30. Matthews, K. R. and Gull, K. (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.
31. Matthews, K. R., Ellis, J. R. and Paterou, A. (2004). Molecular regulation of the life cycle of African trypanosomes. Trends Parasitol. 20, 40-47.
32. McCulloch, R. (2004). Antigenic variation in African trypanosomes: monitoring progress. Trends Parasitol. 20, 117-121.
33. MedinaAcosta, E. and Cross, G. A. M. (1993). Rapid isolation of DNA from Trypanosomatid protozoa using a simple 'mini-prep' procedure. Mol. Biochem. Parasitol. 59, 327-330.
34. Millar, A. E., Sternberg, J., McSharry, C., Wei, X. Q., Liew, F. Y. and Turner, C. M. (1999). T-Cell responses during Trypanosoma brucei infections in mice deficient in inducible nitric oxide synthase. Infect. Immunol. 67, 3334-3338.
35. Navarro, M. and Gull, K. (2001). A pol I transcriptional body associated with VSG mono-allelic expression in Trypanosoma brucei. Nature 414, 759-763. (Pubitemid 34000774)
36. Nolan, D. P., Rolin, S., Rodriguez, J. R., Van Den Abbeele, J. and Pays, E. (2000). Slender and stumpy bloodstream forms of Trypanosoma brucei display a differential response to extracellular acidic and proteolytic stress. Eur. J. Biochem. 267, 18-27.
37. Pays, E., Tebabi, D., Pays, A., Coquelet, H., Revelard, P., Salmon, D. and Steinert, M. (1989). The genes and transcripts of an antigen gene expression site from T. brucei. Cell 57, 835-845.
38. Pays, E., Lips, S., Nolan, D., Vanhamme, L., Perez-Morga, D., Xong, H. V., Chamekh, M., Chimfwembe, C. E., Van Den Abbeele, J., Pays, A. et al. (2001). The VSG expression sites of Trypanosoma brucei: multipurpose tools for the adaptation of the parasite to mammalian hosts Mol. Biochem. Parasitol. 114, 1-16.
39. Pelle, R., McOdimba, F., Chuma, F., Wasawo, D., Pearson, T. W. and Murphy, N. B. (2002). The African trypanosome cyclophilin A homologue contains unusual conserved central and N-terminal domains and is developmentally regulated. Gene 290, 181-191.
40. Robertson, M. (1912). Notes on the polymorphism of Trypanosoma gambiense in the blood and its relation to the exogenous cycvle in Glossina palpalis. Proc. R. Soc. Lond. B. Biol. Sci. 85, 241-539.
41. Robinson, N. P., Burman, N., Melville, S. E. and Barry, J. D. (1999). Predominance of duplicative VSG gene conversion in antigenic variation in African trypanosomes. Mol. Cell. Biol. 19, 5839-5846.
42. Salmon, D., Geuskens, M., Hanocq, F., Hanocq, Q.-J., Nolan, D., Ruben, L. and Pays, E. (1994). A novel heterodimeric transferrin receptor encoded by a pair of VSG expression site-associated genes in T. brucei. Cell 78, 75-86. (Pubitemid 24228302)
43. Sbicego, S., Vassella, E., Kurath, U., Blum, B. and Roditi, I. (1999). The use of transgenic Trypanosoma brucei to identify compounds inducing the differentiation of bloodstream forms to procyclic forms. Mol. Biochem. Parasitol. 104, 311-322.
44. Schell, D., Evers, R., Preis, D., Ziegelbauer, K., Kiefer, H., Lottspeich, F., Cornelissen, A. and Overath, P. (1991). A transferrin-binding protein of Trypanosoma brucei is encoded by one of the genes in the variant surface glycoprotein gene expression site. EMBO J. 10, 1061-1066.
45. Sheader, K., Vaughan, S., Minchin, J., Hughes, K., Gull, K. and Rudenko, G. (2005). Variant surface glycoprotein RNA interference triggers a precytokinesis cell cycle arrest in African trypanosomes. Proc. Natl Acad. Sci. USA 102, 8716-8721.
46. Sternberg, M. J. and Mabbott, N. A. (1996). Nitric oxide-mediated suppression of T cell responses during Trypanosoma brucei infection: soluble trypanosome products and interferon-gamma are synergistic inducers of nitric oxide synthase. Eur. J. Immunol. 26, 539-543.
47. Tasker, M., Wilson, J., Sarkar, M., Hendriks, E. and Matthews, K. (2000). A novel selection regime for differentiation defects demonstrates an essential role for the stumpy form in the life cycle of the African trypanosome. Mol. Biol. Cell 11, 1905-1917.
48. Vanhamme, L., Paturiaux-Hanocq, F., Poelvoorde, P., Nolan, D. P., Lins, L., Van Den Abbeele, J., Pays, A., Tebabi, P., Van Xong, H., Jacquet, A. et al. (2003). Apolipoprotein L-I is the trypanosome lytic factor of human serum. Nature 422, 83-87.
49. Vassella, E., Reuner, B., Yutzy, B. and Boshart, M. (1997). Differentiation of African trypanosomes is controlled by a density sensing mechanism which signals cell cycle arrest via the cAMP pathway. J. Cell Sci. 110, 2661-2671. (Pubitemid 27499424)
50. Wijers, D. and Willett, K. (1960). Factors that may influence the infection rate of Glossina Palpalis with Trypanosoma gambiense. II. - The number and morphology of the trypanosomes present in the blood of ther host at the time of the infective feed. Ann. Trop. Med. Parasitol. 54, 341-350.
51. Xong, H. V., Vanhamme, L., Chamekh, M., Chimfwembe, C. E., Van Den Abbeele, J., Pays, A., Van Meirvenne, N., Hamers, R., De Baetselier, P. and Pays, E. (1998). A VSG expression site-associated gene confers resistance to human serum in Trypanosoma rhodesiense. Cell 95, 839-846.
52. Young, R., Taylor, J. E., Kurioka, A., Becker, M., Louis, E. J. and Rudenko, G. (2008). 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 9, 385.
53. Ziegelbauer, K. and Overath, P. (1990). Surface antigen change during differentiation of Trypanosoma brucei. Biochem. Soc. Trans. 18, 731-733.