Skip to main content
×
Home
    • Aa
    • Aa
  • Get access
    Check if you have access via personal or institutional login
  • Cited by 3
  • Cited by
    This article has been cited by the following publications. This list is generated based on data provided by CrossRef.

    Perdomo, Doranda Bonhivers, Mélanie and Robinson, Derrick 2016. The Trypanosome Flagellar Pocket Collar and Its Ring Forming Protein—TbBILBO1. Cells, Vol. 5, Issue. 1, p. 9.


    Vaughan, Sue and Gull, Keith 2015. Basal body structure and cell cycle-dependent biogenesis in Trypanosoma brucei. Cilia, Vol. 5, Issue. 1,


    GINGER, MICHAEL L. MCKEAN, PAUL G. BURCHMORE, RICHARD and GRANT, KAREN M. 2012. Proteomic insights into parasite biology. Parasitology, Vol. 139, Issue. 09, p. 1101.


    ×

Proteomics on the rims: insights into the biology of the nuclear envelope and flagellar pocket of trypanosomes

  • MARK C. FIELD (a1), VINCENT ADUNG'A (a1), SAMSON OBADO (a2), BRIAN T. CHAIT (a3) and MICHAEL P. ROUT (a2)
  • DOI: http://dx.doi.org/10.1017/S0031182011002125
  • Published online: 06 February 2012
Abstract
SUMMARY

Trypanosomatids represent the causative agents of major diseases in humans, livestock and plants, with inevitable suffering and economic hardship as a result. They are also evolutionarily highly divergent organisms, and the many unique aspects of trypanosome biology provide opportunities in terms of identification of drug targets, the challenge of exploiting these putative targets and, at the same time, significant scope for exploration of novel and divergent cell biology. We can estimate from genome sequences that the degree of divergence of trypanosomes from animals and fungi is extreme, with perhaps one third to one half of predicted trypanosome proteins having no known function based on homology or recognizable protein domains/architecture. Two highly important aspects of trypanosome biology are the flagellar pocket and the nuclear envelope, where in silico analysis clearly suggests great potential divergence in the proteome. The flagellar pocket is the sole site of endo- and exocytosis in trypanosomes and plays important roles in immune evasion via variant surface glycoprotein (VSG) trafficking and providing a location for sequestration of various invariant receptors. The trypanosome nuclear envelope has been largely unexplored but, by analogy with higher eukaryotes, roles in the regulation of chromatin and most significantly, in controlling VSG gene expression are expected. Here we discuss recent successful proteomics-based approaches towards characterization of the nuclear envelope and the endocytic apparatus, the identification of conserved and novel trypanosomatid-specific features, and the implications of these findings.

Copyright
Corresponding author
*Corresponding author: Phone: +44 (0)751-550-7880. E-mail: mcf34@cam.ac.uk
Linked references
Hide All

This list contains references from the content that can be linked to their source. For a full set of references and notes please see the PDF or HTML where available.

C. L. Allen , D. Goulding and M. C. Field (2003). Clathrin-mediated endocytosis is essential in Trypanosoma brucei. EMBO Journal 22, 49915002.

S. Alsford , D. J. Turner , S. O. Obado , A. Sanchez-Flores , L. Glover , M. Berriman , C. Hertz-Fowler and D. Horn (2011). High-throughput phenotyping using parallel sequencing of RNA interference targets in the African trypanosome. Genome Research 21, 915924.

G. H. Borner , M. Harbour , S. Hester , K. S. Lilley and M. S. Robinson (2006). Comparative proteomics of clathrin-coated vesicles. Journal of Cell Biology 175, 571578.

R. Broadhead , H. R. Dawe , H. Farr , S. Griffiths , S. R. Hart , N. Portman , M. K. Shaw , M. L. Ginger , S. J. Gaskell , P. G. McKean and K. Gull (2006). Flagellar motility is required for the viability of the bloodstream trypanosome. Nature 440, 224227.

E. P. Camargo (1999). Phytomonas and other trypanosomatid parasites of plants and fruit. Advances in Parasitology 42, 29112.

A. Cassola , and A. C. Frasch (2009). An RNA recognition motif mediates the nucleocytoplasmic transport of a trypanosome RNA-binding protein. Journal of Biological Chemistry 284, 3501535028.

B. T. Chait (2011). Mass spectrometry in the postgenomic era. Annual Reviews in Biochemistry 80, 239246.

A. L. Chanez , A. B. Hehl , M. Engstler and A. Schneider (2006). Ablation of the single dynamin of T. brucei blocks mitochondrial fission and endocytosis and leads to a precise cytokinesis arrest. Journal of Cell Science 119, 29682974.

I. M. Cristea , R. Williams , B. T. Chait and M. P. Rout (2005). Fluorescent proteins as proteomic probes. Molecular and Cellular Proteomics 4, 19331941.

J. A. DeGrasse , B. T. Chait , M. C. Field and M. P. Rout (2008). High-yield isolation and subcellular proteomic characterization of nuclear and subnuclear structures from trypanosomes. Methods in Molecular Biology 463, 7792.

W. L. Chung , K. F. Leung , M. Carrington and M. C. Field (2008). Position-specific ubiquitylation is required for internalisation and degradation of trans-membrane surface proteins in trypanosomes. Traffic 9, 16811697.

W. L. Chung , M. Carrington and M. C. Field (2004). Carboxy-terminal targeting signals in transmembrane surface glycoproteins of Trypanosoma brucei. Journal of Biological Chemistry 279, 5488754895.

J. A. DeGrasse and D. Devos (2010). A functional proteomic study of the Trypanosoma brucei nuclear pore complex: an informatic strategy. Methods in Molecular Biology 673, 231238.

J. A. DeGrasse , K. N. DuBois , D. Devos , T. N. Siegel , A. Sali , M. C. Field , M. P. Rout and B. T. Chait (2009). Evidence for a shared nuclear pore complex architecture that is conserved from the last common eukaryotic ancestor. Molecular and Cellular Proteomics 8, 21192130.

M. Engstler , T. Pfohl , S. Herminghaus , M. Boshart , G. Wiegertjes , N. Heddergott and P. Overath (2007). Hydrodynamic flow-mediated protein sorting on the cell surface of trypanosomes. Cell 131, 505515.

M. Engstler , L. Thilo , F. Weise , C. G. Grünfelder , H. Schwarz , M. Boshart and P. Overath (2004). Kinetics of endocytosis and recycling of the GPI-anchored variant surface glycoprotein in Trypanosoma brucei. Journal of Cell Science 117, 1105–1015.

M. C. Field and M. Carrington (2009). The trypanosome flagellar pocket. Nature Reviews in Microbiology 7, 775786.

M. C. Field , C. Gabernet-Castello and J. B. Dacks (2007). Reconstructing the evolution of the endocytic system: insights from genomics and molecular cell biology. Advances in Experimental Medicine and Biology 607, 8496.

M. C. Field , J. H. Lumb , V. O. Adung'a , N. G. Jones and M. Engstler (2009). Macromolecular trafficking and immune evasion in African trypanosomes. International Review of Cell and Molecular Biology 278, 167.

C. Gabernet-Castello , J. B. Dacks and M. C. Field , (2009). The single ENTH-domain protein of trypanosomes; endocytic functions and evolutionary relationship with epsin. Traffic 10, 894911.

C. Gabernet-Castello , K. N. Dubois , C. Nimmo and M. C. Field (2011). Rab11 function in Trypanosoma brucei; identification of conserved and novel interaction partners. Eukaryotic Cell 10, 10821094.

K. F. Leung , F. Riley , M. Carrington and M. C. Field (2011). Ubiquitylation as a general mechanism for internalisation of trans-membrane domain surface proteins in trypanosomes. Eukaryotic Cell 10, 916931.

C. G. Grünfelder , M. Engstler , F. Weise , H. Schwarz , Y. D. Stierhof , G. W. Morgan , M. C. Field and P. Overath (2003). Endocytosis of a glycosylphosphatidylinositol-anchored protein via clathrin-coated vesicles, sorting by default in endosomes, and exocytosis via RAB11-positive carriers. Molecular Biology of the Cell 14, 20292040.

P. J. Hotez and M. Gurwith (2011). Europe's neglected infections of poverty. International Journal of Infectious Diseases 15, e6119.

T. Kawahara , T. N. Siegel , A. K. Ingram , S. Alsford , G. A. Cross and D. Horn (2008). Two essential MYST-family proteins display distinct roles in histone H4K10 acetylation and telomeric silencing in trypanosomes. Molecular Microbiology 69, 10541068.

N. G. Kolev , J. B. Franklin , S. Carmi , H. Shi , S. Michaeli and C. Tschudi (2010). The transcriptome of the human pathogen Trypanosoma brucei at single-nucleotide resolution. PLoS Pathogens 6, e1001090.

D. Luz Ambrósio , J. H. Lee , A. K. Panigrahi , T. N. Nguyen , R. M. Cicarelli and A. Günzl (2009) Spliceosomal proteomics in Trypanosoma brucei reveal new RNA splicing factors. Eukaryotic Cell 8, 9901000.

S. Magez and M. Radwanska (2009). African trypanosomiasis and antibodies: implications for vaccination, therapy and diagnosis. Future Microbiology 4, 10751087.

B. J. Mans , V. Anantharaman , L. Aravind and E. V. Koonin (2004). Comparative genomics, evolution and origins of the nuclear envelope and nuclear pore complex. Cell Cycle. 3, 16121637.

G. W. Morgan , D. Goulding and M. C. Field (2004). The single dynamin-like protein of Trypanosoma brucei regulates mitochondrial division and is not required for endocytosis. Journal of Biological Chemistry 279, 1069210701.

S. K. Natesan , L. Peacock , K. F. Leung , W. Gibson and M. C. Field (2010). Evidence that low endocytic activity is not directly responsible for human serum resistance in the insect form of African trypanosomes. BMC Research Notes 3, 63.

M. Oberholzer , G. Langousis , H. T. Nguyen , E. A. Saada , M. M. Shimogawa , Z. O. Jonsson , S. M. Nguyen , J. A. Wohlschlelgel and K. L. Hill (2011). Independent analysis of the flagellum surface and matrix proteomes provides insight into flagellum signaling in mammalian-infectious Trypanosoma brucei. Molecular and Cellular Proteomics 10, M111.010538.

M. Oberholzer , S. Morand , S. Kunz and T. Seebeck (2006). A vector series for rapid PCR-mediated C-terminal in situ tagging of Trypanosoma brucei genes. Molecular and Biochemical Parasitology 145, 117120.

M. Oeffinger , K. E. Wei , R. Rogers , J. A. DeGrasse , B. T. Chait , J. D. Aitchison , and M. P. Rout (2007). Comprehensive analysis of diverse ribonucleoprotein complexes. Nature Methods 4, 951956.

A. Pal , 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. Biochemical Journal 374, 443451.

A. K. Panigrahi , Y. Ogata , A. Zíková , A. Anupama , R. A. Dalley , N. Acestor , P. J. Myler and K. D. Stuart (2009). A comprehensive analysis of Trypanosoma brucei mitochondrial proteome. Proteomics 9, 434450.

M. Parsons , E. A. Worthey , P. N. Ward and J. C. Mottram (2005). Comparative analysis of the kinomes of three pathogenic trypanosomatids: Leishmania major, Trypanosoma brucei and Trypanosoma cruzi. BMC Genomics 6, 127.

A. Rothnie , A. R. Clarke , P. Kuzmic , A. Cameron and C. J. Smith (2011). A sequential mechanism for clathrin cage disassembly by 70-kDa heat-shock cognate protein (Hsc70) and auxilin. Proceedings of the National. Academy of Sciences, USA 108, 6927–3692.

P. P. Simarro , G. Cecchi , M. Paone , J. R. Franco , A. Diarra , J. A. Ruiz , E. M. Fèvre , F. Courtin , R. C. Mattioli and J. G. Jannin (2010). The atlas of human African trypanosomiasis: a contribution to global mapping of neglected tropical diseases. International Journal of Health Geographics 9, 57.

B. Wickstead , J. T. Carrington , E. Gluenz and K. Gull (2010). The expanded Kinesin-13 repertoire of trypanosomes contains only one mitotic Kinesin indicating multiple extra-nuclear roles. PLoS One 5, e15020.

Y. W. Wu , K. T. Tan , H. Waldmann , R. S. Goody and K. Alexandrov (2007). Interaction analysis of prenylated Rab GTPase with Rab escort protein and GDP dissociation inhibitor explains the need for both regulators. Proceedings of the National Academy of Sciences, USA 104, 1229412299.

Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Parasitology
  • ISSN: 0031-1820
  • EISSN: 1469-8161
  • URL: /core/journals/parasitology
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Keywords: