Rab11 function in trypanosoma brucei: Identification of conserved and novel interaction partners

Eukaryotic Cell

Volumn 10, Issue 8, 2011, Pages 1082-1094

  Gabernet Castello, Carme ^a   DuBois, Kelly N ^a   Nimmo, Camus ^a   Field, Mark C ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

HYBRID PROTEIN; MEMBRANE PROTEIN; PROTOZOAL PROTEIN; RAB PROTEIN; RAB11 PROTEIN;

ARTICLE; BIOLOGY; CHEMISTRY; FLAGELLUM; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; NUCLEOTIDE SEQUENCE; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN TRANSPORT; TRYPANOSOMA BRUCEI; TWO HYBRID SYSTEM;

COMPUTATIONAL BIOLOGY; CONSERVED SEQUENCE; FLAGELLA; MEMBRANE PROTEINS; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN TRANSPORT; PROTOZOAN PROTEINS; RAB GTP-BINDING PROTEINS; RECOMBINANT FUSION PROTEINS; TRANSCRIPTION, GENETIC; TRYPANOSOMA BRUCEI BRUCEI; TWO-HYBRID SYSTEM TECHNIQUES;

HOMO SAPIENS; METAZOA; TRYPANOSOMA BRUCEI;

EID: 79961049718     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.05098-11     Document Type: Article

References (90)

1. Ackers, J. P., V. Dhir, and M. C. Field. 2005. A bioinformatic analysis of the RAB genes of Trypanosoma brucei. Mol. Biochem. Parasitol. 141:89-97.
2. Allen, C. L., D. Goulding, and M. C. Field. 2003. Clathrin-mediated endocytosis is essential in Trypanosoma brucei. EMBO J. 22:4991-5002.
3. Berriman, M., et al. 2005. The genome of the African trypanosome Trypanosoma brucei. Science 309:416-422.
4. Briggs, L. J., J. A. Davidge, B. Wickstead, M. L. Ginger, and K. Gull. 2004. More than one way to build a flagellum: comparative genomics of parasitic protozoa. Curr. Biol. 14:R611-612.
5. Broadhead, R., et al. 2006. Flagellar motility is required for the viability of the bloodstream trypanosome. Nature 440:224-227.
6. Cai, H., K. Reinisch, and S. Ferro-Novick. 2007. Coats, tethers, Rabs, and SNAREs work together to mediate the intracellular destination of a transport vesicle. Dev. Cell 12:671-682.
7. Cavalier-Smith, T. 2002. The phagotrophic origin of eukaryotes and phylogenetic classification of Protozoa. Int. J. Syst. Evol. Microbiol. 52:297-354.
8. Conti, F., S. Sertic, A. Reversi, and B. Chini. 2009. Intracellular trafficking of the human oxytocin receptor: evidence of receptor recycling via a Rab4/Rab5 short cycle. Am. J. Physiol. Endocrinol Metab. 296:E532-E542.
9. Cullis, D. N., B. Philip, J. D. Baleja, and L. A. Feig. 2002. Rab11-FIP2, an adaptor protein connecting cellular components involved in internalization and recycling of epidermal growth factor receptors. J. Biol. Chem. 277: 49158-49166.
10. Dacks, J. B., and M. C. Field. 2007. Evolution of the eukaryotic membranetrafficking system: origin, tempo and mode. J. Cell Sci. 120:2977-2985.
11. Dacks, J. B., P. P. Poon, and M. C. Field. 2008. Phylogeny of endocytic components yields insight into the process of nonendosymbiotic organelle evolution. Proc. Natl. Acad. Sci. U. S. A. 105:588-593.
12. Dacks, J. B., A. A. Peden, and M. C. Field. 2009. Evolution of specificity in the eukaryotic endomembrane system. Int. J. Biochem. Cell Biol. 41:330-340.
13. DeGrasse, J. A., et al. 2009. Evidence for a shared nuclear pore complex architecture that is conserved from the last common eukaryotic ancestor. Mol. Cell Proteomics 8:2119-2130.
14. Deininger, K., et al. 2008. The Rab5 guanylate exchange factor Rin1 regulates endocytosis of the EphA4 receptor in mature excitatory neurons. Proc. Natl. Acad. Sci. U. S. A. 105:12539-12544.
15. Dhir, V., D. Goulding, and M. C. Field. 2004. TbRAB1 and TbRAB2 mediate trafficking through the early secretory pathway of Trypanosoma brucei. Mol. Biochem. Parasitol. 137:253-265.
16. Doherty, G. J., and H. T. McMahon. 2009. Mechanisms of endocytosis. Annu. Rev. Biochem. 78:857-902.
17. Ducharme, N. A., et al. 2007. Rab11-FIP2 regulates differentiable steps in transcytosis. Am. J. Physiol. Cell Physiol. 293:C1059-C1072.
18. Fan, G. H., L. A. Lapierre, J. R. Goldenring, J. Sai, and A. Richmond. 2004. Rab11-family interacting protein 2 and myosin Vb are required for CXCR2 recycling and receptor-mediated chemotaxis. Mol. Biol. Cell 15:2456-2469.
19. Field, H., and M. C. Field. 1997. Tandem duplication of rab genes followed by sequence divergence and acquisition of distinct functions in Trypanosoma brucei. J. Biol. Chem. 272:10498-10505.
20. 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.
21. Field, H., T. Sherwin, A. C. Smith, K. Gull, and M. C. Field. 2000. Cell-cycle and developmental regulation of TbRAB31 localisation, a GTP-locked Rab protein from Trypanosoma brucei. Mol. Biochem. Parasitol. 106:21-35.
22. Field, M. C., C. Gabernet-Castello, and J. B. Dacks. 2007. Reconstructing the evolution of the endocytic system: insights from genomics and molecular cell biology. Adv. Exp. Med. Biol. 607:84-96.
23. Field, M. C., and A. J. O'Reilly. 2008. How complex is GTPase signaling in trypanosomes? Trends Parasitol. 24:253-257.
24. Field, M. C., D. Horn, and M. Carrington. 2008. Analysis of small GTPase function in trypanosomes. Methods Enzymol. 438:57-76.
25. Foth, B. J., M. C. Goedecke, and D. Soldati. 2006. New insights into myosin evolution and classification. Proc. Natl. Acad. Sci. U. S. A. 103:3681-3686.
26. Fukuda, M., E. Kanno, K. Ishibashi, and T. Itoh. 2008. Large scale screening for novel rab effectors reveals unexpected broad Rab binding specificity. Mol. Cell Proteomics 7:1031-1042.
27. Gabernet-Castello, C., J. B. Dacks, and M. C. Field. 2009. The single ENTHdomain protein of trypanosomes; endocytic functions and evolutionary relationship with epsin. Traffic 10:894-911.
28. Gadelha, C., et al. 2009. Membrane domains and flagellar pocket boundaries are influenced by the cytoskeleton in African trypanosomes. Proc. Natl. Acad. Sci. U. S. A. 106:17425-17430.
29. Garcia-Mata, R., and K. Burridge. 2007. Catching a GEF by its tail. Trends Cell Biol. 17:36-43.
30. Giansanti, M. G., G. Belloni, and M. Gatti. 2007. Rab11 is required for membrane trafficking and actomyosin ring constriction in meiotic cytokinesis of Drosophila males. Mol. Biol. Cell 18:5034-5047.
31. Grosshans, B. L., D. Ortiz, and P. Novick. 2006. Rabs and their effectors: achieving specificity in membrane traffic. Proc. Natl. Acad. Sci. U. S. A. 103:11821-11827.
32. Grunfelder, C. G., et al. 2003. Endocytosis of a glycosylphosphatidylinositol-anchored protein via clathrin-coated vesicles, sorting by default in endosomes, and exocytosis via RAB11-positive carriers. Mol. Biol. Cell 14:2029-2040.
33. Haas, A. K., E. Fuchs, R. Kopajtich, and F. A. Barr. 2005. A GTPaseactivating protein controls Rab5 function in endocytic trafficking. Nat. Cell Biol. 7:887-893.
34. Hales, C. M., et al. 2001. Identification and characterization of a family of Rab11-interacting proteins. J. Biol. Chem. 276:39067-39075.
35. Hales, C. M., J. P. Vaerman, and J. R. Goldenring. 2002. Rab11 family interacting protein 2 associates with Myosin Vb and regulates plasma membrane recycling. J. Biol. Chem. 277:50415-50421.
36. 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.
37. 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.
38. Hall, B. S., et al. 2005. Developmental variation in Rab11-dependent trafficking in Trypanosoma brucei. Eukaryot. Cell 4:971-980.
39. Hickson, G. R., et al. 2003. Arfophilins are dual Arf/Rab 11 binding proteins that regulate recycling endosome distribution and are related to Drosophila nuclear fallout. Mol. Biol. Cell 14:2908-2920.
40. Horgan, C. P., M. Walsh, T. H. Zurawski, and M. W. McCaffrey. 2004. Rab11-FIP3 localises to a Rab11-positive pericentrosomal compartment during interphase and to the cleavage furrow during cytokinesis. Biochem. Biophys. Res. Commun. 319:83-94.
41. Hsu, S. C., D. TerBush, M. Abraham, and W. Guo. 2004. The exocyst complex in polarized exocytosis. Int. Rev. Cytol. 233:243-265.
42. Innamorati, G., C. Le Gouill, M. Balamotis, and M. Birnbaumer. 2001. The long and the short cycle. Alternative intracellular routes for trafficking of G-protein-coupled receptors. J. Biol. Chem. 276:13096-13103.
43. 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.
44. Jones, M. C., P. T. Caswell, and J. C. Norman. 2006. Endocytic recycling pathways: emerging regulators of cell migration. Curr. Opin. Cell Biol. 18: 549-557.
45. Junutula, J. R., et al. 2004. Molecular characterization of Rab11 interactions with members of the family of Rab11-interacting proteins. J. Biol. Chem. 279:33430-33437.
46. Kohl, L., T. Sherwin, and K. Gull. 1999. Assembly of the paraflagellar rod and the flagellum attachment zone complex during the Trypanosoma brucei cell cycle. J. Eukaryot. Microbiol. 46:105-109.
47. Koumandou, V. L., J. B. Dacks, R. M. Coulson, and M. C. Field. 2007. Control systems for membrane fusion in the ancestral eukaryote; evolution of tethering complexes and SM proteins. BMC Evol. Biol. 7:29.
48. Koumandou, V. L., S. K. Natesan, T. Sergeenko, and M. C. Field. 2008. The trypanosome transcriptome is remodelled during differentiation but displays limited responsiveness within life stages. BMC Genomics 9:298.
49. Langevin, J., et al. 2005. Drosophila exocyst components Sec5, Sec6, and Sec15 regulate DE-Cadherin trafficking from recycling endosomes to the plasma membrane. Dev. Cell 9:365-376.
50. Lapierre, L. A., et al. 2001. Myosin vb is associated with plasma membrane recycling systems. Mol. Biol. Cell 12:1843-1857.
51. Lemmon, S. K., and E. W. Jones. 1987. Clathrin requirement for normal growth of yeast. Science 238:504-509.
52. Leterrier, C., D. Bonnard, D. Carrel, J. Rossier, and Z. Lenkei. 2004. Constitutive endocytic cycle of the CB1 cannabinoid receptor. J. Biol. Chem. 279:36013-36021.
53. Leung, K. F., J. B. Dacks, and M. C. Field. 2008. Evolution of the multivesicular body ESCRT machinery; retention across the eukaryotic lineage. Traffic 9:1698-1716.
54. Li, J. B., et al. 2004. Comparative genomics identifies a flagellar and basal body proteome that includes the BBS5 human disease gene. Cell 117:541-552.
55. Lindsay, A. J., and M. W. McCaffrey. 2002. Rab11-FIP2 functions in transferring recycling and associates with endosomal membranes via its COOHterminal domain. J. Biol. Chem. 277:27193-27199.
56. Lindsay, A. J., et al. 2002. Rab coupling protein (RCP), a novel Rab4 and Rab11 effector protein. J. Biol. Chem. 277:12190-12199.
57. Liu, Y. J., M. C. Hodson, and B. D. Hall. 2006. Loss of the flagellum happened only once in the fungal lineage: phylogenetic structure of kingdom Fungi inferred from RNA polymerase II subunit genes. BMC Evol. Biol. 6:74.
58. Mazelova, J., et al. 2009. Ciliary targeting motif VxPx directs assembly of a trafficking module through Arf4. EMBO J. 28:183-192.
59. Meller, N., S. Merlot, and C. Guda. 2005. CZH proteins: a new family of Rho-GEFs. J. Cell Sci. 118:4937-4946.
60. Merchant, S. S., et al. 2007. The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science 318:245-250.
61. Meyers, J. M., and R. Prekeris. 2002. Formation of mutually exclusive Rab11 complexes with members of the family of Rab11-interacting proteins regulates Rab11 endocytic targeting and function. J. Biol. Chem. 277:49003-49010.
62. Nachury, M. V., et al. 2007. A core complex of BBS proteins cooperates with the GTPase Rab8 to promote ciliary membrane biogenesis. Cell 129:1201-1213.
63. Natesan, S. K., L. Peacock, K. Matthews, W. Gibson, and M. C. Field. 2007. Activation of endocytosis as an adaptation to the mammalian host by trypanosomes. Eukaryot. Cell 6:2029-2037.
64. Natesan, S. K., et al. 2009. The trypanosome Rab-related proteins RabX1 and RabX2 play no role in intracellular trafficking but may be involved in fly infectivity. PLoS One 4:e7217.
65. Odronitz, F., and M. Kollmar. 2007. Drawing the tree of eukaryotic life based on the analysis of 2,269 manually annotated myosins from 328 species. Genome Biol. 8:R196.
66. 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.
67. Prekeris, R., J. Klumperman, and R. H. Scheller. 2000. A Rab11/Rip11 protein complex regulates apical membrane trafficking via recycling endosomes. Mol. Cell 6:1437-1448.
68. Prekeris, R., J. M. Davies, and R. H. Scheller. 2001. Identification of a novel Rab11/25 binding domain present in Eferin and Rip proteins. J. Biol. Chem. 276:38966-38970.
69. Prekeris, R. 2003. Rabs, Rips, FIPs, and endocytic membrane traffic. Cientific World Journal 3:870-880.
70. Redmond, S., J. Vadivelu, and M. C. Field. 2003. RNAit: an automated web-based tool for the selection of RNAi targets in Trypanosoma brucei. Mol. Biochem. Parasitol. 128:115-118.
71. Riggs, B., et al. 2003. Actin cytoskeleton remodeling during early Drosophila furrow formation requires recycling endosomal components Nuclear-fallout and Rab11. J. Cell Biol. 163:143-154.
72. Rossman, K. L., C. J. Der, and J. Sondek. 2005. GEF means go: turning on RHO GTPases with guanine nucleotide-exchange factors. Nat. Rev. Mol. Cell Biol. 6:167-180.
73. Schonteich, E., et al. 2008. The Rip11/Rab11-FIP5 and kinesin II complex regulates endocytic protein recycling. J. Cell Sci. 121:3824-3833.
74. Sonnichsen, B., S. De Renzis, E. Nielsen, J. Rietdorf, and M. Zerial. 2000. Distinct membrane domains on endosomes in the recycling pathway visualized by multicolor imaging of Rab4, Rab5, and Rab11. J. Cell Biol. 149:901-914.
75. Stenmark, H. 2009. Rab GTPases as coordinators of vesicle traffic. Nat. Rev. Mol. Cell Biol. 10:513-525.
76. Swoboda, P., H. T. Adler, and J. H. Thomas. 2000. The RFX-type transcription factor DAF-19 regulates sensory neuron cilium formation in C. elegans. Mol. Cell 5:411-421.
77. Ullrich, O., S. Reinsch, S. Urbe, M. Zerial, and R. G. Parton. 1996. Rab11 regulates recycling through the pericentriolar recycling endosome. J. Cell Biol. 135:913-924.
78. Varthakavi, V., et al. 2006. The pericentriolar recycling endosome plays a key role in Vpu-mediated enhancement of HIV-1 particle release. Traffic 7:298-307.
79. Wallace, D. M., A. J. Lindsay, A. G. Hendrick, and M. W. McCaffrey. 2002. Rab11-FIP4 interacts with Rab11 in a GTP-dependent manner and its overexpression condenses the Rab11 positive compartment in HeLa cells. Biochem. Biophys. Res. Commun. 292:909-915.
80. Wang, F., X. Chen, X. Zhang, and L. Ma. 2008. Phosphorylation state of μ-opioid receptor determines the alternative recycling of receptor via Rab4 or Rab11 pathway Mol. Endocrinol. 22:1881-1892.
81. Wennerberg, K., K. L. Rossman, and C. J. Der. 2005. The Ras superfamily at a glance. J. Cell Sci. 118:843-846.
82. Wickstead, B., and K. Gull. 2007. Dyneins across eukaryotes: a comparative genomic analysis. Traffic 8:1708-1721.
83. Wilcke, M., et al. 2000. Rab11 regulates the compartmentalization of early endosomes required for efficient transport from early endosomes to the trans-golgi network. J. Cell Biol. 151:1207-1220.
84. Wilson, G. M., et al. 2005. The FIP3-Rab11 protein complex regulates recycling endosome targeting to the cleavage furrow during late cytokinesis. Mol. Biol. Cell 16:849-860.
85. Woodland, H. R., and A. M. Fry. 2008. Pix proteins and the evolution of centrioles. PLoS One 3:e3778.
86. Woods, A., et al. 1989. Definition of individual components within the cytoskeleton of Trypanosoma brucei by a library of monoclonal antibodies. J. Cell Sci. 93:491-500.
87. Wu, S., S. Q. Mehta, F. Pichaud, H. J. Bellen, and F. A. Quiocho. 2005. Sec15 interacts with Rab11 via a novel domain and affects Rab11 localization in vivo. Nat. Struct. Mol. Biol. 12:879-885.
88. Zerial, M., and H. McBride. 2001. Rab proteins as membrane organizers. Nat. Rev. Mol. Cell Biol. 2:107-117.
89. Zhang, X. M., S. Ellis, A. Sriratana, C. A. Mitchell, and T. Rowe. 2004. Sec15 is an effector for the Rab11 GTPase in mammalian cells. J. Biol. Chem. 279:43027-43034.
90. Zhu, G., et al. 2004. Structural basis of Rab5-Rabaptin5 interaction in endocytosis. Nat. Struct. Mol. Biol. 11:975-983.