Rab28 function in trypanosomes: Interactions with retromer and ESCRT pathways

Journal of Cell Science

Volumn 124, Issue 22, 2011, Pages 3771-3783

  Lumb, Jennifer H ^a   Leung, Ka Fai ^a   DuBois, Kelly N ^a   Field, Mark C ^a,b  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b ADDENBROOKE S HOSPITAL   (United Kingdom)

Author keywords

Endocytosis; ESCRT; Rab28; Retromer; Trypanosome; Vesicle transport

Indexed keywords

CELL PROTEIN; ESCRT PROTEIN; PROTEIN; RAB28 PROTEIN; UNCLASSIFIED DRUG; VPS23 PROTEIN;

ARTICLE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ENDOCYTOSIS; ENDOSOME; GOLGI COMPLEX; LYSOSOME; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN METABOLISM; PROTEIN PROTEIN INTERACTION; RNA INTERFERENCE; TRYPANOSOMA BRUCEI;

ENDOSOMAL SORTING COMPLEXES REQUIRED FOR TRANSPORT; ENDOSOMES; PROTEIN BINDING; PROTOZOAN PROTEINS; RAB GTP-BINDING PROTEINS; TRYPANOSOMA BRUCEI BRUCEI; VESICULAR TRANSPORT PROTEINS;

EID: 84856804447     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.079178     Document Type: Article

References (87)

1. Ackers, J. P., Dhir, V. and Field, M. C. (2005). A bioinformatic analysis of the RAB genes of Trypanosoma brucei. Mol. Biochem. Parasitol. 141, 89-97.
2. Alexander, D. L., Schwartz, K. J., Balber, A. E. and Bangs, J. D. (2002). Developmentally regulated trafficking of the lysosomal membrane protein p67 in Trypanosoma brucei. J. Cell Sci. 115, 3253-3263.
3. Allen, C. L., Goulding, D. and Field, M. C. (2003). Clathrin-mediated endocytosis is essential in Trypanosoma brucei. EMBO J. 22, 4991-5002.
4. Allen, C. L., Liao, D., Chung, W. L. and Field, M. C. (2007). Dileucine signaldependent and AP-1-independent targeting of a lysosomal glycoprotein in Trypanosoma brucei. Mol. Biochem. Parasitol. 156, 175-190.
5. Alsford, S., Turner, D. J., Obado, S. O., Sanchez-Flores, A., Glover, L., Berriman, M., Hertz-Fowler, C. and Horn, D. (2011). High-throughput phenotyping using parallel sequencing of RNA interference targets in the African trypanosome. Genome Res. 21, 915-924.
6. Arighi, C. N., Hartnell, L. M., Aguilar, R. C., Haft, C. R. and Bonifacino, J. S. (2004). Role of the mammalian retromer in sorting of the cation-independent mannose 6-phosphate receptor. J. Cell Biol. 165, 123-133.
7. Babst, M., Odorizzi, G., Estepa, E. J. and Emr, S. D. (2000). Mammalian tumor susceptibility gene 101 (TSG101) and the yeast homologue, Vps23p, both function in late endosomal trafficking. Traffic 1, 248-258.
8. Bache, K. G., Brech, A., Mehlum, A. and Stenmark, H. (2003). Hrs regulates multivesicular body formation via ESCRT recruitment to endosomes. J. Cell Biol. 162, 435-442.
9. Bastin, P., Ellis, K., Kohl, L. and Gull, K. (2000). Flagellum ontogeny in trypanosomes studied via an inherited and regulated RNA interference system. J. Cell Sci. 113, 3321-3328.
10. Behnia, R. and Munro, S. (2005). Organelle identity and the signposts for membrane traffic. Nature 438, 597-604.
11. Belenkaya, T. Y., Wu, Y., Tang, X., Zhou, B., Cheng, L., Sharma, Y. V., Yan, D., Selva, E. M. and Lin, X. (2008). The retromer complex influences Wnt secretion by recycling wntless from endosomes to the trans-Golgi network. Dev. Cell 14, 120-131.
12. Berriman, M., Ghedin, E., Hertz-Fowler, C., Blandin, G., Renauld, H., Bartholomeu, D. C., Lennard, N. J., Caler, E., Hamlin, N. E., Haas, B. et al. (2005). The genome of the African trypanosome Trypanosoma brucei. Science 309, 416-422.
13. Brauers, A., Schurmann, A., Massmann, S., Muhl-Zurbes, P., Becker, W., Kainulainen, H., Lie, C. and Joost, H. G. (1996). Alternative mRNA splicing of the novel GTPase Rab28 generates isoforms with different C-termini. Eur. J. Biochem. 237, 833-840.
14. Brickman, M. J., Cook, J. M. and Balber, A. E. (1995). Low temperature reversibly inhibits transport from tubular endosomes to a perinuclear, acidic compartment in African trypanosomes. J. Cell Sci. 108, 3611-3621.
15. Brighouse, A., Dacks, J. B. and Field, M. C. (2010). Rab protein evolution and the history of the eukaryotic endomembrane system. Cell Mol. Life Sci. 67, 3449-3465.
16. Cavalier-Smith, T. (2010). Kingdoms Protozoa and Chromista and the eozoan root of the eukaryotic tree. Biol. Lett. 6, 342-345.
17. Chung, W. L., Carrington, M. and Field, M. C. (2004). Cytoplasmic targeting signals in transmembrane invariant surface glycoproteins of trypanosomes. J. Biol. Chem. 279, 54887-54895.
18. Chung, W. L., Leung, K. F., Carrington, M. and Field, M. C. (2008). Ubiquitylation is required for degradation of transmembrane surface proteins in trypanosomes. Traffic 9, 1681-1697.
19. Cross, G. A. (1996). Antigenic variation in trypanosomes: secrets surface slowly. Bioessays 18, 283-291.
20. Delprato, A. and Lambright, D. G. (2007). Structural basis for Rab GTPase activation by VPS9 domain exchange factors. Nat. Struct. Mol. Biol. 14, 406-412.
21. Dhir, V., Goulding, D. and Field, M. C. (2004). TbRAB1 and TbRAB2 mediate trafficking through the early secretory pathway of Trypanosoma brucei. Mol. Biochem. Parasitol. 137, 253-265.
22. Diehl, S., Diehl, F., El-Sayed, N. M., Clayton, C. and Hoheisel, J. D. (2002). Analysis of stage-specific gene expression in the bloodstream and the procyclic form of Trypanosoma brucei using a genomic DNA-microarray. Mol. Biochem. Parasitol. 123, 115-123.
23. Doyotte, A., Russell, M. R., Hopkins, C. R. and Woodman, P. G. (2005). Depletion of TSG101 forms a mammalian "Class E" compartment: a multicisternal early endosome with multiple sorting defects. J. Cell Sci. 118, 3003-3017.
24. Eathiraj, S., Pan, X., Ritacco, C. and Lambright, D. G. (2005). Structural basis of family-wide Rab GTPase recognition by rabenosyn-5. Nature 436, 415-419.
25. Felder, S., Miller, K., Moehren, G., Ullrich, A., Schlessinger, J. and Hopkins, C. R. (1990). Kinase activity controls the sorting of the epidermal growth factor receptor within the multivesicular body. Cell 61, 623-634.
26. Field, H. and Field, M. C. (1997). Tandem duplication of rab genes followed by sequence divergence and acquisition of distinct functions in Trypanosoma brucei. J. Biol. Chem. 272, 10498-10505.
27. Field, H., Farjah, M., Pal, A., Gull, K. and Field, M. C. (1998). Complexity of trypanosomatid endocytosis pathways revealed by Rab4 and Rab5 isoforms in Trypanosoma brucei. J. Biol. Chem. 273, 32102-32110.
28. Field, M. C. and Carrington, M. (2009). The trypanosome flagellar pocket. Nat. Rev. Microbiol. 7, 775-786.
29. Filimonenko, M., Stuffers, S., Raiborg, C., Yamamoto, A., Malerod, L., Fisher, E. M., Isaacs, A., Brech, A., Stenmark, H. and Simonsen, A. (2007). Functional multivesicular bodies are required for autophagic clearance of protein aggregates associated with neurodegenerative disease. J. Cell Biol. 179, 485-500.
30. Fridberg, A., Olson, C. L., Nakayasu, E. S., Tyler, K. M., Almeida, I. C. and Engman, D. M. (2008). Sphingolipid synthesis is necessary for kinetoplast segregation and cytokinesis in Trypanosoma brucei. J. Cell Sci. 121, 5225-5235.
31. Gabernet-Castello, C., Dacks, J. B. and Field, M. C. (2009). The single ENTHdomain protein of trypanosomes; endocytic functions and evolutionary relationship with epsin. Traffic 10, 894-911.
32. Grab, D. J., Wells, C. W., Shaw, M. K., Webster, P. and Russo, D. C. (1992). Endocytosed transferrin in African trypanosomes is delivered to lysosomes and may not be recycled. Eur. J. Cell Biol. 59, 398-404.
33. Grosshans, B. L., Ortiz, D. and Novick, P. (2006). Rabs and their effectors: achieving specificity in membrane traffic. Proc. Natl. Acad. Sci. USA 103, 11821-11827.
34. Hager, K. M., Pierce, M. A., Moore, D. R., Tytler, E. M., Esko, J. D. and Hajduk, S. L. (1994). Endocytosis of a cytotoxic human high density lipoprotein results in disruption of acidic intracellular vesicles and subsequent killing of African trypanosomes. J. Cell Biol. 126,155-167.
35. Hall, B., Allen, C. L., Goulding, D. and Field, M. C. (2004). Both of the Rab5 subfamily small GTPases of Trypanosoma brucei are essential and required for endocytosis. Mol. Biochem. Parasitol. 138, 67-77.
36. Hammond, D. E., Carter, S., McCullough, J., Urbe, S. and Vande Woude, G. (2003). Endosomal dynamics of Met determine signaling output. Mol. Biol. Cell 14, 1346-1354.
37. Hu, Y. H., Warnatz, H. J., Vanhecke, D., Wagner, F., Fiebitz, A., Thamm, S., Kahlem, P., Lehrach, H., Yaspo, M. L. and Janitz, M. (2006). Cell array-based intracellular localization screening reveals novel functional features of human chromosome 21 proteins. BMC Genomics 7, 155.
38. Hung, C. H., Qiao, X., Lee, P. T. and Lee, M. G. (2004). Clathrin-dependent targeting of receptors to the flagellar pocket of procyclic-form Trypanosoma brucei. Eukaryot. Cell 3, 1004-1014.
39. Irminger-Finger, I., Busquets, S., Calabrio, F., Lopez-Soriano, F. J. and Argiles, J. M. (2006). BARD1 content correlates with increased DNA fragmentation associated with muscle wasting in tumour-bearing rats. Oncol. Rep. 15, 1425-1428.
40. Jeffries, T. R., Morgan, G. W. and Field, M. C. (2001). A developmentally regulated rab11 homologue in Trypanosoma brucei is involved in recycling processes. J. Cell Sci. 114, 2617-2626.
41. Katzmann, D. J., Babst, M. and Emr, S. D. (2001). Ubiquitin-dependent sorting into the multivesicular body pathway requires the function of a conserved endosomal protein sorting complex, ESCRT-I. Cell 106, 145-155.
42. Katzmann, D. J., Stefan, C. J., Babst, M. and Emr, S. D. (2003). Vps27 recruits ESCRT machinery to endosomes during MVB sorting. J. Cell Biol. 162, 413-423.
43. Kelley, R. J., Alexander, D. L., Cowan, C., Balber, A. E. and Bangs, J. D. (1999). Molecular cloning of p67, a lysosomal membrane glycoprotein from Trypanosoma brucei. Mol. Biochem. Parasitol. 98, 17-28.
44. Kelly, S., Reed, J., Kramer, S., Ellis, L., Webb, H., Sunter, J., Salje, J., Marinsek, N., Gull, K., Wickstead, B. et al. (2007). Functional genomics in Trypanosoma brucei: a collection of vectors for the expression of tagged proteins from endogenous and ectopic gene loci. Mol. Biochem. Parasitol. 154, 103-109.
45. Kirschbaum, M. H. and Yarden, Y. (2000). The ErbB/HER family of receptor tyrosine kinases: A potential target for chemoprevention of epithelial neoplasms. J. Cell Biochem. Suppl. 34, 52-60.
46. Koumandou, V. L., Natesan, S. K., Sergeenko, T. and Field, M. C. (2008). The trypanosome transcriptome is remodelled during differentiation but displays limited responsiveness within life stages. BMC Genomics 9, 298.
47. Koumandou, V. L., Klute, M. J., Herman, E. K., Nunez-Miguel, R., Dacks, J. B. and Field, M. C. (2011). Evolutionary reconstruction of the retromer complex and its function in Trypanosoma brucei. J. Cell Sci. 124, 1496-1509.
48. Langreth, S. G. and Balber, A. E. (1975). Protein uptake and digestion in bloodstream and culture forms of Trypanosoma brucei. J. Protozool. 22, 40-53.
49. Lee, J. A., Beigneux, A., Ahmad, S. T., Young, S. G. and Gao, F. B. (2007). ESCRTIII dysfunction causes autophagosome accumulation and neurodegeneration. Curr. Biol. 17, 1561-1567.
50. Lee, S. H., Baek, K. and Dominguez, R. (2008). Large nucleotide-dependent conformational change in Rab28. FEBS Lett. 582, 4107-4111.
51. Leung, K. F., Dacks, J. B. and Field, M. C. (2008). Evolution of the multivesicular body ESCRT machinery; retention across the eukaryotic lineage. Traffic 9, 1698-1716.
52. Leung, K. F., Riley, F. S., Carrington, M. and Field, M. C. (2011). Ubiquitylation and developmental regulation of invariant surface protein expression in trypanosomes. Eukaryot. Cell 10, 916-931.
53. Lumb, J. H. and Field, M. C. (2011). Rab23 is a flagellar protein in Trypanosoma brucei. BMC Res. Notes 4, 190.
54. Mackey, Z. B., O'Brien, T. C., Greenbaum, D. C., Blank, R. B. and McKerrow, J. H. (2004). A cathepsin B-like protease is required for host protein degradation in Trypanosoma brucei. J. Biol. Chem. 279, 48426-48433.
55. Mehlert, A., Bond, C. S. and Ferguson, M. A. (2002). The glycoforms of a Trypanosoma brucei variant surface glycoprotein and molecular modeling of a glycosylated surface coat. Glycobiology 12, 607-612.
56. Merithew, E., Hatherly, S., Dumas, J. J., Lawe, D. C., Heller-Harrison, R. and Lambright, D. G. (2001). Structural plasticity of an invariant hydrophobic triad in the switch regions of Rab GTPases is a determinant of effector recognition. J. Biol. Chem. 276, 13982-13988.
57. Moberg, K. H., Schelble, S., Burdick, S. K. and Hariharan, I. K. (2005). Mutations in erupted, the Drosophila ortholog of mammalian tumor susceptibility gene 101, elicit non-cell-autonomous overgrowth. Dev. Cell 9, 699-710.
58. Morgan, G.W., Allen, C. L., Jeffries, T. R., Hollinshead, M. and Field,M. C. (2001). Developmental and morphological regulation of clathrin-mediated endocytosis in Trypanosoma brucei. J. Cell Sci. 114, 2605-2615.
59. Ostermeier, C. and Brunger, A. T. (1999). Structural basis of Rab effector specificity: crystal structure of the small G protein Rab3A complexed with the effector domain of rabphilin-3A. Cell 96, 363-374.
60. Overath, P. and Engstler, M. (2004). Endocytosis, membrane recycling and sorting of GPI-anchored proteins: Trypanosoma brucei as a model system. Mol. Microbiol. 53, 735-744.
61. Overath, P., Chaudhri, M., Steverding, D. and Ziegelbauer, K. (1994). Invariant surface proteins in bloodstream forms of Trypanosoma brucei. Parasitol. Today 10, 53-58.
62. Pal, A., Hall, B. S., Nesbeth, D. N., Field, H. I. and Field, M. C. (2002). Differential endocytic functions of Trypanosoma brucei Rab5 isoforms reveal a glycosylphosphatidylinositol-specific endosomal pathway. J. Biol. Chem. 277, 9529-9539.
63. Pal, A., Hall, B. S., Jeffries, T. R. and Field, M. C. (2003). Rab5 and Rab11 mediate transferrin and anti-variant surface glycoprotein antibody recycling in Trypanosoma brucei. Biochem. J. 374, 443-451.
64. Pays, E., Vanhollebeke, B., Vanhamme, L., Paturiaux-Hanocq, F., Nolan, D. P. and Perez-Morga, D. (2006). The trypanolytic factor of human serum. Nat. Rev. Microbiol. 4, 477-486.
65. Pereira-Leal, J. B. and Seabra, M. C. (2001). Evolution of the Rab family of small GTP-binding proteins. J. Mol. Biol. 313, 889-901.
66. Perez-Morga, D., Vanhollebeke, B., Paturiaux-Hanocq, F., Nolan, D. P., Lins, L., Homble, F., Vanhamme, L., Tebabi, P., Pays, A., Poelvoorde, P. et al. (2005). Apolipoprotein L-I promotes trypanosome lysis by forming pores in lysosomal membranes. Science 309, 469-472.
67. Quijada, L., Guerra-Giraldez, C., Drozdz, M., Hartmann, C., Irmer, H., Ben-Dov, C., Cristodero, M., Ding, M. and Clayton, C. (2002). Expression of the human RNA-binding protein HuR in Trypanosoma brucei increases the abundance of mRNAs containing AU-rich regulatory elements. Nucleic. Acids Res. 30, 4414-4424.
68. Raiborg, C., Malerod, L., Pedersen, N. M. and Stenmark, H. (2008). Differential functions of Hrs and ESCRT proteins in endocytic membrane trafficking. Exp. Cell Res. 314, 801-813.
69. Raper, J., Portela, M. P., Lugli, E., Frevert, U. and Tomlinson, S. (2001). Trypanosome lytic factors: novel mediators of human innate immunity. Curr. Opin. Microbiol. 4, 402-408.
70. Razi, M. and Futter, C. E. (2006). Distinct roles for Tsg101 and Hrs in multivesicular body formation and inward vesiculation. Mol. Biol. Cell 17, 3469-3483.
71. Redmond, S., Vadivelu, J. and Field, M. C. (2003). RNAit: an automated web-based tool for the selection of RNAi targets in Trypanosoma brucei. Mol. Biochem. Parasitol. 128, 115-118.
72. Rink, J., Ghigo, E., Kalaidzidis, Y. and Zerial, M. (2005). Rab conversion as a mechanism of progression from early to late endosomes. Cell 122, 735-749.
73. Seabra, M. C., Mules, E. H. and Hume, A. N. (2002). Rab GTPases, intracellular traffic and disease. Trends Mol. Med. 8, 23-30.
74. Seaman, M. N. (2004). Cargo-selective endosomal sorting for retrieval to the Golgi requires retromer. J. Cell Biol. 165, 111-122.
75. Seaman, M. N., McCaffery, J. M. and Emr. S. D. (1998). A membrane coat complex essential for endosome-to-Golgi retrograde transport in yeast. J. Cell Biol. 142, 665-681.
76. Shorter, J., Watson, R., Giannakou, M. E., Clarke, M., Warren, G. and Barr, F. A. (1999). GRASP55, a second mammalian GRASP protein involved in the stacking of Golgi cisternae in a cell-free system. EMBO J. 18, 4949-4960.
77. Stenmark, H. (2009). Rab GTPases as coordinators of vesicle traffic. Nat. Rev. Mol. Cell. Biol. 10, 513-525.
78. Steverding, D., Stierhof, Y. D., Fuchs, H., Tauber, R. and Overath, P. (1995). Transferrin-binding protein complex is the receptor for transferrin uptake in Trypanosoma brucei. J. Cell Biol. 131, 1173-1182.
79. Tanida, I., Minematsu-Ikeguchi, N., Ueno, T. and Kominami, E. (2005). Lysosomal turnover, but not a cellular level, of endogenous LC3 is a marker for autophagy. Autophagy 1, 84-91.
80. Thompson, B. J., Mathieu, J., Sung, H. H., Loeser, E., Rorth, P. and Cohen, S. M. (2005). Tumor suppressor properties of the ESCRT-II complex component Vps25 in Drosophila. Dev. Cell. 9, 711-720.
81. Vaccari, T. and Bilder, D. (2005). The Drosophila tumor suppressor vps25 prevents nonautonomous overproliferation by regulating notch trafficking. Dev. Cell. 9, 687-698.
82. van Deurs, B., Holm, P. K., Kayser, L., Sandvig, K. and Hansen, S. H. (1993). Multivesicular bodies in HEp-2 cells are maturing endosomes. Eur. J. Cell Biol. 61, 208-224.
83. Vanhollebeke, B., De Muylder, G., Nielsen, M. J., Pays, A., Tebabi, P., Dieu, M., Raes, M., Moestrup, S. K. and Pays, E. (2008). A haptoglobin-hemoglobin receptor conveys innate immunity to Trypanosoma brucei in humans. Science 320, 677-681.
84. Webster, P. and Grab, D. J. (1988). Intracellular colocalization of variant surface glycoprotein and transferrin-gold in Trypanosoma brucei. J. Cell Biol. 106, 279-288.
85. Wirtz, E., Leal, S., Ochatt, C. and Cross, G. A. (1999). A tightly regulated inducible expression system for conditional gene knock-outs and dominant-negative genetics in Trypanosoma brucei. Mol. Biochem. Parasitol. 99, 89-101.
86. Wollert, T. and Hurley, J. H. (2010). Molecular mechanism of multivesicular body biogenesis by ESCRT complexes. Nature 464, 864-869.
87. Yang, R., Frank, B., Hemminki, K., Bartram, C. R., Wappenschmidt, B., Sutter, C., Kiechle, M., Bugert, P., Schmutzler, R. K., Arnold, N. et al. (2008). SNPs in ultraconserved elements and familial breast cancer risk. Carcinogenesis 29, 351-355.