Late endosomal Rab7 regulates lysosomal trafficking of endocytic but not biosynthetic cargo in Trypanosoma brucei

Molecular Microbiology

Volumn 82, Issue 3, 2011, Pages 664-678

  Silverman, Jason S ^a   Schwartz, Kevin J ^a   Hajduk, Stephen L ^b   Bangs, James D ^a  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^b University of Georgia ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FLAGELLAR POCKET RECEPTOR; LECTIN; PROTEIN CATL; PROTEIN P67; PROTOZOAL PROTEIN; RAB7 PROTEIN; TRANSFERRIN RECEPTOR; TRYPANOLYTIC FACTOR; UNCLASSIFIED DRUG;

ARTICLE; CELL MIGRATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENDOCYTOSIS; ENDOSOME; LYSOSOME; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN SYNTHESIS; PROTEIN TRANSPORT; REGULATORY MECHANISM; RNA INTERFERENCE; TRYPANOSOMA BRUCEI;

ENDOCYTOSIS; ENDOSOMES; GENE KNOCKDOWN TECHNIQUES; LECTINS; LYSOSOMES; PROTOZOAN PROTEINS; RAB GTP-BINDING PROTEINS; TRYPANOSOMA BRUCEI BRUCEI;

HEXAPODA; LYCOPERSICON ESCULENTUM; MAMMALIA; TRYPANOSOMA BRUCEI;

EID: 80054835194     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2011.07842.x     Document Type: Article

References (66)

1. 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.
2. Allen, C.L., Goulding, D., and Field, M.C. (2003) Clathrin-mediated endocytosis is essential in Trypanosoma brucei. EMBO J 22: 4991-5002.
3. Allen, C.L., Liao, D., Chung, W.L., and Field, M.C. (2007) Dileucine signal-dependent and AP-1-independent targeting of a lysosomal glycoprotein in Trypanosoma brucei. Mol Biochem Parasitol 156: 175-190.
4. Aslett, M., Aurrecoechea, C., Berriman, M., Brestelli, J., Brunk, B.P., Carrington, M., etal. (2010) TriTrypDB: a functional genomic resource for the Trypanosomatidae. Nucleic Acids Res 38: D457-D462.
5. Balber, A.E., Bangs, J.D., Jones, S.M., and Proia, R.L. (1979) Inactivation or elimination of potentially trypanolytic, complement-activating immune complexes by pathogenic trypanosomes. Infect Immun 24: 617-627.
6. Barry, J.D. (1979) Capping of variable antigen on Trypanosoma brucei, and its immunological and biological significance. J Cell Sci 37: 287-302.
7. 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.
8. Biebinger, S., Helfert, S., Steverding, D., Ansorge, I., and Clayton, C. (2003) Impaired dimerization and trafficking of ESAG6 lacking a glycosyl-phosphatidylinositol anchor. Mol Biochem Parasitol 132: 93-96.
9. Böhme, U., and Cross, G.A. (2002) Mutational analysis of the variant surface glycoprotein GPI-anchor signal sequence in Trypanosoma brucei. J Cell Sci 115: 805-816.
10. Braulke, T., and Bonifacino, J.S. (2009) Sorting of lysosomal proteins. Biochim Biophys Acta 1793: 605-614.
11. Bucci, C., Thomsen, P., Nicoziani, P., McCarthy, J., and van Deurs, B. (2000) Rab7: a key to lysosome biogenesis. Mol Biol Cell 11: 467-480.
12. Burkard, G., Fragoso, C.M., and Roditi, I. (2007) Highly efficient stable transformation of bloodstream forms of Trypanosoma brucei. Mol Biochem Parasitol 153: 220-223.
13. Caffrey, C.R., and Steverding, D. (2009) Kinetoplastid papain-like cysteine peptidases. Mol Biochem Parasitol 167: 12-19.
14. Coppens, I., Opperdoes, F.R., Courtoy, P.J., and Baudhuin, P. (1987) Receptor-mediated endocytosis in the bloodstream form of Trypanosoma brucei. J Protozool 34: 465-473.
15. Drain, J., Bishop, J.R., and Hajduk, S.L. (2001) Haptoglobin-related protein mediates trypanosome lytic factor binding to trypanosomes. J Biol Chem 276: 30254-30260.
16. Engstler, M., Thilo, L., Weise, F., Grunfelder, C.G., Schwarz, H., Boshart, M., and Overath, P. (2004) Kinetics of endocytosis and recycling of the GPI-anchored variant surface glycoprotein in Trypanosoma brucei. J Cell Sci 117: 1105-1115.
17. Engstler, M., Bangs, J.D., and Field, M.C. (2006) Intracellular transport systems in trypanosomes: function, evolution and virulence. In Trypanosomes - After the Genome. Barry, J.D., Mottram, J.C., McCulloch, R., and Acosta-Serrano, A. (eds). Wymondham, UK: Horizon Scientific Press, pp. 281-317.
18. Field, H., Sherwin, T., Smith, A.C., Gull, K., and Field, M.C. (2000) Cell-cycle and develpmental regulation of TbRAB31 localisation, a GTP-locked Rab protein from Trypanosoma brucei. Mol Biochem Parasitol 106: 21-35.
19. Field, M.C., and Carrington, M. (2009) The trypanosome flagellar pocket. Nat Rev Microbiol 7: 775-786.
20. Grosshans, B.L., Ortiz, D., and Novick, P. (2006) Rabs and their effectors: achieving specificity in membrane traffick. Proc Natl Acad Sci 103: 11821-11827.
21. Grünfelder, C.G., Engstler, M., Wieise, F., Schwarz, H., Stierhof, Y.-D., Morgan, G.W., etal. (2003) Endocytosis of a glycosylphosphatidylinositol-anchored protein via clatherin-coated vesicles, sorting by default in endosomes and exocytosis via RAB11-positive carriers. Mol Biol Cell 14: 2029-2040.
22. Gruszynski, A.E., DeMaster, A., Hooper, N.M., and Bangs, J.D. (2003) Surface coat remodeling during differentiation of Trypanosoma brucei. J Biol Chem 278: 24665-24672.
23. 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.
24. Hajduk, S.L., Moore, D.R., Vasudevacharya, J., Siqueira, H., Torri, A.F., Tytler, E.M., and Esko, J.D. (1989) Lysis of Trypanosoma brucei by a toxic subspecies of human high density lipoprotein. J Biol Chem 264: 5210-5217.
25. Hall, B.S., Pal, A., Goulding, D., and Field, M.C. (2004) Rab4 is an essential regulator of lysosomal trafficking in trypanosomes. J Biol Chem 279: 45047-45056.
26. Hall, B.S., Smith, E., Langer, W., Jacobs, L.A., Goulding, D., and Field, M.C. (2005) Developmental variation in Rab11-dependent trafficking in Trypanosoma brucei. Eukaryot Cell 4: 971-980.
27. Huete-Perez, J.A., Engel, J.C., Brinen, J.C., Mottram, J.C., and McKerrow, J.H. (1999) Protease trafficking in two primitive eukaryotes is mediated by a prodomain protein motif. J Biol Chem 274: 16249-16256.
28. 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.
29. Kieft, R., Capewell, P., Turner, C.M., Veitch, N.J., MacLeod, A., and Hajduk, S. (2010) Mechanism of Trypanosoma brucei gambiense (group 1) resistance to human trypanosome lytic factor. Proc Natl Acad Sci 107: 16137-16141.
30. 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.
31. 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.
32. 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.
33. Ligtenberg, M.J., Bitter, W., Kieft, R., Steverding, D., Janssen, H., Calafat, J., and Borst, P. (1994) Reconstitution of a surface transferrin binding complex in insect form Trypanosoma brucei. EMBO J 13: 2565-2573.
34. McCann, A.K., Schwartz, K.J., and Bangs, J.D. (2008) A determination of the steady state lysosomal pH of bloodstream stage African trypanosomes. Mol Biochem Parasitol 159: 146-149.
35. McDowell, M.A., Ransom, D.M., and Bangs, J.D. (1998) Glycosylphosphatidylinositol-dependent secretory transport in Trypanosoma brucei. Biochem J 335: 681-689.
36. 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: 2605-2015.
37. Nolan, D.P., Geuskens, M., and Pays, E. (1999) N-linked glycans containing linear poly-N-acetyllactosamine as sorting signals in endocytosis in Trypanosoma brucei. Curr Biol 9: 1169-1172.
38. 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.
39. Pal, A., Hall, B.S., Jefferies, T.R., and Field, M.C. (2003) Rab5 and Rab11 mediate transferrin and anti-variant surface glycoprotein recycling in Trypanosoma brucei. Biochem J 374: 443-451.
40. Pamer, E.G., So, M., and Davis, C.E. (1989) Identification of a developmentally regulated cysteine protease of Trypanosoma brucei. Mol Biochem Parasitol 33: 27-32.
41. Peck, R.F., Shiflett, A.M., Schwartz, K.J., McCann, A., Hajduk, S.L., and Bangs, J.D. (2008) The LAMP-like protein p67 plays an essential role in the lysosome of African trypanosomes. Mol Microbiol 68: 933-946.
42. Poole, B., and Ohkuma, S. (1981) Effect of weak bases on the intralysosomal pH in mouse peritoneal macrophages. J Cell Biol 90: 665-669.
43. 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.
44. Rifkin, M.R. (1978) Trypanosoma brucei: new radioisotope assay for quantitating cell lysis. Exp Parasitol 46: 207-212.
45. Rojas, R., van Vlijmen, T., Mardones, G.A., Prabhu, Y., Rojas, A.L., Mohammed, S., etal. (2008) Regulation of retromer recruitment to endosomes by sequential action of Rab5 and Rab7. J Cell Biol 183: 513-526.
46. Saftig, P., and Klumperman, J. (2009) Lysosome biogenesis and lysosomal membrane proteins: trafficking meets function. Nat Rev Mol Cell Biol 10: 623-635.
47. Sather, S., and Agabian, N. (1985) A 5' spliced leader is added in trans to both alpha- and beta-tubulin transcripts in Trypanosoma brucei. Proc Natl Acad Sci 82: 5695-5699.
48. Schimmoller, F., and Riezman, H. (1993) Involvement of Ypt7p, a small GTPase, in traffic from late endosome to the vacuole in yeast. J Cell Sci 106: 823-830.
49. Schwartz, K.J., Peck, R.F., Tazeh, N.N., and Bangs, J.D. (2005) GPI valence and the fate of secretory membrane proteins in African trypanosomes. J Cell Sci 118: 5499-5511.
50. Schwede, A., and Carrington, M. (2010) Bloodstream form trypanosome plasma membrane proteins: antigenic variation and invariant antigens. Parasitology 137: 2029-2039.
51. Seabra, M.C., and Wasmeier, C. (2004) Controlling the location and activation of Rab GTPases. Curr Opin Cell Biol 16: 451-457.
52. Selzer, P.M., Pingel, S., Hsieh, I., Ugele, B., Chan, V.J., Engel, J.C., etal. (1999) Cysteine protease inhibitors as chemotherapy: lessons from a parasite target. Proc Natl Acad Sci 96: 11015-11022.
53. Sevova, E.S., and Bangs, J.D. (2009) Streamlined architecture and glycosylphosphatidylinositol-dependent trafficking in the early secretory pathway of African trypanosomes. Mol Biol Cell 20: 4739-4750.
54. Shimamura, M., Hager, K.M., and Hajduk, S.L. (2001) The lysosomal targeting and intracellular metabolism of trypanosome lytic factor by Trypanosoma brucei brucei. Mol Biochem Parasitol 115: 227-237.
55. Steverding, D., Stierhof, Y.D., Chaudhri, M., Ligtenberg, M., Schell, D., Beck-Sickinger, A.G., and Overath, P. (1994) ESAG 6 and 7 products of Trypanosoma brucei form a transferrin binding protein complex. Eur J Cell Biol 64: 78-87.
56. Tazeh, N.N., and Bangs, J.D. (2007) Multiple motifs regulate trafficking of the LAMP-like protein p67 in the ancient eukaryote Trypanosoma brucei. Traffic 8: 1007-1017.
57. Tazeh, N.N., Silverman, J.S., Schwartz, K.J., Sevova, E.S., Sutterwala, S.S., and Bangs, J.D. (2009) Role of AP-1 in developmentally regulated lysosomal trafficking in Trypanosoma brucei. Eukaryot Cell 8: 1352-1361.
58. Triggs, V.P., and Bangs, J.D. (2003) Glycosylphosphatidylinositol-dependent protein trafficking in bloodstream stage Trypanosoma brucei. Eukaryot Cell 2: 76-83.
59. Tschudi, C., and Ullu, E. (1988) Polygene transcripts are precursors to calmodulin mRNAs in trypanosomes. EMBO J 7: 455-463.
60. Vanhamme, L., Paturiaux-Hanocq, F., Poelvoorde, P., Nolan, D.P., Lins, L., Van den Abbeele, J., etal. (2003) Apolipoprotein L-I is the trypanosome lytic factor of human serum. Nature 422: 83-87.
61. Vanhollebeke, B., De Muylder, G., Nielsen, M.J., Pays, A., Tebabi, P., Dieu, M., etal. (2008) A haptoglobin-hemoglobin receptor conveys innate immunity to Trypanosoma brucei in humans. Science 320: 677-681.
62. Vanlandingham, P.A., and Ceresa, B.P. (2009) Rab7 regulates late endocytic trafficking downstream of multivesicular body biogenesis and cargo sequestration. J Biol Chem 284: 12110-12124.
63. Vickerman, K. (1969) The fine structure of Trypanosoma congolense in its bloodstream phase. J Protozool 16: 54-69.
64. Wichmann, H., Hengst, L., and Gallwitz, D. (1992) Endocytosis in yeast: evidence for the involvement of a small GTP-binding protein (Ypt7p). Cell 71: 1131-1142.
65. 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.
66. Wollert, T., and Hurley, J.H. (2010) Molecular mechanism of multivesicular body biogenesis by ESCRT complexes. Nature 464: 864-869.