Serum resistance-associated protein blocks lysosomal targeting of trypanosome lytic factor in Trypanosoma brucei

Eukaryotic Cell

Volumn 5, Issue 1, 2006, Pages 132-139

  Oli, Monika W ^c,d   Cotlin, Laura F ^a,b   Shiflett, April M ^a   Hajduk, Stephen L ^a  

^a MARINE BIOLOGICAL LABORATORY   (United States)

^b UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^c UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^d BANYAN BIOMARKERS INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HIGH DENSITY LIPOPROTEIN; MEMBRANE PROTEIN; MESSENGER RNA; PROTOZOAL PROTEIN; SERUM RESISTANCE ASSOCIATED PROTEIN, TRYPANOSOMA BRUCEI; TLF1 PROTEIN, HUMAN;

ANIMAL; ARTICLE; CELL NUCLEUS; CHEMISTRY; CYTOLOGY; GENETIC TRANSFECTION; GENETICS; GENOTYPE; HUMAN; LYSOSOME; METABOLISM; MITOCHONDRION; PHENOTYPE; PROTEIN BINDING; PROTEIN TRANSPORT; TRYPANOSOMA BRUCEI;

ANIMALS; CELL NUCLEUS; GENOTYPE; HUMANS; LIPOPROTEINS, HDL; LYSOSOMES; MEMBRANE GLYCOPROTEINS; MITOCHONDRIA; PHENOTYPE; PROTEIN BINDING; PROTEIN TRANSPORT; PROTOZOAN PROTEINS; RNA, MESSENGER; TRANSFECTION; TRYPANOSOMA BRUCEI BRUCEI;

ANIMALIA; BOS TAURUS; MAMMALIA; TRYPANOSOMA; TRYPANOSOMA BRUCEI; TRYPANOSOMA BRUCEI BRUCEI; TRYPANOSOMA BRUCEI RHODESIENSE;

EID: 30944467919     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.5.1.132-139.2006     Document Type: Article

References (51)

1. Bangs, J. D., L. Uyetake, M. J. Brickman, A. E. Balber, and J. C. Boothroyd. 1993. Molecular cloning and cellular localization of a BiP homologue in Trypanosoma brucei. Divergent ER retention signals in a lower eukaryote. J. Cell Sci. 105:1101-1113.
2. Bastin, P., Z. Bagherzadeh, K. R. Matthews, and K. Gull. 1996. A novel epitope tag system to study protein targeting and organelle biogenesis in Trypanosoma brucei. Mol. Biochem. Parasitol. 77:235-239.
3. Bishop, J. R., M. Shimamura, and S. L. Hajduk. 2001. Insight into the mechanism of trypanosome lytic factor-1 killing of Trypanosoma brucei brucei. Mol. Biochem. Parasitol. 118:33-40.
4. Black, S. J., J. R. Seed, and N. B. Murphy. 2001. Innate and acquired resistance to African trypanosomiasis. J. Parasitol. 87:1-9.
5. Burnette, W. N. 1981. "Western blotting": electrophoretic transfer of proteins from sodium dodecyl sulfate-polyacrylamide gels to unmodified nitrocellulose and radiographic detection with antibody and radioiodinated protein A. Anal. Biochem. 112:195-203.
6. Campillo, N., and M. Carrington. 2003. The origin of the serum resistance associated (SRA) gene and a model of the structure of the SRA polypeptide from Trypanosoma brucei rhodesiense. Mol. Biochem. Parasitol. 127:79-84.
7. Carruthers, V. B., and G. A. Cross. 1992. High-efficiency clonal growth of bloodstream- and insect-form Trypanosoma brucei on agarose plates. Proc. Natl. Acad. Sci. USA 89:8818-8821.
8. De Greef, C., E. Chimfwembe, J. Kihang'a Wabacha, E. Bajyana Songa, and R. Hamers. 1992. Only the serum-resistant bloodstream forms of Trypanosoma brucei rhodesiense express the serum resistance associated (SRA) protein. Ann. Soc. Belg. Med. Trop. 72:13-21.
9. De Greef, C., and R. Hamers. 1994. The serum resistance-associated (SRA) gene of Trypanosoma brucei rhodesiense encodes a variant surface glycoprotein-like protein. Mol. Biochem. Parasitol. 68:277-284.
10. De Greef, C., H. Imberechts, G. Matthyssens, N. Van Meirvenne, and R. Hamers. 1989. A gene expressed only in serum-resistant variants of Trypanosoma brucei rhodesiense. Mol. Biochem. Parasitol. 36:169-176.
11. Donelson, J. E. 2003. Antigenic variation and the African trypanosome genome. Acta Trop. 85:391-404.
12. Drain, J., J. R. Bishop, and S. L. Hajduk. 2001. Haptoglobin-related protein mediates trypanosome lytic factor binding to trypanosomes. J. Biol. Chem. 276:30254-30260.
13. Duchateau, P. N., C. R. Pullinger, R. E. Orellana, S. T. Kunitake, J. Naya-Vigne, P. M. O'Connor, M. J. Malloy, and J. P. Kane. 1997. Apolipoprotein L, a new human high density lipoprotein apolipoprotein expressed by the pancreas. J. Biol. Chem. 272:25576-25582.
14. Field, H., B. R. Ali, T. Sherwin, K. Gull, S. L. Croft, and M. C. Field. 1999. TbRab2p, a marker for the endoplasmic reticulum of Trypanosoma brucei, localises to the ERGIC in mammalian cells. J. Cell Sci. 112:147-156.
15. 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.
16. 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.
17. 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.
18. Gibson, W., T. Backhouse, and M. Griffiths. 2002. The human serum resistance associated gene is ubiquitous and conserved in Trypanosoma brucei rhodesiense throughout East Africa. Infect. Genet. Evol. 1:207-214.
19. Hager, K. M., and S. L. Hajduk. 1997. Mechanism of resistance of African trypanosomes to cytotoxic human HDL. Nature 385:823-826.
20. Hager, K. M., M. A. Pierce, D. R. Moore, E. M. Tytler, J. D. Esko, and S. L. Hajduk. 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.
21. Hajduk, S. L., D. R. Moore, J. Vasudevacharya, H. Siqueira, A. F. Torri, E. M. Tytler, and J. D. Esko. 1989. Lysis of Trypanosoma brucei by a toxic subspecies of human high density lipoprotein. J. Biol. Chem. 264:5210-5217.
22. Hirumi, H., and K. Hirumi. 1989. Continuous cultivation of Trypanosoma brucei blood stream forms in a medium containing a low concentration of serum protein without feeder cell layers. J. Parasitol. 75:985-989.
23. Kelley, R. J., D. L. Alexander, C. Cowan, A. E. Balber, and J. D. Bangs. 1999. Molecular cloning of p67, a lysosomal membrane glycoprotein from Trypanosoma brucei. Mol. Biochem. Parasitol. 98:17-28.
24. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
25. Ligtenberg, M. J., W. Bitter, R. Kieft, D. Steverding, H. Janssen, J. Calafat, and P. Borst. 1994. Reconstitution of a surface transferrin binding complex in insect form Trypanosoma brucei. EMBO J. 13:2565-2573.
26. Lorenz, P., P. E. Barth, W. Rudin, and B. Betschart. 1994. Importance of acidic intracellular compartments in the lysis of Trypanosoma brucei brucei by normal human serum. Trans. R. Soc. Trop. Med. Hyg. 88:487-488.
27. Matthyssens, G., C. De Greef, P. Kronenberger, E. Wittouck, N. Van Meirvenne, E. Magnus, and R. Hamers. 1987. Presented at the Molecular Strategies of Parasitic Invasion. UCLA Symposia on Molecular and Cellular Biology New Series, New York, N.Y.
28. Mauricio de Mendonca, S. M., J. L. Nepomuceno da Silva, N. Cunha e-Silva, W. de Souza, and U. Gazos Lopes. 2000. Characterization of a Rab11 homologue in Trypanosoma cruzi. Gene 243:179-185.
29. McEvoy, S. M., and N. Maeda. 1988. Complex events in the evolution of the haptoglobin gene cluster in primates. J. Biol. Chem. 263:15740-15747.
30. Medina-Acosta, E., and G. A. M. Cross. 1993. Rapid isolation of DNA from trypanosomatid protozoa using a simple "mini-prep" procedure. Mol. Biochem. Parasitol. 59:327-330.
31. Milner, J. D., and S. L. Hajduk. 1999. Expression and localization of serum resistance associated protein in Trypanosoma brucei rhodesiense. Mol. Biochem. Parasitol. 104:271-283.
32. Molina Portela, M. P., J. Raper, and S. Tomlinson. 2000. An investigation into the mechanism of trypanosome lysis by human serum factors. Mol. Biochem. Parasitol. 110:273-282.
33. Molina Portela, M. P., E. B. Lugli, E. Recio-Pinto, and J. Raper. 2005. Trypanosome lytic factor, a subclass of high-density lipoprotein, forms cation-selective pores in membranes. Mol. Biochem. Parasitol. 144:218-226.
34. Nolan, D. P., M. Geuskens, and E. Pays. 1999. N-linked glycans containing linear poly-N-acetyllactosamine as sorting signals in endocytosis in Trypanosoma brucei. Curr. Biol. 9:1169-1172.
35. Overath, P., and M. Engstler. 2004. Endocytosis, membrane recycling and sorting of GPI-anchored proteins: Trypanosoma brucei as a model system. Mol. Microbiol. 53:735-744.
36. Perez-Morga, D., B. Vanhollebeke, F. Paturiaux-Hanocq, D. P. Nolan, L. Lins, F. Homble, L. Vanhamme, P. Tebabi, A. Pays, P. Poelvoorde, A. Jacquet, R. Brasseur, and E. Pays. 2005. Apolipoprotein L-I promotes trypanosome lysis by forming pores in lysosomal membranes. Science 309:469-472.
37. Radwanska, M., M. Chamekh, L. Vanhamme, F. Claes, S. Magez, E. Magnus, P. De Baetselier, P. B. Uscher, and E. Pays. 2002. The serum resistance-associated gene as a diagnostic tool for the detection of Trypanosoma brucei rhodesiense. Am. J. Trop. Med. Hyg. 67:684-690.
38. Raper, J., M. P. Portela, E. Lugli, U. Frevert, and S. Tomlinson. 2001. Trypanosome lytic factors: novel mediators of human innate immunity. Curr. Opin. Microbiol. 4:402-408.
39. Rifkin, M. R. 1978. Identification of the trypanocidal factor in normal human serum: high density lipoprotein. Proc. Natl. Acad. Sci. USA 75:3450-3454.
40. Rifkin, M. R., C. De Greef, A. Jiwa, F. R. Landsberger, and S. Z. Shapiro. 1994. Human serum-sensitive Trypanosoma brucei rhodesiense: a comparison with serologically identical human serum-resistant clones. Mol. Biochem. Parasitol. 66:211-220.
41. Rudenko, G., P. A. Blundell, A. Dirks-Mulder, R. Kieft, and P. Borst. 1995. A ribosomal DNA promoter replacing the promoter of a telomeric VSG gene expression site can be efficiently switched on and off in T. brucei. Cell 83:547-553.
42. Sambrook, J., and D. W. Russell. 2001. Molecular cloning: a laboratory manual, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
43. Shiflett, A. M., J. R. Bishop, A. Pahwa, and S. L. Hajduk. 2005. Human high density lipoproteins are platforms for the assembly of multi-component innate immune complexes. J. Biol. Chem. 270:32578-32585.
44. Shimamura, M., K. M. Hager, and S. L. Hajduk. 2001. The lysosomal targeting and intracellular metabolism of trypanosome lytic factor by Trypanosoma brucei brucei. Mol. Biochem. Parasitol. 115:227-237.
45. Smith, A. B., J. D. Esko, and S. L. Hajduk. 1995. Killing of trypanosomes by the human haptoglobin-related protein. Science 268:284-286.
46. Tytler, E. M., D. R. Moore, M. A. Pierce, K. M. Hager, J. D. Esko, and S. L. Hajduk. 1995. Reconstitution of the trypanolytic factor from components of a subspecies of human high-density lipoproteins. Mol. Biochem. Parasitol. 69:9-17.
47. Vanhamme, L., F. Paturiaus-Hanocq, P. Poelvoorde, D. P. Nolan, L. Lins, J. VanDen Abbeele, A. Pays, P. Tebabi, H. Van Xong, A. Jacquet, N. Moguilevsky, M. Dieu, J. P. Kane, P. deBaetselier, R. Brasseur, and E. Pays. 2003. Apolipoprotein L-I is the trypanosome lytic factor of human serum. Nature 422:83-87.
48. Vanhamme, L., and E. Pays. 2004. The trypanosome lytic factor of human serum and the molecular basis of sleeping sickness. Int. J. Parasitol. 34:887-898.
49. Welburn, S. C., K. Picozzi, E. M. Fevre, P. G. Coleman, M. Odiit, M. Carrington, and I. Maudlin. 2001. Identification of human-infective trypanosomes in animal reservoir of sleeping sickness in Uganda by means of serum-resistance-associated (SRA) gene. Lancet 358:2017-2019.
50. Wang, J., U. Bohme, and G. A. M. Cross. 2003. Structural features affecting variant surface glycoprotein expression in Trypanosoma brucei. Mol. Biochem. Parasitol. 128:135-145.
51. Xong, H. V., L. Vanhamme, M. Chamekh, C. E. Chimfwembe, J. Van Den Abbeele, A. Pays, N. Van Meirvenne, R. Hamers, P. De Baetselier, and E. Pays. 1998. A VSG expression site-associated gene confers resistance to human serum in Trypanosoma rhodesiense. Cell 95:839-846.