Subcellular proteomics of Trypanosoma cruzi reservosomes

Proteomics

Volumn 9, Issue 7, 2009, Pages 1782-1794

  Sant'Anna, Celso ^a,c   Nakayasu, Ernesto S ^b   Pereira, Miria G ^a   Lourenço, Daniela ^a   De Souza, Wanderley ^a,c   Almeida, Igor C ^b   Cunha e Silva, Narcisa L ^a,d  

^a FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^b UNIVERSITY OF TEXAS AT EL PASO   (United States)

^c INSTITUTO NACIONAL DE METROLOGIA   (Brazil)

^d Av Carlos Chagas Filho 373   (Brazil)

Author keywords

Mass spectrometry; Proteomic analysis; Reservosomes; Trypanosoma cruzi

Indexed keywords

CARRIER PROTEIN; MOLECULAR MARKER; PROTON PUMP;

ARTICLE; CELL FRACTIONATION; ENDOSOME; LIQUID CHROMATOGRAPHY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEOMICS; TANDEM MASS SPECTROMETRY; TRANSMISSION ELECTRON MICROSCOPY; TRYPANOSOMA CRUZI;

TRYPANOSOMA CRUZI;

EID: 65349092770     PISSN: 16159853     EISSN: 16159861     Source Type: Journal    
DOI: 10.1002/pmic.200800730     Document Type: Article

References (56)

1. De Souza, W., From the cell biology to the development of new chemotherapeutic approaches against trypanosomatids: dreams and reality. Kinetoplastid Biol. Dis. 2002, 1, 3.
2. Soares, M. J., De Souza, W., Cytoplasmic organelles of trypanosomatids: a cytochemical and stereological study. J. Submicrosc. Cytol. Pathol. 1988, 20, 349-361.
3. Soares, M. J., de Souza, W., Endocytosis of gold-labeled proteins and LDL by Trypanosoma cruzi. Parasitol. Res. 1991, 77, 461-468.
4. Porto-Carreiro, I., Attias, M., Miranda, K., De Souza, W., Cunha-e-Silva, N., Trypanosoma cruzi epimastigote endocytic pathway: cargo enters the cytostome and passes through an early endosomal network before storage in reservosomes. Eur. J. Cell. Biol. 2000, 79, 858-869.
5. Cunha-e-Silva, N., Sant'Anna, C., Pereira, M. G., Porto-Carreiro, I. et al., Reservosomes: multipurpose organelles? Parasitol. Res. 2006, 99, 325-327.
6. Raposo, G., Marks, M. S., Cutler, D. F., Lysosome-related organelles: driving post-Golgi compartments into specialisation. Curr. Opin. Cell. Biol. 2007, 19, 394-401.
7. Sant'Anna, C., Parussini, R, Lourengo, D., de Souza, W. et al., All Trypanosoma cruzi developmental forms present lysosome-related organelles. Histochem. Cell. Biol. 2008, DOI: 10.1007/S00418-008-0486-8.
8. Soares, M. J., Souto-Padron, T., De Souza, W., Identification of a large prelysosomal compartment in the pathogenic protozoon Trypanosoma cruzi. J. Cell Sci. 1992, 102,157- 167.
9. Sant'Anna, C., Pereira, M. G., Lemgruber, L, de Souza, W., Cunha e Silva, N. L, New insights into the morphology of Trypanosoma cruzi reservosome. Microsc. Res. Tech. 2008, 71, 599-605.
10. Souto-Padron, T., Campetella, O. E., Cazzulo, J. J., de Souza, W., Cysteine proteinase in Trypanosoma cruzi: immunocytochemical localization and involvement in parasite-host cell interaction. J. Cell Sci. 1990, 96, 485-490.
11. Cunha-e-Silva, N. L, Atella, G. C., Porto-Carreiro, I. A., Morgado-Diaz, J. A. et al., Isolation and characterization of a reservosome fraction from Trypanosoma cruzi. FEMS Microbiol. Lett. 2002, 214, 7-12.
12. Parussini, F., Garcia, M., Mucci, J., Aguero, F. et al., Characterization of a lysosomal serine carboxypeptidase from Trypanosoma cruzi. Mol. Biochem. Parasitol. 2003, 131, 11-23.
13. Santos, C. C., Sant'Anna, C., Terres, A., Cunha-e-Silva, N. L. et al., Chagasin, the endogenous cysteine-protease inhibitor of Trypanosoma cruzi, modulates parasite differentiation and invasion of mammalian cells. J. Cell Sci. 2005, 118, 901- 915.
14. +-ATPase of yeast and plants. Biochem. Soc. Trans. 1992, 20, 562-566.
15. +-ATPase in the acidification of the endocytic pathway of Trypanosoma cruzi. Biochem. J. 2005, 392, 467- 474.
16. Ullrich, O., Reinsch, S., Urbe, S., Zerial, M., Parton, R. G., Rabii regulates recycling through the pericentriolar recycling endosome. J. Cell Biol. 1996, 135, 913-924.
17. Mendonca, S. M., Nepomuceno da Silva, J. L, Cunha e- Silva, N., de Souza, W., Gazos Lopes, U., Characterization of a Rabii homologue in Trypanosoma cruzi. Gene 2000, 243, 179-185.
18. Camargo, E. P., Growth and Differentiation in Trypanosoma cruzi. I. Origin of Metacyclic Trypanosomes in Liquid Media. Rev. Inst. Med. Trop. Sao. Paulo. 1964, 12, 93-100.
19. Stone, K. L., Williams, K. R., Enzymatic digestion of proteins in solution and in SDS polyacrylamide gel, in: Walker, J. M. (Ed.), The Protein Protocol Handbook, Humana Press, New Jersey 1996, pp.415-425.
20. Jurado, J. D., Rael, E. D., Lieb, C. S., Nakayasu, E. et al., Complement inactivating proteins and intraspecies venom variation in Crotalus oreganus helleri. Toxicon 2007, 49, 339- 350.
21. Rodrigues, M. L., Nakayasu, E. S., Oliveira, D. L., Nimrichter, L. et al., Extracellular vesicles produced by Cryptococcus neoformans contain protein components associated with virulence. Eukaryot. Cell 2008, 7, 58-67.
22. Eng, J. K., McCormack, A. L., Yates, J. R. Ill, An approach to correlate tandem mass spectral data of peptides with amino acid sequences in a protein database. J. Am. Soc. Mass Spectrom. 1994, 5, 976-989.
23. Groth, D., Lehrach, H., Hennig, S., GOblet: a platform for Gene Ontology annotation of anonymous sequence data. Nucleic Acids Res. 2004, 32, W313-317.
24. Torres, C., Perez-Victoria, F. J., Parodi-Talice, A., Castanys, S., Gamarro, F., Characterization of an ABCA-like transporter involved in vesicular trafficking in the protozoan parasite Trypanosoma cruzi. Mol. Microbiol. 2004, 54, 632-646.
25. Cuevas, I. C., Rohloff, P., Sanchez, D. O., Docampo, R., Characterization of farnesylated protein tyrosine phosphatase TcPRL-1 from Trypanosoma cruzi. Eukaryot. Cell 2005, 4, 1550-1561.
26. Jentsch, T. J., CLC chloride channels and transporters: from genes to protein structure, pathology and physiology. Crit. Rev. Biochem. Mol. Biol. 2008, 43, 3-36.
27. Attie, A. D., ABCA1: at the nexus of cholesterol, HDL and atherosclerosis. Trends. Biochem. Sci. 2007, 32, 172-179.
28. Alexander, D. L, Schwartz, K. J., Balber, A. E., Bangs, J. D., Developmentally regulated trafficking of the lysosomal membrane protein p67 in Trypanosoma brucei. J. Cell Sci. 2002, 115, 3253-3263.
29. Dreger, M., Subcellular proteomics. Mass Spectrom. Rev. 2003, 22, 27-56.
30. De Souza, W., Cunha-e-Silva, N., Cell fractionation of parasitic protozoa -a review. Mem Inst. Oswaldo Cruz. 2003, 98, 151-170.
31. Ferella, M., Nilsson, D., Darban, H., Rodrigues, C. et al., Proteomics in Trypanosoma cruzi-localization of novel proteins to various organelles. Proteomics 2008, 8, 2735-2749.
32. da Silva, R. A., Bartholomeu, D. C., Teixeira, S. M., Control mechanisms of tubulin gene expression in Trypanosoma cruzi. Int. J. Parasitol. 2006, 36, 87-96.
33. Zerial, M., McBride, H., Rab proteins as membrane organizers. Nat. Rev. Mol. Cell. Biol. 2001, 2, 107-117.
34. Tisdale, E. J., Bourne, J. R., Khosravi-Far, R., Der, C. J., Balch, W. E., GTP-binding mutants of rabi and rab2 are potent inhibitors of vesicular transport from the endoplasmic reticulum to the Golgi complex. J. Cell Biol. 1992, 179, 749-761.
35. Dhir, V., Goulding, D., Field, M. C., TbRAB1 and TbRAB2 mediate trafficking through the early secretory pathway of Trypanosoma brucei. Mol. Biochem. Parasitol. 2004, 137, 253-265.
36. Feng, Y, Press, B., Wandinger-Ness, A., Rab 7: an important regulator of late endocytic membrane traffic. J. Cell Biol. 1995, 131, 1435-1452.
37. Bucci, C., Thomsen, P., Nicoziani, P., McCarthy, J., van Deurs, B., Rab7: a key to lysosome biogenesis. Mol. Biol. Cell 2000, 11, 467-480.
38. Denny, P. W., Lewis, S., Tempero, J. E., Goulding, D. et al., Leishmania RAB7: characterisation of terminal endocytic stages in an intracellular parasite. Mol. Biochem. Parasitol. 2002, 123, 105-113.
39. Morgan, G. W., Hall, B. S., Denny, P. W., Field, M. C., Carrington, M., The endocytic apparatus of the kinetoplastida. Part II: machinery and components of the system. Trends Parasitol. 2002, 18, 540-546.
40. Araripe, J. R., Cunha e Silva, N. L, Leal, S. T, de Souza, W., Rondinelli, E., Trypanosoma cruzi: TcRAB7 protein is localized at the Golgi apparatus in epimastigotes. Biochem. Biophys. Res. Commun. 2004, 321, 397-402.
41. Martin, S., Parton, R. G., Characterization of Rab18, a lipid droplet-associated small GTPase. Methods Enzymol. 2008, 438, 109-129.
42. Jeffries, T. R., Morgan, G. W., Field, M. C., TbRAB18, a developmentally regulated Golgi GTPase from Trypanosoma brucei. Mol. Biochem. Parasitol. 2002, 121, 63-74.
43. Hu, Z. Z., Valencia, J. C., Huang, H., Chi, A. et al., Comparative bioinformatics analyses and profiling of lysosomerelated organelle proteomes. Int. J. Mass Spectrom. 2007, 259,147-160.
44. Sant'Anna, C., de Souza, W., Cunha-e-Silva, N., Biogenesis of the reservosomes of Trypanosoma cruzi. Microsc. Microanal. 2004, 10, 637-646.
45. Lara, F. A., Sant'anna, C., Lemos, D., Laranja, G. A. et al., Heme requirement and intracellular trafficking in Trypanosoma cruzi epimastigotes. Biochem. Biophys. Res. Commun. 2007, 355, 16-22.
46. Adade, C. M., de Castro, S. L., Soares, M. J., Ultrastructural localization of Trypanosoma cruzi lysosomes by aryl sulphatase cytochemistry. Micron 2007, 38, 252-256.
47. Alvarez, V. E., Kosec, G., Sant Anna, C., Turk, V. et al., Blocking autophagy to prevent parasite differentiation: a possible new strategy for fighting parasitic infections? Autophagy 2008, 4, 361-363.
48. Alvarez, V. E., Kosec, G., Sant'Anna, C., Turk, V. et al., Autophagy is involved in nutritional stress response and differentiation in Trypanosoma cruzi. J. Biol. Chem. 2008, 283, 3454-3464.
49. Andersen, J. S., Mann, M., Organellar proteomics: turning inventories into insights. EMBO Rep. 2006, 7, 874-879.
50. Foster, L. J., de Hoog, C. L, Zhang, Y, Zhang, Y, et. al., A mammalian organelle map by protein correlation profiling. Cell 2006, 125, 187-199.
51. Okada, M., Huston, C. D., Mann, B.J., Petri, W.A. Jr. et al., Proteomic analysis of phagocytosis in the enteric protozoan parasite Entamoeba histolytica. Eukaryot. Cell 2005, 4, 827- 831.
52. Gotthardt, D., Warnatz, H. J., Henschel, O., Brückert, F. et al., High-resolution dissection of phagosome maturation reveals distinct membrane trafficking phases. Mol. Biol. Cell 2002, 13, 3508-3520.
53. Broadhead, R., Dawe, H. R., Farr, H., Griffiths, S. et al., Flagellar motility is required for the viability of the bloodstream trypanosome. Nature 2006, 440, 224-227.
54. Colasante, C., Ellis, M., Ruppert, T., Voncken, F., Comparative proteomics of glycosomes from bloodstream form and procyclic culture form Trypanosoma brucei brucei. Proteomics 2006, 6, 3275-3293.
55. Vertommen, D., Van Roy, J., Szikora, J. P., Rider, M. H. et al., Differential expression of glycosomal and mitochondrial proteins in the two major life-cycle stages of Trypanosoma brucei. Mol. Biochem. Parasitol. 2008, 158, 189-201.
56. Ouaissi, M. A., Dubremetz, J. F., Schöneck, R., Fernandez- Gomez, R. et al., Trypanosoma cruzi: a 52 kDa protein sharing sequence homology with GST is localized in parasite organelles morphologically resembling reservosomes. Exp. Parasitol. 1995, 81, 453-461.