Quantitative proteomics of Trypanosoma cruzi during metacyclogenesis

Proteomics

Volumn 12, Issue 17, 2012, Pages 2694-2703

  de Godoy, Lyris Martins Franco ^a,b   Marchini, Fabricio Klerynton ^a   Pavoni, Daniela Parada ^a   Rampazzo, Rita de Cássia Pontello ^a   Probst, Christian Macagnan ^a   Goldenberg, Samuel ^a   Krieger, Marco Aurelio ^a  

^a INSTITUTO CARLOS CHAGAS   (Brazil)

^b MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

Author keywords

Cellular differentiation; Label free quantification; Mass spectrometry based proteomics; Metacyclogenesis; Trypanosoma cruzi

Indexed keywords

ANTITRYPANOSOMAL AGENT; BENZNIDAZOLE;

ARTICLE; CELL DIFFERENTIATION; CELL POPULATION; DRUG TARGETING; EPIMASTIGOTE; HUMAN; INFECTION; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; METACERCARIA; METACYCLOGENESIS; NONHUMAN; PARASITE DEVELOPMENT; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEOMICS; TRYPANOSOMA CRUZI; TRYPOMASTIGOTE;

CHAGAS DISEASE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; PROTEOMICS; PROTOZOAN PROTEINS; TANDEM MASS SPECTROMETRY; TRYPANOSOMA CRUZI;

HEXAPODA; MAMMALIA; TRYPANOSOMA CRUZI;

EID: 84865562118     PISSN: 16159853     EISSN: 16159861     Source Type: Journal    
DOI: 10.1002/pmic.201200078     Document Type: Article

References (58)

1. Chagas, C., Nova tripanosomiase humana. Estudos sobre a morfolojia e o cyclo evolutivo do Schizotrypanum cruzi n. gen., n. sp., ajente etiolójico de nova morbidade do homem. Mem. Inst. Oswaldo. Cruz. 1909, 1, 159-218.
2. Coura, J. R., Dias, J. C., Epidemiology, control and surveillance of Chagas disease: 100 years after its discovery. Mem. Inst. Oswaldo. Cruz. 2009, 104, Suppl 1, 31-40.
3. Rassi, A., Jr., Rassi, A., Marin-Neto, J. A., Chagas disease. Lancet 2010, 375, 1388-1402.
4. WHO, Chagas disease (American trypanosomiasis). World Health Organization: Fact Sheet 2010, 340.
5. De Souza, W., Basic cell biology of Trypanosoma cruzi. Curr. Pharm. Des. 2002, 8, 269-285.
6. Contreras, V. T., Morel, C. M., Goldenberg, S., Stage specific gene expression precedes morphological changes during Trypanosoma cruzi metacyclogenesis. Mol. Biochem. Parasitol. 1985, 14, 83-96.
7. Goldenberg, S., Salles, J. M., Contreras, V. T., Lima Franco, M. P. et al., Characterization of messenger RNA from epimastigotes and metacyclic trypomastigotes of Trypanosoma cruzi. FEBS Lett. 1985, 180, 265-270.
8. Contreras, V. T., Araujo-Jorge, T. C., Bonaldo, M. C., Thomaz, N. et al., Biological aspects of the Dm 28c clone of Trypanosoma cruzi after metacyclogenesis in chemically defined media. Mem. Inst. Oswaldo. Cruz. 1988, 83, 123-133.
9. Avila, A. R., Dallagiovanna, B., Yamada-Ogatta, S. F., Monteiro-Goes, V. et al., Stage-specific gene expression during Trypanosoma cruzi metacyclogenesis. Genet. Mol. Res. 2003, 2, 159-168.
10. Teixeira, S. M., Kirchhoff, L. V., Donelson, J. E., Post-transcriptional elements regulating expression of mRNAs from the amastin/tuzin gene cluster of Trypanosoma cruzi. J. Biol. Chem. 1995, 270, 22586-22594.
11. Yamada-Ogatta, S. F., Motta, M. C., Toma, H. K., Monteiro-Goes, V. et al., Trypanosoma cruzi: cloning and characterization of two genes whose expression is up-regulated in metacyclic trypomastigotes. Acta Trop. 2004, 90, 171-179.
12. Dallagiovanna, B., Plazanet-Menut, C., Ogatta, S. F., Avila, A. R. et al., Trypanosoma cruzi: a gene family encoding chitin-binding-like proteins is posttranscriptionally regulated during metacyclogenesis. Exp. Parasitol. 2001, 99, 7-16.
13. Avila, A. R., Yamada-Ogatta, S. F., da Silva Monteiro, V., Krieger, M. A. et al., Cloning and characterization of the metacyclogenin gene, which is specifically expressed during Trypanosoma cruzi metacyclogenesis. Mol. Biochem. Parasitol. 2001, 117, 169-177.
14. Minning, T. A., Weatherly, D. B., Atwood, J., 3rd, Orlando, R. et al., The steady-state transcriptome of the four major life-cycle stages of Trypanosoma cruzi. BMC Genomics 2009, 10, 370.
15. Araujo, P. R., Teixeira, S. M., Regulatory elements involved in the post-transcriptional control of stage-specific gene expression in Trypanosoma cruzi: a review. Mem. Inst. Oswaldo. Cruz. 2011, 106, 257-266.
16. Haile, S., Papadopoulou, B., Developmental regulation of gene expression in trypanosomatid parasitic protozoa. Curr. Opin. Microbiol. 2007, 10, 569-577.
17. Clayton, C., Shapira, M., Post-transcriptional regulation of gene expression in trypanosomes and leishmanias. Mol. Biochem. Parasitol. 2007, 156, 93-101.
18. Vanhamme, L., Pays, A., Tebabi, P., Alexandre, S. et al., Specific binding of proteins to the noncoding strand of a crucial element of the variant surface glycoprotein, procyclin, and ribosomal promoters of Trypanosoma brucei. Mol. Cell. Biol. 1995, 15, 5598-5606.
19. Aebersold, R., Mann, M., Mass spectrometry-based proteomics. Nature 2003, 422, 198-207.
20. Bantscheff, M., Schirle, M., Sweetman, G., Rick, J. et al., Quantitative mass spectrometry in proteomics: a critical review. Anal. Bioanal. Chem. 2007, 389, 1017-1031.
21. Ong, S. E., Mann, M., Mass spectrometry-based proteomics turns quantitative. Nat. Chem. Biol. 2005, 1, 252-262.
22. Panchaud, A., Affolter, M., Moreillon, P., Kussmann, M., Experimental and computational approaches to quantitative proteomics: status quo and outlook. J. Proteomics 2008, 71, 19-33.
23. Luber, C. A., Cox, J., Lauterbach, H., Fancke, B. et al., Quantitative proteomics reveals subset-specific viral recognition in dendritic cells. Immunity 2010, 32, 279-289.
24. Atwood, J. A., 3rd, Weatherly, D. B., Minning, T. A., Bundy, B. et al., The Trypanosoma cruzi proteome. Science 2005, 309, 473-476.
25. Parodi-Talice, A., Monteiro-Goes, V., Arrambide, N., Avila, A. R. et al., Proteomic analysis of metacyclic trypomastigotes undergoing Trypanosoma cruzi metacyclogenesis. J. Mass. Spectrom. 2007, 42, 1422-1432.
26. Contreras, V. T., Salles, J. M., Thomas, N., Morel, C. M. et al., In vitro differentiation of Trypanosoma cruzi under chemically defined conditions. Mol. Biochem. Parasitol. 1985, 16, 315-327.
27. Cox, J., Mann, M., MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol. 2008, 26, 1367-1372.
28. El-Sayed, N. M., Myler, P. J., Blandin, G., Berriman, M. et al., Comparative genomics of trypanosomatid parasitic protozoa. Science 2005, 309, 404-409.
29. 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.
30. de Sousa, M. A., A simple method to purify biologically and antigenically preserved bloodstream trypomastigotes of Trypanosoma cruzi using DEAE-cellulose columns. Mem. Inst. Oswaldo. Cruz. 1983, 78, 317-333.
31. Rappsilber, J., Ishihama, Y., Mann, M., Stop and go extraction tips for matrix-assisted laser desorption/ionization, nanoelectrospray, and LC/MS sample pretreatment in proteomics. Anal. Chem. 2003, 75, 663-670.
32. Olsen, J. V., Blagoev, B., Gnad, F., Macek, B. et al., Global, in vivo, and site-specific phosphorylation dynamics in signaling networks. Cell 2006, 127, 635-648.
33. Cox, J., Neuhauser, N., Michalski, A., Scheltema, R. A. et al., Andromeda: a peptide search engine integrated into the MaxQuant environment. J. Proteome Res. 2011, 10, 1794-1805.
34. El-Sayed, N. M., Myler, P. J., Bartholomeu, D. C., Nilsson, D. et al., The genome sequence of Trypanosoma cruzi, etiologic agent of Chagas disease. Science 2005, 309, 409-415.
35. Smyth, G. K., Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat. Appl. Genet. Mol. Biol. 2004, 3, Article3.
36. Benjamini, Y., Hochberg, Y., A practical and powerful approach to multiple testing. J. R. Stat. Soc. Ser. B 1995, 57, 289-300.
37. Conesa, A., Gotz, S., Garcia-Gomez, J. M., Terol, J. et al., Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 2005, 21, 3674-3676.
38. de Godoy, L. M., Olsen, J. V., Cox, J., Nielsen, M. L. et al., Comprehensive mass spectrometry-based proteome quantification of haploid versus diploid yeast. Nature 2008, 455, 1251-1254.
39. D'Orso, I., De Gaudenzi, J. G., Frasch, A. C., RNA-binding proteins and mRNA turnover in trypanosomes. Trends Parasitol. 2003, 19, 151-155.
40. Franceschetti, M., Bueno, E., Wilson, R. A., Tucker, S. L. et al., Fungal virulence and development is regulated by alternative pre-mRNA 3′end processing in Magnaporthe oryzae. PLoS Pathog. 2011, 7, e1002441.
41. Bonaldo, M. C., Souto-Padron, T., de Souza, W., Goldenberg, S., Cell-substrate adhesion during Trypanosoma cruzi differentiation. J. Cell. Biol. 1988, 106, 1349-1358.
42. Basombrio, M. A., Gomez, L., Padilla, A. M., Ciaccio, M. et al., Targeted deletion of the gp72 gene decreases the infectivity of Trypanosoma cruzi for mice and insect vectors. J. Parasitol. 2002, 88, 489-493.
43. Beck, J. T., Ullman, B., Nutritional requirements of wild-type and folate transport-deficient Leishmania donovani for pterins and folates. Mol. Biochem. Parasitol. 1990, 43, 221-230.
44. Scott, D. A., Coombs, G. H., Sanderson, B. E., Folate utilisation by Leishmania species and the identification of intracellular derivatives and folate-metabolising enzymes. Mol. Biochem. Parasitol. 1987, 23, 139-149.
45. Olliaro, P. L., Yuthavong, Y., An overview of chemotherapeutic targets for antimalarial drug discovery. Pharmacol. Ther. 1999, 81, 91-110.
46. Vickers, T. J., Beverley, S. M., Folate metabolic pathways in Leishmania. Essays Biochem. 2011, 51, 63-80.
47. Senkovich, O., Bhatia, V., Garg, N., Chattopadhyay, D., Lipophilic antifolate trimetrexate is a potent inhibitor of Trypanosoma cruzi: prospect for chemotherapy of Chagas' disease. Antimicrob. Agents Chemother. 2005, 49, 3234-3238.
48. Blumenstiel, K., Schoneck, R., Yardley, V., Croft, S. L. et al., Nitrofuran drugs as common subversive substrates of Trypanosoma cruzi lipoamide dehydrogenase and trypanothione reductase. Biochem. Pharmacol. 1999, 58, 1791-1799.
49. Schoneck, R., Billaut-Mulot, O., Numrich, P., Ouaissi, M. A. et al., Cloning, sequencing and functional expression of dihydrolipoamide dehydrogenase from the human pathogen Trypanosoma cruzi. Eur. J. Biochem. 1997, 243, 739-747.
50. Sreider, C. M., Grinblat, L., Stoppani, A. O., Reduction of nitrofuran compounds by heart lipoamide dehydrogenase: role of flavin and the reactive disulfide groups. Biochem. Int. 1992, 28, 323-334.
51. Ramos, E. I., Garza, K. M., Krauth-Siegel, R. L., Bader, J. et al., 2, 3-diphenyl-1, 4-naphthoquinone: a potential chemotherapeutic agent against Trypanosoma cruzi. J. Parasitol. 2009, 95, 461-466.
52. Gutierrez-Correa, J., Trypanosoma cruzi dihydrolipoamide dehydrogenase as target of reactive metabolites generated by cytochrome c/hydrogen peroxide (or linoleic acid hydroperoxide)/phenol systems. Free Radic. Res. 2010, 44, 1345-1358.
53. Murta, S. M., Krieger, M. A., Montenegro, L. R., Campos, F. F. et al., Deletion of copies of the gene encoding old yellow enzyme (TcOYE), a NAD(P)H flavin oxidoreductase, associates with in vitro-induced benznidazole resistance in Trypanosoma cruzi. Mol. Biochem. Parasitol. 2006, 146, 151-162.
54. Lundberg, E., Fagerberg, L., Klevebring, D., Matic, I. et al., Defining the transcriptome and proteome in three functionally different human cell lines. Mol. Syst. Biol. 2010, 6, 450.
55. Marchini, F. K., de Godoy, L. M., Rampazzo, R. C., Pavoni, D. P. et al., Profiling the Trypanosoma cruzi phosphoproteome. PLoS One 2011, 6, e25381.
56. Rangel-Aldao, R., Triana, F., Fernandez, V., Comach, G. et al., Cyclic AMP as an inducer of the cell differentiation of Trypanosoma cruzi. Biochem. Int. 1988, 17, 337-344.
57. Gonzales-Perdomo, M., Romero, P., Goldenberg, S., Cyclic AMP and adenylate cyclase activators stimulate Trypanosoma cruzi differentiation. Exp. Parasitol. 1988, 66, 205-212.
58. Souza, W., Structural organization of Trypanosoma cruzi. Mem. Inst. Oswaldo. Cruz. 2009, 104, Suppl 1, 89-100.