Analysis of proteasomal proteolysis during the in vitro metacyclogenesis of Trypanosoma cruzi

PLoS ONE

Volumn 6, Issue 6, 2011, Pages

  Cardoso, Josiane ^a   de Paula Lima, Carla ^a   Leal, Tiago ^b   Gradia, Daniela F ^a   Fragoso, Stênio P ^a   Goldenberg, Samuel ^a   de Sá, Renata Guerra ^b   Krieger, Marco A ^a  

^a INSTITUTO CARLOS CHAGAS   (Brazil)

^b FEDERAL UNIVERSITY OF OURO PRETO   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

CARBONYL DERIVATIVE; PROTEASOME; UBIQUITIN;

ARTICLE; CELL DIFFERENTIATION; CELL STRESS; CONTROLLED STUDY; EPIMASTIGOTE; IMMUNOLOCALIZATION; KINETOPLASTID LIFE CYCLE STAGE; METACYCLOGENESIS; NONHUMAN; OXIDATION; PROTEIN ANALYSIS; PROTEIN CONTENT; PROTEIN DEGRADATION; PROTEIN LOCALIZATION; TRYPANOSOMA CRUZI; TRYPOMASTIGOTE; UBIQUITINATION; ANIMAL; ENZYMOLOGY; HYDROLYSIS; METABOLISM; PHYSIOLOGY; WESTERN BLOTTING;

TRYPANOSOMA CRUZI;

ANIMALS; BLOTTING, WESTERN; HYDROLYSIS; PROTEASOME ENDOPEPTIDASE COMPLEX; TRYPANOSOMA CRUZI; UBIQUITINATION;

EID: 79959210732     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0021027     Document Type: Article

References (51)

1. Hochstrasser M, (1995) Ubiquitin, proteasomes, and the regulation of intracellular protein degradation. Curr Opin Cell Biol 7: 215-223.
2. Rubin DM, Finley D, (1995) Proteolysis. The proteasome: a protein-degrading organelle. Curr Biol 8: 854-858.
3. Pahl HL, Baeuerle PA, (1996) Control of gene expression by proteolysis. Curr Opin Cell Biol 8: 340-347.
4. Groettrup M, Souza A, Kuckelkorn U, Kloetzelt PM, (1996) Peptide antigen production by the proteasome: complexity provides efficiency. Immunol Today 17: 429-435.
5. Bonifacino JS, Weissman AM, (1998) Ubiquitin and the control of protein fate in the secretory and endocytic pathways. Annu Rev Cell Biol 14: 19-57.
6. Schubert U, Antón LC, Gibbs J, Norbury CC, Yewdell JW, et al. (2000) Rapid degradation of a large fraction of newly synthesized proteins by proteasomes. Nature 404: 770-774.
7. De Martino GN, Slaughter CA, (1999) The proteasome, a novel protease regulated by multiple mechanisms. J Biol Chem 274: 22123-22136.
8. Barojek M, Glickmam MH, (2004) Keepers at the final gates: regulatory complexes and gating of the proteasome channel. Cell Mol Life Sci 61: 1579-1588.
9. Tanaka K, (1998) Proteasomes: Structure and Biology. J Biochem 123: 195-20412.
10. Grune T, Reinheckel T, Davies K J, (1996) Degradation of oxidized proteins in K562 human hematopoietic cells by proteasome. J Biol Chem 271: 15504-15509.
11. Grune T, Reinheckel T, Davies K J, (1997) Degradation of oxidized proteins in mammalian cells. FASEB J 11: 526-534.
12. Grune T, Reinheckel T, Joshi M, Davies KJ, (1995) Proteolysis in cultured liver epithelial cells during oxidative stress. Role of the multicatalytic proteinase complex, proteasome. J Biol Chem 270: 2344-2351.
13. Reinheckel T, Sitte N, Ullrich O, Kuckelkorn U, Davies KJ, et al. (1998) Comparative resistance of the 20S and 26S proteasome to oxidative stress. Biochem J 335: 637-642.
14. Reinheckel T, Ullrich O, Sitte N, Grune T, (2000) Differential impairment of 20S and 26S proteasome activities in human hematopoietic K562 cells during oxidative stress. Arch Biochem Biophys 377: 65-68.
15. Brooks P, Fuertes G, Murray RZ, Bose S, Knecht E, et al. (2000) Subcellular localization of proteasomes and their regulatory complexes in mammalian cells. Biochem J 346: 155-161.
16. Yao Y, Huang L, Krutchinsky A, Wong ML, Standing KG, et al. (1999) Structural and functional characterizations of the proteasome-activating protein PA26 from Trypanosoma brucei. J Biol Chem 274: 33921-33930.
17. Preckel T, Fung-Leung WP, Cai Z, Vitiello A, Salter-Cid L, et al. (1999) Impaired immunoproteasome assembly and immune responses in PA28-/- mice. Science 286: 2162-2165.
18. Contreras VT, Araujo-Jorge TC, Bonaldo MC, Thomaz N, Barbosa HS, et al. (1988) Biological aspects of the Dm28c clone of Trypanosoma cruzi after metacyclogenesis in chemically defined media. Mem Inst Oswaldo Cruz 83: 123-133.
19. Figueiredo RC, Rosa DS, Soares MJ, (2000) Differentiation of Trypanosoma cruzi epimastigotes: metacyclogenesis and adhesion to substrate are triggered by nutritional stress. J Parasitol 86: 1213-1218.
20. Wainszelbaum MJ, Belaunzaran ML, Lammel EM, Florin-Christensen M, Isola EL, (2003) Free fatty acids induce cell differentiation to infective forms in Trypanosoma cruzi. Biochem J 375: 705-712.
21. Cardoso J, Soares MJ, Menna-Barreto RFS, Le Bloas R, Sotomaior V, et al. (2008) Inhibition of proteasome activity blocks Trypanosoma cruzi growth and metacyclogenesis. Parasitol Res 103: 941-951.
22. De Diego JL, Katz JM, Marshall P, Gutiérrez B, Manning JE, et al. (2001) The ubiquitin proteasome pathway plays an essential role in proteolysis during Trypanosoma cruzi remodeling. Biochemistry 40: 1053-1062.
23. Gutiérrez B, Osorio L, Motta MC, Huima-Byron T, Erdjument-Bromage H, et al. (2009) Molecular characterization and intracellular distribution of the alpha 5 subunit of Trypanosoma cruzi 20S proteasome. Parasitol Int 4: 367-74.
24. Gonzalez J, Pinto-Ramalho JF, Frevert U, Ghiso J, Tomlinso S, et al. (1996) Proteasome activity is required for the stage-specific transformation of a protozoan parasite. J Exp Med 184: 1909-1918.
25. Shaw MK, He CY, Ross DS, Tilney LG, (2000) Proteasome inhibitors block intracellular growth and replication of Toxoplasma gondii. Parasitol 121: 35-47.
26. Gantt SM, Myung MJ, Briones MS, Li WD, Corey JE, et al. (1998) Proteasome inhibitors block development of Plasmodium spp. Antimic Ag Chemot 42: 2731-2738.
27. Ciechanover A, (2006) Intracellular protein degradation: from a vague idea thru the lysosome and the ubiquitin-proteasome system and onto human diseases and drug targeting. Hematology Am Soc Hematol Educ Program 505: 1-12.
28. Goldberg AL, (2007) Functions of the proteasome: from protein degradation and immune surveillance to cancer therapy. Biochem Soc Trans 35: 12-17.
29. Lee H, Goldeberg AL, (1998) Proteasome inhibitors: valuable new tools for cell biologists. Trends in Cell Biol 8: 397-403.
30. Paugam A, Bulteau A, Dupouy-Camet J, Creuzet C, Friguet B, (2003) Characterization and role of protozoan parasite proteasomes. Trends Parasitol 19: 55-59.
31. Jariel-Encontre I, Bossis G, Marc Piechaczyk, (2008) Ubiquitin-independent degradation of proteins by the proteasome. Biochimica et Biophysica Acta 1786: 153-177.
32. Atwood JA, Weatherly DB, Minning TA, Bundy B, Cavola C, et al. (2005) The Trypanosoma cruzi proteome. Science 309: 473-476.
33. Parodi-Talice A, Monteiro-Goes V, Arrambide N, Ávila AR, Duran R, et al. (2007) Proteomic analysis of metacyclic trypomastigotes undergoing Trypanosoma cruzi metacyclogenesis. J Mass Spectrom 42: 1422-1432.
34. Goldenberg S, Contreras VT, Bonaldo MC, Salles JM, Lima-Franco MPA, et al. (1987) In vitro differentiation systems for the study of differential gene expression during Trypanosoma cruzi development. Molecular strategies of parasitic invasion 203-212.
35. Cadenas E, Kevin JAD, (2000) Mitochondrial free radical generation, oxidative stress, and aging. Free Radical Biology & Medicine 29: 222-230.
36. Grune T, Merker K, Sandig G, Davies KJ, (2003) Selective degradation of oxidatively modified protein substrates by the proteasome. Biochem Biophys Res Commun 305: 709-718.
37. Baugh JM, Viktorova EG, Pilipenko EV, (2009) Proteasomes can degrade a significant proportion of cellular proteins independent of ubiquitination. J Mol Biol 386: 814-827.
38. Ferrington DA, Sun H, Murray KK, Costa J, Williams TD, et al. (2001) Selective degradation of oxidized calmodulin by the 20 S proteasome. J Biol Chem 276: 937-945.
39. Hoyt MA, Coffino P, (2004) Ubiquitin-free routes into the proteasome. Cell Mol Life Sci 61: 1596-1600.
40. Mendez J, Zou-yang XH, kim S, Hidaka M, Tansey W, et al. (2002) Human origin recognition complex large subunit is degraded by ubiquitinmediated proteolysis after initiation of DNA replication. Mol Cell 9: 481-491.
41. Chen M, Von Mikecz A, (2005) Xenobiotic-induced recruitment of autoantigens to nuclear proteasomes suggests a role for altered antigen processing in scleroderma. Ann. N. Y. Acad. Sci 1051: 1-8.
42. Baker SP, Grant PA, (2005) The proteasome: not just degrading anymore. Cell 123: 361-363.
43. Gardner RG, Nelson ZW, Gottschling DE, (2005) Degradation-mediated protein quality control in the nucleus. Cell 120: 803-815.
44. Rockel TD, Stuhlmann D, Von Mikecz A, (2005) Proteasomes degrade proteins in focal subdomains of the human cell nucleus. J.Cell Sci 118: 5231-5242.
45. Contreras VT, Araujo-Jorge TC, Bonaldo MC, Thomas N, Barbosa HS, et al. (1988) Biological aspects of the DM 28C clone of Trypanosoma cruzi after metacyclogenesis in chemically defined media. Mem Inst Oswaldo Cruz 83: 123-33.
46. Camargo EP, (1964) Growth and differentiation of Trypanosoma cruzi. Origin of metacyclic trypanosomes in liquid media. Rev Inst Med Trop São Paulo 93: 93-100.
47. Sousa MA, (1983) A simple method to purify biologically and antigenically preserved bloodstream trypomastigotes of Trypanosoma cruzi using DEAE-cellulose columns. Mem Inst Oswaldo Cruz 78: 317-333.
48. Guerra-Sa R, Castro-Borges W, Evangelista EA, Kettelhut IC, Rodrigues V, (2005) Schistosoma mansoni: Functional proteasomes are required for development in the vertebrate host. Exp Parasitol 109: 228-236.
49. Smith PK, Krohn RI, Hermanson GT, Malia HK Gartner FH, et al. (1985) Measurement of protein using bicinchoninic acid. Anal Biochem 150: 76-85.
50. Levine RL, Williams JA, Stadtman ER, Shacter E, (1994) Carbonyl assays for determination of oxidatively modified proteins. Meth Enzymol 233: 346-35753.
51. Towbin H, Staehelin NT, Gordon J, (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: Procedure and some applications. PNAS 76: 4350-4.