SUMOylation pathway in Trypanosoma cruzi: Functional characterization and proteomic analysis of target proteins

Molecular and Cellular Proteomics

Volumn 10, Issue 12, 2011, Pages

  Bayona, Julio C ^a   Nakayasu, Ernesto S ^b,f   Laverrière, Marc ^a   Aguilar, Clemente ^b   Sobreira, Tiago J P ^c   Choi, Hyungwon ^d,g   Nesvizhskii, Alexey I ^d,e   Almeida, Igor C ^b   Cazzulo, Juan J ^a   Alvarez, Vanina E ^a  

^a INSTITUTO DE INVESTIGACIONES BIOTECNOLÓGICAS   (Argentina)

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

^c UNIVERSITY OF SÃO PAULO   (Brazil)

^d UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^e UNIVERSITY OF MICHIGAN   (United States)

^f PACIFIC NORTHWEST NATIONAL LABORATORY   (United States)

^g NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; METACASPASE 3; PROTEOME; PROTOZOAL PROTEIN; SUMO PROTEIN; UNCLASSIFIED DRUG;

AFFINITY CHROMATOGRAPHY; AMINO ACID SEQUENCE; ARTICLE; CONJUGATION; CONTROLLED STUDY; ENZYMOLOGY; EPIMASTIGOTE; FUNCTIONAL PROTEOMICS; GENETICS; IMMUNOFLUORESCENCE; ISOLATION AND PURIFICATION; LIQUID CHROMATOGRAPHY; METABOLISM; MOLECULAR GENETICS; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; PRIORITY JOURNAL; PROTEIN PROCESSING; PROTEOMICS; SEQUENCE ALIGNMENT; SUMOYLATION; TANDEM MASS SPECTROMETRY; TRYPANOSOMA CRUZI;

AMINO ACID SEQUENCE; CHROMATOGRAPHY, AFFINITY; CONSERVED SEQUENCE; ENZYMOLOGY; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; MOLECULAR SEQUENCE DATA; PHYSIOLOGY; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEOME; PROTEOMICS; PROTOZOAN PROTEINS; SEQUENCE ALIGNMENT; SMALL UBIQUITIN-RELATED MODIFIER PROTEINS; SUMOYLATION; TANDEM MASS SPECTROMETRY; TRYPANOSOMA CRUZI;

EID: 83055163826     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M110.007369     Document Type: Article

References (70)

1. Kerscher, O., Felberbaum, R., and Hochstrasser, M. (2006) Modification of proteins by ubiquitin and ubiquitin-like proteins. Annu. Rev. Cell Dev. Biol. 22, 159-180
2. Johnson, E. S. (2004) Protein modification by SUMO. Annu. Rev. Biochem. 73, 355-382
3. Meulmeester, E., and Melchior, F. (2008) Cell biology: SUMO. Nature 452, 709-711 (Pubitemid 351521073)
4. Braschi, E., Zunino, R., and McBride, H. M. (2009) MAPL is a new mitochondrial SUMO E3 ligase that regulates mitochondrial fission. EMBO Rep. 10, 748-754
5. Geiss-Friedlander, R., and Melchior, F. (2007) Concepts in sumoylation: a decade on. Nat. Rev. Mol. Cell Biol. 8, 947-956 (Pubitemid 350176509)
6. Li, T., Evdokimov, E., Shen, R. F., Chao, C. C., Tekle, E., Wang, T., Stadtman, E. R., Yang, D. C., and Chock, P. B. (2004) Sumoylation of heterogeneous nuclear ribonucleoproteins, zinc finger proteins, and nuclear pore complex proteins: a proteomic analysis. Proc. Natl. Acad. Sci. U.S.A. 101, 8551-8556 (Pubitemid 38745808)
7. Denison, C., Rudner, A. D., Gerber, S. A., Bakalarski, C. E., Moazed, D., and Gygi, S. P. (2005) A proteomic strategy for gaining insights into protein sumoylation in yeast. Mol. Cell Proteomics 4, 246-254 (Pubitemid 40439768)
8. Issar, N., Roux, E., Mattei, D., and Scherf, A. (2008) Identification of a novel post-translational modification in Plasmodium falciparum: protein sumoylation in different cellular compartments. Cell Microbiol. 10, 1999-2011
9. Vertegaal, A. C., Ogg, S. C., Jaffray, E., Rodriguez, M. S., Hay, R. T., Andersen, J. S., Mann, M., and Lamond, A. I. (2004) A proteomic study of SUMO-2 target proteins. J. Biol. Chem. 279, 33791-33798 (Pubitemid 39063028)
10. Rosas-Acosta, G., Russell, W. K., Deyrieux, A., Russell, D. H., and Wilson, V. G. (2005) A universal strategy for proteomic studies of SUMO and other ubiquitin-like modifiers. Mol. Cell Proteomics 4, 56-72 (Pubitemid 40309325)
11. Zhou, W., Ryan, J. J., and Zhou, H. (2004) Global analyses of sumoylated proteins in Saccharomyces cerevisiae. Induction of protein sumoylation by cellular stresses. J. Biol. Chem. 279, 32262-32268 (Pubitemid 39014675)
12. Wohlschlegel, J. A., Johnson, E. S., Reed, S. I., and Yates, J. R., 3rd (2004) Global analysis of protein sumoylation in Saccharomyces cerevisiae. J. Biol. Chem. 279, 45662-45668 (Pubitemid 39491554)
13. Panse, V. G., Hardeland, U., Werner, T., Kuster, B., and Hurt, E. (2004) A proteome-wide approach identifies sumoylated substrate proteins in yeast. J. Biol. Chem. 279, 41346-41351 (Pubitemid 39313573)
14. Hannich, J. T., Lewis, A., Kroetz, M. B., Li, S. J., Heide, H., Emili, A., and Hochstrasser, M. (2005) Defining the SUMO-modified proteome by multiple approaches in Saccharomyces cerevisiae. J. Biol. Chem. 280, 4102-4110 (Pubitemid 40288574)
15. Nie, M., Xie, Y., Loo, J. A., and Courey, A. J. (2009) Genetic and proteomic evidence for roles of Drosophila SUMO in cell cycle control, Ras signaling, and early pattern formation. PLoS One 4, e5905
16. Miller, M. J., Barrett-Wilt, G. A., Hua, Z., and Vierstra, R. D. Proteomic analyses identify a diverse array of nuclear processes affected by small ubiquitin-like modifier conjugation in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 107, 16512-16517
17. Braun, L., Cannella, D., Pinheiro, A. M., Kieffer, S., Belrhali, H., Garin, J., and Hakimi, M. A. (2009) The small ubiquitin-like modifier (SUMO)-conjugating system of Toxoplasma gondii. Int. J. Parasitol. 39, 81-90
18. Obado, S. O., Bot, C., Echeverry, M. C., Bayona, J. C., Alvarez, V. E., Taylor, M. C., and Kelly, J. M. (2010) Centromere-associated topoisomerase activity in bloodstream form Trypanosoma brucei. Nucleic Acids Res.
19. Liao, S., Wang, T., Fan, K., and Tu, X. (2010) The small ubiquitin-like modifier (SUMO) is essential in cell cycle regulation in Trypanosoma brucei. Exp. Cell Res. 316, 704-715
20. Cazzulo, J. J., Franke de Cazzulo, B. M., Engel, J. C., and Cannata, J. J. (1985) End products and enzyme levels of aerobic glucose fermentation in trypanosomatids. Mol. Biochem. Parasitol. 16, 329-343 (Pubitemid 16248529)
21. de Sousa, M. A. (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
22. Andrews, N. W., and Colli, W. (1982) Adhesion and interiorization of Trypanosoma cruzi in mammalian cells. J. Protozool. 29, 264-269 (Pubitemid 12025798)
23. Harlow, E., and Lane, D., eds. (1988) Antibodies: A Laboratory Manual, Cold Spring Harbor Laboratory, Cold Spring Harbor, NY
24. Kelly, J. M., Ward, H. M., Miles, M. A., and Kendall, G. (1992) A shuttle vector which facilitates the expression of transfected genes in Trypanosoma cruzi and Leishmania. Nucleic Acids Res. 20, 3963-3969
25. Kosec, G., Alvarez, V. E., Aguero, F., Sanchez, D., Dolinar, M., Turk, B., Turk, V., and Cazzulo, J. J. (2006) Metacaspases of Trypanosoma cruzi: possible candidates for programmed cell death mediators. Mol. Biochem. Parasitol. 145, 18-28 (Pubitemid 41691851)
26. Stone, K. L., and Willians, K. R. (1996) Enzymatic digestion of proteins in solution and in SDS polyacrylamide gel. In: Walker, J. M., ed. The protein protocol handbook, pp. 415-421, Humana Press Inc., Totowa, N.J.
27. Sant'Anna, C., Nakayasu, E. S., Pereira, M. G., Lourenço, D., de Souza, W., Almeida, I. C., and Cunha-E-Silva, N. L. (2009) Subcellular proteomics of Trypanosoma cruzi reservosomes. Proteomics 9, 1782-1794
28. Emmer, B. T., Nakayasu, E. S., Souther, C., Choi, H., Sobreira, T. J., Epting, C. L., Nesvizhskii, A. I., Almeida, I. C., and Engman, D. M. (2011) Global analysis of protein palmitoylation in African trypanosomes. Eukaryot. Cell 10, 455-463
29. Choi, H., Fermin, D., and Nesvizhskii, A. I. (2008) Significance analysis of spectral count data in label-free shotgun proteomics. Mol. Cell Proteomics 7, 2373-2385
30. Taylor, M. C., and Kelly, J. M. (2006) pTcINDEX: a stable tetracycline-regulated expression vector for Trypanosoma cruzi. BMC Biotechnol. 6, 32
31. Kamitani, T., Nguyen, H. P., and Yeh, E. T. (1997) Preferential modification of nuclear proteins by a novel ubiquitin-like molecule. J. Biol. Chem. 272, 14001-14004 (Pubitemid 27232794)
32. Rodriguez, M. S., Dargemont, C., and Hay, R. T. (2001) SUMO-1 conjugation in vivo requires both a consensus modification motif and nuclear targeting. J. Biol. Chem. 276, 12654-12659
33. Li, S. J., and Hochstrasser, M. (2000) The yeast ULP2 (SMT4) gene encodes a novel protease specific for the ubiquitin-like Smt3 protein. Mol. Cell Biol. 20, 2367-2377
34. Li, S. J., and Hochstrasser, M. (1999) A new protease required for cell-cycle progression in yeast. Nature 398, 246-251
35. Mukhopadhyay, D., and Dasso, M. (2007) Modification in reverse: the SUMO proteases. Trends Biochem. Sci. 32, 286-295 (Pubitemid 46874931)
36. Yeh, E. T., Gong, L., and Kamitani, T. (2000) Ubiquitin-like proteins: new wines in new bottles. Gene 248, 1-14 (Pubitemid 30259196)
37. Bailey, D., and O'Hare, P. (2004) Characterization of the localization and proteolytic activity of the SUMO-specific protease, SENP1. J. Biol. Chem. 279, 692-703 (Pubitemid 38044874)
38. Johnson, E. S., Schwienhorst, I., Dohmen, R. J., and Blobel, G. (1997) The ubiquitin-like protein Smt3p is activated for conjugation to other proteins by an Aos1p/Uba2p heterodimer. EMBO J. 16, 5509-5519 (Pubitemid 27399843)
39. Lois, L. M., and Lima, C. D. (2005) Structures of the SUMO E1 provide mechanistic insights into SUMO activation and E2 recruitment to E1. EMBO J. 24, 439-451 (Pubitemid 40343247)
40. Desterro, J. M., Thomson, J., and Hay, R. T. (1997) Ubch9 conjugates SUMO but not ubiquitin. FEBS Lett. 417, 297-300 (Pubitemid 27511608)
41. Galisson, F., Mahrouche, L., Courcelles, M., Bonneil, E., Meloche, S., Chelbi-Alix, M. K., and Thibault, P. (2011) A novel proteomics approach to identify SUMOylated proteins and their modification sites in human cells. Mol. Cell Proteomics 10, M110.004796
42. Westman, B. J., Verheggen, C., Hutten, S., Lam, Y. W., Bertrand, E., and Lamond, A. I. (2010) A proteomic screen for nucleolar SUMO targets shows SUMOylation modulates the function of Nop5/Nop58. Mol. Cell 39, 618-631
43. Ren, J., Gao, X., Jin, C., Zhu, M., Wang, X., Shaw, A., Wen, L., Yao, X., and Xue, Y. (2009) Systematic study of protein sumoylation: Development of a site-specific predictor of SUMOsp 2.0. Proteomics 9, 3409-3412
44. Makhnevych, T., Sydorskyy, Y., Xin, X., Srikumar, T., Vizeacoumar, F. J., Jeram, S. M., Li, Z., Bahr, S., Andrews, B. J., Boone, C., and Raught, B. (2009) Global map of SUMO function revealed by protein-protein interaction and genetic networks. Mol. Cell 33, 124-135
45. Kamitani, T., Kito, K., Nguyen, H. P., Fukuda-Kamitani, T., and Yeh, E. T. (1998) Characterization of a second member of the sentrin family of ubiquitin-like proteins. J. Biol. Chem. 273, 11349-11353 (Pubitemid 28204990)
46. Moldovan, G. L., Pfander, B., and Jentsch, S. (2007) PCNA, the maestro of the replication fork. Cell 129, 665-679 (Pubitemid 46802385)
47. Hoege, C., Pfander, B., Moldovan, G. L., Pyrowolakis, G., and Jentsch, S. (2002) RAD6-dependent DNA repair is linked to modification of PCNA by ubiquitin and SUMO. Nature 419, 135-141 (Pubitemid 35025438)
48. Song, J., Durrin, L. K., Wilkinson, T. A., Krontiris, T. G., and Chen, Y. (2004) Identification of a SUMO-binding motif that recognizes SUMO-modified proteins. Proc. Natl. Acad. Sci. U.S.A. 101, 14373-14378 (Pubitemid 39346756)
49. Hecker, C. M., Rabiller, M., Haglund, K., Bayer, P., and Dikic, I. (2006) Specification of SUMO1- and SUMO2-interacting motifs. J. Biol. Chem. 281, 16117-16127 (Pubitemid 43848507)
50. Kerscher, O. (2007) SUMO junction-what's your function? New insights through SUMO-interacting motifs. EMBO Rep. 8, 550-555
51. Sun, H., Leverson, J. D., and Hunter, T. (2007) Conserved function of RNF4 family proteins in eukaryotes: targeting a ubiquitin ligase to SUMOylated proteins. EMBO J. 26, 4102-4112 (Pubitemid 47462098)
52. Uzunova, K., Göttsche, K., Miteva, M., Weisshaar, S. R., Glanemann, C., Schnellhardt, M., Niessen, M., Scheel, H., Hofmann, K., Johnson, E. S., Praefcke, G. J., and Dohmen, R. J. (2007) Ubiquitin-dependent proteolytic control of SUMO conjugates. J. Biol. Chem. 282, 34167-34175 (Pubitemid 350159437)
53. Meulmeester, E., Kunze, M., Hsiao, H. H., Urlaub, H., and Melchior, F. (2008) Mechanism and consequences for paralog-specific sumoylation of ubiquitin-specific protease 25. Mol. Cell 30, 610-619 (Pubitemid 351755059)
54. Ouyang, J., and Gill, G. (2009) SUMO engages multiple corepressors to regulate chromatin structure and transcription. Epigenetics 4, 440-444
55. Campbell, D. A., Thomas, S., and Sturm, N. R. (2003) Transcription in kinetoplastid protozoa: why be normal? Microbes Infect 5, 1231-1240 (Pubitemid 37410256)
56. Liang, X. H., Haritan, A., Uliel, S., and Michaeli, S. (2003) trans and cis splicing in trypanosomatids: mechanism, factors, and regulation. Eukaryot. Cell 2, 830-840 (Pubitemid 37298696)
57. Minning, T. A., Weatherly, D. B., Atwood, J., 3rd, Orlando, R., and Tarleton, R. L. (2009) The steady-state transcriptome of the four major life-cycle stages of Trypanosoma cruzi. BMC Genomics 10, 370
58. Cuervo, P., Domont, G. B., and De Jesus, J. B. Proteomics of trypanosomatids of human medical importance. J. Proteomics 73, 845-867
59. Atwood, J. A., 3rd, Weatherly, D. B., Minning, T. A., Bundy, B., Cavola, C., Opperdoes, F. R., Orlando, R., and Tarleton, R. L. (2005) The Trypanosoma cruzi proteome. Science 309, 473-476
60. Xu, X., Vatsyayan, J., Gao, C., Bakkenist, C. J., and Hu, J. (2010) Sumoylation of eIF4E activates mRNA translation. EMBO Rep. 11, 299-304
61. Xu, X., Vatsyayan, J., Gao, C., Bakkenist, C. J., and Hu, J. (2010) HDAC2 promotes eIF4E sumoylation and activates mRNA translation gene specifically. J. Biol. Chem. 285, 18139-18143
62. Stuart, K. D., Schnaufer, A., Ernst, N. L., and Panigrahi, A. K. (2005) Complex management: RNA editing in trypanosomes. Trends Biochem. Sci. 30, 97-105 (Pubitemid 40187302)
63. Panse, V. G., Kressler, D., Pauli, A., Petfalski, E., Gnädig, M., Tollervey, D., and Hurt, E. (2006) Formation and nuclear export of preribosomes are functionally linked to the small-ubiquitin-related modifier pathway. Traffic 7, 1311-1321 (Pubitemid 44364170)
64. Smith, M., Bhaskar, V., Fernandez, J., and Courey, A. J. (2004) Drosophila Ulp1, a nuclear pore-associated SUMO protease, prevents accumulation of cytoplasmic SUMO conjugates. J. Biol. Chem. 279, 43805-43814 (Pubitemid 39390686)
65. Uren, A. G., O'Rourke, K., Aravind, L. A., Pisabarro, M. T., Seshagiri, S., Koonin, E. V., and Dixit, V. M. (2000) Identification of paracaspases and metacaspases: two ancient families of caspase-like proteins, one of which plays a key role in MALT lymphoma. Mol. Cell 6, 961-967
66. Vercammen, D., Declercq, W., Vandenabeele, P., and Van Breusegem, F. (2007) Are metacaspases caspases? J. Cell Biol. 179, 375-380 (Pubitemid 350074782)
67. Shirakura, H., Hayashi, N., Ogino, S., Tsuruma, K., Uehara, T., and Nomura, Y. (2005) Caspase recruitment domain of procaspase-2 could be a target for SUMO-1 modification through Ubc9. Biochem. Biophys. Res. Commun. 331, 1007-1015 (Pubitemid 40692461)
68. Hayashi, N., Shirakura, H., Uehara, T., and Nomura, Y. (2006) Relationship between SUMO-1 modification of caspase-7 and its nuclear localization in human neuronal cells. Neurosci. Lett 397, 5-9 (Pubitemid 43348364)
69. Besnault-Mascard, L., Leprince, C., Auffredou, M. T., Meunier, B., Bourgeade, M. F., Camonis, J., Lorenzo, H. K., and Vazquez, A. (2005) Caspase-8 sumoylation is associated with nuclear localization. Oncogene 24, 3268-3273 (Pubitemid 40695108)
70. Wang, H. C., Huang, Y. S., Ho, C. C., Jeng, J. C., and Shih, H. M. (2009) SUMO modification modulates the activity of calpain-2. Biochem. Biophys. Res. Commun. 384, 444-449