Global profiling of proteolysis during rupture of Plasmodium falciparum from the host erythrocyte

Molecular and Cellular Proteomics

Volumn 10, Issue 5, 2011, Pages

  Bowyer, Paul W ^a   Simon, Gabriel M ^b   Cravatt, Benjamin F ^b   Bogyo, Matthew ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DIPEPTIDYL AMINOPEPTIDASE 3; DIPEPTIDYL PEPTIDASE; UNCLASSIFIED DRUG; CYSTEINE PROTEINASE INHIBITOR; MEMBRANE PROTEIN; PEPTIDE FRAGMENT; PROTEOME;

APOPTOSIS; ARTICLE; CONTROLLED STUDY; ERYTHROCYTE; HOST CELL; NONHUMAN; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROCESSING; PROTEOMICS; AMINO ACID SEQUENCE; CHEMISTRY; COMPUTER PROGRAM; CULTURE TECHNIQUE; CYTOPLASM; DRUG ANTAGONISM; HOST PARASITE INTERACTION; HUMAN; MALARIA FALCIPARUM; MEROZOITE; METABOLISM; MOLECULAR WEIGHT; PARASITOLOGY; PATHOLOGY; PHYSIOLOGY;

PLASMODIUM FALCIPARUM;

AMINO ACID SEQUENCE; CELL CULTURE TECHNIQUES; CYSTEINE PROTEINASE INHIBITORS; CYTOPLASM; DIPEPTIDYL-PEPTIDASES AND TRIPEPTIDYL-PEPTIDASES; ERYTHROCYTES; HOST-PARASITE INTERACTIONS; HUMANS; MALARIA, FALCIPARUM; MEMBRANE PROTEINS; MEROZOITES; MOLECULAR WEIGHT; PEPTIDE FRAGMENTS; PLASMODIUM FALCIPARUM; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEOME; SOFTWARE;

EID: 79955769490     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M110.001636     Document Type: Article

References (32)

1. Arastu-Kapur, S., Ponder, E. L., Fonoviæ, U. P., Yeoh, S., Yuan, F., Fonoviæ, M., Grainger, M., Phillips, C. I., Powers, J. C., and Bogyo, M. (2008) Identification of proteases that regulate erythrocyte rupture by the malaria parasite Plasmodium falciparum. Nat. Chem. Biol. 4, 203-213
2. Chandramohanadas, R., Davis, P. H., Beiting, D. P., Harbut, M. B., Darling, C., Velmourougane, G., Lee, M. Y., Greer, P. A., Roos, D. S., and Greenbaum, D. C. (2009) Apicomplexan parasites co-opt host calpains to facilitate their escape from infected cells. Science 324, 794-797
3. Yeoh, S., O'Donnell, R. A., Koussis, K., Dluzewski, A. R., Ansell, K. H., Osborne, S. A., Hackett, F., Withers-Martinez, C., Mitchell, G. H., Bannister, L. H., Bryans, J. S., Kettleborough, C. A., and Blackman, M. J. (2007) Subcellular discharge of a serine protease mediates release of invasive malaria parasites from host erythrocytes. Cell 131, 1072-1083
4. Gevaert, K., Goethals, M., Martens, L., Van Damme, J., Staes, A., Thomas, G. R., and Vandekerckhove, J. (2003) Exploring proteomes and analyzing protein processing by mass spectrometric identification of sorted N-terminal peptides. Nat. Biotechnol. 21, 566-569
5. Impens, F., Colaert, N., Helsens, K., Ghesquière, B., Timmerman, E., De Bock, P. J., Chain, B. M., Vandekerckhove, J., and Gevaert, K. (2010) A quantitative proteomics design for systematic identification of protease cleavage events. Mol. Cell. Proteomics 9, 2327-2333
6. Dix, M. M., Simon, G. M., and Cravatt, B. F. (2008) Global mapping of the topography and magnitude of proteolytic events in apoptosis. Cell 134, 679-691
7. Mahrus, S., Trinidad, J. C., Barkan, D. T., Sali, A., Burlingame, A. L., and Wells, J. A. (2008) Global sequencing of proteolytic cleavage sites in apoptosis by specific labeling of protein N termini. Cell 134, 866-876
8. Timmer, J. C., Enoksson, M., Wildfang, E., Zhu, W., Igarashi, Y., Denault, J. B., Ma, Y., Dummitt, B., Chang, Y. H., Mast, A. E., Eroshkin, A., Smith, J. W., Tao, W. A., and Salvesen, G. S. (2007) Profiling constitutive proteolytic events in vivo. Biochem. J. 407, 41-48 (Pubitemid 47535579)
9. Kleifeld, O., Doucet, A., auf dem Keller, U., Prudova, A., Schilling, O., Kainthan, R. K., Starr, A. E., Foster, L. J., Kizhakkedathu, J. N., and Overall, C. M. (2010) Isotopic labeling of terminal amines in complex samples identifies protein N-termini and protease cleavage products. Nat. Biotechnol. 28, 281-288
10. Simon, G. M., Dix, M. M., and Cravatt, B. F. (2009) Comparative assessment of large-scale proteomic studies of apoptotic proteolysis. ACS Chem. Biol. 4, 401-408
11. Le Roch, K. G., Zhou, Y., Blair, P. L., Grainger, M., Moch, J. K., Haynes, J. D., De La Vega, P., Holder, A. A., Batalov, S., Carucci, D. J., and Winzeler, E. A. (2003) Discovery of gene function by expression profiling of the malaria parasite life cycle. Science 301, 1503-1508
12. Lambros, C., and Vanderberg, J. P. (1979) Synchronization of Plasmodium falciparum erythrocytic stages in culture. J. Parasitol. 65, 418-420 (Pubitemid 10222999)
13. Pasvol, G., Wilson, R. J., Smalley, M. E., and Brown, J. (1978) Separation of viable schizont-infected red cells of Plasmodium falciparum from human blood. Ann. Trop. Med. Parasitol. 72, 87-88
14. Taylor, H. M., Grainger, M., and Holder, A. A. (2002) Variation in the expression of a Plasmodium falciparum protein family implicated in erythrocyte invasion. Infect. Immun. 70, 5779-5789
15. Tabb, D. L., McDonald, W. H., and Yates, J. R., 3rd (2002) DTASelect and Contrast: tools for assembling and comparing protein identifications from shotgun proteomics. J. Proteome Res. 1, 21-26
16. Elias, J. E., and Gygi, S. P. (2007) Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry. Nat. Methods 4, 207-214 (Pubitemid 46358868)
17. Florens, L., Liu, X., Wang, Y., Yang, S., Schwartz, O., Peglar, M., Carucci, D. J., Yates, J. R., 3rd, and Wub, Y. (2004) Proteomics approach reveals novel proteins on the surface of malaria-infected erythrocytes. Mol. Biochem. Parasitol. 135, 1-11
18. Florens, L., Washburn, M. P., Raine, J. D., Anthony, R. M., Grainger, M., Haynes, J. D., Moch, J. K., Muster, N., Sacci, J. B., Tabb, D. L., Witney, A. A., Wolters, D., Wu, Y., Gardner, M. J., Holder, A. A., Sinden, R. E., Yates, J. R., and Carucci, D. J. (2002) A proteomic view of the Plasmodium falciparum life cycle. Nature 419, 520-526
19. Aurrecoechea, C., Brestelli, J., Brunk, B. P., Dommer, J., Fischer, S., Gajria, B., Gao, X., Gingle, A., Grant, G., Harb, O. S., Heiges, M., Innamorato, F., Iodice, J., Kissinger, J. C., Kraemer, E., Li, W., Miller, J. A., Nayak, V., Pennington, C., Pinney, D. F., Roos, D. S., Ross, C., Stoeckert, C. J., Jr., Treatman, C., and Wang, H. (2009) PlasmoDB: a functional genomic database for malaria parasites. Nucleic Acids Res. 37, D539-D543
20. Cottingham, K. (2010) 1DE proves its worth . . . again. J. Proteome Res. 9, 1636
21. Marchler-Bauer, A., Anderson, J. B., Chitsaz, F., Derbyshire, M. K., DeWeese-Scott, C., Fong, J. H., Geer, L. Y., Geer, R. C., Gonzales, N. R., Gwadz, M., He, S., Hurwitz, D. I., Jackson, J. D., Ke, Z., Lanczycki, C. J., Liebert, C. A., Liu, C., Lu, F., Lu, S., Marchler, G. H., Mullokandov, M., Song, J. S., Tasneem, A., Thanki, N., Yamashita, R. A., Zhang, D., Zhang, N., and Bryant, S. H. (2009) CDD: specific functional annotation with the Conserved Domain Database. Nucleic Acids Res. 37, D205-D210
22. Marchler-Bauer, A., and Bryant, S. H. (2004) CD-Search: protein domain annotations on the fly. Nucleic Acids Res. 32, W327-W331
23. Liu, H., Sadygov, R. G., and Yates, J. R., 3rd (2004) A model for random sampling and estimation of relative protein abundance in shotgun proteomics. Anal. Chem. 76, 4193-4201
24. Bozdech, Z., Llinás, M., Pulliam, B. L., Wong, E. D., Zhu, J., and DeRisi, J. L. (2003) The transcriptome of the intraerythrocytic developmental cycle of Plasmodium falciparum. PLoS Biol. 1, E5
25. Bendtsen, J. D., Nielsen, H., von Heijne, G., and Brunak, S. (2004) Improved prediction of signal peptides: SignalP 3.0. J. Mol. Biol. 340, 783-795
26. Nielsen, H., Engelbrecht, J., Brunak, S., and von Heijne, G. (1997) Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng. 10, 1-6
27. Banerjee, R., Francis, S. E., and Goldberg, D. E. (2003) Food vacuole plasmepsins are processed at a conserved site by an acidic convertase activity in Plasmodium falciparum. Mol. Biochem. Parasitol. 129, 157-165
28. Sijwali, P. S., Shenai, B. R., Gut, J., Singh, A., and Rosenthal, P. J. (2001) Expression and characterization of the Plasmodium falciparum haemoglobinase falcipain-3. Biochem. J. 360, 481-489 (Pubitemid 33151343)
29. Subramanian, S., Sijwali, P. S., and Rosenthal, P. J. (2007) Falcipain cysteine proteases require bipartite motifs for trafficking to the Plasmodium falciparum food vacuole. J. Biol. Chem. 282, 24961-24969
30. Aly, A. S., and Matuschewski, K. (2005) A malarial cysteine protease is necessary for Plasmodium sporozoite egress from oocysts. J. Exp. Med. 202, 225-230
31. Koussis, K., Withers-Martinez, C., Yeoh, S., Child, M., Hackett, F., Knuepfer, E., Juliano, L., Woehlbier, U., Bujard, H., and Blackman, M. J. (2009) A multifunctional serine protease primes the malaria parasite for red blood cell invasion. EMBO J. 28, 725-735
32. Klemba, M., Gluzman, I., and Goldberg, D. E. (2004) A Plasmodium falciparum dipeptidyl aminopeptidase I participates in vacuolar hemoglobin degradation. J. Biol. Chem. 279, 43000-43007