Proteomic analysis of cleavage events reveals a dynamic two-step mechanism for proteolysis of a key parasite adhesive complex

Molecular and Cellular Proteomics

Volumn 3, Issue 6, 2004, Pages 565-576

  Zhou, Xing W ^a   Blackman, Michael J ^b   Howell, Steven A ^b   Carruthers, Vern B ^a  

^a JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

^b NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CELL ADHESION MOLECULE; MEMBRANE ENZYME; MEMBRANE PROTEIN; PROTEIN INHIBITOR; PROTEIN M2AP; PROTEIN MIC2; PROTEINASE; UNCLASSIFIED DRUG;

ANALYTIC METHOD; ARTICLE; CELL ANCHORAGE; CELL INVASION; CELL SURFACE; COMPLEX FORMATION; CONTROLLED STUDY; ENZYMATIC DEGRADATION; ENZYME SUBSTRATE; FLUORESCENCE; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MOLECULAR DYNAMICS; MOLECULAR MODEL; NONHUMAN; PARASITE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN PROCESSING; PROTEIN STRUCTURE; PROTEOMICS; TOXOPLASMA GONDII; TWO DIMENSIONAL GEL ELECTROPHORESIS;

AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; CELL ADHESION MOLECULES; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; PEPTIDE HYDROLASES; PROTEASE INHIBITORS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEOMICS; PROTOZOAN PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; TOXOPLASMA;

TOXOPLASMA GONDII;

EID: 2442690776     PISSN: 15359476     EISSN: None     Source Type: Journal    
DOI: 10.1074/mcp.M300123-MCP200     Document Type: Article

References (42)

1. Jones, J. L., Kruszon-Moran, D., Wilson, M., McQuillan, G., Navin, T., and McAuley, J. B. (2001) Toxoplasma gondii infection in the United States: Seroprevalence and risk factors. Am. J. Epidemiol. 154, 357-365
2. Klemba, M., and Goldberg, D. E. (2002) Biological roles of proteases in parasitic protozoa. Annu. Rev. Biochem. 71, 275-305
3. Shaw, M. K., Roos, D. S., and Tilney, L. G. (2002) Cysteine and serine protease inhibitors block intracellular development and disrupt the secretory pathway of Toxoplasma gondii. Microbes Infect. 4, 119-132
4. Conseil, V., Soete, M., and Dubremetz, J. F. (1999) Serine protease inhibitors block invasion of host cells by Toxoplasma gondii. Antimicrob. Agents Chemother. 43, 1358-1361
5. Sinai, A. P., and Joiner, K. A. (1997) Safe haven: the cell biology of nonfusogenic pathogen vacuoles. Annu. Rev. Microbiol. 51, 415-462
6. Carruthers, V. B. (1999) Armed and dangerous: Toxoplasma gondii uses an arsenal of secretory proteins to infect host cells. Parasitol. Int. 48, 1-10
7. Carruthers, V. B., and Sibley, L. D. (1997) Sequential protein secretion from three distinct organelles of Toxoplasma gondii accompanies invasion of human fibroblasts. Eur. J. Cell Biol. 73, 114-123
8. Soldati, D., Dubremetz, J. F., and Lebrun, M. (2001) Microneme proteins: structural and functional requirements to promote adhesion and invasion by the apicomplexan parasite Toxoplasma gondii. Int. J. Parasitol. 31, 1293-1302
9. Wan, K. L., Carruthers, V. B., Sibley, L. D., and Ajioka, J. W. (1997) Molecular characterization of an expressed sequence tag locus of Toxoplasma gondii encoding the micronemal protein MIC2. Mol. Biochem. Parasitol. 84, 203-214
10. Jewett, T. J., and Sibley, L. D. (2003) Aldolase forms a bridge between cell surface adhesins and the actin cytoskeleton in apicomplexan parasites. Mol. Cell 11, 885-894
11. Rabenau, K. E., Sohrabi, A., Tripathy, A., Reitter, C., Ajioka, J. W., Tomley, F. M., and Carruthers, V. B. (2001) TgM2AP participates in Toxoplasma gondii invasion of host cells and is tightly associated with the adhesive protein TgMIC2. Mol, Microbiol. 41, 537-547
12. Morisaki, J. H., Heuser, J. E., and Sibley, L. D. (1995) Invasion of Toxoplasma gondii occurs by active penetration of the host cell. J. Cell Sci. 108,2457-2464
13. Meissner, M., Schluter, D., and Soldati, D. (2002) Role of Toxoplasma gondii myosin A in powering parasite gliding and host cell invasion. Science 298, 837-840
14. Carruthers, V. B., Giddings, O. K., and Sibley, L. D. (1999) Secretion of micronemal proteins is associated with Toxoplasma invasion of host cells. Cell. Microbiol. 1, 225-235
15. Carruthers, V. B., Sherman, G. D., and Sibley, L. D. (2000) The Toxoplasma adhesive protein MIC2 is proteolytically processed at multiple sites by two parasite-derived proteases. J. Biol. Chem. 275, 14346-14353
16. Brossier, F., Jewett, T. J., Lovett, J. L., and Sibley, L. D. (2003) C-terminal processing of the toxoplasma protein MIC2 is essential for invasion into host cells. J. Biol. Chem. 278, 6229-6234
17. Huynh, M. H., Rabenau, K. E., Harper, J. M., Beatty, W. L., Sibley, L. D., and Carruthers, V. B. (2003) Rapid invasion of host cells by Toxoplasma requires secretion of the MIC2-M2AP adhesive protein complex. EMBO J. 22, 2082-2090
18. Donahue, C. G., Carruthers, V. B., Gilk, S. D., and Ward, G. E. (2000) The Toxoplasma homolog of Plasmodium apical membrane antigen-1 (AMA-1) is a microneme protein secreted in response to elevated intracellular calcium levels. Mol. Biochem. Parasitol. 111, 15-30
19. Cerede, O., Dubremetz, J. F., Bout, D., and Lebrun, M. (2002) The Toxoplasma gondii protein MIC3 requires pro-peptide cleavage and dimerization to function as adhesin. EMBO J. 21, 2526-2536
20. Opitz, C., Di Cristina, M., Reiss, M., Ruppert, T., Crisanti, A., and Soldati, D. (2002) Intramembrane cleavage of microneme proteins at the surface of the apicomplexan parasite Toxoplasma gondii. EMBO J. 21, 1577-1585
21. Neuhoff, V., Arold, N., Taube, D., and Ehrhardt, W. (1988) Improved staining of proteins in polyacrylamide gels including isoelectric focusing gels with clear background at nanogram sensitivity using Coomassie Brilliant Blue G-250 and R-250. Electrophoresis 9, 255-262
22. Tonge, R., Shaw, J., Middleton, B., Rowlinson, R., Rayner, S., Young, J., Pognan, F., Hawkins, E., Currie, I., and Davison, M. (2001) Validation and development of fluorescence two-dimensional differential gel electrophoresis proteomics technology. Proteomics 1, 377-396
23. Cohen, S. L., and Chait, B. T. (1997) Mass spectrometry of whole proteins eluted from sodium dodecyl sulfate-polyacrylamide gel electrophoresis gels. Anal. Biochem. 247, 257-267
24. Shevchenko, A., Wilm, M., Vorm, O., and Mann, M. (1996) Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal. Chem. 68, 850-858
25. Onnerfjord, P., Ekstrom, S., Bergquist, J., Nilsson, J., Laurell, T., and Marko-Varga, G. (1999) Homogeneous sample preparation for automated high throughput analysis with matrix-assisted laser desorption/ionisation time-of-flight mass spectrometry. Rapid Commun. Mass Spectrom. 13, 315-322
26. Howell, S. A., Well, I., Fleck, S. L., Kettleborough, C., Collins, C. R., and Blackman, M. J. (2003) A single malaria merozoite serine protease mediates shedding of multiple surface proteins by juxtamembrane cleavage. J. Biol. Chem. 278, 23890-23898
27. Wright, H. T. (1991) Nonenzymatic deamidation of asparaginyl and glutaminyl residues in proteins. Crit. Rev. Biochem. Mol. Biol. 26, 1-52
28. Schey, K. L., Little, M., Fowler, J. G., and Crouch, R. K. (2000) Characterization of human lens major intrinsic protein structure. Invest. Ophthalmol. Vis. Sci. 41, 175-182
29. Brecht, S., Carruthers, V. B., Ferguson, D. J., Giddings, O. K., Wang, G., Jaekle, U., Harper, J. M., Sibley, L. D., and Soldati, D. (2001) The Toxoplasma micronemal protein MIC4 is an adhesin composed of six conserved apple domains. J. Biol. Chem. 276, 4119-4127
30. 18O into peptide fragments and its application for protein sequencing by electrospray and matrix-assisted laser desorption/ionization mass spectrometry. Electrophoresis 17, 945-953
31. Biemann, K., and Scoble, H. A. (1987) Characterization by tandem mass spectrometry of structural modifications in proteins. Science 237, 992-998
32. Golde, T. E., and Eckman, C. B. (2003) Physiologic and pathologic events mediated by intrannembranous and juxtamembranous proteolysis. Sci. STKE 2003, RE4
33. Brown, M. S., Ye, J., Rawson, R. B., and Goldstein, J. L. (2000) Regulated intramembrane proteolysis: A control mechanism conserved from bacteria to humans. Cell 100, 391-398
34. Urban, S., and Freeman, M. (2003) Substrate specificity of rhomboid intramembrane proteases is governed by helix-breaking residues in the substrate transmembrane domain. Mol. Cell 11, 1425-1434
35. Brown, M. S., and Goldstein, J. L. (1999) A proteotytic pathway that controls the cholesterol content of membranes, cells, and blood. Proc. Natl. Acad. Sci. U. S. A. 96, 11041-11048
36. De Strooper, B., Annaert, W., Cupers, P., Saftig, P., Craessaerts, K., Mumm, J. S., Schroeter, E. H., Schrijvers, V., Wolfe, M. S., Ray, W. J., Goate, A., and Kopan, R. (1999) A presenilin-1-dependent γ-secretase-like protease mediates release of Notch intracellular domain. Nature 398, 518-522
37. Urban, S., Lee, J. R., and Freeman, M. (2002) A family of Rhomboid intramembrane proteases activates all Drosophila membrane-tethered EGF ligands. EMBO J. 21, 4277-4286
38. Weihofen, A., Binns, K., Lemberg, M. K., Ashman, K., and Martoglio, B. (2002) Identification of signal peptide peptidase, a presenilin-type aspartic protease. Science 296, 2215-2218
39. Selkoe, D. J. (1996) Amyloid beta-protein and the genetics of Alzheimer's disease. J. Biol. Chem. 271, 18295-18298
40. Suss-Toby, E., Zimmerberg, J., and Ward, G. E. (1996) Toxoplasma invasion: The parasitophorous vacuole is formed from host cell plasma membrane and pinches off via a fission pore. Proc. Natl. Acad. Sci. U S. A. 93, 8413-8418
41. Blackman, M. J. (2000) Proteases involved in erythrocyte invasion by the malaria parasite: Function and potential as chemotherapeutic targets. Curr. Drug Targets 1, 59-83
42. Uthaipibull, C., Aufiero, B., Syed, S. E., Hansen, B., Guevara Patino, J. A., Angov, E., Ling, I. T., Fegeding, K., Morgan, W. D., Ockenhouse, C., Birdsall, B., Feeney, J., Lyon, J. A., and Holder, A.A. (2001) Inhibitory and blocking monoclonal antibody epitopes on merozoite surface protein 1 of the malaria parasite Plasmodium falciparum. J. Mol. Biol. 307, 1381-1394