Proteases as regulators of pathogenesis: Examples from the Apicomplexa

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1824, Issue 1, 2012, Pages 177-185

  Li, Hao ^a   Child, Matthew A ^a   Bogyo, Matthew ^a  

^a STANFORD UNIVERSITY   (United States)

Author keywords

Apicomplexans; Malaria; Pathogenesis; Plasmodium; Proteases; Toxoplasma

Indexed keywords

ANTIMALARIAL AGENT; ARTEMISIN DERIVATIVE; CALPAIN; CYSTEINE PROTEINASE; HEMOGLOBIN; METALLOPROTEINASE; PARASITE ANTIGEN; PROTEINASE; PROTEINASE INHIBITOR; SERINE PROTEINASE; SERINE REPEAT ANTIGEN; UNCLASSIFIED DRUG;

ANTIMALARIAL ACTIVITY; APICOMPLEXA; APICOMPLEXAN INFECTION; CATABOLISM; DRUG TARGETING; ENZYME ACTIVITY; HOST CELL; HOST PARASITE INTERACTION; HUMAN; MALARIA; NONHUMAN; PARASITE; PATHOGENESIS; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROTEIN DEGRADATION; REVIEW; TOXOPLASMA GONDII; TOXOPLASMOSIS;

ANIMALS; APICOMPLEXA; DISEASE; DRUG DESIGN; HOST-PARASITE INTERACTIONS; HUMANS; IMMUNITY; MODELS, BIOLOGICAL; PEPTIDE HYDROLASES; PROTOZOAN INFECTIONS;

APICOMPLEXA; PLASMODIUM (APICOMPLEXA); PLASMODIUM FALCIPARUM; TOXOPLASMA; TOXOPLASMA GONDII;

EID: 82755161049     PISSN: 15709639     EISSN: 18781454     Source Type: Journal    
DOI: 10.1016/j.bbapap.2011.06.002     Document Type: Review

References (142)

1. G.M. Cohen Caspases: the executioners of apoptosis Biochem. J. 326 1997 1 16 (Pubitemid 27386911)
2. S.J. Li, and M. Hochstrasser A new protease required for cell-cycle progression in yeast Nature 398 1999 246 251
3. A. Huttenlocher, S.P. Palecek, Q. Lu, W.L. Zhang, R.L. Mellgren, D.A. Lauffenburger, M.H. Ginsberg, and A.F. Horwitz Regulation of cell migration by the calcium-dependent protease calpain J. Biol. Chem. 272 1997 32719 32722 (Pubitemid 28023599)
4. M. Klemba, and D.E. Goldberg Biological roles of proteases in parasitic protozoa Annu. Rev. Biochem. 71 2002 275 305 (Pubitemid 34800222)
5. K. Kim Role of proteases in host cell invasion by Toxoplasma gondii and other apicomplexa Acta Trop. 91 2004 69 81 (Pubitemid 38670386)
6. M.J. Blackman Proteases in host cell invasion by the malaria parasite Cell. Microbiol. 6 2004 893 903 (Pubitemid 39255603)
7. A.F. Cowman, and B.S. Crabb Invasion of red blood cells by malaria parasites Cell 124 2006 755 766 (Pubitemid 43261450)
8. M.J. Blackman, and L.H. Bannister Apical organelles of apicomplexa: biology and isolation by subcellular fractionation Mol. Biochem. Parasitol. 117 2001 11 25 (Pubitemid 32823479)
9. R.F. Walter, and G.I. McFadden The apicoplast: a review of the derived plastid of apicomplexan parasites Curr. Issues Mol. Biol. 7 2005 57 79
10. R.W. Snow, C.A. Guerra, A.M. Noor, H.Y. Myint, and S.I. Hay The global distribution of clinical episodes of Plasmodium falciparum malaria Nature 434 2005 214 217 (Pubitemid 40388051)
11. A.M. Tenter, A.R. Heckeroth, and L.M. Weiss Toxoplasma gondii: from animals to humans Int. J. Parasitol. 30 2000 1217 1258
12. J.G. Montoya, and O. Liesenfeld Toxoplasmosis Lancet 363 2004 1965 1976 (Pubitemid 38759657)
13. M.W. Black, and J.C. Boothroyd Lytic cycle of Toxoplasma gondii Microbiol. Mol. Biol. Rev. 64 2000 607 -+
14. B. Striepen, C.N. Jordan, S. Reiff, and G.G. van Dooren Building the perfect parasite: cell division in apicomplexa PLoS Pathog. 3 2007 691 698
15. J.H. McKerrow, C. Caffrey, B. Kelly, P. Loke, and M. Sajid Proteases in parasitic diseases Ann. Rev. Pathol. -Mech. Disease 1 2006 497 536
16. J.E. Smith A ubiquitous intracellular parasite - the cellular biology of toxoplasma-gondii Int. J. Parasitol. 25 1995 1301 1309
17. D. Soldati, B.J. Foth, and A.F. Cowman Molecular and functional aspects of parasite invasion Trends Parasitol. 20 2004 567 574 (Pubitemid 39446747)
18. D. Soldati, J.F. Dubremetz, and M. Lebrun Microneme proteins: structural and functional requirements to promote adhesion and invasion by the apicomplexan parasite Toxoplasma gondii Int. J. Parasitol. 31 2001 1293 1302 (Pubitemid 32868709)
19. M.H. Huynh, J.M. Harper, and V.B. Carruthers Preparing for an invasion: charting the pathway of adhesion proteins to Toxoplasma micronemes Parasitol. Res. 98 2006 389 395
20. C. Withers-Martinez, L. Jean, and M.J. Blackman Subtilisin-like proteases of the malaria parasite Mol. Microbiol. 53 2004 55 63
21. M. Sajid, C. Withers-Martinez, and M.J. Blackman Maturation and specificity of Plasmodium falciparum subtilisin-like protease-1, a malaria merozoite subtilisin-like serine protease J. Biol. Chem. 275 2000 631 641 (Pubitemid 30039028)
22. M.J. Blackman, H. Fujioka, W.H.L. Stafford, M. Sajid, B. Clough, S.L. Fleck, M. Aikawa, M. Grainger, and F. Hackett A subtilisin-like protein in secretory organelles of Plasmodium falciparum merozoites J. Biol. Chem. 273 1998 23398 23409 (Pubitemid 28417529)
23. S. Yeoh, R.A. O'Donnell, K. Koussis, A.R. Dluzewski, K.H. Ansell, S.A. Osborne, F. Hackett, C. Withers-Martinez, G.H. Mitchell, L.H. Bannister, J.S. Bryans, C.A. Kettleborough, and M.J. Blackman Subcellular discharge of a serine protease mediates release of invasive malaria parasites from host erythrocytes Cell 131 2007 1072 1083 (Pubitemid 350235024)
24. K. Koussis, C. Withers-Martinez, S. Yeoh, M. Child, F. Hackett, E. Knuepfer, L. Juliano, U. Woehlbier, H. Bujard, and M.J. Blackman A multifunctional serine protease primes the malaria parasite for red blood cell invasion EMBO J. 28 2009 725 735
25. N.C. Silmon de Monerri, H.R. Flynn, M.G. Campos, F. Hackett, K. Koussis, C. Withers-Martinez, J.M. Skehel, and M.J. Blackman Global identification of multiple substrates for Plasmodium falciparum SUB1, an essential malarial processing protease Infect. Immun. 79 2011 1086 1097
26. P.K. Harris, S. Yeoh, A.R. Dluzewski, R.A. O'Donnell, C. Withers-Martinez, F. Hackett, L.H. Bannister, G.H. Mitchell, and M.J. Blackman Molecular identification of a malaria merozoite surface sheddase PLoS Pathog. 1 2005 241 251
27. J.L. Green, L. Hinds, M. Grainger, E. Knueffer, and A.A. Holder Plasmodium thrombospondin related apical merozoite protein (PTRAMP) is shed from the surface of merozoites by PfSUB2 upon invasion of erythrocytes Mol. Biochem. Parasitol. 150 2006 114 117 (Pubitemid 44332577)
28. S.A. Miller, E.M. Binder, M.J. Blackman, V.B. Carruthers, and K. Kim A conserved subtilisin-like protein TgSUB1 in microneme organelles of Toxoplasma gondii J. Biol. Chem. 276 2001 45341 45348
29. E.M. Binder, V. Lagal, and K. Kim The prodomain of Toxoplasma gondii GPI-anchored subtilase TgSUB1 mediates its targeting to micronemes Traffic 9 2008 1485 1496
30. V. Lagal, E.M. Binder, M.H. Huynh, B.F. Kafsack, P.K. Harris, R. Diez, D. Chen, R.N. Cole, V.B. Carruthers, and K. Kim Toxoplasma gondii protease TgSUB1 is required for cell surface processing of micronemal adhesive complexes and efficient adhesion of tachyzoites Cell. Microbiol. 12 2010 1792 1808
31. S.A. Miller, V. Thathy, J.W. Ajioka, M.J. Blackman, and K. Kim TgSUB2 is a Toxoplasma gondii rhoptry organelle processing proteinase Mol. Microbiol. 49 2003 883 894 (Pubitemid 36981336)
32. S. Urban, J.R. Lee, and M. Freeman Drosophila Rhomboid-1 defines a family of putative intramembrane serine proteases Cell 107 2001 173 182 (Pubitemid 33035944)
33. S. Urban, and M. Freeman Intramembrane proteolysis controls diverse signalling pathways throughout evolution Curr. Opin. Genet. Dev. 12 2002 512 518 (Pubitemid 35013532)
34. S. Urban, D. Schlieper, and M. Freeman Conservation of intramembrane proteolytic activity and substrate specificity in prokaryotic and eukaryotic rhomboids Curr. Biol. 12 2002 1507 1512 (Pubitemid 35036649)
35. M. Freeman Rhomboid proteases and their biological functions Annu. Rev. Genet. 42 2008 191 210
36. X.W. Zhou, M.J. Blackman, S.A. Howell, and V.B. Carruthers Proteomic analysis of cleavage events reveals a dynamic two-step mechanism for proteolysis of a key parasite adhesive complex Mol. Cell. Proteomics 3 2004 565 576 (Pubitemid 38878516)
37. T.J. Dowse, J.C. Pascall, K.D. Brown, and D. Soldati Apicomplexan rhomboids have a potential role in microneme protein cleavage during host cell invasion Int. J. Parasitol. 35 2005 747 756 (Pubitemid 40733613)
38. F. Brossier, T.J. Jewett, L.D. Sibley, and S. Urban A spatially localized rhomboid protease cleaves cell surface adhesins essential for invasion by Toxoplasma Proc. Natl. Acad. Sci. U.S.A. 102 2005 4146 4151 (Pubitemid 40388570)
39. J.S. Buguliskis, F. Brossier, J. Shuman, and L.D. Sibley Rhomboid 4 (ROM4) affects the processing of surface adhesins and facilitates host cell invasion by Toxoplasma gondii PLoS Pathog. 6 2010
40. J.M. Santos, D.J.P. Ferguson, M.J. Blackman, and D. Soldati-Favre Intramembrane cleavage of AMA1 triggers toxoplasma to switch from an invasive to a replicative mode Science 331 2011 473 477
41. F. Brossier, G.L. Starnes, W.L. Beatty, and L.D. Sibley Microneme rhomboid protease TgROM1 is required for efficient intracellular growth of Toxoplasma gondii Eukaryot. Cell 7 2008 664 674 (Pubitemid 351959901)
42. R.P. Baker, R. Wijetilaka, and S. Urban Two Plasmodium rhomboid proteases preferentially cleave different adhesins implicated in all invasive stages of malaria PLoS Pathog. 2 2006 922 932
43. R.A. O'Donnell, F. Hackett, S.A. Howell, M. Treeck, N. Struck, Z. Krnajski, C. Withers-Martinez, T.W. Gilberger, and M.J. Blackman Intramembrane proteolysis mediates shedding of a key adhesin during erythrocyte invasion by the malaria parasite J. Cell Biol. 174 2006 1023 1033
44. P. Srinivasan, I. Coppens, and M. Jacobs-Lorena Distinct roles of Plasmodium Rhomboid 1 in parasite development and malaria pathogenesis PLoS Pathog. 5 2009
45. D.C. Greenbaum, A. Baruch, M. Grainger, Z. Bozdech, K.F. Medzihradszky, J. Engel, J. DeRisi, A.A. Holder, and M. Bogyo A role for the protease falcipain 1 in host cell invasion by the human malaria parasite Science 298 2002 2002 2006 (Pubitemid 35425258)
46. P.S. Sijwali, K. Kato, K.B. Seydel, J. Gut, J. Lehman, M. Klemba, D.E. Goldberg, L.H. Miller, and P.J. Rosenthal Plasmodium falciparum cysteine protease falcipain-1 is not essential in erythrocytic stage malaria parasites Proc. Natl. Acad. Sci. U.S.A. 101 2004 8721 8726 (Pubitemid 38745838)
47. S. Eksi, B. Czesny, D.C. Greenbaum, M. Bogyo, and K.C. Williamson Targeted disruption of Plasmodium falciparum cysteine protease, falcipain 1, reduces oocyst production, not erythrocytic stage growth Mol. Microbiol. 53 2004 243 250 (Pubitemid 38901394)
48. X.C. Que, H.A. Ngo, J. Lawton, M. Gray, Q. Liu, J. Engel, L. Brinen, P. Ghosh, K.A. Joiner, and S.L. Reed The cathepsin B of Toxoplasma gondii, toxopain-1, is critical for parasite invasion and rhoptry protein processing J. Biol. Chem. 277 2002 25791 25797 (Pubitemid 34951900)
49. X.C. Que, A. Wunderlich, K.A. Joiner, and S.L. Reed Toxopain-1 is critical for infection in a novel chicken embryo model of congenital toxoplasmosis Infect. Immun. 72 2004 2915 2921 (Pubitemid 38542422)
50. F. Parussini, I. Coppens, P.P. Shah, S.L. Diamond, and V.B. Carruthers Cathepsin L occupies a vacuolar compartment and is a protein maturase within the endo/exocytic system of Toxoplasma gondii Mol. Microbiol. 76 2010 1340 1357
51. J. Laliberte, and V.B. Carruthers Toxoplasma gondii toxolysin 4 is an extensively processed putative metalloproteinase secreted from micronemes Mol. Biochem. Parasitol. 177 2011 49 56
52. S.H. Kappe, A.M. Vaughan, J.A. Boddey, and A.F. Cowman That was then but this is now: malaria research in the time of an eradication agenda Science 328 2010 862 866
53. D.E. Goldberg Hemoglobin degradation, in: Malaria: Drugs Disease Post-Genom. Biol. 295 2005 275 291
54. S.E. Francis, D.J. Sullivan, and D.E. Goldberg Hemoglobin metabolism in the malaria parasite Plasmodium falciparum Annu. Rev. Microbiol. 51 1997 97 123 (Pubitemid 27433044)
55. G.H. Coombs, D.E. Goldberg, M. Klemba, C. Berry, J. Kay, and J.C. Mottram Aspartic proteases of Plasmodium falciparum and other parasitic protozoa as drug targets Trends Parasitol. 17 2001 532 537 (Pubitemid 34185360)
56. S.E. Francis, R. Banerjee, and D.E. Goldberg Biosynthesis and maturation of the malaria aspartic hemoglobinases plasmepsins I and II J. Biol. Chem. 272 1997 14961 14968 (Pubitemid 27251770)
57. J. Liu, I.Y. Gluzman, M.E. Drew, and D.E. Goldberg The role of Plasmodium falciparum food vacuole plasmepsins J. Biol. Chem. 280 2005 1432 1437
58. K.E. Luker, S.E. Francis, I.Y. Gluzman, and D.E. Goldberg Kinetic analysis of plasmepsins I and II, aspartic proteases of the Plasmodium falciparum digestive vacuole Mol. Biochem. Parasitol. 79 1996 71 78 (Pubitemid 26241906)
59. A.M. Silva, A.Y. Lee, S.V. Gulnik, P. Majer, J. Collins, T.N. Bhat, P.J. Collins, R.E. Cachau, K.E. Luker, I.Y. Gluzman, S.E. Francis, A. Oksman, D.E. Goldberg, and J.W. Erickson Structure and inhibition of plasmepsin II, a hemoglobin-degrading enzyme from Plasmodium falciparum Proc. Natl. Acad. Sci. U.S.A. 93 1996 10034 10039 (Pubitemid 26314569)
60. R. Banerjee, J. Liu, W. Beatty, L. Pelosof, M. Klemba, and D.E. Goldberg Four plasmepsins are active in the Plasmodium falciparum food vacuole, including a protease with an active-site histidine Proc. Natl. Acad. Sci. U.S.A. 99 2002 990 995 (Pubitemid 34106623)
61. J.B. Dame, C.A. Yowell, L. Omara-Opyene, J.M. Carlton, R.A. Cooper, and T. Li Plasmepsin 4, the food vacuole aspartic proteinase found in all Plasmodium spp. infecting man Mol. Biochem. Parasitol. 130 2003 1 12 (Pubitemid 37205156)
62. J. Liu, E.S. Istvan, I.Y. Gluzman, J. Gross, and D.E. Goldberg Plasmodium falciparum ensures its amino acid supply with multiple acquisition pathways and redundant proteolytic enzyme systems Proc. Natl. Acad. Sci. U.S.A. 103 2006 8840 8845 (Pubitemid 43878106)
63. J.A. Bonilla, P.A. Moura, T.D. Bonilla, C.A. Yowell, D.A. Fidock, and J.B. Dame Effects on growth, hemoglobin metabolism and paralogous gene expression resulting from disruption of genes encoding the digestive vacuole plasmepsins of Plasmodium falciparum Int. J. Parasitol. 37 2007 317 327 (Pubitemid 46215589)
64. K.K. Eggleson, K.L. Duffin, and D.E. Goldberg Identification and characterization of falcilysin, a metallopeptidase involved in hemoglobin catabolism within the malaria parasite Plasmodium falciparum J. Biol. Chem. 274 1999 32411 32417
65. C.E. Murata, and D.E. Goldberg Plasmodium falciparum falcilysin: an unprocessed food vacuole enzyme Mol. Biochem. Parasitol. 129 2003 123 126 (Pubitemid 36703229)
66. S.A. Ralph Subcellular multitasking - multiple destinations and roles for the Plasmodium falcilysin protease Mol. Microbiol. 63 2007 309 313 (Pubitemid 46058921)
67. F. Salas, J. Fichmann, G.K. Lee, M.D. Scott, and P.J. Rosenthal Functional expression of falcipain, A plasmodium-falciparum cysteine proteinase, supports its role as a malarial hemoglobinase Infect. Immun. 63 1995 2120 2125
68. P.S. Sijwali, B.R. Shenai, J. Gut, A. Singh, and P.J. Rosenthal Expression and characterization of the Plasmodium falciparum haemoglobinase falcipain-3 Biochem. J. 360 2001 481 489 (Pubitemid 33151343)
69. Y.A. Sabnis, P.V. Desai, P.J. Rosenthal, and M.A. Avery Probing the structure of falcipain-3, a cysteine protease from Plasmodium falciparum: comparative protein modeling and docking studies Protein Sci. 12 2003 501 509 (Pubitemid 36241108)
70. N. Singh, P.S. Sijwali, K.C. Pandey, and P.J. Rosenthal Plasmodium falciparum: biochemical characterization of the cysteine protease falcipain-2′ Exp. Parasitol. 112 2006 187 192 (Pubitemid 43247780)
71. M. Klemba, I. Gluzman, and D.E. Goldberg A Plasmodium falciparum dipeptidyl aminopeptidase I participates in vacuolar hemoglobin degradation J. Biol. Chem. 279 2004 43000 43007 (Pubitemid 39372193)
72. M.E. Drew, R. Banerjee, E.W. Uffman, S. Gilbertson, P.J. Rosenthal, and D.E. Goldberg Plasmodium food vacuole plasmepsins are activated by falcipains J. Biol. Chem. 283 2008 12870 12876
73. P.J. Rosenthal, J.E. Olson, G.K. Lee, J.T. Palmer, J.L. Klaus, and D. Rasnick Antimalarial effects of vinyl sulfone cysteine proteinase inhibitors Antimicrob. Agents Chemother. 40 1996 1600 1603 (Pubitemid 26227342)
74. B.R. Shenai, P.S. Sijwali, A. Singh, and P.J. Rosenthal Characterization of native and recombinant falcipain-2, a principal trophozoite cysteine protease and essential hemoglobinase of Plasmodium falciparum J. Biol. Chem. 275 2000 29000 29010
75. P.S. Sijwali, and P.J. Rosenthal Gene disruption confirms a critical role for the cysteine protease falcipain-2 in hemoglobin hydrolysis by Plasmodium falciparum Proc. Natl. Acad. Sci. U.S.A. 101 2004 4384 4389 (Pubitemid 38437421)
76. I.D. Kerr, J.H. Lee, C.J. Farady, R. Marion, M. Rickert, M. Sajid, K.C. Pandey, C.R. Caffrey, J. Legac, E. Hansell, J.H. McKerrow, C.S. Craik, P.J. Rosenthal, and L.S. Brinen Vinyl sulfones as antiparasitic agents and a structural basis for drug design J. Biol. Chem. 284 2009 25697 25703
77. F. Wang, P. Krai, E. Deu, B. Bibb, C. Lauritzen, J. Pedersen, M. Bogyo, and M. Klemba Biochemical characterization of Plasmodium falciparum dipeptidyl aminopeptidase 1 Mol. Biochem. Parasitol. 175 2011 10 20
78. E. Deu, M.J. Leyva, V.E. Albrow, M.J. Rice, J.A. Ellman, and M. Bogyo Functional studies of Plasmodium falciparum dipeptidyl aminopeptidase I using small molecule inhibitors and active site probes Chem. Biol. 17 2010 808 819
79. S.S. Mahajan, E. Deu, E.M. Lauterwasser, M.J. Leyva, J.A. Ellman, M. Bogyo, and A.R. Renslo A fragmenting hybrid approach for targeted delivery of multiple therapeutic agents to the malaria parasite ChemMedChem 6 2011 415 419
80. S. Dalal, and M. Klemba Roles for two aminopeptidases in vacuolar hemoglobin catabolism in Plasmodium falciparum J. Biol. Chem. 282 2007 35978 35987 (Pubitemid 350277126)
81. C.S. Gavigan, J.P. Dalton, and A. Bell The role of aminopeptidases in haemoglobin degradation in Plasmodium falciparum-infected erythrocytes Mol. Biochem. Parasitol. 117 2001 37 48 (Pubitemid 32823481)
82. C.M. Stack, J. Lowther, E. Cunningham, S. Donnelly, D.L. Gardiner, K.R. Trenholme, T.S. Skinner-Adams, F. Teuscher, J. Grembecka, A. Mucha, P. Kafarski, L. Lua, A. Bell, and J.P. Dalton Characterization of the Plasmodium falciparum M17 leucyl aminopeptidase - a protease involved in amino acid regulation with potential for antimalarial drug development J. Biol. Chem. 282 2007 2069 2080 (Pubitemid 47076702)
83. T.S. Skinner-Adams, C.M. Stack, K.R. Trenholme, C.L. Brown, J. Grembecka, J. Lowther, A. Mucha, M. Drag, P. Kafarski, S. McGowan, J.C. Whisstock, D.L. Gardiner, and J.P. Dalton Plasmodium falciparum neutral aminopeptidases: new targets for anti-malarials Trends Biochem. Sci. 35 2010 53 61
84. M. Allary, J. Schrevel, and I. Florent Properties, stage-dependent expression and localization of Plasmodium falciprum M1 family zinc-aminopeptidase Parasitology 125 2002 1 10 (Pubitemid 34785744)
85. S. McGowan, C.J. Porter, J. Lowther, C.M. Stack, S.J. Golding, T.S. Skinner-Adams, K.R. Trenholme, F. Teuscher, S.M. Donnelly, J. Grembecka, A. Mucha, P. Kafarski, R. DeGori, A.M. Buckle, D.L. Gardiner, J.C. Whisstock, and J.P. Dalton Structural basis for the inhibition of the essential Plasmodium falciparum M1 neutral aminopeptidase Proc. Natl. Acad. Sci. U.S.A. 106 2009 2537 2542
86. O. Azimzadeh, C. Sow, M. Geze, J. Nyalwidhe, and I. Florent Plasmodium falciparum PfA-M1 aminopeptidase is trafficked via the parasitophorous vacuole and marginally delivered to the food vacuole Malar. J. 9 2010
87. S. McGowan, C.A. Oellig, W.A. Birru, T.T. Caradoc-Davies, C.M. Stack, J. Lowther, T. Skinner-Adams, A. Mucha, P. Kafarski, J. Grembecka, K.R. Trenholme, A.M. Buckle, D.L. Gardiner, J.P. Dalton, and J.C. Whisstock Structure of the Plasmodium falciparum M17 aminopeptidase and significance for the design of drugs targeting the neutral exopeptidases Proc. Natl. Acad. Sci. U.S.A. 107 2010 2449 2454
88. O. Coux, K. Tanaka, and A.L. Goldberg Structure and functions of the 20S and 26S proteasomes Annu. Rev. Biochem. 65 1996 801 847 (Pubitemid 26255262)
89. L. Borissenko, and M. Groll 20S proteasome and its inhibitors: crystallographic knowledge for drug development Chem. Rev. 107 2007 687 717 (Pubitemid 46502369)
90. P.G. Richardson, C. Mitsiades, T. Hideshima, and K.C. Anderson Bortezomib: proteasome inhibition as an effective anticancer therapy Annu. Rev. Med. 57 2006 33 47 (Pubitemid 43261977)
91. S.M. Gantt, J.M. Myung, M.R.S. Briones, W.D. Li, E.J. Corey, S. Omura, V. Nussenzweig, and P. Sinnis Proteasome inhibitors block development of Plasmodium spp Antimicrob. Agents Chemother. 42 1998 2731 2738 (Pubitemid 28462924)
92. C. Lindenthal, N. Weich, Y.S. Chia, V. Heussler, and M.Q. Klinkert The proteasome inhibitor MLN-273 blocks exoerythrocytic and erythrocytic development of Plasmodium parasites Parasitology 131 2005 37 44 (Pubitemid 41008807)
93. T. Hatabu, M. Hagiwara, N. Taguchi, M. Kiyozawa, M. Suzuki, S. Kano, and K. Sato Plasmodium falciparum: the fungal metabolite gliotoxin inhibits proteasome proteolytic activity and exerts a plasmodicidal effect on Plasmodium falciparum Exp. Parasitol. 112 2006 179 183 (Pubitemid 43247778)
94. A. Kreidenweiss, P.G. Kremsner, and B. Mordmuller Comprehensive study of proteasome inhibitors against Plasmodium falciparum laboratory strains and field isolates from Gabon Malar. J. 7 2008
95. B. Czesny, S. Goshu, J.L. Cook, and K.C. Williamson The proteasome inhibitor epoxomicin has potent Plasmodium falciparum gametocytocidal activity Antimicrob. Agents Chemother. 53 2009 4080 4085
96. M.N. Aminake, S. Schoof, L. Sologub, M. Leubner, M. Kirschner, H.D. Arndt, and G. Pradel Thiostrepton derivatives exhibit antimalarial and gametocytocidal activity by dually targeting parasite proteasome and apicoplast Antimicrob. Agents Chemother. 2011
97. X.C. Que, J.C. Engel, D. Ferguson, A. Wunderlich, S. Tomavo, and S.L. Reed Cathepsin Cs are key for the intracellular survival of the protozoan parasite, Toxoplasma gondii J. Biol. Chem. 282 2007 4994 5003 (Pubitemid 47100936)
98. M. Klemba, and D.E. Goldberg Characterization of plasmepsin V, a membrane-bound aspartic protease homolog in the endoplasmic reticulum of Plasmodium falciparum Mol. Biochem. Parasitol. 143 2005 183 191 (Pubitemid 41206472)
99. J.A. Boddey, A.N. Hodder, S. Gunther, P.R. Gilson, H. Patsiouras, E.A. Kapp, J.A. Pearce, T.F. de Koning-Ward, R.J. Simpson, B.S. Crabb, and A.F. Cowman An aspartyl protease directs malaria effector proteins to the host cell Nature 463 2010 U627 U652
100. I. Russo, S. Babbitt, V. Muralidharan, T. Butler, A. Oksman, and D.E. Goldberg Plasmepsin V licenses Plasmodium proteins for export into the host erythrocyte Nature 463 2010 632 636
101. S. Haase, and T.F. de Koning-Ward New insights into protein export in malaria parasites Cell. Microbiol. 12 2010 580 587
102. D.E. Goldberg, and A.F. Cowman Moving in and renovating: exporting proteins from Plasmodium into host erythrocytes Nat. Rev. Microbiol. 8 2010 617 621
103. M.J. Blackman Malarial proteases and host cell egress: an 'emerging' cascade Cell. Microbiol. 10 2008 1925 1934
104. P.R. Gilson, and B.S. Crabb Morphology and kinetics of the three distinct phases of red blood cell invasion by Plasmodium falciparum merozoites Int. J. Parasitol. 39 2009 91 96
105. S. Glushakova, D. Yin, T. Li, and J. Zimmerberg Membrane transformation during malaria parasite release from human red blood cells Curr. Biol. 15 2005 1645 1650 (Pubitemid 41323742)
106. J.A. Lyon, and J.D. Haynes Plasmodium falciparum antigens synthesized by schizonts and stabilized at the merozoite surface when schizonts mature in the presence of protease inhibitors J. Immunol. 136 1986 2245 2251 (Pubitemid 16122314)
107. S. Arastu-Kapur, E.L. Ponder, U.P. Fonovic, S. Yeoh, F. Yuan, M. Fonovic, M. Grainger, C.I. Phillips, J.C. Powers, and M. Bogyo Identification of proteases that regulate erythrocyte rupture by the malaria parasite Plasmodium falciparum Nat. Chem. Biol. 4 2008 203 213 (Pubitemid 351264129)
108. M.D. Lavine, and G. Arrizabalaga Invasion and egress by the obligate intracellular parasite Toxoplasma gondii: potential targets for the development of new antiparasitic drugs Curr. Pharm. Des. 13 2007 641 651 (Pubitemid 46485266)
109. B.F. Kafsack, J.D. Pena, I. Coppens, S. Ravindran, J.C. Boothroyd, and V.B. Carruthers Rapid membrane disruption by a perforin-like protein facilitates parasite exit from host cells Science 323 2009 530 533
110. S. Aoki, J. Li, S. Itagaki, B.A. Okech, T.G. Egwang, H. Matsuoka, N.M. Palacpac, T. Mitamura, and T. Horii Serine repeat antigen (SERA5) is predominantly expressed among the SERA multigene family of Plasmodium falciparum, and the acquired antibody titers correlate with serum inhibition of the parasite growth J. Biol. Chem. 277 2002 47533 47540 (Pubitemid 36159272)
111. X.L. Pang, T. Mitamura, and T. Horii Antibodies reactive with the N-terminal domain of Plasmodium falciparum serine repeat antigen inhibit cell proliferation by agglutinating merozoites and schizonts Infect. Immun. 67 1999 1821 1827 (Pubitemid 29144402)
112. W.D. Fairlie, T.P. Spurck, J.E. McCoubrie, P.R. Gilson, S.K. Miller, G.I. McFadden, R. Malby, B.S. Crabb, and A.N. Hodder Inhibition of malaria parasite development by a cyclic peptide that targets the vital parasite protein SERA5 Infect. Immun. 76 2008 4332 4344
113. J.E. McCoubrie, S.K. Miller, T. Sargeant, R.T. Good, A.N. Hodder, T.P. Speed, T.F. de Koning-Ward, and B.S. Crabb Evidence for a common role for the serine-type Plasmodium falciparum serine repeat antigen proteases: implications for vaccine and drug design Infect. Immun. 75 2007 5565 5574 (Pubitemid 350207793)
114. A.N. Hodder, R.L. Malby, O.B. Clarke, W.D. Fairlie, P.M. Colman, B.S. Crabb, and B.J. Smith Structural insights into the protease-like antigen Plasmodium falciparum SERA5 and its noncanonical active-site serine J. Mol. Biol. 392 2009 154 165
115. A.N. Hodder, D.R. Drew, V.C. Epa, M. Delorenzi, R. Bourgon, S.K. Miller, R.L. Moritz, D.F. Frecklington, R.J. Simpson, T.P. Speed, R.N. Pike, and B.S. Crabb Enzymic, phylogenetic, and structural characterization of the unusual papain-like protease domain of Plasmodium falciparum SERA5 J. Biol. Chem. 278 2003 48169 48177 (Pubitemid 37523270)
116. A.S. Aly, and K. Matuschewski A malarial cysteine protease is necessary for Plasmodium sporozoite egress from oocysts J. Exp. Med. 202 2005 225 230 (Pubitemid 41043818)
117. J. Li, T. Mitamura, B.A. Fox, D.J. Bzik, and T. Horii Differential localization of processed fragments of Plasmodium falciparum serine repeat antigen and further processing of its N-terminal 47 kDa fragment Parasitol. Int. 51 2002 343 352 (Pubitemid 35287506)
118. R. Chandramohanadas, P.H. Davis, D.P. Beiting, M.B. Harbut, C. Darling, G. Velmourougane, M.Y. Lee, P.A. Greer, D.S. Roos, and D.C. Greenbaum Apicomplexan parasites co-opt host calpains to facilitate their escape from infected cells Science 324 2009 794 797
119. J.C. Powers, J.L. Asgian, O.D. Ekici, and K.E. James Irreversible inhibitors of serine, cysteine, and threonine proteases Chem. Rev. 102 2002 4639 4750
120. M.J. Gardner, N. Hall, E. Fung, O. White, M. Berriman, R.W. Hyman, J.M. Carlton, A. Pain, K.E. Nelson, S. Bowman, I.T. Paulsen, K. James, J.A. Eisen, K. Rutherford, S.L. Salzberg, A. Craig, S. Kyes, M.S. Chan, V. Nene, S.J. Shallom, B. Suh, J. Peterson, S. Angiuoli, M. Pertea, J. Allen, J. Selengut, D. Haft, M.W. Mather, A.B. Vaidya, D.M.A. Martin, A.H. Fairlamb, M.J. Fraunholz, D.S. Roos, S.A. Ralph, G.I. McFadden, L.M. Cummings, G.M. Subramanian, C. Mungall, J.C. Venter, D.J. Carucci, S.L. Hoffman, C. Newbold, R.W. Davis, C.M. Fraser, and B. Barrell Genome sequence of the human malaria parasite Plasmodium falciparum Nature 419 2002 498 511
121. J.C. Boothroyd Toxoplasma gondii: 25 years and 25 major advances for the field Int. J. Parasitol. 39 2009 935 946
122. A.M. Gopalakrishnan, and C. Lopez-Estrano Comparative analysis of stage specific gene regulation of apicomplexan parasites: Plasmodium falciparum and Toxoplasma gondii Infect. Disord. Drug Targets 10 2010 303 311
123. Z. Bozdech, M. Llinas, B.L. Pulliam, E.D. Wong, J. Zhu, and J.L. DeRisi The transcriptome of the intraerythrocytic developmental cycle of Plasmodium falciparum PLoS Biol. 1 2003 E5
124. G. Hu, A. Cabrera, M. Kono, S. Mok, B.K. Chaal, S. Haase, K. Engelberg, S. Cheemadan, T. Spielmann, P.R. Preiser, T.W. Gilberger, and Z. Bozdech Transcriptional profiling of growth perturbations of the human malaria parasite Plasmodium falciparum Nat. Biotechnol. 28 2010 91 98
125. M. Meissner, M.S. Breinich, P.R. Gilson, and B.S. Crabb Molecular genetics tools in Toxoplasma and Plasmodium: achievements and future needs Curr. Opin. Microbiol. 10 2007 349 356 (Pubitemid 47404957)
126. M.R. van Dijk, A.P. Waters, and C.J. Janse Stable transfection of malaria parasite blood stages Science 268 1995 1358 1362
127. Y. Wu, C.D. Sifri, H.H. Lei, X.Z. Su, and T.E. Wellems Transfection of Plasmodium falciparum within human red blood cells Proc. Natl. Acad. Sci. U.S.A. 92 1995 973 977
128. L. Aravind, L.M. Iyer, T.E. Wellems, and L.H. Miller Plasmodium biology: genomic gleanings Cell 115 2003 771 785 (Pubitemid 38058491)
129. M.J. Blackman RNAi in protozoan parasites: what hope for the apicomplexa? Protist 154 2003 177 180 (Pubitemid 37029264)
130. D.C. Greenbaum Is chemical genetics the new frontier for malaria biology? Trends Pharmacol. Sci. 29 2008 51 56
131. L.A. Banaszynski, L.C. Chen, L.A. Maynard-Smith, A.G. Ooi, and T.J. Wandless A rapid, reversible, and tunable method to regulate protein function in living cells using synthetic small molecules Cell 126 2006 995 1004 (Pubitemid 44310772)
132. C.M. Armstrong, and D.E. Goldberg An FKBP destabilization domain modulates protein levels in Plasmodium falciparum Nat. Methods 4 2007 1007 1009 (Pubitemid 350201770)
133. I. Russo, A. Oksman, B. Vaupel, and D.E. Goldberg A calpain unique to alveolates is essential in Plasmodium falciparum and its knockdown reveals an involvement in pre-S-phase development Proc. Natl. Acad. Sci. U.S.A. 106 2009 1554 1559
134. J.D. Dvorin, D.C. Martyn, S.D. Patel, J.S. Grimley, C.R. Collins, C.S. Hopp, A.T. Bright, S. Westenberger, E. Winzeler, M.J. Blackman, D.A. Baker, T.J. Wandless, and M.T. Duraisingh A plant-like kinase in Plasmodium falciparum regulates parasite egress from erythrocytes Science 328 2010 910 912
135. V. Muralidharan, A. Oksman, M. Iwamoto, T.J. Wandless, and D.E. Goldberg Asparagine repeat function in a Plasmodium falciparum protein assessed via a regulatable fluorescent affinity tag Proc. Natl. Acad. Sci. U.S.A. 108 2011 4411 4416
136. M. Meissner, E. Krejany, P.R. Gilson, T.F. de Koning-Ward, D. Soldati, and B.S. Crabb Tetracycline analogue-regulated transgene expression in Plasmodium falciparum blood stages using Toxoplasma gondii transactivators Proc. Natl. Acad. Sci. U.S.A. 102 2005 2980 2985 (Pubitemid 40299902)
137. A.M. Sadaghiani, S.H.L. Verhelst, and M. Bogyo Tagging and detection strategies for activity-based proteomics Curr. Opin. Chem. Biol. 11 2007 20 28 (Pubitemid 46216128)
138. E. Deu, Z. Yang, F. Wang, M. Klemba, and M. Bogyo Use of activity-based probes to develop high throughput screening assays that can be performed in complex cell extracts PLoS One 5 2010 e11985
139. P.W. Bowyer, G.M. Simon, B.F. Cravatt, and M. Bogyo Global profiling of proteolysis during rupture of P. falciparum from the host erythrocyte Mol. Cell. Proteomics 2010
140. S. Tschan, B. Mordmuller, and J.F. Kun Threonine peptidases as drug targets against malaria Expert Opin. Ther. Targets 2011
141. B. Mordmuller, R. Fendel, A. Kreidenweiss, C. Gille, R. Hurwitz, W.G. Metzger, J.F.J. Kun, T. Lamkemeyer, A. Nordheim, and P.G. Kremsner Plasmodia express two threonine-peptidase complexes during asexual development Mol. Biochem. Parasitol. 148 2006 79 85 (Pubitemid 43795866)
142. G. Ramasamy, D. Gupta, A. Mohmmed, and V.S. Chauhan Characterization and localization of Plasmodium falciparum homolog of prokaryotic C1pQ/Hs1V protease Mol. Biochem. Parasitol. 152 2007 139 148