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Roles of Proteases during Invasion and Egress by Plasmodium and Toxoplasma

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Part of the book series: Subcellular Biochemistry ((SCBI,volume 47))

Abstract

Apicomplexan pathogens replicate exclusively within the confines of a host cell. Entry into (invasion) and exit from (egress) these cells requires an array of specialized parasite molecules, many of which have long been considered to have potential as targets of drug or vaccine-based therapies. In this chapter the authors discuss the current state of knowledge regarding the role of parasite proteolytic enzymes in these critical steps in the life cycle of two clinically important apicomplexan genera, Plasmodium and Toxoplasma. At least three distinct proteases of the cysteine mechanistic class have been implicated in egress of the malaria parasite from cells of its vertebrate and insect host. In contrast, the bulk of the evidence indicates a prime role for serine proteases of the subtilisin and rhomboid families in invasion by both parasites. Whereas proteases involved in egress may function predominantly to degrade host cell structures, proteases involved in invasion probably act primarily as maturases and’ sheddases’, required to activate and ultimately remove ligands involved in interactions with the host cell.

These authors contributed equally to this work.

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References

  1. Alberts B. Molecular Biology of the Cell. 3rd ed. New York: Garland Pub., 1994.

    Google Scholar 

  2. Lopez-Otin C, Overall CM. Protease degradomics: A new challenge for proteomics. Nat Rev Mol Cell Biol 2002; 3(7):509–519.

    Article  PubMed  CAS  Google Scholar 

  3. Barrett AJ, Rawlings ND, Woessner JF. Handbook of proteolytic enzymes. San Diego: Academic Press, 2004.

    Google Scholar 

  4. Alexander DL, Mital J, Ward GE et al. Identification of the moving junction complex of Toxoplasma gondii: A collaboration between distinct secretory organelles. PLoS Pathog 2005; 1(2):e17.

    Article  PubMed  Google Scholar 

  5. Hoff EF, Carruthers VB. Is Toxoplasma egress the first step in invasion? Trends Parasitol 2002; 18(6):251–255.

    Article  PubMed  CAS  Google Scholar 

  6. Dowse T, Soldati D. Host cell invasion by the apicomplexans: The significance of microneme protein proteolysis. Curr Opin Microbiol 2004; 7(4):388–396.

    Article  PubMed  CAS  Google Scholar 

  7. Kim K. Role of proteases in host cell invasion by Toxoplasma gondii and other Apicomplexa. Acta Trop 2004; 91(1):69–81.

    Article  PubMed  CAS  Google Scholar 

  8. Blackman MJ. Proteases involved in erythrocyte invasion by the malaria parasite: Function and potential as chemotherapeutic targets. Curr Drug Targets 2000; 1(1):59–83.

    Article  PubMed  CAS  Google Scholar 

  9. Carruthers VB, Sherman GD, Sibley LD. The Toxoplasma adhesive protein MIC2 is proteolytically processed at multiple sites by two parasite-derived proteases. J Biol Chem 2000; 275(19):14346–14353.

    Article  PubMed  CAS  Google Scholar 

  10. Carruthers VB, Blackman MJ. A new release on life: Emerging concepts in proteolysis and parasite invasion. Mol Microbiol 2005; 55(6):1617–1630.

    Article  PubMed  CAS  Google Scholar 

  11. Opitz C, Di Cristina M, Reiss M et al. Intramembrane cleavage of microneme proteins at the surface of the apicomplexan parasite Toxoplasma gondii. EMBO J 2002; 21(7):1577–1585.

    Article  PubMed  CAS  Google Scholar 

  12. Tomley FM, Billington KJ, Bumstead JM et al. EtMIC4: A microneme protein from Eimeria tenella that contains tandem arrays of epidermal growth factor-like repeats and thrombospondin type-I repeats. Int J Parasitol 2001; 31(12):1303–1310.

    Article  PubMed  CAS  Google Scholar 

  13. Brossier F, Jewett TJ, Lovett JL et al. C-terminal processing of the Toxoplasma protein MIC2 is essential for invasion into host cells. J Biol Chem 2003; 278(8):6229–6234.

    Article  PubMed  CAS  Google Scholar 

  14. Zhou XW, Blackman MJ, Howell SA et al. Proteomic analysis of cleavage events reveals a dynamic two-step mechanism for proteolysis of a key parasite adhesive complex. Mol Cell Proteomics 2004; 3(6):565–576.

    Article  PubMed  CAS  Google Scholar 

  15. Urban S, Lee JR, Freeman M. Drosophila rhomboid-1 defines a family of putative intramembrane serine proteases. Cell 2001; 107(2):173–182.

    Article  PubMed  CAS  Google Scholar 

  16. Koonin EV, Makarova KS, Rogozin IB et al. The rhomboids: A nearly ubiquitous family of intramembrane serine proteases that probably evolved by multiple ancient horizontal gene transfers. Genome Biol 2003; 4(3):R19.

    Article  PubMed  Google Scholar 

  17. Freeman M. Proteolysis within the membrane: Rhomboids revealed. Nat Rev Mol Cell Biol 2004; 5(3):188–197.

    Article  PubMed  CAS  Google Scholar 

  18. Reiss M, Viebig N, Brecht S et al. Identification and characterization of an escorter for two secretory adhesins in Toxoplasma gondii. J Cell Biol 2001; 152(3):563–578.

    Article  PubMed  CAS  Google Scholar 

  19. Howell SA, Hackett F, Jongco AM et al. Distinct mechanisms govern proteolytic shedding of a key invasion protein in apicomplexan pathogens. Mol Microbiol 2005; 57(5):1342–1356.

    Article  PubMed  CAS  Google Scholar 

  20. Miller SA, Binder EM, Blackman MJ et al. A conserved subtilisin-like protein TgSUB1 in microneme organelles of Toxoplasma gondii. J Biol Chem 2001; 276(48):45341–45348.

    Article  PubMed  CAS  Google Scholar 

  21. Urban S, Freeman M. Substrate specificity of rhomboid intramembrane proteases is governed by helix-breaking residues in the substrate transmembrane domain. Mol Cell 2003; 11(6):1425–1434.

    Article  PubMed  CAS  Google Scholar 

  22. Brossier F, Jewett TJ, Sibley LD et al. A spatially localized rhomboid protease cleaves cell surface adhesins essential for invasion by Toxoplasma. Proc Natl Acad Sci USA 2005; 102(11):4146–4151.

    Article  PubMed  CAS  Google Scholar 

  23. Dowse TJ, Pascall JC, Brown KD et al. Apicomplexan rhomboids have a potential role in microneme protein cleavage during host cell invasion. Int J Parasitol 2005; 35(7):747–756.

    Article  PubMed  CAS  Google Scholar 

  24. Baker RP, Wijetilaka R, Urban S. Two plasmodium rhomboid proteases preferentially cleave different adhesins implicated in all invasive stages of malaria. PLoS Pathog 2006; 2(10):e113.

    Article  PubMed  Google Scholar 

  25. Dowse TJ, Soldati D. Rhomboid-like proteins in Apicomplexa: Phylogeny and nomenclature. Trends Parasitol 2005; 21(6):254–258.

    Article  PubMed  CAS  Google Scholar 

  26. O’Donnell RA, Hackett F, Howell SA et al. Intramembrane proteolysis mediates shedding of a key adhesin during erythrocyte invasion by the malaria parasite. J Cell Biol 2006; 174(7):1023–1033.

    Article  PubMed  CAS  Google Scholar 

  27. Carruthers VB, Sibley LD. Sequential protein secretion from three distinct organelles of Toxoplasma gondii accompanies invasion of human fibroblasts. Eur J Cell Biol 1997; 73(2):114–123.

    PubMed  CAS  Google Scholar 

  28. Mital J, Meissner M, Soldati D et al. Conditional expression of Toxoplasma gondii apical membrane antigen-1 (TgAMA1) demonstrates that TgAMA1 plays a critical role in host cell invasion. Mol Biol Cell 2005; 16(9):4341–4349.

    Article  PubMed  CAS  Google Scholar 

  29. Silvie O, Franetich JF, Charrin S et al. A role for apical membrane antigen 1 during invasion of hepatocytes by Plasmodium falciparum sporozoites. J Biol Chem 2004; 279(10):9490–9496.

    Article  PubMed  CAS  Google Scholar 

  30. Reed MB, Caruana SR, Batchelor AH et al. Targeted disruption of an erythrocyte binding antigen in Plasmodium falciparum is associated with a switch toward a sialic acid-independent pathway of invasion. Proc Natl Acad Sci USA 2000; 97(13):7509–75l4.

    Article  PubMed  CAS  Google Scholar 

  31. Stubbs J, Simpson KM, Triglia T et al. Molecular mechanism for switching of P. falciparum invasion pathways into human erythrocytes. Science 2005; 309(5739):1384–1387.

    Article  PubMed  CAS  Google Scholar 

  32. Wang Y, Zhang Y, Ha Y. Crystal structure of a rhomboid family intramembrane protease. Nature 2006.

    Google Scholar 

  33. Li X, Chen H, Oo TH et al. A coligand complex anchors Plasmodium falciparum merozoites to the erythrocyte invasion receptor band 3. J Biol Chem 2004; 279(7):5765–5771.

    Article  PubMed  CAS  Google Scholar 

  34. Pachebat JA, Ling IT, Grainger M et al. The 22 kDa component of the protein complex on the surface of Plasmodium falciparum merozoites is derived from a larger precursor, merozoite surface protein 7. Mol Biochem Parasitol 2001; 117(1):83–89.

    Article  PubMed  CAS  Google Scholar 

  35. Trucco C, Fernandez-Reyes D, Howell S et al. The merozoite surface protein 6 gene codes for a 36 kDa protein associated with the Plasmodium falciparum merozoite surface protein-1 complex. Mol Biochem Parasitol 2001; 112(1):91–101.

    Article  PubMed  CAS  Google Scholar 

  36. Blackman MJ, Dennis ED, Hirst EM et al. Plasmodium knowlesi: Secondary processing of the malaria merozoite surface protein-1. Exp Parasitol 1996; 83(2):229–239.

    Article  PubMed  CAS  Google Scholar 

  37. Blackman MJ, Scott-Finnigan TJ, Shai S et al. Antibodies inhibit the protease-mediated processing of a malaria merozoite surface protein. J Exp Med 1994; 180(1):389–393.

    Article  PubMed  CAS  Google Scholar 

  38. Fleck SL, Birdsall B, Babon J et al. Suramin and suramin analogues inhibit merozoite surface protein-1 secondary processing and erythrocyte invasion by the malaria parasite Plasmodium falciparum. J Biol Chem 2003; 278(48):47670–47677.

    Article  PubMed  CAS  Google Scholar 

  39. Blackman MJ, Holder AA. Secondary processing of the Plasmodium falciparum merozoite surface protein-1 (MSP1) by a calcium-dependent membrane-bound serine protease: Shedding of MSP133 as a noncovalently associated complex with other fragments of the MSP1. Mol Biochem Parasitol 1992; 50(2):307–315.

    Article  PubMed  CAS  Google Scholar 

  40. Dutta S, Haynes JD, Moch JK et al. Invasion-inhibitory antibodies inhibit proteolytic processing of apical membrane antigen 1 of Plasmodium falciparum merozoites. Proc Natl Acad Sci USA 2003; 100(21):12295–12300.

    Article  PubMed  CAS  Google Scholar 

  41. Dutta S, Haynes JD, Barbosa A et al. Mode of action of invasion-inhibitory antibodies directed against Apical Membrane Antigen 1 of Plasmodium falciparum. Infect Immun 2005; 73(4):2116–2122.

    Article  PubMed  CAS  Google Scholar 

  42. Howell SA, Well I, Fleck SL et al. A single malaria merozoite serine protease mediates shedding of multiple surface proteins by juxtamembrane cleavage. J Biol Chem 2003; 278(26):23890–23898.

    Article  PubMed  CAS  Google Scholar 

  43. Howell SA, Withers-Martinez C, Kocken CH et al. Proteolytic processing and primary structure of Plasmodium falciparum apical membrane antigen-1. J Biol Chem 2001; 276(33):31311–31320.

    Article  PubMed  CAS  Google Scholar 

  44. Blackman MJ. Proteases in host cell invasion by the malaria parasite. Cell Microbiol 2004; 6(10):893–903.

    Article  PubMed  CAS  Google Scholar 

  45. Morgan WD, Birdsall B, Frenkiel TA et al. Solution structure of an EGF module pair from the Plasmodium falciparum merozoite surface protein 1. J Mol Biol 1999; 289(1):113–122.

    Article  PubMed  CAS  Google Scholar 

  46. Chitarra V, Holm I, Bentley GA et al. The crystal structure of C-terminal merozoite surface protein 1 at 1.8 A resolution, a highly protective malaria vaccine candidate. Mol Cell 1999; 3(4):457–464.

    Article  PubMed  CAS  Google Scholar 

  47. Wu Y, Wang X, Liu X et al. Data-mining approaches reveal hidden families of proteases in the genome of malaria parasite. Genome Res 2003; 13(4):601–616.

    Article  PubMed  CAS  Google Scholar 

  48. Blackman MJ, Fujioka H, Stafford WH et al. A subtilisin-like protein in secretory organelles of Plasmodium falciparum merozoites. J Biol Chem 1998; 273(36):23398–23409.

    Article  PubMed  CAS  Google Scholar 

  49. Withers-Martinez C, Jean L, Blackman MJ. Subtilisin-like proteases of the malaria parasite. Mol Microbiol 2004; 53(1):55–63.

    Article  PubMed  CAS  Google Scholar 

  50. Blackman MJ, Corrie JE, Croney JC et al. Structural and biochemical characterization of a fluorogenic rhodamine-labeled malarial protease substrate. Biochemistry 2002; 41(40):12244–12252.

    Article  PubMed  CAS  Google Scholar 

  51. Jean L, Hackett F, Martin SR et al. Functional characterization of the propeptide of Plasmodium falciparum subtilisin-like protease-1. J Biol Chem 2003; 278(31):28572–28579.

    Article  PubMed  CAS  Google Scholar 

  52. Barale JC, Blisnick T, Fujioka H et al. Plasmodium falciparum subtilisin-like protease 2, a merozoite candidate for the merozoite surface protein 1–42 maturase. Proc Natl Acad Sci USA 1999; 96(11):6445–6450.

    Article  PubMed  CAS  Google Scholar 

  53. Hackett F, Sajid M, Withers-Martinez C et al. PfSUB-2: A second subtilisin-like protein in Plasmodium falciparum merozoites. Mol Biochem Parasitol 1999; 103(2):183–195.

    Article  PubMed  CAS  Google Scholar 

  54. Harris PK, Yeoh S, Dluzewski AR et al. Molecular identification of a malaria merozoite surface sheddase. PLoS Pathog 2005; 1(3):e29.

    Article  Google Scholar 

  55. Green JL, Hinds L, Grainger M et al. Plasmodium thrombospondin related apical merozoite protein (PTRAMP) is shed from the surface of merozoites by PfSUB2 upon invasion of erythrocytes. Mol Biochem Parasitol 2006.

    Google Scholar 

  56. Pizarro JC, Vulliez-Le Normand B, Chesne-Seck ML et al. Crystal structure of the malaria vaccine candidate apical membrane antigen 1. Science 2005; 308(5720):408–411.

    Article  PubMed  CAS  Google Scholar 

  57. Brecht S, Carruthers VB, Ferguson DJ et al. The Toxoplasma micronemal protein MIC4 is an adhesin composed of six conserved apple domains. J Biol Chem 2001; 276(6):4119–4127.

    Article  PubMed  CAS  Google Scholar 

  58. Barragan A, Brossier F, Sibley LD. Transepithelial migration of Toxoplasma gondii involves an interaction of intercellular adhesion molecule 1 (ICAM-1) with the parasite adhesin MIC2. Cell Microbiol 2005; 7(4):561–568.

    Article  PubMed  CAS  Google Scholar 

  59. Miller SA, Thathy V, Ajioka JW et al. TgSUB2 is a Toxoplasma gondii rhoptry organelle processing proteinase. Mol Microbiol 2003; 49(4):883–894.

    Article  PubMed  CAS  Google Scholar 

  60. Greenbaum DC, Baruch A, Grainger M et al. A role for the protease falcipain 1 in host cell invasion by the human malaria parasite. Science 2002; 298(5600):2002–2006.

    Article  PubMed  CAS  Google Scholar 

  61. Sijwali PS, Kato K, Seydel KB et al. Plasmodium falciparum cysteine protease falcipain-1 is not essential in erythrocytic stage malaria parasites. Proc Natl Acad Sci USA 2004; 101(23):8721–8726.

    Article  PubMed  CAS  Google Scholar 

  62. Eksi S, Czesny B, Greenbaum DC et al. Targeted disruption of Plasmodium falciparum cysteine protease, falcipain 1, reduces oocyst production, not erythrocytic stage growth. Mol Microbiol 2004; 53(l):243–250.

    Article  PubMed  CAS  Google Scholar 

  63. Braun-Breton C, Rosenberry TL, da Silva LP. Induction of the proteolytic activity of a membrane protein in Plasmodium falciparum by phosphatidyl inositol-specific phospholipase C. Nature 1988; 332(6l63):457–459.

    Article  PubMed  CAS  Google Scholar 

  64. Roggwiller E, Betoulle ME, Blisnick T et al. A role for erythrocyte band 3 degradation by the parasite gp76 serine protease in the formation of the parasitophorous vacuole during invasion of erythrocytes by Plasmodium falciparum. Mol Biochem Parasitol 1996; 82(1):13–24.

    Article  PubMed  CAS  Google Scholar 

  65. McPherson RA, Donald DR, Sawyer WH et al. Proteolytic digestion of band 3 at an external site alters the erythrocyte membrane organisation and may facilitate malarial invasion. Mol Biochem Parasitol 1993; 62(2):233–242.

    Article  PubMed  CAS  Google Scholar 

  66. Conseil V, Soete M, Dubremetz JF. Serine protease inhibitors block invasion of host cells by Toxoplasma gondii. Antimicrob Agents Chemother 1999; 43(6):1358–1361.

    PubMed  CAS  Google Scholar 

  67. Winograd E, Clavijo CA, Bustamante LY et al. Release of merozoites from Plasmodium falciparum-infected erythrocytes could be mediated by a nonexplosive event. Parasitol Res 1999; 85(8–9):621–624.

    Article  PubMed  CAS  Google Scholar 

  68. Salmon BL, Oksman A, Goldberg DE. Malaria parasite exit from the host erythrocyte: A two-step process requiring extraerythrocytic proteolysis. Proc Natl Acad Sci USA 2001; 98(1):271–276.

    Article  PubMed  CAS  Google Scholar 

  69. Wickham ME, Culvenor JG, Cowman AF. Selective inhibition of a two-step egress of malaria parasites from the host erythrocyte. J Biol Chem 2003; 278(39):37658–37663.

    Article  PubMed  CAS  Google Scholar 

  70. Lyon JA, Haynes JD, Diggs CL et al. Plasmodium falciparum antigens synthesized by schizonts and stabilized at the merozoite surface by antibodies when schizonts mature in the presence of growth inhibitory immune serum. J Immunol 1986; 136(6):2252–2258.

    PubMed  CAS  Google Scholar 

  71. Soni S, Dhawan S, Rosen KM et al. Characterization of events preceding the release of malaria parasite from the host red blood cell. Blood Cells Mol Dis 2005; 35(2):201–211.

    Article  PubMed  CAS  Google Scholar 

  72. Glushakova S, Yin D, Li T et al. Membrane transformation during malaria parasite release from human red blood cells. Curr Biol 2005; 15(18):1645–1650.

    Article  PubMed  CAS  Google Scholar 

  73. Shenai BR, Rosenthal PJ. Reducing requirements for hemoglobin hydrolysis by Plasmodium falciparum cysteine proteases. Mol Biochem Parasitol 2002; 122(1):99–104.

    Article  PubMed  CAS  Google Scholar 

  74. Sijwali PS, Rosenthal PJ. Gene disruption confirms a critical role for the cysteine protease falcipain-2 in hemoglobin hydrolysis by Plasmodium falciparum. Proc Natl Acad Sci USA 2004; 101(13):4384–4389.

    Article  PubMed  CAS  Google Scholar 

  75. Dasaradhi PV, Mohmmed A, Kumar A et al. A role of falcipain-2, principal cysteine proteases of Plasmodium falciparum in merozoite egression. Biochem Biophys Res Commun 2005; 336(4):1062–1068.

    Article  PubMed  CAS  Google Scholar 

  76. Hanspal M, Dua M, Takakuwa Y et al. Plasmodium falciparum cysteine protease falcipain-2 cleaves erythrocyte membrane skeletal proteins at late stages of parasite development. Blood 2002; 100(3):1048–1054.

    Article  PubMed  CAS  Google Scholar 

  77. Blackman MJ. RNAi in protozoan parasites: What hope for the Apicomplexa? Protist 2003; 154(2):177–180.

    Article  PubMed  Google Scholar 

  78. Sijwali PS, Shenai BR, Gut J et al. Expression and characterization of the Plasmodium falciparum haemoglobinase falcipain-3. Biochem J 2001; 360 (Pt 2):481–489.

    Article  PubMed  CAS  Google Scholar 

  79. Dahl EL, Rosenthal PJ. Biosynthesis, localization, and processing of falcipain cysteine proteases of Plasmodium falciparum. Mol Biochem Parasitol 2005; 139(2):205–212.

    Article  PubMed  CAS  Google Scholar 

  80. Silva AM, Lee AY, Gulnik SV et al. Structure and inhibition of plasmepsin II, a hemoglobin-degrading enzyme from Plasmodium falciparum. Proc Natl Acad Sci USA 1996; 93(19):10034–10039.

    Article  PubMed  CAS  Google Scholar 

  81. Le Bonniec S, Deregnaucourt C, Redeker V et al. Plasmepsin II, an acidic hemoglobinase from the Plasmodium falciparum food vacuole, is active at neutral pH on the host erythrocyte membrane skeleton. J Biol Chem 1999; 274(20):14218–14223.

    Article  PubMed  Google Scholar 

  82. Francis SE, Gluzman IY, Oksman A et al. Molecular characterization and inhibition of a Plasmodium falciparum aspartic hemoglobinase. EMBO J 1994; 13(2):306–317.

    PubMed  CAS  Google Scholar 

  83. Liu J, Gluzman IY, Drew ME et al. The role of Plasmodium falciparum food vacuole plasmepsins. J Biol Chem 2005; 280(2):1432–1437.

    Article  PubMed  CAS  Google Scholar 

  84. Miller SK, Good RT, Drew DR et al. A subset of Plasmodium falciparum SERA genes are expressed and appear to play an important role in the erythrocytic cycle. J Biol Chem 2002; 277(49):47524–47532.

    Article  PubMed  CAS  Google Scholar 

  85. Hodder AN, Drew DR, Epa VC et al. Enzymic, phylogenetic, and structural characterization of the unusual papain-like protease domain of Plasmodium falciparum SERA5. J Biol Chem 2003; 278(48):48169–48177.

    Article  PubMed  CAS  Google Scholar 

  86. Li J, Matsuoka H, Mitamura T et al. Characterization of proteases involved in the processing of Plasmodium falciparum serine repeat antigen (SERA). Mol Biochem Parasitol 2002; 120(2):177–186.

    Article  PubMed  CAS  Google Scholar 

  87. Pang XL, Mitamura T, Horii T. Antibodies reactive with the N-terminal domain of Plasmodium falciparum serine repeat antigen inhibit cell proliferation by agglutinating merozoites and schizonts. Infect Immun 1999; 67(4):1821–1827.

    PubMed  CAS  Google Scholar 

  88. Aly AS, Matuschewski K. A malarial cysteine protease is necessary for Plasmodium sporozoite egress from oocysts. J Exp Med 2005; 202(2):225–230.

    Article  PubMed  CAS  Google Scholar 

  89. Black MW, Boothroyd JC. Lytic cycle of Toxoplasma gondii. Microbiol Mol Biol Rev 2000; 64(3):607–623.

    Article  PubMed  CAS  Google Scholar 

  90. Que X, Ngo H, Lawton J et al. The cathepsin B of Toxoplasma gondii, toxopain-1, is critical for parasite invasion and rhoptry protein processing. J Biol Chem 2002; 277(28):25791–25797.

    Article  PubMed  CAS  Google Scholar 

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Correspondence to Dominique Soldati-Favre .

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Dowse, T.J., Koussis, K., Blackman, M.J., Soldati-Favre, D. (2008). Roles of Proteases during Invasion and Egress by Plasmodium and Toxoplasma . In: Burleigh, B.A., Soldati-Favre, D. (eds) Molecular Mechanisms of Parasite Invasion. Subcellular Biochemistry, vol 47. Springer, New York, NY. https://doi.org/10.1007/978-0-387-78267-6_10

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