Skip to main content
SpringerLink
Log in

Current and Emerging Approaches to Studying Invasion in Apicomplexan Parasites

  • Chapter
Molecular Mechanisms of Parasite Invasion

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

Abstract

In this chapter, we outline the tools and techniques available to study the process of host cell invasion by apicomplexan parasites and we provide specific examples of how these methods have been used to further our understanding of apicomplexan invasive mechanisms. Throughout the chapter we focus our discussion on Toxoplasma gondii, because T. gondii is the most experimentally accessible model organism for studying apicomplexan invasion (discussed further in the section, “Toxoplasma as a Model Apicomplexan”) and more is known about invasion in T. gondii than in any other apicomplexan.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Mercier C, Adjogble KD, Daubener W et al. Dense granules: Are they key organelles to help understand the parasitophorous vacuole of all apicomplexa parasites? Int J Parasitol 2005; 35(8):829–849.

    Article  PubMed  Google Scholar 

  2. Kappe SH, Buscaglia CA, Bergman LW et al. Apicomplexan gliding motility and host cell invasion: Overhauling the motor model. Trends Parasitol 2004; 20(1): 13–16.

    Article  PubMed  CAS  Google Scholar 

  3. Hakansson S, Morisaki H, Heuser J et al. Time-lapse video microscopy of gliding motility in Toxoplasma gondii reveals a novel, biphasic mechanism of cell locomotion. Mol Biol Cell 1999; 10(11):3539–3547.

    PubMed  CAS  Google Scholar 

  4. Hu K, Roos DS, Murray JM. A novel polymer of tubulin forms the conoid of Toxoplasma gondii. J Cell Biol 2002; 156(6):1039–1050.

    Article  PubMed  CAS  Google Scholar 

  5. Morrissette NS, Sibley LD. Cytoskeleton of apicomplexan parasites. Microbiol Mol Biol Rev 2002; 66(1):21–38.

    Article  PubMed  Google Scholar 

  6. 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 

  7. 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 

  8. 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 

  9. Suss-Toby E, Zimmerberg J, Ward GE. Toxoplasma invasion: The parasitophorous vacuole is formed from host cell plasma membrane and pinches off via a fission pore. Proc Natl Acad Sci USA 1996; 93(16):8413–8418.

    Article  PubMed  CAS  Google Scholar 

  10. Meissner M, Schluter D, Soldati D. Role of Toxoplasma gondii myosin A in powering parasite gliding and host cell invasion. Science 2002; 298(5594):837–840.

    Article  PubMed  CAS  Google Scholar 

  11. Dobrowolski JM, Carruthers VB, Sibley LD. Participation of myosin in gliding motility and host cell invasion by Toxoplasma gondii. Mol Microbiol 1997; 26(1): 163–173.

    Article  PubMed  CAS  Google Scholar 

  12. Sibley LD. Intracellular parasite invasion strategies. Science 2004; 304(5668):248–253.

    Article  PubMed  CAS  Google Scholar 

  13. 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  CAS  Google Scholar 

  14. Lebrun M, Michelin A, El Hajj H et al. The rhoptry neck protein RON4 relocalizes at the moving junction during Toxoplasma gondii invasion. Cell Microbiol 2005; 7(12): 1823–1833.

    Article  PubMed  CAS  Google Scholar 

  15. Mordue DG, Hakansson S, Niesman I et al. Toxoplasma gondii resides in a vacuole that avoids fusion with host cell endocytic and exocytic vesicular trafficking pathways. Exp Parasitol 1999; 92(2):87–99.

    Article  PubMed  CAS  Google Scholar 

  16. Lingelbach K, Joiner KA. The parasitophorous vacuole membrane surrounding Plasmodium and Toxoplasma: An unusual compartment in infected cells. J Cell Sci 1998; 111 (Pt 11): 1467–1475.

    PubMed  CAS  Google Scholar 

  17. Morisaki JH, Heuser JE, Sibley LD. Invasion of Toxoplasma gondii occurs by active penetration of the host cell. J Cell Sci 1995; 108 (Pt 6):2457–2464.

    PubMed  CAS  Google Scholar 

  18. Sinai AP, Webster P, Joiner KA. Association of host cell endoplasmic reticulum and mitochondria with the Toxoplasma gondii parasitophorous vacuole membrane: A high affinity interaction. J Cell Sci 1997; 110 (Pt 17):2117–2128.

    PubMed  CAS  Google Scholar 

  19. Augustine PC. Cell: Sporozoite interactions and invasion by apicomplexan parasites of the genus Eimeria. Int J Parasitol 2001; 31(1):1–8.

    Article  PubMed  CAS  Google Scholar 

  20. Buxton D, McAllister MM, Dubey JP. The comparative pathogenesis of neosporosis. Trends Parasitol 2002; 18(12):546–552.

    Article  PubMed  CAS  Google Scholar 

  21. Smith HV, Nichols RA, Grimason AM. Cryptosporidium excystation and invasion: Getting to the guts of the matter. Trends Parasitol 2005; 21(3):133–142.

    Article  PubMed  CAS  Google Scholar 

  22. Moltmann UG, Mehlhorn H, Schein E et al. Fine structure of Babesia equi Laveran, 1901 within lymphocytes and erythrocytes of horses: An in vivo and in vitro study. J Parasitol 1983; 69(1):111–120.

    Article  PubMed  CAS  Google Scholar 

  23. Miller LH, Aikawa M, Johnson JG et al. Interaction between cytochalasin B-treated malarial parasites and erythrocytes. Attachment and junction formation. J Exp Med 1979; 149(1): 172–84.

    Article  PubMed  CAS  Google Scholar 

  24. Shaw MK. Cell invasion by Theileria sporozoites. Trends Parasitol 2003; 19(1):2–6.

    Article  PubMed  Google Scholar 

  25. Pfefferkorn ER, Pfefferkorn LC. Toxoplasma gondii: Isolation and preliminary characterization of temperature-sensitive mutants. Exp Parasitol 1976; 39(3):365–376.

    Article  PubMed  CAS  Google Scholar 

  26. Saffer LD, Long Krug SA, Schwartzman JD. The role of phospholipase in host cell penetration by Toxoplasma gondii. Am J Trop Med Hyg 1989; 40(2): 145–149.

    PubMed  CAS  Google Scholar 

  27. Hehl AB, Lekutis C, Grigg ME et al. Toxoplasma gondii homologue of Plasmodium apical membrane antigen 1 is involved in invasion of host cells. Infect Immun 2000; 68(12):7078–7086.

    Article  PubMed  CAS  Google Scholar 

  28. Schwartzman JD, PfefFerkorn ER. Pyrimidine synthesis by intracellular Toxoplasma gondii. J Parasitol 1981; 67(2):150–158.

    Article  PubMed  CAS  Google Scholar 

  29. Camps M, Boothroyd JC. Toxoplasma gondii: Selective killing of extracellular parasites by oxidation using pyrrolidine dithiocarbamate. Exp Parasitol 2001; 98(4):206–214.

    Article  PubMed  CAS  Google Scholar 

  30. Soldati D, Kim K, Kampmeier J et al. Complementation of a Toxoplasma gondii ROP1 knock-out mutant using phleomycin selection. Mol Biochem Parasitol 1995; 74(1):87–97.

    Article  PubMed  CAS  Google Scholar 

  31. Carruthers VB, Giddings OK, Sibley LD. Secretion of micronemal proteins is associated with Toxoplasma invasion of host cells. Cell Microbiol 1999; 1(3):225–235.

    Article  PubMed  CAS  Google Scholar 

  32. Seeber F, Boothroyd JC. Escherichia coli beta-galactosidase as an in vitro and in vivo reporter enzyme and stable transfection marker in the intracellular protozoan parasite Toxoplasma gondii. Gene 1996; 169(1):39–45.

    Article  PubMed  CAS  Google Scholar 

  33. Sibley LD, Howe DK, Wan KL et al. Toxoplasma as a model genetic system. In: Smith DF, Parsons M, eds. Molecular Biology of Parasitic Protozoa. New York: Oxford University Press, 1996:55–74.

    Google Scholar 

  34. Howe DK, Mercier C, Messina M et al. Expression of Toxoplasma gondii genes in the closely-related apicomplexan parasite Neospora caninum. Mol Biochem Parasitol 1997; 86(1):29–36.

    PubMed  CAS  Google Scholar 

  35. Soldati D, Boothroyd JC. Transient transfection and expression in the obligate intracellular parasite Toxoplasma gondii. Science 1993; 260(5106):349–352.

    Article  PubMed  CAS  Google Scholar 

  36. Donald RG, Roos DS. Stable molecular transformation of Toxoplasma gondii: A selectable dihydrofolate reductase-thymidylate synthase marker based on drug-resistance mutations in malaria. Proc Natl Acad Sci USA 1993; 90(24):11703–11707.

    Article  PubMed  CAS  Google Scholar 

  37. Black MW, Boothroyd JC. Development of a stable episomal shuttle vector for Toxoplasma gondii. J Biol Chem 1998; 273(7):3972–3979.

    Article  PubMed  CAS  Google Scholar 

  38. Kim K, Soldati D, Boothroyd JC. Gene replacement in Toxoplasma gondii with chlorarnphenicol acetyltransferase as selectable marker. Science 1993; 262(5135):911–914.

    Article  PubMed  CAS  Google Scholar 

  39. Roos DS, Donald RG, Morrissette NS et al. Molecular tools for genetic dissection of the protozoan parasite Toxoplasma gondii. Methods Cell Biol 1994; 27-63.

    Google Scholar 

  40. Garcia-Reguet N, Lebrun M, Fourmaux M et al. The microneme protein MIC3 of Toxoplasma gondii is a secretory adhesin that binds to both the surface of the host cells and the surface of the parasite. Cell Microbiol 2000; 2(4):353–364.

    Article  PubMed  CAS  Google Scholar 

  41. Messina M, Niesman I, Mercier C et al. Stable DNA transformation of Toxoplasma gondii using phleomycin selection. Gene 1995; 165(2):213–217.

    Article  PubMed  CAS  Google Scholar 

  42. Donald RGK, Carter D, Ullman B et al. Insertional tagging, cloning, and expression of the Toxoplasma gondii hypoxanthine-xanthine-guanine phosphoribosyltransferase gene. Use as a selectable marker for stable transformation. J Biol Chem 1996; 271(24):14010–14019.

    Article  PubMed  CAS  Google Scholar 

  43. Donald RG, Roos DS. Insertional mutagenesis and marker rescue in a protozoan parasite: Cloning of the uracil phosphoribosyltransferase locus from Toxoplasma gondii. Proc Natl Acad Sci USA 1995; 92(12):5749–5753.

    Article  PubMed  CAS  Google Scholar 

  44. Radke JR, White MW. A cell cycle model for the tachyzoite of Toxoplasma gondii using the Herpes simplex virus thymidine kinase. Mol Biochem Parasitol 1998; 94(2):237–247.

    Article  PubMed  CAS  Google Scholar 

  45. Sibley LD, Messina M, Niesman IR. Stable DNA transformation in the obligate intracellular parasite Toxoplasma gondii by complementation of tryptophan auxotrophy. Proc Natl Acad Sci USA 1994; 91(12):5508–5512.

    Article  PubMed  CAS  Google Scholar 

  46. Van Tarn T, Rooney PJ, Knoll LJ. Nourseothricin acetyltransferease: A positive selectable marker for Toxoplasma gondii. J Parasitol 2006; 92(3):668–670.

    Article  Google Scholar 

  47. Mercier C, Lefebvre-Van Hende S, Garber GE et al. Common cis-acting elements critical for the expression of several genes of Toxoplasma gondii. Mol Microbiol 1996; 21(2):421–428.

    Article  PubMed  CAS  Google Scholar 

  48. Dobrowolski JM, Sibley LD. Toxoplasma invasion of mammalian cells is powered by the actin cytoskeleton of the parasite. Cell 1996; 84(6):933–939.

    Article  PubMed  CAS  Google Scholar 

  49. Black M, Seeber F, Soldati D et al. Restriction enzyme-mediated integration elevates transformation frequency and enables cotransfection of Toxoplasma gondii. Mol Biochem Parasitol 1995; 74(1):55–63.

    Article  PubMed  CAS  Google Scholar 

  50. Carey KL, Westwood NJ, Mitchison TJ et al. A small-molecule approach to studying invasive mechanisms of Toxoplasma gondii. Proc Natl Acad Sci USA 2004; 101(19):7433–7438.

    Article  PubMed  CAS  Google Scholar 

  51. Striepen B, He CY, Matrajt M et al. Expression, selection, and organellar targeting of the green fluorescent protein in Toxoplasma gondii. Mol Biochem Parasitol 1998; 92(2):325–338.

    Article  PubMed  CAS  Google Scholar 

  52. Matrajt M, Nishi M, Fraunholz MJ et al. Amino-terminal control of transgenic protein expression levels in Toxoplasma gondii. Mol Biochem Parasitol 2002; 120(2):285–289.

    Article  PubMed  CAS  Google Scholar 

  53. Wu Y, Sifri CD, Lei HH et al. Transfection of Plasmodium falciparum within human red blood cells. Proc Natl Acad Sci USA 1995; 92(4):973–977.

    Article  PubMed  CAS  Google Scholar 

  54. van Dijk MR, Waters AP, Janse CJ. Stable transfection of malaria parasite blood stages. Science 1995; 268(5215):1358–1362.

    Article  PubMed  Google Scholar 

  55. 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 

  56. Crabb BS, Cowman AF. Characterization of promoters and stable transfection by homologous and nonhomologous recombination in Plasmodium falciparum. Proc Natl Acad Sci USA 1996; 93(14):7289–7294.

    Article  PubMed  CAS  Google Scholar 

  57. Kadekoppala M, Cheresh P, Catron D et al. Rapid recombination among transfected plasmids, chimeric episome formation and trans gene expression in Plasmodium falciparum. Mol Biochem Parasitol 2001; 112(2):211–218.

    Article  PubMed  CAS  Google Scholar 

  58. Carvalho TG, Menard R. Manipulating the Plasmodium genome. Curr Issues Mol Biol 2005; 7(1):39–55.

    PubMed  CAS  Google Scholar 

  59. de Koning-Ward TF, Fidock DA, Thathy V et al. The selectable marker human dihydrofolate reductase enables sequential genetic manipulation of the Plasmodium berghei genome. Mol Biochem Parasitol 2000; 106(2):199–212.

    Article  PubMed  Google Scholar 

  60. Mamoun CB, Gluzman IY, Goyard S et al. A set of independent selectable markers for transfection of the human malaria parasite Plasmodium falciparum. Proc Natl Acad Sci USA 1999; 96(15):8716–8720.

    Article  PubMed  CAS  Google Scholar 

  61. Cowman AF, Crabb BS. Invasion of red blood cells by malaria parasites. Cell 2006; 124(4):755–766.

    Article  PubMed  CAS  Google Scholar 

  62. Duraisingh MT, Triglia T, Cowman AF. Negative selection of Plasmodium falciparum reveals targeted gene deletion by double crossover recombination. Int J Parasitol 2002; 32(1):81–89.

    Article  PubMed  CAS  Google Scholar 

  63. Deitsch K, Driskill C, Wellems T. Transformation of malaria parasites by the spontaneous uptake and expression of DNA from human erythrocytes. Nucleic Acids Res 2001; 29(3):850–853.

    Article  PubMed  CAS  Google Scholar 

  64. Waller RF, Reed MB, Cowman AF et al. Protein trafficking to the plastid of Plasmodium falciparum is via the secretory pathway. EMBO J 2000; 19(8):1794–1802.

    Article  PubMed  CAS  Google Scholar 

  65. Howe DK, Sibley LD. Development of molecular genetics for Neospora caninum: A complementary system to Toxoplasma gondii. Methods 1997; 13(2): 123–133.

    Article  PubMed  CAS  Google Scholar 

  66. Kelleher M, Tomley FM. Transient expression of beta-galactosidase in differentiating sporozoites of Eimeria tenella. Mol Biochem Parasitol 1998; 97(1–2):21–31.

    Article  PubMed  CAS  Google Scholar 

  67. Adamson R, Lyons K, Sharrard M et al. Transient transfection of Theileria annulata. Mol Biochem Parasitol 2001; 114(1):53–61.

    Article  PubMed  CAS  Google Scholar 

  68. Gardner MJ, Bishop R, Shah T et al. Genome sequence of Theileria parva, a bovine pathogen that transforms lymphocytes. Science 2005; 309(5731):134–137.

    Article  PubMed  CAS  Google Scholar 

  69. Suarez CE, Palmer GH, LeRoith T et al. Intergenic regions in the rhoptry associated protein-1 (rap-1) locus promote exogenous gene expression in Babesia bovis. Int J Parasitol 2004; 34(10): 1177–1184.

    Article  PubMed  CAS  Google Scholar 

  70. Vaishnava S, Morrison DP, Gaji RY et al. Plastid segregation and cell division in the apicomplexan parasite Sarcocystis neurona. J Cell Sci 2005; 118 (Pt 15):3397–3407.

    Article  PubMed  CAS  Google Scholar 

  71. Huynh MH, Rabenau KE, Harper JM et al. Rapid invasion of host cells by Toxoplasma requires secretion of the MIC2-M2AP adhesive protein complex. EMBO J 2003; 22(9):2082–2090.

    Article  PubMed  CAS  Google Scholar 

  72. Gaji RY, Zhang D, Breathnach CC et al. Molecular genetic transfection of the coccidian parasite Sarcocystis neurona. Mol Biochem Parasitol 2006; 150(1): 1–9.

    Article  PubMed  CAS  Google Scholar 

  73. Lovett JL, Sibley LD. Intracellular calcium stores in Toxoplasma gondii govern invasion of host cells. J Cell Sci 2003; 116(Pt 14):3009–3016.

    Article  PubMed  CAS  Google Scholar 

  74. Naguleswaran A, Muller N, Hemphill A. Neospora caninum and Toxoplasma gondii: A novel adhesion/invasion assay reveals distinct differences in tachyzoite-host cell interactions. Exp Parasitol 2003; 104(3–4):149–158.

    Article  PubMed  CAS  Google Scholar 

  75. 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 

  76. Mital J, Schwarz J, Taatjes DJ et al. Laser scanning cytometer-based assays for measuring host cell attachment and invasion by the human pathogen Toxoplasma gondii. Cytometry A 2006; 69(1):13–19.

    PubMed  Google Scholar 

  77. Gay-Andrieu F, Cozon GJ, Ferrandiz J et al. Flow cytometric quantification of Toxoplasma gondii cellular infection and replication. J Parasitol 1999; 85(3):545–549.

    Article  PubMed  CAS  Google Scholar 

  78. Sultan AA, Thathy V, Frevert U et al. TRAP is necessary for gliding motility and infectivity of Plasmodium sporozoites. Cell 1997; 90(3):511–522.

    Article  PubMed  CAS  Google Scholar 

  79. 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):7509–7514.

    Article  PubMed  CAS  Google Scholar 

  80. Bharara R, Singh S, Pattnaik P et al. Structural analogs of sialic acid interfere with the binding of erythrocyte binding antigen-175 to glycophorin A, an interaction crucial for erythrocyte invasion by Plasmodium falciparum. Mol Biochem Parasitol 2004; 138(1):123–129.

    Article  PubMed  CAS  Google Scholar 

  81. Casey JL, Coley AM, Anders RF et al. Antibodies to malaria peptide mimics inhibit Plasmodium falciparum invasion of erythrocytes. Infect Immun 2004; 72(2):1126–1134.

    Article  PubMed  CAS  Google Scholar 

  82. Singh AP, Ozwara H, Kocken CH et al. Targeted deletion of Plasmodium knowlesi Duffy binding protein confirms its role in junction formation during invasion. Mol Microbiol 2005; 55(6):1925–1934.

    Article  PubMed  CAS  Google Scholar 

  83. Xu L, Chaudhuri A. Plasmodium yoelii: A differential fluorescent technique using Acridine Orange to identify infected erythrocytes and reticulocytes in Duffy knockout mouse. Exp Parasitol 2005; 110(1):80–87.

    Article  PubMed  CAS  Google Scholar 

  84. Kocken CH, Withers-Martinez C, Dubbeld MA et al. High-level expression of the malaria blood-stage vaccine candidate Plasmodium falciparum apical membrane antigen 1 and induction of antibodies that inhibit erythrocyte invasion. Infect Immun 2002; 70(8):4471–4476.

    Article  PubMed  CAS  Google Scholar 

  85. Kocken CH, Ozwara H, van der Wel A et al. Plasmodium knowlesi provides a rapid in vitro and in vivo transfection system that enables double-crossover gene knockout studies. Infect Immun 2002; 70(2):655–660.

    Article  PubMed  CAS  Google Scholar 

  86. Malagon F, Castillo O. On the labeling of malaria parasites In Vivo with 3H-hipoxanthine while developing an infection in the mouse. Acta Protozool 2000; 39:281–288.

    Google Scholar 

  87. Makler MT, Ries JM, Williams JA et al. Parasite lactate dehydrogenase as an assay for Plasmodium falciparum drug sensitivity. Am J Trop Med Hyg 1993; 48(6):739–741.

    PubMed  CAS  Google Scholar 

  88. Makler MT, Hinrichs DJ. Measurement of the lactate dehydrogenase activity of Plasmodium falciparum as an assessment of parasitemia. Am J Trop Med Hyg 1993; 48(2):205–210.

    PubMed  CAS  Google Scholar 

  89. Drew DR, O’Donnell RA, Smith BJ et al. A common cross-species function for the double epidermal growth factor-like modules of the highly divergent Plasmodium surface proteins MSP-1 and MSP-8. J Biol Chem 2004; 279(19):20147–20153.

    Article  PubMed  CAS  Google Scholar 

  90. Labbe M, de Venevelles P, Girard-Misguich F et al. Eimeria tenella microneme protein EtMIC3: Identification, localisation and role in host cell infection. Mol Biochem Parasitol 2005; 140(1):43–53.

    Article  PubMed  CAS  Google Scholar 

  91. Ward GE, Fujioka H, Aikawa M et al. Staurosporine inhibits invasion of erythrocytes by malarial merozoites. Exp Parasitol 1994; 79(3):480–487.

    Article  PubMed  CAS  Google Scholar 

  92. Gaffar FR, Yatsuda AP, Franssen FF et al. Erythrocyte invasion by Babesia bovis merozoites is inhibited by polyclonal antisera directed against peptides derived from a homologue of Plasmodium falciparum apical membrane antigen 1. Infect Immun 2004; 72(5):2947–2955.

    Article  PubMed  CAS  Google Scholar 

  93. Franssen FF, Gaffar FR, Yatsuda AP et al. Characterisation of erythrocyte invasion by Babesia bovis merozoites efficiently released from their host cell after high-voltage pulsing. Microbes Infect 2003; 5(5):365–372.

    Article  PubMed  Google Scholar 

  94. Rathore D, Hrstka SC, Sacci Jr JB et al. Molecular mechanism of host specificity in Plasmodium falciparum infection: Role of circumsporozoite protein. J Biol Chem 2003; 278(42):40905–40910.

    Article  PubMed  CAS  Google Scholar 

  95. 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 

  96. Brahimi K, Badell E, Sauzet JP et al. Human antibodies against Plasmodium falciparum liver-stage antigen 3 cross-react with Plasmodium yoelii preerythrocytic-stage epitopes and inhibit sporozoite invasion in vitro and in vivo. Infect Immun 2001; 69(6):3845–3852.

    Article  PubMed  CAS  Google Scholar 

  97. Kafsack BF, Beckers C, Carruthers VB. Synchronous invasion of host cells by Toxoplasma gondii. Mol Biochem Parasitol 2004; 136(2):309–311.

    Article  PubMed  CAS  Google Scholar 

  98. Wetzel DM, Hakansson S, Hu K et al. Actin filament polymerization regulates gliding motility by apicomplexan parasites. Mol Biol Cell 2003; 14(2):396–406.

    Article  PubMed  CAS  Google Scholar 

  99. Chen XM, O’Hara SP, Huang BQ et al. Apical organelle discharge by Cryptosporidium parvum is temperature, cytoskeleton, and intracellular calcium dependent and required for host cell invasion. Infect Immun 2004; 72(12):6806–6816.

    Article  PubMed  CAS  Google Scholar 

  100. Wetzel DM, Schmidt J, Kuhlenschmidt MS et al. Gliding motility leads to active cellular invasion by Cryptosporidium parvum sporozoites. Infect Immun 2005; 73(9):5379–5387.

    Article  PubMed  CAS  Google Scholar 

  101. Entzeroth R, Zgrzebski G, Dubremetz JF. Secretion of trials during gliding motility of Eimeria (Apicomplexa, Coccidia) sporozoites visualized by a monoclonal antibody and immuno-gold-silver enhancement. Parasitol Res 1989; 76(2):174–175.

    Article  PubMed  CAS  Google Scholar 

  102. Wiersma HI, Galuska SE, Tomley FM et al. A role for coccidian cGMP-dependent protein kinase in motility and invasion. Int J Parasitol 2004; 34(3):369–380.

    Article  PubMed  CAS  Google Scholar 

  103. Stewart MJ, Vanderberg JP. Electron microscopic analysis of circumsporozoite protein trail formation by gliding malaria sporozoites. J Protozool 1992; 39(6):663–671.

    PubMed  CAS  Google Scholar 

  104. Bumstead J, Tomley F. Induction of secretion and surface capping of microneme proteins in Eimeria tenella. Mol Biochem Parasitol 2000; 110(2):311–321.

    Article  PubMed  CAS  Google Scholar 

  105. Siden-Kiamos I, Ecker A, Nyback S et al. Plasmodium berghei calcium-dependent protein kinase 3 is required for ookinete gliding motility and mosquito midgut invasion. Mol Microbiol 2006; 60(6):1355–1363.

    Article  PubMed  CAS  Google Scholar 

  106. Mondragon R, Frixione E. Ca(2+)-dependence of conoid extrusion in Toxoplasma gondii tachyzoites. J Eukaryot Microbiol 1996; 43(2):120–127.

    Article  PubMed  CAS  Google Scholar 

  107. Carruthers VB, Moreno SN, Sibley LD. Ethanol and acetaldehyde elevate intracellular [Ca2+] and stimulate microneme discharge in Toxoplasma gondii. Biochem J 1999; 342 (Pt 2):379–386.

    Article  PubMed  CAS  Google Scholar 

  108. Hoane JS, Carruthers VB, Striepen B et al. Analysis of the Sarcocystis neurona microneme protein SnMIC10: Protein characteristics and expression during intracellular development. Int J Parasitol 2003; 33(7):671–679.

    Article  PubMed  CAS  Google Scholar 

  109. Keller N, Riesen M, Naguleswaran A et al. Identification and characterization of a Neospora caninum microneme-associated protein (NcMIC4) that exhibits unique lactose-binding properties. Infect Immun 2004; 72(8):4791–4800.

    Article  PubMed  CAS  Google Scholar 

  110. Camus D, Hadley TJ. A Plasmodium falciparum antigen that binds to host erythrocytes and merozoites. Science 1985; 230(4725):553–556.

    Article  PubMed  CAS  Google Scholar 

  111. Adams JH, Hudson DE, Torii M et al. The duffy receptor family of Plasmodium knowlesi is located within the micronemes of invasive malaria merozoites. Cell 1990; 63:141–153.

    Article  PubMed  CAS  Google Scholar 

  112. 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 

  113. Phillips CI, Bogyo M. Proteomics meets microbiology: Technical advances in the global mapping of protein expression and function. Cell Microbiol 2005; 7(8):1061–1076.

    Article  PubMed  CAS  Google Scholar 

  114. Mineo JR, Kasper LH. Attachment of Toxoplasma gondii to host cells involves major surface protein, SAG-1 (P30). Exp Parasitol 1994; 79(1):11–20.

    Article  PubMed  CAS  Google Scholar 

  115. Silva SR, Meirelles SS, De Souza W. Mechanism of entry of Toxoplasma gondii into vertebrate cells. J Submicrosc Cytol 1982; 14(3):471–482.

    PubMed  CAS  Google Scholar 

  116. Friedman MJ, Blankenberg T, Sensabaugh G et al. Recognition and invasion of human erythrocytes by malarial parasites: Contribution of sialoglycoproteins to attachment and host specificity. J Cell Biol 1984; 98(5):1672–1677.

    Article  PubMed  CAS  Google Scholar 

  117. Mosqueda J, McElwain TF, Stiller D et al. Babesia bovis merozoite surface antigen 1 and rhoptry-associated protein 1 are expressed in sporozoites, and specific antibodies inhibit sporozoite attachment to erythrocytes. Infect Immun 2002; 70(3):1599–1603.

    Article  PubMed  CAS  Google Scholar 

  118. Fraser TS, Kappe SH, Narum DL et al. Erythrocyte-binding activity of Plasmodium yoelii apical membrane antigen-1 expressed on the surface of transfected COS-7 cells. Mol Biochem Parasitol 2001; 117(1):49–59.

    Article  PubMed  CAS  Google Scholar 

  119. Jacquet A, Coulon L, De Neve J et al. The surface antigen SAG3 mediates the attachment of Toxoplasma gondii to cell-surface proteoglycans. Mol Biochem Parasitol 2001;116(1):35–44.

    Article  PubMed  CAS  Google Scholar 

  120. Urquiza M, Suarez JE, Cardenas C et al. Plasmodium falciparum AMA-1 erythrocyte binding peptides implicate AMA-1 as erythrocyte binding protein. Vaccine 2000; 19(4-5):508–513.

    Article  PubMed  CAS  Google Scholar 

  121. Hakansson S, Charron AJ, Sibley LD. Toxoplasma evacuoles: A two-step process of secretion and fusion forms the parasitophorous vacuole. EMBO J 2001; 20(12):3132–3144.

    Article  PubMed  CAS  Google Scholar 

  122. Carey KL, Jongco AM, Kim K et al. The Toxoplasma gondii rhoptry protein ROP4 is secreted into the parasitophorous vacuole and becomes phosphorylated in infected cells. Eukaryot Cell 2004; 3(5):1320–1330.

    Article  PubMed  CAS  Google Scholar 

  123. Carey KL, Donahue CG, Ward GE. Identification and molecular characterization of GRA8, a novel, proline-rich, dense granule protein of Toxoplasma gondii. Mol Biochem Parasitol 2000; 105(1):25–37.

    Article  PubMed  CAS  Google Scholar 

  124. Aikawa M, Miller LH, Rabbege JR et al. Freeze-fracture study on the erythrocyte membrane during malarial parasite invasion. J Cell Biol 1981; 91(1):55–62.

    Article  PubMed  CAS  Google Scholar 

  125. Miller LH, Aikawa M, Johnson JG et al. Interaction between cytochalasin B-treated malarial parasites and erythrocytes. Attachment and junction formation. J Exp Med 1979; 149(1):172–184.

    Article  PubMed  CAS  Google Scholar 

  126. Donald RG, Roos DS. Homologous recombination and gene replacement at the dihydrofolate reductase-thymidylate synthase locus in Toxoplasma gondii. Mol Biochem Parasitol 1994; 63(2):243–253.

    Article  PubMed  CAS  Google Scholar 

  127. Roos DS, Sullivan WJ, Striepen B et al. Tagging genes and trapping promoters in Toxoplasma gondii by insertional mutagenesis. Methods 1997; 13(2):112–122.

    Article  PubMed  CAS  Google Scholar 

  128. Sullivan Jr WJ, Chiang CW, Wilson CM et al. Insertional tagging of at least two loci associated with resistance to adenine arabinoside in Toxoplasma gondii, and cloning of the adenosine kinase locus. Mol Biochem Parasitol 1999; 103(1):1–14.

    Article  PubMed  CAS  Google Scholar 

  129. Matrajt M, Donald RG, Singh U et al. Identification and characterization of differentiation mutants in the protozoan parasite Toxoplasma gondii. Mol Microbiol 2002; 44(3):735–747.

    Article  PubMed  CAS  Google Scholar 

  130. Vanchinathan P, Brewer JL, Harb OS et al. Disruption of a locus encoding a nucleolar zinc finger protein decreases tachyzoite-to-bradyzoite differentiation in Toxoplasma gondii. Infect Immun 2005; 73(10):6680–6688.

    Article  PubMed  CAS  Google Scholar 

  131. Striepen B, White MW, Li C et al. Genetic complementation in apicomplexan parasites. Proc Natl Acad Sci USA 2002; 16:16.

    Google Scholar 

  132. Black MW, Arrizabalaga G, Boothroyd JC. Ionophore-resistant mutants of Toxoplasma gondii reveal host cell permeabilization as an early event in egress. Mol Cell Biol 2000; 20(24):9399–9408.

    Article  PubMed  CAS  Google Scholar 

  133. Radke JR, Guerini MN, White MW. Toxoplasma gondii: Characterization of temperature-sensitive tachyzoite cell cycle mutants. Exp Parasitol 2000; 96(3):168–177.

    Article  PubMed  CAS  Google Scholar 

  134. Singh U, Brewer JL, Boothroyd JC. Genetic analysis of tachyzoite to bradyzoite differentiation mutants in Toxoplasma gondii reveals a hierarchy of gene induction. Mol Microbiol 2002; 44(3):721–733.

    Article  PubMed  CAS  Google Scholar 

  135. Lindsay DS, Lenz SD, Blagburn BL et al. Characterization of temperature-sensitive strains of Neospora caninum in mice. J Parasitol 1999; 85(1):64–67.

    Article  PubMed  CAS  Google Scholar 

  136. White MW, Jerome ME, Vaishnava S et al. Genetic rescue of a Toxoplasma gondii conditional cell cycle mutant. Mol Microbiol 2005; 55(4):1060–1071.

    Article  PubMed  CAS  Google Scholar 

  137. Mercier C, Howe DK, Mordue D et al. Targeted disruption of the GRA2 locus in Toxoplasma gondii decreases acute virulence in mice. Infect Immun 1998; 66(9):4176–4182.

    PubMed  CAS  Google Scholar 

  138. Dzierszinski F, Mortuaire M, Cesbron-Delauw MF et al. Targeted disruption of the glycosylphosphatidylinositol-anchored surface antigen SAG3 gene in Toxoplasma gondii decreases host cell adhesion and drastically reduces virulence in mice. Mol Microbiol 2000; 37(3):574–582.

    Article  PubMed  CAS  Google Scholar 

  139. Mercier C, Rauscher B, Lecordier L et al. Lack of expression of the dense granule protein GRA5 does not affect the development of Toxoplasma tachyzoites. Mol Biochem Parasitol 2001; 116(2):247–251.

    Article  PubMed  CAS  Google Scholar 

  140. Donald RG, Roos DS. Gene knock-outs and allelic replacements in Toxoplasma gondii: HXGPRT as a selectable marker for hit-and-run mutagenesis. Mol Biochem Parasitol 1998; 91(2):295–305.

    Article  PubMed  CAS  Google Scholar 

  141. Arrizabalaga G, Ruiz F, Moreno S et al. Ionophore-resistant mutant of Toxoplasma gondii reveals involvement of a sodium/hydrogen exchanger in calcium regulation. J Cell Biol 2004; 165(5):653–662.

    Article  PubMed  CAS  Google Scholar 

  142. Wichroski MJ, Ward GE. Biosynthesis of glycosylphosphatidylinositol is essential to the survival of the protozoan parasite Toxoplasma gondii. Eukaryot Cell 2003; 2(5):1132–1136.

    Article  PubMed  CAS  Google Scholar 

  143. Donald RG, Allocco J, Singh SB et al. Toxoplasma gondii cyclic GMP-dependent kinase: Chemotherapeutic targeting of an essential parasite protein kinase. Eukaryot Cell 2002; 1(3):317–328.

    Article  PubMed  CAS  Google Scholar 

  144. Cerede O, Dubremetz JF, Soete M et al. Synergistic role of micronemal proteins in Toxoplasma gondii virulence. J Exp Med 2005; 201(3):453–463.

    Article  PubMed  CAS  Google Scholar 

  145. Lekutis C, Ferguson DJ, Grigg ME et al. Surface antigens of Toxoplasma gondii: Variations on a theme. Int J Parasitol 2001; 31(12):1285–1292.

    Article  PubMed  CAS  Google Scholar 

  146. Duraisingh MT, Triglia T, Ralph SA et al. Phenotypic variation of Plasmodium falciparum merozoite proteins directs receptor targeting for invasion of human erythrocytes. EMBO J 2003; 22(5):1047–1057.

    Article  PubMed  CAS  Google Scholar 

  147. Khater EI, Sinden RE, Dessens JT. A malaria membrane skeletal protein is essential for normal morphogenesis, motility, and infectivity of sporozoites. J Cell Biol 2004; 167(3):425–432.

    Article  PubMed  CAS  Google Scholar 

  148. 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 

  149. 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 

  150. Tewari R, Ogun SA, Gunaratne RS et al. Disruption of Plasmodium berghei merozoite surface protein 7 gene modulates parasite growth in vivo. Blood 2005; 105(1):394–396.

    Article  PubMed  CAS  Google Scholar 

  151. Cowman AF, Baldi DL, Healer J et al. Functional analysis of proteins involved in Plasmodium falciparum merozoite invasion of red blood cells. FEBS Lett 2000; 476(1–2):84–88.

    Article  PubMed  CAS  Google Scholar 

  152. Eksi S, Haile Y, Furuya T et al. Identification of a subtelomeric gene family expressed during the asexual-sexual stage transition in Plasmodium falciparum. Mol Biochem Parasitol 2005; 143(1):90–99.

    Article  PubMed  CAS  Google Scholar 

  153. Mueller AK, Camargo N, Kaiser K et al. Plasmodium liver stage developmental arrest by depletion of a protein at the parasite-host interface. Proc Natl Acad Sci USA 2005; 102(8):3022–3027.

    Article  PubMed  CAS  Google Scholar 

  154. Yuda M, Ishino T. Liver invasion by malarial parasites-how do malarial parasites break through the host barrier? Cell Microbiol 2004; 6(12):1119–1125.

    Article  PubMed  CAS  Google Scholar 

  155. Kappe SH, Buscaglia CA, Nussenzweig V. Plasmodium sporozoite molecular cell biology. Annu Rev Cell Dev Biol 2004; 20:29–59.

    Article  PubMed  CAS  Google Scholar 

  156. Mota MM, Rodriguez A. Invasion of mammalian host cells by Plasmodium sporozoites. Bioessays 2002; 24(2):149–156.

    Article  PubMed  Google Scholar 

  157. Menard R. Gliding motility and cell invasion by Apicomplexa: Insights from the Plasmodium sporozoite. Cell Microbiol 2001; 3(2):63–73.

    Article  PubMed  CAS  Google Scholar 

  158. Huynh MH, Carruthers VB. Toxoplasma MIC2 is a major determinant of invasion and virulence. PLoS Pathog 2006; 2(8).

    Google Scholar 

  159. Mazumdar JE, HW, Masek K et al. Apicoplast fatty acid synthesis is essential for organelle biogenesis and parasite survival in Toxoplasma gondii. Proc Natl Acad Sci USA 2006; 103(35):13192–13197.

    Article  PubMed  CAS  Google Scholar 

  160. Meissner M, Krejany E, Gilson PR et al. Tetracycline analogue-regulated transgene expression in Plasmodium falciparum blood stages using Toxoplasma gondii transactivators. Proc Natl Acad Sci USA 2005; 102(8):2980–2985.

    Article  PubMed  CAS  Google Scholar 

  161. Carvalho TG, Thiberge S, Sakamoto H et al. Conditional mutagenesis using site-specific recombination in Plasmodium berghei. Proc Natl Acad Sci USA 2004; 101(41):14931–14936.

    Article  PubMed  CAS  Google Scholar 

  162. Al-Anouti F, Ananvoranich S. Comparative analysis of antisense RNA, double-stranded RNA, and delta ribozyme-mediated gene regulation in Toxoplasma gondii. Antisense Nucleic Acid Drug Dev 2002; 12(4):275–281.

    Article  PubMed  CAS  Google Scholar 

  163. Nakaar V, Ngo EO, Joiner KA. Selection based on the expression of antisense hypoxanthine-xanthine-guanine-phosphoribosyltransferase RNA in Toxoplasma gondii. Mol Biochem Parasitol 2000; 110(1):43–51.

    Article  PubMed  CAS  Google Scholar 

  164. Nakaar V, Ngo HM, Aaronson EP et al. Pleiotropic effect due to targeted depletion of secretory rhoptry protein ROP2 in Toxoplasma gondii. J Cell Sci 2003; 116 (Pt 11):2311–2320.

    Article  PubMed  CAS  Google Scholar 

  165. Nakaar V, Samuel BU, Ngo EO et al. Targeted reduction of nucleoside triphosphate hydrolase by antisense RNA inhibits Toxoplasma gondii proliferation. J Biol Chem 1999; 274(8):5083–5087.

    Article  PubMed  CAS  Google Scholar 

  166. Ngo HM, Yang M, Paprotka K et al. AP-1 in Toxoplasma gondii mediates biogenesis of the rhoptry secretory organelle from a post-Golgi compartment. J Biol Chem 2003; 278(7):5343–5352.

    Article  PubMed  CAS  Google Scholar 

  167. Bermudes D, Peck KR, Afifi MA et al. Tandemly repeated genes encode nucleoside triphosphate hydrolase isoforms secreted into the parasitophorous vacuole of Toxoplasma gondii. J Biol Chem 1994; 269(46):29252–29260.

    PubMed  CAS  Google Scholar 

  168. Gardiner DL, Holt DC, Thomas EA et al. Inhibition of Plasmodium falciparum clag9 gene function by antisense RNA. Mol Biochem Parasitol 2000; 110(1):33–41.

    Article  PubMed  CAS  Google Scholar 

  169. Noonpakdee W, Pothikasikorn J, Nimitsantiwong W et al. Inhibition of Plasmodium falciparum proliferation in vitro by antisense oligodeoxynucleotides against malarial topoisomerase II. Biochem Biophys Res Commun 2003; 302(4):659–664.

    Article  PubMed  CAS  Google Scholar 

  170. Ullu E, Tschudi C, Chakraborty T. RNA interference in protozoan parasites. Cell Microbiol 2004; 6(6):509–519.

    Article  PubMed  CAS  Google Scholar 

  171. Aravind L, Iyer LM, Wellems TE et al. Plasmodium biology: Genomic gleanings. Cell 2003; 115(7):771–785.

    Article  PubMed  CAS  Google Scholar 

  172. McRobert L, McConkey GA. RNA interference (RNAi) inhibits growth of Plasmodium falciparum. Mol Biochem Parasitol 2002; 119(2):273–278.

    Article  PubMed  CAS  Google Scholar 

  173. Malhotra P, Dasaradhi PV, Kumar A et al. Double-stranded RNA-mediated gene silencing of cysteine proteases (falcipain-1 and-2) of Plasmodium falciparum. Mol Microbiol 2002; 45(5):1245–1254.

    Article  PubMed  CAS  Google Scholar 

  174. Mohmmed A, Dasaradhi PV, Bhatnagar RK et al. In vivo gene silencing in Plasmodium berghei—a mouse malaria model. Biochem Biophys Res Commun 2003; 309(3):506–511.

    Article  PubMed  CAS  Google Scholar 

  175. Al-Anouti F, Tomavo S, Parmley S et al. The expression of lactate dehydrogenase is important for the cell cycle of Toxoplasma gondii. J Biol Chem 2004.

    Google Scholar 

  176. Adams B, Musiyenko A, Kumar R et al. A novel class of dual-family immunophilins. J Biol Chem 2005; 280(26):24308–24314.

    Article  PubMed  CAS  Google Scholar 

  177. Sheng J, Al-Anouti F, Ananvoranich S. Engineered delta ribozymes can simultaneously knock down the expression of the genes encoding uracil phosphoribosyltransferase and hypoxanthine-xanthine-guanine phosphoribosyltransferase in Toxoplasma gondii. Int J Parasitol 2004; 34(3):253–263.

    Article  PubMed  CAS  Google Scholar 

  178. Beckers CJ, Wakefield T, Joiner KA. The expression of Toxoplasma proteins in Neospora caninum and the identification of a gene encoding a novel rhoptry protein. Mol Biochem Parasitol 1997; 89(2):209–223.

    Article  PubMed  CAS  Google Scholar 

  179. Kim K, Bulow R, Kampmeier J et al. Conformationally appropriate expression of the Toxoplasma antigen SAG1 (p30) in CHO cells. Infect Immun 1994; 62(1):203–209.

    PubMed  CAS  Google Scholar 

  180. Gardner MJ, Hall N, Fung E et al. Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 2002; 419(6906):498–511.

    Article  PubMed  CAS  Google Scholar 

  181. Withers-Martinez C, Carpenter EP, Hackett F et al. PCR-based gene synthesis as an efficient approach for expression of the A+T-rich malaria genome. Protein Eng 1999; 12(12):1113–1120.

    Article  PubMed  CAS  Google Scholar 

  182. Flick K, Ahuja S, Chene A et al. Optimized expression of Plasmodium falciparum erythrocyte membrane protein 1 domains in Escherichia coli. Malar J 2004; 3(1):50.

    Article  PubMed  CAS  Google Scholar 

  183. Yadava A, Ockenhouse CF. Effect of codon optimization on expression levels of a functionally folded malaria vaccine candidate in prokaryotic and eukaryotic expression systems. Infect Immun 2003; 71(9):4961–4969.

    Article  PubMed  CAS  Google Scholar 

  184. Mehlin C, Boni E, Buckner FS et al. Heterologous expression of proteins from Plasmodium falciparum: Results from 1000 genes. Mol Biochem Parasitol 2006; 148(2):144–160.

    Article  PubMed  CAS  Google Scholar 

  185. Brossier F, David Sibley L. Toxoplasma gondii: Microneme protein MIC2. Int J Biochem Cell Biol 2005; 37(11):2266–2272.

    Article  PubMed  CAS  Google Scholar 

  186. Jewett TJ, Sibley LD. The Toxoplasma proteins MIC2 and M2AP form a hexameric complex necessary for intracellular survival. J Biol Chem 2004; 279(10):9362–9369.

    Article  PubMed  CAS  Google Scholar 

  187. Kappe S, Bruderer T, Gantt S et al. Conservation of a gliding motility and cell invasion machinery in Apicomplexan parasites. J Cell Biol 1999; 147(5):937–944.

    Article  PubMed  CAS  Google Scholar 

  188. O’Connor RM, Kim K, Khan F et al. Expression of Cpgp40/15 in Toxoplasma gondii: A surrogate system for the study of Cryptosporidium glycoprotein antigens. Infect Immun 2003; 71(10):6027–6034.

    Article  PubMed  CAS  Google Scholar 

  189. Triglia T, Healer J, Caruana SR et al. Apical membrane antigen 1 plays a central role in erythrocyte invasion by Plasmodium species. Mol Microbiol 2000; 38(4):706–718.

    Article  PubMed  CAS  Google Scholar 

  190. Tewari R, Rathore D, Crisanti A. Motility and infectivity of Plasmodium berghei sporozoites expressing avian Plasmodium gallinaceum circumsporozoite protein. Cell Microbiol 2005; 7(5):699–707.

    Article  PubMed  CAS  Google Scholar 

  191. Chitnis CE, Miller LH. Identification of the erythrocyte binding domains of Plasmodium vivax and Plasmodium knowlesi proteins involved in erythrocyte invasion. J Exp Med 1994; 180(2):497–506.

    Article  PubMed  CAS  Google Scholar 

  192. Chattopadhyay R, Taneja T, Chakrabarti K et al. Molecular analysis of the cytoadherence phenotype of a Plasmodium falciparum field isolate that binds intercellular adhesion molecule-1. Mol Biochem Parasitol 2004; 133(2):255–265.

    Article  PubMed  CAS  Google Scholar 

  193. Sim BK, Chitnis CE, Wasniowska K et al. Receptor and ligand domains for invasion of erythrocytes by Plasmodium falciparum. Science 1994; 264(5167):1941–1944.

    Article  PubMed  CAS  Google Scholar 

  194. Ward GE, Chitnis CE, Miller LH. The invasion of erythrocytes by malarial merozoites. In: Russell DG, ed. Clinical Infectious Diseases: International Practice and Research, Strategies for Intracellular Survival of Microbes. 1st ed. London: Bailliere Tindall, 1994:155–190.

    Google Scholar 

  195. Saouros S, Edwards-Jones B, Reiss M et al. A novel galectin-like domain from Toxoplasma gondii micronemal protein 1 assists the folding, assembly, and transport of a cell adhesion complex. J Biol Chem 2005; 280(46):38583–38591.

    Article  PubMed  CAS  Google Scholar 

  196. Kato K, Mayer DC, Singh S et al. Domain III of Plasmodium falciparum apical membrane antigen 1 binds to the erythrocyte membrane protein Kx. Proc Natl Acad Sci USA 2005; 102(15):5552–5557.

    Article  PubMed  CAS  Google Scholar 

  197. Grimwood J, Smith JE. Toxoplasma gondii: The role of a 30-kDa surface protein in host cell invasion. Exp Parasitol 1992; 74(1):106–111.

    Article  PubMed  CAS  Google Scholar 

  198. Grimwood J, Smith JE. Toxoplasma gondii: The role of parasite surface and secreted proteins in host cell invasion. Int J Parasitol 1996; 26(2):169–173.

    Article  PubMed  CAS  Google Scholar 

  199. Mineo JR, McLeod R, Mack D et al. Antibodies to Toxoplasma gondii major surface protein (SAG-1, P30) inhibit infection of host cells and are produced in murine intestine after peroral infection. J Immunol 1993; 150(9):3951–3964.

    PubMed  CAS  Google Scholar 

  200. Uchida Y, Ike K, Kurotaki T et al. Monoclonal antibodies preventing invasion of Neospora caninum tachyzoites into host cells. J Vet Med Sci 2004; 66(11):1355–1358.

    Article  PubMed  Google Scholar 

  201. Augustine PC, Jenkins MC, Dubey JP. Effect of polyclonal antisera developed against dense granule-associated Neospora caninum proteins on cell invasion and development in vitro by N. caninum tachyzoites. Parasitology 1999; 119 (Pt 5):441–445.

    Article  PubMed  Google Scholar 

  202. Augustine PC. Reduced invasion of cultured cells pretreated with a monoclonal antibody elicited against refractile body antigens of avian coccidial sporozoites. J Eukaryot Microbiol 1999; 46(3):254–258.

    Article  PubMed  CAS  Google Scholar 

  203. 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 

  204. Singh AP, Puri SK, Chitnis CE. Antibodies raised against receptor-binding domain of Plasmodium knowlesi Duffy binding protein inhibit erythrocyte invasion. Mol Biochem Parasitol 2002; 121(1):21–31.

    Article  PubMed  CAS  Google Scholar 

  205. Mitchell GH, Thomas AW, Margos G et al. Apical membrane antigen 1, a major malaria vaccine candidate, mediates the close attachment of invasive merozoites to host red blood cells. Infect Immun 2004; 72(1):154–158.

    Article  PubMed  CAS  Google Scholar 

  206. Ramasamy R, Ramasamy M, Yasawardena S. Antibodies and Plasmodium falciparum merozoites. Trends Parasitol 2001; 17(4):194–197.

    Article  PubMed  CAS  Google Scholar 

  207. 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 

  208. 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 

  209. Ryning FW, Remington JS. Effect of cytochalasin D on Toxoplasma gondii cell entry. Infect Immun 1978; 20(3):739–743.

    PubMed  CAS  Google Scholar 

  210. Schwartzman JD, Pfefferkorn ER. Immunofluorescent localization of myosin at the anterior pole of the coccidian, Toxoplasma gondii. J Protozool 1983; 30(4):657–661.

    PubMed  CAS  Google Scholar 

  211. Carruthers VB, Sibley LD. Mobilization of intracellular calcium stimulates microneme discharge in Toxoplasma gondii. Mol Microbiol 1999; 31(2):421–428.

    Article  PubMed  CAS  Google Scholar 

  212. Ward GE, Carey KL, Westwood NJ. Using small molecules to study big questions in cellular microbiology. Cell Microbiol 2002; 4(8):471–482.

    Article  PubMed  CAS  Google Scholar 

  213. Morgan RE, Evans KM, Patterson S et al. Targeting invasion and egress: From tools to drugs? Current Drug Targets 2006, (In Press).

    Google Scholar 

  214. Mayer TU. Chemical genetics: Tailoring tools for cell biology. Trends Cell Biol 2003; 13(5):270–277.

    Article  PubMed  CAS  Google Scholar 

  215. Stockwell BR. Chemical genetics: Ligand-based discovery of gene function. Nat Rev Genet 2000; 1(2):116–125.

    Article  PubMed  CAS  Google Scholar 

  216. Asai T, Takeuchi T, Diffenderfer J et al. Identification of small-molecule inhibitors of nucleoside triphosphate hydrolase in Toxoplasma gondii. Antimicrob Agents Chemother 2002; 46(8):2393–2399.

    Article  PubMed  CAS  Google Scholar 

  217. Baldwin J, Michnoff CH, Malmquist NA et al. High-throughput screening for potent and selective inhibitors of Plasmodium falciparum dihydroorotate dehydrogenase. J Biol Chem 2005; 280(23):21847–21853.

    Article  PubMed  CAS  Google Scholar 

  218. Carruthers VB, Hakansson S, Giddings OK et al. Toxoplasma gondii uses sulfated proteoglycans for substrate and host cell attachment. Infect Immun 2000; 68(7):4005–4011.

    Article  PubMed  CAS  Google Scholar 

  219. Ortega-Barria E, Boothroyd JC. A Toxoplasma lectin-like activity specific for sulfated polysaccharides is involved in host cell infection. J Biol Chem 1999; 274(3):1267–1276.

    Article  PubMed  CAS  Google Scholar 

  220. Grimwood J, Mineo JR, Kasper LH. Attachment of Toxoplasma gondii to host cells is host cell cycle dependent. Infect Immun 1996; 64(10):4099–4104.

    PubMed  CAS  Google Scholar 

  221. Dvorak JA, Crane MS. Vertebrate cell cycle modulates infection by protozoan parasites. Science 1981; 214(4524):1034–1036.

    Article  PubMed  CAS  Google Scholar 

  222. Dutta C, Grimwood J, Kasper LH. Attachment of Toxoplasma gondii to a specific membrane fraction of CHO cells. Infect Immun 2000; 68(12):7198–7201.

    Article  PubMed  CAS  Google Scholar 

  223. Miller LH, Mason SJ, Dvorak JA et al. Erythrocyte receptors for (Plasmodium knowlesi) malaria: Duffy blood group determinants. Science 1975; 189(4202):561–563.

    Article  PubMed  CAS  Google Scholar 

  224. Su XZ, Heatwole VM, Wertheimer SP et al. The large diverse gene family var encodes proteins involved in cytoadherence and antigenic variation of Plasmodium falciparum-infected erythrocytes. Cell 1995; 82(1):89–100.

    Article  PubMed  CAS  Google Scholar 

  225. Miller LH, Haynes JD, McAuliffe FM et al. Evidence for differences in erythrocyte surface receptors for the malarial parasites, Plasmodium falciparum and Plasmodium knowlesi. J Exp Med 1977; 146(1):277–281.

    Article  PubMed  CAS  Google Scholar 

  226. Kaneko O, Fidock DA, Schwartz OM et al. Disruption of the C-terminal region of EBA-175 in the Dd2/Nm clone of Plasmodium falciparum does not affect erythrocyte invasion. Mol Biochem Parasitol 2000; 110(1):135–146.

    Article  PubMed  CAS  Google Scholar 

  227. Klotz FW, Orlandi PA, Reuter G et al. Binding of Plasmodium falciparum 175-kilodalton erythrocyte binding antigen and invasion of murine erythrocytes requires N-acetylneuraminic acid but not its O-acetylated form. Mol Biochem Parasitol 1992; 51(1):49–54.

    Article  PubMed  CAS  Google Scholar 

  228. Gaur D, Mayer DC, Miller LH. Parasite ligand-host receptor interactions during invasion of erythrocytes by Plasmodium merozoites. Int J Parasitol 2004; 34(13–14):1413–1429.

    Article  PubMed  CAS  Google Scholar 

  229. 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 

  230. 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 

  231. 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 

  232. 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 

  233. 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 

  234. 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 

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

    Article  PubMed  CAS  Google Scholar 

  236. Cleary MD, Singh U, Blader IJ et al. Toxoplasma gondii asexual development: Identification of developmentally regulated genes and distinct patterns of gene expression. Eukaryotic Cell 2002; 1(3):329–340.

    Article  PubMed  CAS  Google Scholar 

  237. Cleary MD, Meiering CD, Jan E et al. Biosynthetic labeling of RNA with uracil phosphoribosyltransferase allows cell-specific microarray analysis of mRNA synthesis and decay. Nat Biotechnol 2005; 23(2):232–237.

    Article  PubMed  CAS  Google Scholar 

  238. Kappe SH, Gardner MJ, Brown SM et al. Exploring the transcriptome of the malaria sporozoite stage. Proc Natl Acad Sci USA 2001; 98(17):9895–9900.

    Article  PubMed  CAS  Google Scholar 

  239. Le Roch KG, Zhou Y, Blair PL et al. Discovery of gene function by expression profiling of the malaria parasite life cycle. Science 2003; 301(5639):1503–1508.

    Article  PubMed  Google Scholar 

  240. Bozdech Z, Llinas M, Pulliam BL et al. The transcriptome of the intraerythrocytic developmental cycle of Plasmodium falciparum. PLoS Biol 2003; 1(1):E5.

    Article  PubMed  Google Scholar 

  241. Blader IJ, Manger ID, Boothroyd JC. Microarray analysis reveals previously unknown changes in Toxoplasma gondii-infected human cells. J Biol Chem 2001; 276(26):24223–24231.

    Article  PubMed  CAS  Google Scholar 

  242. Bishop R, Shah T, Pelle R et al. Analysis of the transcriptome of the protozoan Theileria parva using MPSS reveals that the majority of genes are transcriptionally active in the schizont stage. Nucleic Acids Res 2005; 33(17):5503–5511.

    Article  PubMed  CAS  Google Scholar 

  243. Bradley PJ, Ward C, Cheng SJ et al. Proteomic analysis of rhoptry organelles reveals many novel constituents for host-parasite interactions in Toxoplasma gondii. J Biol Chem 2005; 280(40):34245–34258.

    Article  PubMed  CAS  Google Scholar 

  244. Zhou XW, Kafsack BF, Cole RN et al. The opportunistic pathogen Toxoplasma gondii deploys a diverse legion of invasion and survival proteins. J Biol Chem 2005; 280(40):34233–34244.

    Article  PubMed  CAS  Google Scholar 

  245. Bromley E, Leeds N, Clark J et al. Defining the protein repertoire of microneme secretory organelles in the apicomplexan parasite Eimeria tenella. Proteomics 2003; 3(8):1553–1561.

    Article  PubMed  CAS  Google Scholar 

  246. Gilson PR, Nebl T, Vukcevic D et al. Identification and stoichiometry of glycosylphosphatidylinositol-anchored membrane proteins of the human malaria parasite Plasmodium falciparum. Mol Cell Proteomics 2006; 5(7):1286–1299.

    Article  PubMed  CAS  Google Scholar 

  247. Thomas AW, Deans JA, Mitchell GH et al. The Fab fragments of monoclonal IgG to a merozoite surface antigen inhibit Plasmodium knowlesi invasion of erythrocytes. Mol Biochem Parasitol 1984; 13(2):187–199.

    Article  PubMed  CAS  Google Scholar 

  248. Deans JA. Protective antigens of bloodstage Plasmodium knowlesi parasites. Philos Trans R Soc Lond B Biol Sci 1984; 307(1131):159–169.

    Article  PubMed  CAS  Google Scholar 

  249. Li F, Dluzewski A, Coley AM et al. Phage-displayed peptides bind to the malarial protein apical membrane antigen-1 and inhibit the merozoite invasion of host erythrocytes. J Biol Chem 2002; 277(52):50303–50310.

    Article  PubMed  CAS  Google Scholar 

  250. Keizer DW, Miles LA, Li F et al. Structures of phage-display peptides that bind to the malarial surface protein, apical membrane antigen 1, and block erythrocyte invasion. Biochemistry 2003; 42(33):9915–9923.

    Article  PubMed  CAS  Google Scholar 

  251. Donahue CG, Carruthers VB, Gilk SD et al. 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 2000; 111(1):15–30.

    Article  PubMed  CAS  Google Scholar 

  252. Gurnett AM, Liberator PA, Dulski PM et al. Purification and molecular characterization of cGMP-dependent protein kinase from Apicomplexan parasites: A novel chemotherapeutic target. J Biol Chem 2002; 277(18):15913–15922.

    Article  PubMed  CAS  Google Scholar 

  253. Trager W, Zung J, Tershakovec M. Initial extracellular development in vitro of erythrocytic stages of malaria parasites (Plasmodium falciparum). Proc Natl Acad Sci USA 1990; 87(15):5618–5622.

    Article  PubMed  CAS  Google Scholar 

  254. Tomley FM, Soldati DS. Mix and match modules: Structure and function of microneme proteins in apicomplexan parasites. Trends Parasitol 2001; 17(2):81–88.

    Article  PubMed  CAS  Google Scholar 

  255. Kim K, Weiss LM. Toxoplasma gondii: The model apicomplexan. Int J Parasitol 2004; 34(3):423–432.

    Article  PubMed  CAS  Google Scholar 

  256. Di Cristina M, Ghouze F, Kocken CH et al. Transformed Toxoplasma gondii tachyzoites expressing the circumsporozoite protein of Plasmodium knowlesi elicit a specific immune response in rhesus monkeys. Infect Immun 1999; 67(4):1677–1682.

    PubMed  Google Scholar 

  257. Charest H, Sedegah M, Yap GS et al. Recombinant attenuated Toxoplasma gondii expressing the Plasmodium yoelii circumsporozoite protein provides highly effective priming for CD8+ T cell-dependent protective immunity against malaria. J Immunol 2000; 165(4):2084–2092.

    PubMed  CAS  Google Scholar 

  258. Kenny B, DeVinney R, Stein M et al. Enteropathogenic E. coli (EPEC) transfers its receptor for intimate adherence into mammalian cells. Cell 1997; 91(4):511–520.

    Article  PubMed  CAS  Google Scholar 

  259. Hu K, Johnson J, Florens L et al. Cytoskeletal components of an invasion machine-the apical complex of Toxoplasma gondii. PLoS Pathog 2006; 2(2):e13.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Microbiology and Molecular Genetics, University of Vermont, Burlington, VT, 05405, USA

    Jeffrey Mital & Gary E. Ward

Authors
  1. Jeffrey Mital
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Gary E. Ward
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Gary E. Ward .

Editor information

Editors and Affiliations

  1. Department of Immunology and Infectious Diseases, Harvard School of Public Health, Boston, Massachusetts, USA

    Barbara A. Burleigh PhD

  2. Department of Biological Sciences, Imperial College, London, UK

    Dominique Soldati-Favre PhD

  3. Département de Microbiologie et Medecine Moléculaire, Université de Genève, Geneve, Switzerland

    Dominique Soldati-Favre PhD

Rights and permissions

Reprints and permissions

Copyright information

© 2008 Landes Bioscience and Springer Science+Business Media

About this chapter

Cite this chapter

Mital, J., Ward, G.E. (2008). Current and Emerging Approaches to Studying Invasion in Apicomplexan Parasites. 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_1

Download citation

Publish with us

Policies and ethics

Search

Navigation