Biogenesis of and Activities at the Toxoplasma gondii Parasitophorous Vacuole Membrane

  • Anthony P. Sinai
Part of the Subcellular Biochemistry book series (SCBI, volume 47)


Apicomplexan parasites like Toxoplasma gondii are distinctive in their utilization of para site encoded motor systems to invade cells. Invasion results in the establishment of the parasitophorous vacuole (PV) within the infected cell. Most apicomplexans complete their intracellular tenure within the infected cell in the PV that is demarcated from the host cytoplasm by the parasitophorous vacuole membrane (PVM). In this chapter I focus on the events surrounding the formation of the PVM and selected activities attributed to it. Its central role as the interface between the parasite and its immediate environment, the host cytoplasm, is validated by the diversity of functions attributed to it. While functions in structural organization, nutrient acquisitions and signaling have been defined their molecular bases remain largely unknown. Several recent studies and the decoding of the Toxoplasma genome have set the stage for a rapid expansion in our understanding of the role of the PVM in parasite biology.

Toxoplasma gondii, like all apicomplexan parasites are obligate intracellular pathogens. This family of parasites utilize their own actin-myosin based motor systems to gain entry into susceptible cells1 establishing themselves, in some cases transiently (e.g., Theileria spp 2) in specialized vacuolar compartment, the parasitophorous vacuole (PV). The T. gondii PV is highly dynamic compartment defining the replication permissive niche for the parasite.3 The delimiting membrane defining the parasitophorous vacuole, the parasitophorous vacuole membrane or PVM is increasingly being recognized as a specialized “organelle” that in the context of the infected cell is extracorporeal to the parent organism, the parasite. A systematic study of this enigmatic organelle has been severely limited by several issues. Primary among these is the fact that it is formed only in the context of the infected cell thereby limiting the amount of material. Secondly, unlike other cellular organelles that can often be purified by conventional approaches, the PVM, cannot be purified away from host cell organelles4 (see below). In spite of these significant obstacles considerable progress has been made in recent years toward understanding the biogenesis of the PVM, identification of its protein complement and the characterization of activities within it. These studies demonstrate that the PVM, on its own and by virtue of its interactions with cellular components, plays critical functions in the structural integrity of the vacuole, nutrient acquisition and the manipulation of cellular functions.3,5 In addition it appears that the repertoire of activities at the PVM is likely to be plastic reflecting temporal changes associated with the replicative phase of parasite growth.5 Finally, the PVM likely forms the foundation for the cyst wall as the parasite differentiates in the establishment of latent infection.6 As the critical border crossing between the parasite and invaded cell the study of the PVM provides a fertile area for new investigation aided by the recent decoding of the Toxoplasma genome (available at and the application of proteomic analyses7, 8, 9 to basic questions in parasite biology.


Dense Granule Toxoplasma Gondii Parasitophorous Vacuole Host Plasma Membrane Host Cell Invasion 
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  1. 1.
    Dobrowolski JM, Sibley LD. Toxoplasma invasion of mammalian cells is powered by the actin cytoskeleton. Cell 1996; 84:933–939.PubMedCrossRefGoogle Scholar
  2. 2.
    Shaw MK. The same but different: The biology of Theileria sporozoite entry into bovine cells. Int J Parasitol 1997; 27(5):457–474.PubMedCrossRefGoogle Scholar
  3. 3.
    Sinai AP, Joiner KA. Safe haven: The cell biology of nonfusogenic pathogen vacuoles. Annu Rev Microbiol 1997; 51:415–462.PubMedCrossRefGoogle Scholar
  4. 4.
    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; 110:2117–2128.PubMedGoogle Scholar
  5. 5.
    Lingelbach K, Joiner K. The parasitophorous vacuole membrane surrounding Plasmodium and Toxoplasma: An unusual compartment in infected cells. J Cell Sci 1998; 111:1467–1475.PubMedGoogle Scholar
  6. 6.
    Weiss LM, Kim K. The development and biology of bradyzoites of Toxoplasma gondii. Front Biosci 2000; 5:D391–405.PubMedCrossRefGoogle Scholar
  7. 7.
    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.PubMedCrossRefGoogle Scholar
  8. 8.
    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.PubMedCrossRefGoogle Scholar
  9. 9.
    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.PubMedCrossRefGoogle Scholar
  10. 10.
    Jutras I, Desjardins M. Phagocytosis: At the crossroads of innate and adaptive immunity. Annu Rev Cell Dev Biol 2005; 21:511–527.PubMedCrossRefGoogle Scholar
  11. 11.
    Desjardins M, Huber L, Parton R et al. Biogenesis of phagolysosomes proceeds through a sequential series of interactions with the endocytic apparatus. J Cell Biol 1994; 124:677–688.PubMedCrossRefGoogle Scholar
  12. 12.
    Carruthers VB. Host cell invasion by the opportunistic pathogen Toxoplasma gondii. Acta Trop 2002; 81(2):111–122.PubMedCrossRefGoogle Scholar
  13. 13.
    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.PubMedCrossRefGoogle Scholar
  14. 14.
    Nichols BA, Chiappino ML, O’Connor GR. Secretion from the rhoptries of Toxoplasma gondii during host-cell invasion. J Ultrastruct Res 1983; 83:85–98.PubMedCrossRefGoogle Scholar
  15. 15.
    Coppens I, Joiner KA. Host but not parasite cholesterol controls Toxoplasma cell entry by modulating organelle discharge. Mol Biol Cell 2003; 14(9):3804–3820.PubMedCrossRefGoogle Scholar
  16. 16.
    Porchet-Hennere E, Vivier E, Torpier G. Origine des membranes de la paroi chez Toxoplasma. Annales de parasitologie humaine et compar 1985; 60:101–110.Google Scholar
  17. 17.
    Porchet-Hennere EGT. Relations entre Toxoplasma et sa cellule-hote. Protistologica 1983; 19:357–370.Google Scholar
  18. 18.
    Mordue DG, Desai N, Dustin M et al. Invasion by Toxoplasma gondii establishes a moving junction that selectively excludes host cell plasma membrane proteins on the basis of their membrane anchoring. J Exp Med 1999; 190(12):1783–1792.PubMedCrossRefGoogle Scholar
  19. 19.
    Charron AJ, Sibley LD. Molecular partitioning during host cell penetration by Toxoplasma gondii. Traffic 2004; 5(11):855–867.PubMedCrossRefGoogle Scholar
  20. 20.
    Aikawa M, Miller LH, Johnson J et al. Erythrocyte entry by malaria parasites: A moving junction between erythrocyte and parasite. J Cell Biol 1978; 77:77–82.CrossRefGoogle Scholar
  21. 21.
    Michel R, Schupp S, Raether W et al. Formation of a close junction during invasion of eythrocytes by Toxoplasma gondii in vitro. Int J Parasitol 1980; 10:309–313.PubMedCrossRefGoogle Scholar
  22. 22.
    Aikawa M, Komata Y, Asai T et al. Transmission and scanning electron microscopy of host cell entry by Toxoplasma. Am J Pathol 1977; 87:285–296.PubMedGoogle Scholar
  23. 23.
    Nichols BA, O’Connor GR. Penetration of mouse peritoneal macrophages by the protozoon Toxoplasma gondii. Lab Invest 1981; 44:324–334.PubMedGoogle Scholar
  24. 24.
    de Souza W. Microscopy and cytochemistry of the biogenesis of the parasitophorous vacuole. Histochem Cell Biol 2005; 123(1):1–18.PubMedCrossRefGoogle Scholar
  25. 25.
    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 1996; 93:8413–8418.PubMedCrossRefGoogle Scholar
  26. 26.
    Dubremetz JF, C R, Ferreira E. Toxoplasma gondii: Redistribution of monoclonal antibodies on tachyzoites during host cell invasion. Exp Parasitol 1985; 59:24–32.PubMedCrossRefGoogle Scholar
  27. 27.
    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.PubMedCrossRefGoogle Scholar
  28. 28.
    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.PubMedCrossRefGoogle Scholar
  29. 29.
    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.PubMedCrossRefGoogle Scholar
  30. 30.
    Coppens I, Vielemeyer O. Insights into unique physiological features of neutral lipids in Apicomplexa: From storage to potential mediation in parasite metabolic activities. Int J Parasitol 2005; 35(6):597–615.PubMedCrossRefGoogle Scholar
  31. 31.
    Foussard F, Leriche MA, Dubremetz JF. Characterization of the lipid content of Toxoplasma gondii rhoptries. Parasitology 1991; 102:367–370.PubMedCrossRefGoogle Scholar
  32. 32.
    Carruthers VB. Armed and dangerous: Toxoplasma gondii uses an arsenal of secretory proteins to infect host cells. Parasitol Int 1999; 48(1):1–10.PubMedCrossRefGoogle Scholar
  33. 33.
    Carruthers V, Sibley L. Sequential protein secretion from three distinct organelles of Toxoplasma gondii accompanies invasion of human fibroblasts. Eur J Cell Biol 1997; 73:114–123.PubMedGoogle Scholar
  34. 34.
    Dubremetz JF, Achbarou A, Bermudes D et al. Kinetics of apical organelle exocytosis during Toxoplasma gondii host cell interaction. Parasitol Res 1993; 79:402–408.PubMedCrossRefGoogle Scholar
  35. 35.
    Ossorio PN, Schwartzman JD, Boothroyd JC. A Toxoplasma gondii rhoptry protein associated with host cell penetration has unusual charge assymetry. Mol Biochem Parasitol 1992; 50:1–16.PubMedCrossRefGoogle Scholar
  36. 36.
    Beckers CJM, Dubremetz JF, Mercereau-Puijalon O et al. The Toxoplasma gondii rhoptry protein ROP2 is inserted into the parasitophorous vacuole membrane, surrounding the intracellular parasite, and is exposed to the host cell cytoplasm. J Cell Biol 1994; 127:947–961.PubMedCrossRefGoogle Scholar
  37. 37.
    Sibley LD, Krahenbuhl JL, Adams GMW et al. Toxoplasma modifies macrophage phagosomes by secretion of a vesicular network rich in surface proteins. J Cell Biol 1986; 103:867–874.PubMedCrossRefGoogle Scholar
  38. 38.
    Bermudes D, Dubremetz JF, Joiner KA. Molecular characterization of the dense granule protein GRA3 from Toxoplasma gondii. Mol Biochem Parasit 1994; 68:247–257.CrossRefGoogle Scholar
  39. 39.
    Henriquez FL, Nickdel MB, McLeod R et al. Toxoplasma gondii dense granule protein 3 (GRA3) is a type I transmembrane protein that possesses a cytoplasmic dilysine (KKXX) endoplasmic reticulum (ER) retrieval motif. Parasitology 2005; 131 (Pt 2):169–179.PubMedCrossRefGoogle Scholar
  40. 40.
    Ahn HJ, Kim S, Nam HW. Host cell binding of GRA10, a novel, constitutively secreted dense granular protein from Toxoplasma gondii. Biochem Biophys Res Commun 2005; 331(2):614–620.PubMedCrossRefGoogle Scholar
  41. 41.
    Lecordier L, Mercier C, Sibley LD et al. Transmembrane insertion of the Toxoplasma gondii GRA5 protein occurs after soluble secretion into the host cell. Mol Biol Cell 1999; 10(4):1277–1287.PubMedGoogle Scholar
  42. 42.
    Jacobs D, Dubremetz JF, Loyens A et al. Identification and heterologous expression of a new dense granule protein (GRA7) from Toxoplasma gondii. Molec Biochem Parasitol 1998; 91:237–249.CrossRefGoogle Scholar
  43. 43.
    Carey KL, Donahue CG, Ward GE. Identification and molecular characterization of GRA8, a novel, prolinerich, dense granule protein of Toxoplasma gondii. Mol Biochem Parasitol 2000; 105(1):25–37.PubMedCrossRefGoogle Scholar
  44. 44.
    Adjogble KD, Mercier C, Dubremetz JF et al. GRA9, a new Toxoplasma gondii dense granule protein associated with the intravacuolar network of tubular membranes. Int J Parasitol 2004; 34(11):1255–1264.PubMedCrossRefGoogle Scholar
  45. 45.
    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.PubMedCrossRefGoogle Scholar
  46. 46.
    Karsten V, Qi H, Beckers CJM et al. The protozoan parasite Toxoplasma gondii targets proteins to dense granules and vacuolar space using both conserved and unusual mechanisms. J Cell Biol 1998; 141:911–914.CrossRefGoogle Scholar
  47. 47.
    Tomavo S, Fortier B, Soete M et al. Characterization of bradyzoite-specific antigens of Toxoplasma gondii. Infect Immun 1991; 59:3750–3753.PubMedGoogle Scholar
  48. 48.
    Zhang YW, Halonen SK, Ma YF et al. Initial characterization of CST1, a Toxoplasma gondii cyst wall glycoprotein. Infect Immun 2001; 69(1):501–507.PubMedCrossRefGoogle Scholar
  49. 49.
    Magno RC, Lemgruber L, Vommaro RC et al. Intravacuolar network may act as a mechanical support for Toxoplasma gondii inside the parasitophorous vacuole. Microsc Res Tech 2005; 67(1):45–52.PubMedCrossRefGoogle Scholar
  50. 50.
    Sibley LD, Niesman IR, Parmley SF et al. Regulated secretion of multi-lamellar vesicles leads to formation of a tubulo-vesicular network in host-cell vacuoles occupied by Toxoplasma gondii. J Cell Sci 1995; 108:1669–1677.PubMedGoogle Scholar
  51. 51.
    Labruyere E, Lingnau M, Mercier C et al. Differential membrane targeting of the secretory proteins GRA4 and GRA6 within the parasitophorous vacuole formed by Toxoplasma gondii. Mol Biochem Parasitol 1999; 102(2):311–324.PubMedCrossRefGoogle Scholar
  52. 52.
    Mercier C, Cesbron-Delauw MF, Sibley LD. The amphipathic alpha helices of the toxoplasma protein GRA2 mediate post-secretory membrane association. J Cell Sci 1998; 111 (Pt 15):2171–2180.PubMedGoogle Scholar
  53. 53.
    Lecordier L, Meleon-Borodowski I, Dubremetz JF et al. Characterization of a dense granule antigen of Toxoplasma gondii (GRA6) associated to the network of the parasitophorous vacuole. Mol Biochem Parasitol 1995; 70:85–94.PubMedCrossRefGoogle Scholar
  54. 54.
    Mercier C, Lecordier L, Darcy F et al. Molecular characterization of a dense granule antigen (GRA2) associated with the network of the parasitophorous vacuole in Toxoplasma gondii. Mol Biochem Parasitol 1993; 58:71–82.PubMedCrossRefGoogle Scholar
  55. 55.
    Schatten H, Ris H. Three-dimensional imaging of Toxoplasma gondii-host cell interactions within the parasitophorous vacuole. Microsc Microanal 2004; 10(5):580–585.PubMedCrossRefGoogle Scholar
  56. 56.
    Schatten H, Ris H. Unconventional specimen preparation techniques using high resolution low voltage field emission scanning electron microscopy to study cell motility, host cell invasion, and internal cell structures in Toxoplasma gondii. Microsc Microanal 2002; 8(2):94–103.PubMedCrossRefGoogle Scholar
  57. 57.
    Coppens I, Dunn JD, Romano JD et al. Toxoplasma gondii sequesters lysosomes from mammalian hosts in the vacuolar space. Cell 2006; 125(2):261–274.PubMedCrossRefGoogle Scholar
  58. 58.
    Magno RC, Straker LC, de Souza W et al. Interrelations between the parasitophorous vacuole of Toxoplasma gondii and host cell organelles. Microsc Microanal 2005; 11(2):166–174.PubMedCrossRefGoogle Scholar
  59. 59.
    Melo EJ, de Souza W. Relationship between the host cell endoplasmic reticulum and the parasitophorous vacuole containing Toxoplasma gondii. Cell Struct Funct 1997; 22(3):317–323.PubMedGoogle Scholar
  60. 60.
    de Melo EJ, de Carvalho TU, de Souza W. Penetration of Toxoplasma gondii into host cells induces changes in the distribution of the mitochondria and the endoplasmic reticulum. Cell Struct Funct 1992; 17(5):311–317.PubMedGoogle Scholar
  61. 61.
    Sehgal A, Bettiol S, Pypaert M et al. Peculiarities of host cholesterol transport to the unique intra-cellular vacuole containing toxoplasma. Traffic 2005; 6(12):1125–1141.PubMedCrossRefGoogle Scholar
  62. 62.
    Andrade EF, Stumbo AC, Monteiro-Leal LH et al. Do microtubules around the Toxoplasma gondii-containing parasitophorous vacuole in skeletal muscle cells form a barrier for the phagolysosomal fusion? J Submicrosc Cytol Pathol 2001; 33(3):337–341.PubMedGoogle Scholar
  63. 63.
    Melo EJ, Carvalho TM, De Souza W. Behaviour of microtubules in cells infected with Toxoplasma gondii. Biocell 2001; 25(1):53–59.PubMedGoogle Scholar
  64. 64.
    Halonen SK, Weidner E. Overcoating of Toxoplasma parasitophorous vacuoles with host cell vimentin type intermediate filaments. J Euk Microbiol 1994; 41:65–71.PubMedCrossRefGoogle Scholar
  65. 65.
    Cintra WM, De Souza W. Immunocytochemical localization of cytoskeletal proteins and electron microscopy of detergent extracted tachyzoites of Toxoplasma gondii. J Submicrosc Cytol 1985; 17(4):503–508.PubMedGoogle Scholar
  66. 66.
    Sinai AP, Joiner KA. The Toxoplasma gondii protein ROP2 mediates host organelle association with the parasitophorous vacuole membrane. J Cell Biol 2001; 154(1):95–108.PubMedCrossRefGoogle Scholar
  67. 67.
    Sadak A, Taghy Z, Fortier B et al. Characterization of a family of rhoptry proteins of Toxoplasma gondii. Mol Biochem Parasitol 1988; 29:203–211.PubMedCrossRefGoogle Scholar
  68. 68.
    Horwich AL, Kalouse F, Mellmann I et al. A leader peptide is sufficient to direct mitochondrial import of a chimeric protein. EMBO J 1985; 4:1129–1135.PubMedGoogle Scholar
  69. 69.
    von Heijne G. Protein targeting signals. Curr Opin Cell Biol 1990; 2:604–608.CrossRefGoogle Scholar
  70. 70.
    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; H6 (Pt 11):2311–2320.CrossRefGoogle Scholar
  71. 71.
    Jones TC, Veh S, Hirsch JG. The interaction between Toxoplasma gondii and mammalian cells. I. Mechanism of entry and intracelluar fate of the parasite. J Exp Med 1972; 136:1157–1172.PubMedCrossRefGoogle Scholar
  72. 72.
    Jones TC, Hirsch JG. The interaction between Toxoplasma gondii and mammalian cells. II. The absence of lysosomal fusion with phagocytic vacuoles containing living parasites. J Exp Med 1972; 136:1173.PubMedCrossRefGoogle Scholar
  73. 73.
    De Carvalho L, deSouza W. Cytochemical localization of plasma membrane enzyme markers during interiorization of tachyzoites of Toxoplasma gondii by macrophages. J Protozol 1989; 36:164–170.Google Scholar
  74. 74.
    Joiner KA, Fuhrman SA, Mietinnen H et al. Toxoplasma gondii: Fusion competence of parasitophorous vacuoles in Fc receptor transfected fibroblasts. Science 1990; 249:641–646.PubMedCrossRefGoogle Scholar
  75. 75.
    Mordue D, Sibley L. Intracellular fate of vacuoles containing Toxoplasma gondii is determined at the time of formation and depends on the mechanism of entry. J immunol 1997; 159:4452–4459.PubMedGoogle Scholar
  76. 76.
    DeMelo EJT, Souza WD. Pathway for C6-NBD-ceramide on the host cell infected with Toxoplasma gondii. Cell Struct Funct 1996; 21:47–52.CrossRefGoogle Scholar
  77. 77.
    Sibley LD, Weidner E, Krahenbuhl JL. Phagosome acidification blocked by intracellular Toxoplasma gondii. Nature 1985; 315:416–419.PubMedCrossRefGoogle Scholar
  78. 78.
    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.PubMedCrossRefGoogle Scholar
  79. 79.
    Coppens I, Sinai AP, Joiner KA. Toxoplasma gondii exploits host low-density lipoprotein receptor-mediated endocytosis for cholesterol acquisition. J Cell Biol 2000; 149(1):167–180.PubMedCrossRefGoogle Scholar
  80. 80.
    Morris MT, Coppin A, Tomavo S et al. Functional analysis of Toxoplasma gondii protease inhibitor 1. J Biol Chem 2002; 277(47):45259–45266.PubMedCrossRefGoogle Scholar
  81. 81.
    Schwab JC, Beckers CJM, Joiner KA. The parasitophorous vacuole membrane surrounding intracellular Toxoplasma gondii functions as a molecular sieve. Proc Natl Acad Sci 1994; 91:509–513.PubMedCrossRefGoogle Scholar
  82. 82.
    Vance JE, Shiao YI. Intracellular trafficking of phospholipids: Import of phosphatidylserine into mitochondria. Anticancer Res 1996; 16:1333–1340.PubMedGoogle Scholar
  83. 83.
    Vance JE, Vance DE. Phospholipid biosynthesis in mammalian cells. Biochem Cell Biol 2004; 82(1):113–128.PubMedCrossRefGoogle Scholar
  84. 84.
    Charron AJ, Sibley LD. Host cells: Mobilizable lipid resources for the intracellular parasite Toxoplasma gondii. J Cell Sci 2002; 115 (Pt 15):3049–3059.PubMedGoogle Scholar
  85. 85.
    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.PubMedCrossRefGoogle Scholar
  86. 86.
    Wastling JM, Burchmore R, Nelson M. Manipualtion of the host cell proteome by Toxoplasma gondii. Porticcio, Corsica, France: Paper presented at: 8th international Congress on Toxoplasmosis, 2005.Google Scholar
  87. 87.
    Molestina RE, Payne TM, Coppens I et al. Activation of NF-{kappa}B by Toxoplasma gondii correlates with increased expression of antiapoptotic genes and localization of phosphorylated I{kappa}B to the parasitophorous vacuole membrane. J Cell Sci 2003 2003; 116:4359–4371.PubMedCrossRefGoogle Scholar
  88. 88.
    Molestina RE, Sinai AP. Host and parasite-derived IKK activities direct distinct temporal phases of NF-{kappa}B activation and target gene expression following Toxoplasma gondii infection. J Cell Sci 2005; 118 (Pt 24):5785–5796.PubMedCrossRefGoogle Scholar
  89. 89.
    Brenier-Pinchart MP, Pelloux H, Simon J et al. Toxoplasma gondii induces the secretion of mono-cyte chemotactic protein-1 in human fibroblasts, in vitro. Mol Cell Biochem 2000; 209(1–2):79–87.PubMedCrossRefGoogle Scholar
  90. 90.
    Denney CF, Eckmann L, Reed SL. Chemokine secretion of human cells in response to Toxoplasma gondii infection. Infect Immun 1999; 67(4):1547–1552.PubMedGoogle Scholar
  91. 91.
    Kim JM, Oh YK, Kim YJ et al. Nuclear factor-kappa B plays a major role in the regulation of chemokine expression of HeLa cells in response to Toxoplasma gondii infection. Parasitol Res 2001; 87(9):758–763.PubMedCrossRefGoogle Scholar
  92. 92.
    Ghosh S, Karin M. Missing pieces in the NF-kappaB puzzle. Cell 2002; 109(Suppl):S81–96.PubMedCrossRefGoogle Scholar
  93. 93.
    Molestina RE, Sinai AP. Detection of a novel parasite kinase activity at the Toxoplasma gondii parasitophorous vacuole membrane capable of phosphorylating host IkBa. Cell Microbiol 2005; 7(3):351–362.PubMedCrossRefGoogle Scholar
  94. 94.
    Aebersold R, Mann M. Mass spectrometry-based proteomics. Nature 2003; 422(6928):198–207.PubMedCrossRefGoogle Scholar

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© Landes Bioscience and Springer Science+Business Media 2008

Authors and Affiliations

  1. 1.Department of Microbiology Immunology and Molecular GeneticsUniversity of Kentucky College of MedicineLexingtonUSA

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