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Annual Review of Microbiology

Volume 73, 2019

Signaling Cascades Governing Entry into and Exit from Host Cells by

Abstract

The Apicomplexa phylum includes a large group of obligate intracellular protozoan parasites responsible for important diseases in humans and animals. is a widespread parasite with considerable versatility, and it is capable of infecting virtually any warm-blooded animal, including humans. This outstanding success can be attributed at least in part to an efficient and continuous sensing of the environment, with a ready-to-adapt strategy. This review updates the current understanding of the signals governing the lytic cycle of , with particular focus on egress from infected cells, a key step for balancing survival, multiplication, and spreading in the host. We cover the recent advances in the conceptual framework of regulation of microneme exocytosis that ensures egress, motility, and invasion. Particular emphasis is given to the trigger molecules and signaling cascades regulating exit from host cells.

Keyword(s): Apicomplexa, calcium, cyclic nucleotides, diacylglycerol kinase, egress, guanylate cyclase, kinase, microneme, motility, phosphatidic acid, signaling, Toxoplasma gondii
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2019-09-08
2024-04-25
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Literature Cited

  1. 1. 
    Alves E, Bartlett PJ, Garcia CR, Thomas AP 2011. Melatonin and IP3-induced Ca2+ release from intracellular stores in the malaria parasite Plasmodium falciparum within infected red blood cells. J. Biol. Chem. 286:5905–12
     [Google Scholar]
  2. 2. 
    Baba M, Batanova T, Kitoh K, Takashima Y 2017. Adhesion of Toxoplasma gondii tachyzoite-infected vehicle leukocytes to capillary endothelial cells triggers timely parasite egression. Sci. Rep. 7:5675
     [Google Scholar]
  3. 3. 
    Baker DA, Drought LG, Flueck C, Nofal SD, Patel A et al. 2017. Cyclic nucleotide signalling in malaria parasites. Open Biol 7:170213
     [Google Scholar]
  4. 4. 
    Baker DA, Stewart LB, Large JM, Bowyer PW, Ansell KH et al. 2017. A potent series targeting the malarial cGMP-dependent protein kinase clears infection and blocks transmission. Nat. Commun. 8:430
     [Google Scholar]
  5. 5. 
    Berridge MJ. 2009. Inositol trisphosphate and calcium signalling mechanisms. Biochim. Biophys. Acta 1793:933–40
     [Google Scholar]
  6. 6. 
    Besteiro S, Bertrand-Michel J, Lebrun M, Vial H, Dubremetz JF 2008. Lipidomic analysis of Toxoplasma gondii tachyzoites rhoptries: further insights into the role of cholesterol. Biochem. J. 415:87–96
     [Google Scholar]
  7. 7. 
    Besteiro S, Dubremetz JF, Lebrun M 2011. The moving junction of apicomplexan parasites: a key structure for invasion. Cell Microbiol 13:797–805
     [Google Scholar]
  8. 8. 
    Billker O, Lindo V, Panico M, Etienne AE, Paxton T et al. 1998. Identification of xanthurenic acid as the putative inducer of malaria development in the mosquito. Nature 392:289–92
     [Google Scholar]
  9. 9. 
    Billker O, Lourido S, Sibley LD 2009. Calcium-dependent signaling and kinases in apicomplexan parasites. Cell Host Microbe 5:612–22
     [Google Scholar]
  10. 10. 
    Bisio H, Lunghi M, Brochet M, Soldati-Favre D 2019. Phosphatidic acid governs natural egress in Toxoplasma gondii via a guanylate cyclase receptor platform. Nat. Microbiol. 4:420–28
     [Google Scholar]
  11. 11. 
    Black MW, Arrizabalaga G, Boothroyd JC 2000. Ionophore-resistant mutants of Toxoplasma gondii reveal host cell permeabilization as an early event in egress. Mol. Cell Biol. 20:9399–408
     [Google Scholar]
  12. 12. 
    Black MW, Boothroyd JC. 2000. Lytic cycle of Toxoplasma gondii. Microbiol. Mol. Biol. Rev 64:607–23
     [Google Scholar]
  13. 13. 
    Blader IJ, Coleman BI, Chen CT, Gubbels MJ 2015. Lytic cycle of Toxoplasma gondii: 15 years later. Annu. Rev. Microbiol. 69:463–85
     [Google Scholar]
  14. 14. 
    Borges-Pereira L, Budu A, McKnight CA, Moore CA, Vella SA et al. 2015. Calcium signaling throughout the Toxoplasma gondii lytic cycle: a study using genetically encoded calcium indicators. J. Biol. Chem. 290:26914–26
     [Google Scholar]
  15. 15. 
    Boucher LE, Bosch J. 2015. The apicomplexan glideosome and adhesins—structures and function. J. Struct. Biol. 190:93–114
     [Google Scholar]
  16. 16. 
    Bradley PJ, Ward C, Cheng SJ, Alexander DL, Coller S et al. 2005. Proteomic analysis of rhoptry organelles reveals many novel constituents for host-parasite interactions in Toxoplasma gondii. J. Biol. Chem 280:34245–58
     [Google Scholar]
  17. 17. 
    Breinich MS, Ferguson DJ, Foth BJ, van Dooren GG, Lebrun M et al. 2009. A dynamin is required for the biogenesis of secretory organelles in Toxoplasma gondii. Curr. Biol 19:277–86
     [Google Scholar]
  18. 18. 
    Brochet M, Collins MO, Smith TK, Thompson E, Sebastian S et al. 2014. Phosphoinositide metabolism links cGMP-dependent protein kinase G to essential Ca2+ signals at key decision points in the life cycle of malaria parasites. PLOS Biol 12:e1001806
     [Google Scholar]
  19. 19. 
    Brown KM, Long S, Sibley LD 2017. Plasma membrane association by N-acylation governs PKG function in Toxoplasma gondii. mBio 8:e00375–17
     [Google Scholar]
  20. 20. 
    Brown KM, Lourido S, Sibley LD 2016. Serum albumin stimulates protein kinase G-dependent microneme secretion in Toxoplasma gondii. J. Biol. Chem 291:9554–65
     [Google Scholar]
  21. 21. 
    Brown KM, Sibley LD. 2018. Essential cGMP signaling in Toxoplasma is initiated by a hybrid P-type ATPase-guanylate cyclase. Cell Host Microbe 24:804–16.e6
     [Google Scholar]
  22. 22. 
    Bullen HE, Jia Y, Yamaryo-Botte Y, Bisio H, Zhang O et al. 2016. Phosphatidic acid-mediated signaling regulates microneme secretion in Toxoplasma. Cell Host Microbe 19:349–60
     [Google Scholar]
  23. 23. 
    Bullen HE, Soldati-Favre D. 2016. A central role for phosphatidic acid as a lipid mediator of regulated exocytosis in apicomplexa. FEBS Lett. 590:2469–81
     [Google Scholar]
  24. 24. 
    Caldas LA, Attias M, de Souza W 2018. A structural analysis of the natural egress of Toxoplasma gondii. Microbes Infect. 20:57–62
     [Google Scholar]
  25. 25. 
    Carruthers VB, Moreno SN, Sibley LD 1999. Ethanol and acetaldehyde elevate intracellular [Ca2+] and stimulate microneme discharge in Toxoplasma gondii. Biochem. J. 342:Part 2379–86
     [Google Scholar]
  26. 26. 
    Carruthers VB, Sibley LD. 1997. Sequential protein secretion from three distinct organelles of Toxoplasma gondii accompanies invasion of human fibroblasts. Eur. J. Cell Biol. 73:114–23
     [Google Scholar]
  27. 27. 
    Carruthers VB, Sibley LD. 1999. Mobilization of intracellular calcium stimulates microneme discharge in Toxoplasma gondii. Mol. Microbiol. 31:421–28
     [Google Scholar]
  28. 28. 
    Carucci DJ, Witney AA, Muhia DK, Warhurst DC, Schaap P et al. 2000. Guanylyl cyclase activity associated with putative bifunctional integral membrane proteins in Plasmodium falciparum. J. Biol. Chem 275:22147–56
     [Google Scholar]
  29. 29. 
    Chang L, Dykes EJ, Li J, Moreno SNJ, Hortua Triana MA 2018. Characterization of two EF-hand domain-containing proteins from Toxoplasma gondii. . J. Eukaryot. Microbiol 66:343–53
     [Google Scholar]
  30. 30. 
    Child MA, Garland M, Foe I, Madzelan P, Treeck M et al. 2017. Toxoplasma DJ-1 regulates organelle secretion by a direct interaction with calcium-dependent protein kinase 1. mBio 8:e02189–16
     [Google Scholar]
  31. 31. 
    Chini EN, Nagamune K, Wetzel DM, Sibley LD 2005. Evidence that the cADPR signalling pathway controls calcium-mediated microneme secretion in Toxoplasma gondii. Biochem. J 389:269–77
     [Google Scholar]
  32. 32. 
    Coleman BI, Saha S, Sato S, Engelberg K, Ferguson DJP et al. 2018. A member of the ferlin calcium sensor family is essential for Toxoplasma gondii rhoptry secretion. mBio 9:e01510–18
     [Google Scholar]
  33. 33. 
    Darvill N, Dubois DJ, Rouse SL, Hammoudi PM, Blake T et al. 2018. Structural basis of phosphatidic acid sensing by APH in apicomplexan parasites. Structure 26:1059–71.e6
     [Google Scholar]
  34. 34. 
    Del Carmen MG, Mondragón M, González S, Mondragón R 2009. Induction and regulation of conoid extrusion in Toxoplasma gondii. Cell Microbiol 11:6967–82
     [Google Scholar]
  35. 35. 
    Denninger JW, Marletta MA. 1999. Guanylate cyclase and the ⋅NO/cGMP signaling pathway. Biochim. Biophys. Acta Bioenerg. 1411:334–50
     [Google Scholar]
  36. 36. 
    Dobrowolski JM, Sibley LD. 1996. Toxoplasma invasion of mammalian cells is powered by the actin cytoskeleton of the parasite. Cell 84:933–39
     [Google Scholar]
  37. 37. 
    Dogga SK, Mukherjee B, Jacot D, Kockmann T, Molino L et al. 2017. A druggable secretory protein maturase of Toxoplasma essential for invasion and egress. eLife 6:e27480
     [Google Scholar]
  38. 38. 
    Dogga SK, Soldati-Favre D. 2016. Biology of rhomboid proteases in infectious diseases. Semin. Cell Dev. Biol. 60:38–45
     [Google Scholar]
  39. 39. 
    Donald RG, Liberator PA. 2002. Molecular characterization of a coccidian parasite cGMP dependent protein kinase. Mol. Biochem. Parasitol. 120:165–75
     [Google Scholar]
  40. 40. 
    Dubey JP. 2004. Toxoplasmosis—a waterborne zoonosis. Vet. Parasitol. 126:57–72
     [Google Scholar]
  41. 41. 
    Dubremetz JF. 2007. Rhoptries are major players in Toxoplasma gondii invasion and host cell interaction. Cell Microbiol 9:841–48
     [Google Scholar]
  42. 42. 
    Eaton MS, Weiss LM, Kim K 2006. Cyclic nucleotide kinases and tachyzoite-bradyzoite transition in Toxoplasma gondii. Int. J. Parasitol 36:107–14
     [Google Scholar]
  43. 43. 
    Fang J, Marchesini N, Moreno SN 2006. A Toxoplasma gondii phosphoinositide phospholipase C (TgPI-PLC) with high affinity for phosphatidylinositol. Biochem. J. 394:417–25
     [Google Scholar]
  44. 44. 
    Farrell A, Thirugnanam S, Lorestani A, Dvorin JD, Eidell KP et al. 2012. A DOC2 protein identified by mutational profiling is essential for apicomplexan parasite exocytosis. Science 335:218–21
     [Google Scholar]
  45. 45. 
    Fazio F, Lionetto L, Curto M, Iacovelli L, Cavallari M et al. 2015. Xanthurenic acid activates mGlu2/3 metabotropic glutamate receptors and is a potential trait marker for schizophrenia. Sci. Rep. 5:17799
     [Google Scholar]
  46. 46. 
    Francia ME, Dubremetz JF, Morrissette NS 2015. Basal body structure and composition in the apicomplexans Toxoplasma and Plasmodium. Cilia 5:3
     [Google Scholar]
  47. 47. 
    Frenal K, Dubremetz JF, Lebrun M, Soldati-Favre D 2017. Gliding motility powers invasion and egress in Apicomplexa. Nat. Rev. Microbiol. 15:645–60
     [Google Scholar]
  48. 48. 
    Frenal K, Jacot D, Hammoudi PM, Graindorge A, Maco B, Soldati-Favre D 2017. Myosin-dependent cell-cell communication controls synchronicity of division in acute and chronic stages of Toxoplasma gondii. Nat. Commun 8:15710
     [Google Scholar]
  49. 49. 
    Fruth IA, Arrizabalaga G. 2007. Toxoplasma gondii: induction of egress by the potassium ionophore nigericin. Int. J. Parasitol. 37:1559–67
     [Google Scholar]
  50. 50. 
    Gao H, Yang Z, Wang X, Qian P, Hong R et al. 2018. ISP1-anchored polarization of GCβ/CDC50A complex initiates malaria ookinete gliding motility. Curr. Biol. 28:2763–76.e6
     [Google Scholar]
  51. 51. 
    Garrison E, Treeck M, Ehret E, Butz H, Garbuz T et al. 2012. A forward genetic screen reveals that calcium-dependent protein kinase 3 regulates egress in Toxoplasma. PLOS Pathog 8:e1003049
     [Google Scholar]
  52. 52. 
    Gilk SD, Gaskins E, Ward GE, Beckers CJ 2009. GAP45 phosphorylation controls assembly of the Toxoplasma myosin XIV complex. Eukaryot. Cell 8:190–96
     [Google Scholar]
  53. 53. 
    Gill DL, Ghosh TK, Mullaney JM 1989. Calcium signalling mechanisms in endoplasmic reticulum activated by inositol 1,4,5-trisphosphate and GTP. Cell Calcium 10:363–74
     [Google Scholar]
  54. 54. 
    Graindorge A, Frenal K, Jacot D, Salamun J, Marq JB, Soldati-Favre D 2016. The conoid associated motor MyoH is indispensable for Toxoplasma gondii entry and exit from host cells. PLOS Pathog 12:e1005388
     [Google Scholar]
  55. 55. 
    Hakansson S, Charron AJ, Sibley LD 2001. Toxoplasma evacuoles: a two-step process of secretion and fusion forms the parasitophorous vacuole. EMBO J 20:3132–44
     [Google Scholar]
  56. 56. 
    Hanlon CD, Andrew DJ. 2015. Outside-in signaling—a brief review of GPCR signaling with a focus on the Drosophila GPCR family. J. Cell Sci. 128:3533–42
     [Google Scholar]
  57. 57. 
    Haste NM, Talabani H, Doo A, Merckx A, Langsley G, Taylor SS 2012. Exploring the Plasmodium falciparum cyclic-adenosine monophosphate (cAMP)-dependent protein kinase (PfPKA) as a therapeutic target. Microbes Infect 14:838–50
     [Google Scholar]
  58. 58. 
    Heissler SM, Sellers JR. 2014. Myosin light chains: Teaching old dogs new tricks. Bioarchitecture 4:169–88
     [Google Scholar]
  59. 59. 
    Herm-Gotz A, Weiss S, Stratmann R, Fujita-Becker S, Ruff C et al. 2002. Toxoplasma gondii myosin A and its light chain: a fast, single-headed, plus-end-directed motor. EMBO J 21:2149–58
     [Google Scholar]
  60. 60. 
    Hopp CS, Flueck C, Solyakov L, Tobin A, Baker DA 2012. Spatiotemporal and functional characterisation of the Plasmodium falciparum cGMP-dependent protein kinase. PLOS ONE 7:e48206
     [Google Scholar]
  61. 61. 
    Hortua Triana MA, Márquez-Nogueras KM, Chang L, Stasic AJ, Li C et al. 2018. Tagging of weakly expressed Toxoplasma gondii calcium-related genes with high-affinity tags. J Eukaryot. Microbiol. 65:5709–21
     [Google Scholar]
  62. 62. 
    Howard BL, Harvey KL, Stewart RJ, Azevedo MF, Crabb BS et al. 2015. Identification of potent phosphodiesterase inhibitors that demonstrate cyclic nucleotide-dependent functions in apicomplexan parasites. ACS Chem. Biol. 10:1145–54
     [Google Scholar]
  63. 63. 
    Hu K. 2008. Organizational changes of the daughter basal complex during the parasite replication of Toxoplasma gondii. PLOS Pathog 4:e10
     [Google Scholar]
  64. 64. 
    Huynh MH, Carruthers VB. 2006. Toxoplasma MIC2 is a major determinant of invasion and virulence. PLOS Pathog 2:e84
     [Google Scholar]
  65. 65. 
    Jacot D, Frenal K, Marq JB, Sharma P, Soldati-Favre D 2014. Assessment of phosphorylation in Toxoplasma glideosome assembly and function. Cell Microbiol 16:1518–32
     [Google Scholar]
  66. 66. 
    Jacot D, Tosetti N, Pires I, Stock J, Graindorge A et al. 2016. An apicomplexan actin-binding protein serves as a connector and lipid sensor to coordinate motility and invasion. Cell Host Microbe 20:731–43
     [Google Scholar]
  67. 67. 
    Jean S, Zapata-Jenks MA, Farley JM, Tracy E, Mayer DC 2014. Plasmodium falciparum double C2 domain protein, PfDOC2, binds to calcium when associated with membranes. Exp. Parasitol. 144:91–95
     [Google Scholar]
  68. 68. 
    Jia Y, Marq JB, Bisio H, Jacot D, Mueller C et al. 2017. Crosstalk between PKA and PKG controls pH-dependent host cell egress of Toxoplasma gondii. EMBO J 36:3250–67
     [Google Scholar]
  69. 69. 
    Kafsack BF, Pena JD, Coppens I, Ravindran S, Boothroyd JC, Carruthers VB 2009. Rapid membrane disruption by a perforin-like protein facilitates parasite exit from host cells. Science 323:530–33
     [Google Scholar]
  70. 70. 
    Katris NJ, Ke H, McFadden GI, van Dooren GG, Waller RF 2019. Calcium negatively regulates secretion from dense granules in Toxoplasma gondii. Cell Microbiol 21:e13011
     [Google Scholar]
  71. 71. 
    Kemp LE, Yamamoto M, Soldati-Favre D 2013. Subversion of host cellular functions by the apicomplexan parasites. FEMS Microbiol. Rev. 37:607–31
     [Google Scholar]
  72. 72. 
    Kirkman LA, Weiss LM, Kim K 2001. Cyclic nucleotide signaling in Toxoplasma gondii bradyzoite differentiation. Infect. Immun. 69:148–53
     [Google Scholar]
  73. 73. 
    Konradt C, Ueno N, Christian DA, Delong JH, Pritchard GH et al. 2016. Endothelial cells are a replicative niche for entry of Toxoplasma gondii to the central nervous system. Nat. Microbiol. 1:16001
     [Google Scholar]
  74. 74. 
    Kotloff KL, Nataro JP, Blackwelder WC, Nasrin D, Farag TH et al. 2013. Burden and aetiology of diarrhoeal disease in infants and young children in developing countries (the Global Enteric Multicenter Study, GEMS): a prospective, case-control study. Lancet 382:209–22
     [Google Scholar]
  75. 75. 
    Kurokawa H, Kato K, Iwanaga T, Sugi T, Sudo A et al. 2011. Identification of Toxoplasma gondii cAMP dependent protein kinase and its role in the tachyzoite growth. PLOS ONE 6:e22492
     [Google Scholar]
  76. 76. 
    Kursula P. 2014. The many structural faces of calmodulin: a multitasking molecular jackknife. Amino Acids 46:2295–304
     [Google Scholar]
  77. 77. 
    LaFavers KA, Marquez-Nogueras KM, Coppens I, Moreno SNJ, Arrizabalaga G 2017. A novel dense granule protein, GRA41, regulates timing of egress and calcium sensitivity in Toxoplasma gondii. Cell Microbiol 19:e12749
     [Google Scholar]
  78. 78. 
    Lagal V, Binder EM, Huynh MH, Kafsack BF, Harris PK et al. 2010. Toxoplasma gondii protease TgSUB1 is required for cell surface processing of micronemal adhesive complexes and efficient adhesion of tachyzoites. Cell Microbiol 12:121792–808
     [Google Scholar]
  79. 79. 
    Lemmon MA. 2008. Membrane recognition by phospholipid-binding domains. Nat. Rev. Mol. Cell Biol. 9:99–111
     [Google Scholar]
  80. 80. 
    Linder JU, Engel P, Reimer A, Kruger T, Plattner H et al. 1999. Guanylyl cyclases with the topology of mammalian adenylyl cyclases and an N-terminal P-type ATPase-like domain in Paramecium, Tetrahymena and Plasmodium. EMBO J 18:4222–32
     [Google Scholar]
  81. 81. 
    Liu J, Pace D, Dou Z, King TP, Guidot D et al. 2014. A vacuolar-H+-pyrophosphatase (TgVP1) is required for microneme secretion, host cell invasion, and extracellular survival of Toxoplasma gondii. Mol. Microbiol 93:698–712
     [Google Scholar]
  82. 82. 
    Lochner A, Moolman JA. 2006. The many faces of H89: a review. Cardiovasc. Drug Rev. 24:261–74
     [Google Scholar]
  83. 83. 
    Long S, Brown KM, Drewry LL, Anthony B, Phan IQH, Sibley LD 2017. Calmodulin-like proteins localized to the conoid regulate motility and cell invasion by Toxoplasma gondii. PLOS Pathog 13:e1006379
     [Google Scholar]
  84. 84. 
    Lourido S, Jeschke GR, Turk BE, Sibley LD 2013. Exploiting the unique ATP-binding pocket of Toxoplasma calcium-dependent protein kinase 1 to identify its substrates. ACS Chem. Biol. 8:1155–62
     [Google Scholar]
  85. 85. 
    Lourido S, Moreno SN. 2015. The calcium signaling toolkit of the Apicomplexan parasites Toxoplasma gondii and Plasmodium spp. Cell Calcium 57:186–93
     [Google Scholar]
  86. 86. 
    Lourido S, Shuman J, Zhang C, Shokat KM, Hui R, Sibley LD 2010. Calcium-dependent protein kinase 1 is an essential regulator of exocytosis in Toxoplasma. Nature 465:359–62
     [Google Scholar]
  87. 87. 
    Lourido S, Tang K, Sibley LD 2012. Distinct signalling pathways control Toxoplasma egress and host-cell invasion. EMBO J 31:4524–34
     [Google Scholar]
  88. 88. 
    Lovett JL, Marchesini N, Moreno SN, Sibley LD 2002. Toxoplasma gondii microneme secretion involves intracellular Ca2+ release from inositol 1,4,5-triphosphate (IP3)/ryanodine-sensitive stores. J. Biol. Chem. 277:25870–76
     [Google Scholar]
  89. 89. 
    Lovett JL, Sibley LD. 2003. Intracellular calcium stores in Toxoplasma gondii govern invasion of host cells. J. Cell Sci. 116:3009–16
     [Google Scholar]
  90. 90. 
    Luo S, Ruiz FA, Moreno SN 2005. The acidocalcisome Ca2+-ATPase (TgA1) of Toxoplasma gondii is required for polyphosphate storage, intracellular calcium homeostasis and virulence. Mol. Microbiol. 55:1034–45
     [Google Scholar]
  91. 91. 
    McCoy JM, Whitehead L, van Dooren GG, Tonkin CJ 2012. TgCDPK3 regulates calcium-dependent egress of Toxoplasma gondii from host cells. PLOS Pathog 8:e1003066
     [Google Scholar]
  92. 92. 
    McRobert L, Taylor CJ, Deng W, Fivelman QL, Cummings RM et al. 2008. Gametogenesis in malaria parasites is mediated by the cGMP-dependent protein kinase. PLOS Biol 6:e139
     [Google Scholar]
  93. 93. 
    Millholland MG, Mishra S, Dupont CD, Love MS, Patel B et al. 2013. A host GPCR signaling network required for the cytolysis of infected cells facilitates release of apicomplexan parasites. Cell Host Microbe 13:15–28
     [Google Scholar]
  94. 94. 
    Moraes MS, Budu A, Singh MK, Borges-Pereira L, Levano-Garcia J et al. 2017. Plasmodium falciparum GPCR-like receptor SR25 mediates extracellular K+ sensing coupled to Ca2+ signaling and stress survival. Sci. Rep. 7:9545
     [Google Scholar]
  95. 95. 
    Moreno SN, Zhong L. 1996. Acidocalcisomes in Toxoplasma gondii tachyzoites. Biochem. J. 313:Part 2655–59
     [Google Scholar]
  96. 96. 
    Moudy R, Manning TJ, Beckers CJ 2001. The loss of cytoplasmic potassium upon host cell breakdown triggers egress of Toxoplasma gondii. J. Biol. Chem 276:41492–501
     [Google Scholar]
  97. 97. 
    Mueller C, Samoo A, Hammoudi PM, Klages N, Kallio JP et al. 2016. Structural and functional dissection of Toxoplasma gondii armadillo repeats only protein. J. Cell Sci. 129:1031–45
     [Google Scholar]
  98. 98. 
    Muhia DK, Swales CA, Deng W, Kelly JM, Baker DA 2001. The gametocyte-activating factor xanthurenic acid stimulates an increase in membrane-associated guanylyl cyclase activity in the human malaria parasite Plasmodium falciparum. Mol. Microbiol 42:553–60
     [Google Scholar]
  99. 99. 
    Nagamune K, Beatty WL, Sibley LD 2007. Artemisinin induces calcium-dependent protein secretion in the protozoan parasite Toxoplasma gondii. Eukaryot. Cell 6:2147–56
     [Google Scholar]
  100. 100. 
    Nagamune K, Hicks LM, Fux B, Brossier F, Chini EN, Sibley LD 2008. Abscisic acid controls calcium-dependent egress and development in Toxoplasma gondii. Nature 451:207–10
     [Google Scholar]
  101. 101. 
    Nagamune K, Sibley LD. 2006. Comparative genomic and phylogenetic analyses of calcium ATPases and calcium-regulated proteins in the Apicomplexa. Mol. Biol. Evol. 23:1613–27
     [Google Scholar]
  102. 102. 
    Obrova K, Cyrklaff M, Frank R, Mair GR, Mueller AK 2018. Transmission of the malaria parasite requires ferlin for gamete egress from the red blood cell. Cell Microbiol 21:5e12999
     [Google Scholar]
  103. 103. 
    Okada T, Marmansari D, Li ZM, Adilbish A, Canko S et al. 2013. A novel dense granule protein, GRA22, is involved in regulating parasite egress in Toxoplasma gondii. Mol. Biochem. Parasitol 189:5–13
     [Google Scholar]
  104. 104. 
    Ono T, Cabrita-Santos L, Leitao R, Bettiol E, Purcell LA et al. 2008. Adenylyl cyclase alpha and cAMP signaling mediate Plasmodium sporozoite apical regulated exocytosis and hepatocyte infection. PLOS Pathog 4:e1000008
     [Google Scholar]
  105. 105. 
    Pace DA, McKnight CA, Liu J, Jimenez V, Moreno SN 2014. Calcium entry in Toxoplasma gondii and its enhancing effect of invasion-linked traits. J. Biol. Chem. 289:19637–47
     [Google Scholar]
  106. 106. 
    Paul AS, Saha S, Engelberg K, Jiang RH, Coleman BI et al. 2015. Parasite calcineurin regulates host cell recognition and attachment by apicomplexans. Cell Host Microbe 18:49–60
     [Google Scholar]
  107. 107. 
    Periz J, Whitelaw J, Harding C, Gras S, Del Rosario Minina MI et al. 2017. Toxoplasma gondii F-actin forms an extensive filamentous network required for material exchange and parasite maturation. eLife 6:e24119
     [Google Scholar]
  108. 108. 
    Persson EK, Agnarson AM, Lambert H, Hitziger N, Yagita H et al. 2007. Death receptor ligation or exposure to perforin trigger rapid egress of the intracellular parasite Toxoplasma gondii. J. Immunol 179:8357–65
     [Google Scholar]
  109. 109. 
    Plattner H, Kissmehl R. 2005. Molecular aspects of rapid, reversible, Ca2+-dependent de-phosphorylation of pp63/parafusin during stimulated exo-endocytosis in Paramecium cells. Cell Calcium 38:319–27
     [Google Scholar]
  110. 110. 
    Polonais V, Javier Foth B, Chinthalapudi K, Marq JB, Manstein DJ et al. 2011. Unusual anchor of a motor complex (MyoD-MLC2) to the plasma membrane of Toxoplasma gondii. Traffic 12:287–300
     [Google Scholar]
  111. 111. 
    Prole DL, Taylor CW. 2011. Identification of intracellular and plasma membrane calcium channel homologues in pathogenic parasites. PLOS ONE 6:e26218
     [Google Scholar]
  112. 112. 
    Reiss M, Viebig N, Brecht S, Fourmaux MN, Soete M et al. 2001. Identification and characterization of an escorter for two secretory adhesins in Toxoplasma gondii. J. Cell Biol 152:563–78
     [Google Scholar]
  113. 113. 
    Roiko MS, Carruthers VB. 2009. New roles for perforins and proteases in apicomplexan egress. Cell Microbiol 11:1444–52
     [Google Scholar]
  114. 114. 
    Roiko MS, Svezhova N, Carruthers VB 2014. Acidification activates Toxoplasma gondii motility and egress by enhancing protein secretion and cytolytic activity. PLOS Pathog 10:e1004488
     [Google Scholar]
  115. 115. 
    Rutaganira FU, Barks J, Dhason MS, Wang Q, Lopez MS et al. 2017. Inhibition of calcium dependent protein kinase 1 (CDPK1) by pyrazolopyrimidine analogs decreases establishment and reoccurrence of central nervous system disease by Toxoplasma gondii. J. Med. Chem 60:9976–89
     [Google Scholar]
  116. 116. 
    Saha S, Coleman BI, Dubey R, Blader IJ, Gubbels MJ 2017. Two phosphoglucomutase paralogs facilitate ionophore-triggered secretion of the Toxoplasma micronemes. mSphere 2:e00521–17
     [Google Scholar]
  117. 117. 
    Salazar E, Bank EM, Ramsey N, Hess KC, Deitsch KW et al. 2012. Characterization of Plasmodium falciparum adenylyl cyclase-beta and its role in erythrocytic stage parasites. PLOS ONE 7:e39769
     [Google Scholar]
  118. 118. 
    Santos JM, Lebrun M, Daher W, Soldati D, Dubremetz JF 2009. Apicomplexan cytoskeleton and motors: key regulators in morphogenesis, cell division, transport and motility. Int. J. Parasitol. 39:153–62
     [Google Scholar]
  119. 119. 
    Schwab JC, Beckers CJ, Joiner KA 1994. The parasitophorous vacuole membrane surrounding intracellular Toxoplasma gondii functions as a molecular sieve. PNAS 91:509–13
     [Google Scholar]
  120. 120. 
    Sidik SM, Hortua Triana MA, Paul AS, El Bakkouri M, Hackett CG et al. 2016. Using a genetically encoded sensor to identify inhibitors of Toxoplasma gondii Ca2+ signaling. J. Biol. Chem. 291:9566–80
     [Google Scholar]
  121. 121. 
    Sidik SM, Huet D, Ganesan SM, Huynh MH, Wang T et al. 2016. A genome-wide CRISPR screen in Toxoplasma identifies essential apicomplexan genes. Cell 166:1423–35.e12
     [Google Scholar]
  122. 122. 
    Singh S, Alam MM, Pal-Bhowmick I, Brzostowski JA, Chitnis CE 2010. Distinct external signals trigger sequential release of apical organelles during erythrocyte invasion by malaria parasites. PLOS Pathog 6:e1000746
     [Google Scholar]
  123. 123. 
    Stommel EW, Ely KH, Schwartzman JD, Kasper LH 1997. Toxoplasma gondii: dithiol-induced Ca2+ flux causes egress of parasites from the parasitophorous vacuole. Exp. Parasitol. 87:88–97
     [Google Scholar]
  124. 124. 
    Sudhof TC, Rizo J. 2011. Synaptic vesicle exocytosis. Cold Spring Harb. Perspect. Biol. 3:a005637
     [Google Scholar]
  125. 125. 
    Sugi T, Ma YF, Tomita T, Murakoshi F, Eaton MS et al. 2016. Toxoplasma gondii cyclic AMP-dependent protein kinase subunit 3 is involved in the switch from tachyzoite to bradyzoite development. mBio 7:e00755–16
     [Google Scholar]
  126. 126. 
    Taylor SS, Ilouz R, Zhang P, Kornev AP 2012. Assembly of allosteric macromolecular switches: lessons from PKA. Nat. Rev. Mol. Cell Biol. 13:646–58
     [Google Scholar]
  127. 127. 
    Tosetti N, Dos Santos Pacheco N, Soldati-Favre D, Jacot D 2019. Three F-actin assembly centers regulate organelle inheritance, cell-cell communication and motility in Toxoplasma gondii. eLife 8:e42669
     [Google Scholar]
  128. 128. 
    Treeck M, Sanders JL, Gaji RY, LaFavers KA, Child MA et al. 2014. The calcium-dependent protein kinase 3 of Toxoplasma influences basal calcium levels and functions beyond egress as revealed by quantitative phosphoproteome analysis. PLOS Pathog 10:e1004197
     [Google Scholar]
  129. 129. 
    Uboldi AD, Wilde ML, McRae EA, Stewart RJ, Dagley LF et al. 2018. Protein kinase A negatively regulates Ca2+ signalling in Toxoplasma gondii. PLOS Biol 16:e2005642
     [Google Scholar]
  130. 130. 
    Vaandrager AB, Ehlert EM, Jarchau T, Lohmann SM, de Jonge HR 1996. N-terminal myristoylation is required for membrane localization of cGMP-dependent protein kinase type II. J. Biol. Chem. 271:7025–29
     [Google Scholar]
  131. 131. 
    Vieira MC, Moreno SN. 2000. Mobilization of intracellular calcium upon attachment of Toxoplasma gondii tachyzoites to human fibroblasts is required for invasion. Mol. Biochem. Parasitol. 106:157–62
     [Google Scholar]
  132. 132. 
    Wallbank BA, Dominicus CS, Broncel M, Legrave N, Kelly G et al. 2019. Characterisation of the Toxoplasma gondii tyrosine transporter and its phosphorylation by the calcium-dependent protein kinase 3. Mol. Microbiol. 111:1167–81
     [Google Scholar]
  133. 133. 
    Wang S, Li Y, Ma C 2016. Synaptotagmin-1 C2B domain interacts simultaneously with SNAREs and membranes to promote membrane fusion. eLife 5:e14211
     [Google Scholar]
  134. 134. 
    Wentzinger L, Bopp S, Tenor H, Klar J, Brun R et al. 2008. Cyclic nucleotide-specific phosphodiesterases of Plasmodium falciparum: PfPDEα, a non-essential cGMP-specific PDE that is an integral membrane protein. Int. J. Parasitol. 38:1625–37
     [Google Scholar]
  135. 135. 
    Wetzel DM, Chen LA, Ruiz FA, Moreno SN, Sibley LD 2004. Calcium-mediated protein secretion potentiates motility in Toxoplasma gondii. Cell Sci 117:Part 245739–48
     [Google Scholar]
  136. 136. 
    Wiersma HI, Galuska SE, Tomley FM, Sibley LD, Liberator PA, Donald RG 2004. A role for coccidian cGMP-dependent protein kinase in motility and invasion. Int. J. Parasitol. 34:369–80
     [Google Scholar]
  137. 137. 
    Williams MJ, Alonso H, Enciso M, Egarter S, Sheiner L et al. 2015. Two essential light chains regulate the MyoA lever arm to promote Toxoplasma gliding motility. mBio 6:e00845–15
     [Google Scholar]
  138. 138. 
    Wong SY, Remington JS. 1994. Toxoplasmosis in pregnancy. Clin. Infect. Dis. 18:853–61
     [Google Scholar]
  139. 139. 
    Yan X, Ji Y, Liu X, Suo X 2015. Nitric oxide stimulates early egress of Toxoplasma gondii tachyzoites from human foreskin fibroblast cells. Parasites Vectors 8:420
     [Google Scholar]
  140. 140. 
    Yang L, Uboldi AD, Seizova S, Wilde ML, Coffey MJ et al. 2019. An apically located hybrid guanylate cyclase-ATPase is critical for the initiation of Ca2+ signalling and motility in Toxoplasma gondii. J. Biol. Chem 294:8959–72
     [Google Scholar]
  141. 141. 
    Yao J, Gaffaney JD, Kwon SE, Chapman ER 2011. Doc2 is a Ca2+ sensor required for asynchronous neurotransmitter release. Cell 147:666–77
     [Google Scholar]
  142. 142. 
    Zeniou-Meyer M, Zabari N, Ashery U, Chasserot-Golaz S, Haeberle AM et al. 2007. Phospholipase D1 production of phosphatidic acid at the plasma membrane promotes exocytosis of large dense-core granules at a late stage. J. Biol. Chem. 282:21746–57
     [Google Scholar]
  143. 143. 
    Zhang X, Zhang H, Fu Y, Liu J, Liu Q 2018. Effects of estradiol and progesterone-induced intracellular calcium fluxes on Toxoplasma gondii gliding, microneme secretion, and egress. Front. Microbiol. 9:1266
     [Google Scholar]
/content/journals/10.1146/annurev-micro-020518-120235
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Signaling Cascades Governing Entry into and Exit from Host Cells by Toxoplasma gondii
Annual Review of Microbiology 73, 579 (2019); https://doi.org/10.1146/annurev-micro-020518-120235
/content/journals/10.1146/annurev-micro-020518-120235
/content/journals/10.1146/annurev-micro-020518-120235
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