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Annual Review of Microbiology

Volume 76, 2022

How Apicomplexa Parasites Secrete and Build Their Invasion Machinery

Abstract

Apicomplexa are obligatory intracellular parasites that sense and actively invade host cells. Invasion is a conserved process that relies on the timely and spatially controlled exocytosis of unique specialized secretory organelles termed micronemes and rhoptries. Microneme exocytosis starts first and likely controls the intricate mechanism of rhoptry secretion. To assemble the invasion machinery, micronemal proteins—associated with the surface of the parasite—interact and form complexes with rhoptry proteins, which in turn are targeted into the host cell. This review covers the molecular advances regarding microneme and rhoptry exocytosis and focuses on how the proteins discharged from these two compartments work in synergy to drive a successful invasion event. Particular emphasis is given to the structure and molecular components of the rhoptry secretion apparatus, and to the current conceptual framework of rhoptry exocytosis that may constitute an unconventional eukaryotic secretory machinery closely related to the one described in ciliates.

Keyword(s): Apicomplexa, exocytosis, invasion, microneme, moving junction, rhoptry
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2022-09-08
2024-05-02
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Literature Cited

  1. 1.
    Aikawa M, Miller LH, Johnson J, Rabbege J 1978. Erythrocyte entry by malarial parasites: a moving junction between erythrocyte and parasite. J. Cell Biol. 77:172–82
     [Google Scholar]
  2. 2.
    Aikawa M, Miller LH, Rabbege JR, Epstein N. 1981. Freeze-fracture study on the erythrocyte membrane during malarial parasite invasion. J. Cell Biol. 91:155–62
     [Google Scholar]
  3. 3.
    Alexander DL, Mital J, Ward GE, Bradley P, Boothroyd JC. 2005. Identification of the moving junction complex of Toxoplasma gondii: a collaboration between distinct secretory organelles. PLOS Pathog 1:2e17
     [Google Scholar]
  4. 4.
    Aniweh Y, Gao X, Hao P, Meng W, Lai SK et al. 2017. P. falciparum RH5-Basigin interaction induces changes in the cytoskeleton of the host RBC. Cell Microbiol 19:9e12747
     [Google Scholar]
  5. 5.
    Aquilini E, Cova MM, Mageswaran SK, Dos Santos Pacheco N, Sparvoli D et al. 2021. An Alveolata secretory machinery adapted to parasite host cell invasion. Nat. Microbiol. 6:4425–34
     [Google Scholar]
  6. 6.
    Arredondo SA, Schepis A, Reynolds L, Kappe SHI. 2021. Secretory organelle function in the Plasmodium sporozoite. Trends Parasitol 37:7651–63
     [Google Scholar]
  7. 7.
    Arredondo SA, Swearingen KE, Martinson T, Steel R, Dankwa DA et al. 2018. The micronemal Plasmodium proteins P36 and P52 act in concert to establish the replication-permissive compartment within infected hepatocytes. Front. Cell. Infect. Microbiol. 8:413
     [Google Scholar]
  8. 8.
    Ayong L, DaSilva T, Mauser J, Allen CM, Chakrabarti D. 2011. Evidence for prenylation-dependent targeting of a Ykt6 SNARE in Plasmodium falciparum. Mol. Biochem. Parasitol. 175:2162–68
     [Google Scholar]
  9. 9.
    Ayong L, Pagnotti G, Tobon AB, Chakrabarti D. 2007. Identification of Plasmodium falciparum family of SNAREs. Mol. Biochem. Parasitol. 152:2113–22
     [Google Scholar]
  10. 10.
    Ayong L, Raghavan A, Schneider TG, Taraschi TF, Fidock DA, Chakrabarti D. 2009. The longin domain regulates the steady-state dynamics of Sec22 in Plasmodium falciparum. Eukaryot. Cell 8:91330–40
     [Google Scholar]
  11. 11.
    Bai T, Becker M, Gupta A, Strike P, Murphy VJ et al. 2005. Structure of AMA1 from Plasmodium falciparum reveals a clustering of polymorphisms that surround a conserved hydrophobic pocket. PNAS 102:3612736–41
     [Google Scholar]
  12. 12.
    Baker RP, Wijetilaka R, Urban S. 2006. Two Plasmodium rhomboid proteases preferentially cleave different adhesins implicated in all invasive stages of malaria. PLOS Pathog 2:10e113
     [Google Scholar]
  13. 13.
    Bargieri D, Lagal V, Tardieux I, Menard R. 2012. Host cell invasion by apicomplexans: What do we know?. Trends Parasitol 28:4131–35
     [Google Scholar]
  14. 14.
    Beck JR, Chen AL, Kim EW, Bradley PJ 2014. RON5 is critical for organization and function of the Toxoplasma moving junction complex. PLOS Pathog 10:3e1004025
     [Google Scholar]
  15. 15.
    Ben Chaabene R, Lentini G, Soldati-Favre D. 2021. Biogenesis and discharge of the rhoptries: key organelles for entry and hijack of host cells by the Apicomplexa. Mol. Microbiol. 115:3453–65
     [Google Scholar]
  16. 16.
    Besteiro S, Dubremetz J-F, Lebrun M. 2011. The moving junction of apicomplexan parasites: a key structure for invasion. Cell Microbiol 13:6797–805
     [Google Scholar]
  17. 17.
    Besteiro S, Michelin A, Poncet J, Dubremetz J-F, Lebrun M. 2009. Export of a Toxoplasma gondii rhoptry neck protein complex at the host cell membrane to form the moving junction during invasion. PLOS Pathog 5:2e1000309
     [Google Scholar]
  18. 18.
    Bisio H, Chaabene RB, Sabitzki R, Maco B, Marq JB et al. 2020. The ZIP code of vesicle trafficking in Apicomplexa: SEC1/Munc18 and SNARE proteins. mBio 11:5e02092–20
     [Google Scholar]
  19. 19.
    Bisio H, Krishnan A, Mark JB, Soldati-Favre D. 2022. PLOS Pathog 18:3e1010438
  20. 20.
    Bisio H, Soldati-Favre D. 2019. Signaling cascades governing entry into and exit from host cells by Toxoplasma gondii. Annu. Rev. Microbiol. 73:579–99
     [Google Scholar]
  21. 21.
    Bisson C, Hecksel CW, Gilchrist JB, Fleck RA. 2021. Preparing lamellae from vitreous biological samples using a dual-beam scanning electron microscope for cryo-electron tomography. J. Vis. Exp. 174:e62350
     [Google Scholar]
  22. 22.
    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. 280:4034245–58
     [Google Scholar]
  23. 23.
    Bullen HE, Jia Y, Yamaryo-Botté Y, Bisio H, Zhang O et al. 2016. Phosphatidic acid-mediated signaling regulates microneme secretion in Toxoplasma. Cell Host Microbe 19:3349–60
     [Google Scholar]
  24. 24.
    Burrell A, Marugan-Hernandez V, Moreira-Leite F, Ferguson DJP, Tomley FM, Vaughan S. 2021. Cellular electron tomography of the apical complex in the apicomplexan parasite Eimeria tenella shows a highly organised gateway for regulated secretion. bioRxiv 2021.06.17.448283, June 17
  25. 25.
    Campos Y, Qiu X, Gomero E, Wakefield R, Horner L et al. 2016. Alix-mediated assembly of the actomyosin-tight junction polarity complex preserves epithelial polarity and epithelial barrier. Nat. Commun. 7:11876
     [Google Scholar]
  26. 26.
    Cao S, Yang J, Fu J, Chen H, Jia H. 2021. The dissection of SNAREs reveals key factors for vesicular trafficking to the endosome-like compartment and apicoplast via the secretory system in Toxoplasma gondii. mBio 12:4e0138021
     [Google Scholar]
  27. 27.
    Carruthers VB, Sibley LD. 1997. Sequential protein secretion from three distinct organelles of Toxoplasma gondii accompanies invasion of human fibroblasts. Eur. J. Cell Biol. 73:2114–23
     [Google Scholar]
  28. 28.
    Carruthers VB, Tomley FM. 2008. Microneme proteins in apicomplexans. Subcell. Biochem. 47:33–45
     [Google Scholar]
  29. 29.
    Chaiyawong N, Ishizaki T, Hakimi H, Asada M, Kazuhide Y, Kaneko O. 2022. Distinct effects on the secretion of MTRAP and AMA1 in Plasmodium yoelii following deletion of acylated pleckstrin homology domain-containing protein. Parasitol. Int. 86:102479
     [Google Scholar]
  30. 30.
    Chasen NM, Asady B, Lemgruber L, Vommaro RC, Kissinger JC et al. 2017. A glycosylphosphatidylinositol-anchored carbonic anhydrase-related protein of Toxoplasma gondii is important for rhoptry biogenesis and virulence. mSphere 2:3e00027–17
     [Google Scholar]
  31. 31.
    Chen K, Günay-Esiyok Ö, Klingeberg M, Marquardt S, Pomorski TG, Gupta N. 2021. Aminoglycerophospholipid flipping and P4-ATPases in Toxoplasma gondii. J. Biol. Chem. 296:100315
     [Google Scholar]
  32. 32.
    Chen L, Christian DA, Kochanowsky JA, Phan AT, Clark JT et al. 2020. The Toxoplasma gondii virulence factor ROP16 acts in cis and trans, and suppresses T cell responses. J. Exp. Med. 217:3e20181757
     [Google Scholar]
  33. 33.
    Chen L, Lopaticki S, Riglar DT, Dekiwadia C, Uboldi AD et al. 2011. An EGF-like protein forms a complex with PfRh5 and is required for invasion of human erythrocytes by Plasmodium falciparum. PLOS Pathog 7:9e1002199
     [Google Scholar]
  34. 34.
    Chen L, Xu Y, Healer J, Thompson JK, Smith BJ et al. 2014. Crystal structure of PfRh5, an essential P. falciparum ligand for invasion of human erythrocytes. eLife 3:e04187
     [Google Scholar]
  35. 35.
    Coleman BI, Saha S, Sato S, Engelberg K, Ferguson DJP et al. 2021. A member of the ferlin calcium sensor family is essential for Toxoplasma gondii rhoptry secretion. mBio 9:5e01510–18
     [Google Scholar]
  36. 36.
    Collins CR, Hackett F, Howell SA, Snijders AP, Russell MR et al. 2020. The malaria parasite sheddase SUB2 governs host red blood cell membrane sealing at invasion. eLife 9:e61121
     [Google Scholar]
  37. 37.
    Counihan NA, Kalanon M, Coppel RL, de Koning-Ward TF. 2013. Plasmodium rhoptry proteins: why order is important. Trends Parasitol 29:5228–36
     [Google Scholar]
  38. 38.
    Cowman AF, Tonkin CJ, Tham WH, Duraisingh MT. 2017. The molecular basis of erythrocyte invasion by malaria parasites. Cell Host Microbe 22:2232–45
     [Google Scholar]
  39. 39.
    Crawford J, Tonkin ML, Grujic O, Boulanger MJ. 2010. Structural characterization of apical membrane antigen 1 (AMA1) from Toxoplasma gondii. J. Biol. Chem. 285:2015644–52
     [Google Scholar]
  40. 40.
    Crosnier C, Bustamante LY, Bartholdson SJ, Bei AK, Theron M et al. 2011. BASIGIN is a receptor essential for erythrocyte invasion by Plasmodium falciparum. Nature 480:7378534–37
     [Google Scholar]
  41. 41.
    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 26:81059–1071.e6
     [Google Scholar]
  42. 42.
    Dubois DJ, Soldati-Favre D. 2019. Biogenesis and secretion of micronemes in Toxoplasma gondii. Cell. Microbiol. 21:5e13018
     [Google Scholar]
  43. 43.
    Dubremetz JF. 2007. Rhoptries are major players in Toxoplasma gondii invasion and host cell interaction. Cell Microbiol 9:4841–48
     [Google Scholar]
  44. 44.
    Dubremetz JF, Torpier G. 1978. Freeze fracture study of the pellicle of an eimerian sporozoite (Protozoa, Coccidia). J. Ultrastruct. Res. 62:294–109
     [Google Scholar]
  45. 45.
    Ebrahimzadeh Z, Mukherjee A, Crochetière M-È, Sergerie A, Amiar S et al. 2019. A pan-apicomplexan phosphoinositide-binding protein acts in malarial microneme exocytosis. EMBO Rep 20:6e47102
     [Google Scholar]
  46. 46.
    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 335:6065218–21
     [Google Scholar]
  47. 47.
    Fernandes P, Loubens M, Le Borgne R, Marinach C, Ardin B et al. 2022. The AMA1-RON complex drives Plasmodium sporozoite invasion in the mosquito and mammalian hosts. bioRxiv 2022.01.04.474787, Jan. 04
  48. 48.
    Frénal K, Dubremetz JF, Lebrun M, Soldati-Favre D. 2017. Gliding motility powers invasion and egress in Apicomplexa. Nat. Rev. Microbiol. 15:11645–60
     [Google Scholar]
  49. 49.
    Galaway F, Yu R, Constantinou A, Prugnolle F, Wright GJ. 2019. Resurrection of the ancestral RH5 invasion ligand provides a molecular explanation for the origin of P. falciparum malaria in humans. PLOS Biol 17:10e3000490
     [Google Scholar]
  50. 50.
    Geoghegan ND, Evelyn C, Whitehead LW, Pasternak M, McDonald P et al. 2021. 4D analysis of malaria parasite invasion offers insights into erythrocyte membrane remodeling and parasitophorous vacuole formation. Nat. Commun. 12:13620
     [Google Scholar]
  51. 51.
    Ghosh S, Kennedy K, Sanders P, Matthews K, Ralph SA et al. 2017. The Plasmodium rhoptry associated protein complex is important for parasitophorous vacuole membrane structure and intraerythrocytic parasite growth. Cell. Microbiol. 19:8e12733
     [Google Scholar]
  52. 52.
    Gilson PR, Crabb BS. 2009. Morphology and kinetics of the three distinct phases of red blood cell invasion by Plasmodium falciparum merozoites. Int. J. Parasitol. 39:191–96
     [Google Scholar]
  53. 53.
    Giovannini D, Spath S, Lacroix C, Perazzi A, Bargieri D et al. 2011. Independent roles of apical membrane antigen 1 and rhoptry neck proteins during host cell invasion by Apicomplexa. Cell Host Microbe 10:6591–602
     [Google Scholar]
  54. 54.
    Gonzalez V, Combe A, David V, Malmquist NA, Delorme V et al. 2009. Host cell entry by Apicomplexa parasites requires actin polymerization in the host cell. Cell Host Microbe 5:3259–72
     [Google Scholar]
  55. 55.
    Guérin A, Corrales RM, Parker ML, Lamarque MH, Jacot D et al. 2017. Efficient invasion by Toxoplasma depends on the subversion of host protein networks. Nat. Microbiol. 2:101358–66
     [Google Scholar]
  56. 56.
    Guérin A, El Hajj H, Penarete-Vargas D, Besteiro S, Lebrun M. 2017. RON4L1 is a new member of the moving junction complex in Toxoplasma gondii. Sci. Rep. 7:117907
     [Google Scholar]
  57. 57.
    Gui L, O'Shaughnessy WJ, Cai K, Reetz E, Reese M, Nicastro D. 2022. Cryo-electron tomography of the apicomplexan invasion machinery in its native state reveals rigid body motion of the conoid and docked secretory machinery. bioRxiv 2022.04.23.489287, Apr. 24
  58. 58.
    Hadjebi O, Casas-Terradellas E, Garcia-Gonzalo FR, Rosa JL. 2008. The RCC1 superfamily: from genes, to function, to disease. Biochim. Biophys. Acta Mol. Cell Res. 1783:81467–79
     [Google Scholar]
  59. 59.
    Hakimi M-A, Olias P, Sibley LD. 2017. Toxoplasma effectors targeting host signaling and transcription. Clin. Microbiol. Rev. 30:3615–45
     [Google Scholar]
  60. 60.
    Hammoudi P-M, Maco B, Dogga SK, Frénal K, Soldati-Favre D. 2018. Toxoplasma gondii TFP1 is an essential transporter family protein critical for microneme maturation and exocytosis. Mol. Microbiol. 109:225–44
     [Google Scholar]
  61. 61.
    Hanssen E, Dekiwadia C, Riglar DT, Rug M, Lemgruber L et al. 2013. Electron tomography of Plasmodium falciparum merozoites reveals core cellular events that underpin erythrocyte invasion. Cell Microbiol 15:91457–72
     [Google Scholar]
  62. 62.
    Harvey KL, Yap A, Gilson PR, Cowman AF, Crabb BS. 2014. Insights and controversies into the role of the key apicomplexan invasion ligand, Apical Membrane Antigen 1. Int. J. Parasitol 44:12853–57
     [Google Scholar]
  63. 63.
    Hayton K, Gaur D, Liu A, Takahashi J, Henschen B et al. 2008. Erythrocyte binding protein PfRH5 polymorphisms determine species-specific pathways of Plasmodium falciparum invasion. Cell Host Microbe 4:140–51
     [Google Scholar]
  64. 64.
    Hayward RD, McGhie EJ, Koronakis V. 2000. Membrane fusion activity of purified SipB, a Salmonella surface protein essential for mammalian cell invasion. Mol. Microbiol. 37:4727–39
     [Google Scholar]
  65. 65.
    Howell SA, Hackett F, Jongco AM, Withers-Martinez C, Kim K et al. 2005. Distinct mechanisms govern proteolytic shedding of a key invasion protein in apicomplexan pathogens. Mol. Microbiol. 57:51342–56
     [Google Scholar]
  66. 66.
    Ishino T, Murata E, Tokunaga N, Baba M, Tachibana M et al. 2019. Rhoptry neck protein 2 expressed in Plasmodium sporozoites plays a crucial role during invasion of mosquito salivary glands. Cell Microbiol 21:1e12964
     [Google Scholar]
  67. 67.
    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 20:6731–43
     [Google Scholar]
  68. 68.
    Jean S, Zapata-Jenks MA, Farley JM, Tracy E, Mayer DCG 2014. Plasmodium falciparum double C2 domain protein, PfDOC2, binds to calcium when associated with membranes. Exp. Parasitol. 144:91–95
     [Google Scholar]
  69. 69.
    Jia Y, Marq J, 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 36:213250–67
     [Google Scholar]
  70. 70.
    Johnson RI, Seppa MJ, Cagan RL. 2008. The Drosophila CD2AP/CIN85 orthologue Cindr regulates junctions and cytoskeleton dynamics during tissue patterning. J. Cell Biol. 180:61191–204
     [Google Scholar]
  71. 71.
    Kehrer J, Singer M, Lemgruber L, Silva PAGC, Frischknecht F, Mair GR. 2016. A putative small solute transporter is responsible for the secretion of G377 and TRAP-containing secretory vesicles during Plasmodium gamete egress and sporozoite motility. PLOS Pathog 12:7e1005734
     [Google Scholar]
  72. 72.
    Kemp LE, Yamamoto M, Soldati-Favre D. 2013. Subversion of host cellular functions by the apicomplexan parasites. FEMS Microbiol. Rev. 37:4607–31
     [Google Scholar]
  73. 73.
    Kessler H, Herm-Götz A, Hegge S, Rauch M, Soldati-Favre D et al. 2008. Microneme protein 8—a new essential invasion factor in Toxoplasma gondii. J. Cell Sci. 121:Part 7947–56
     [Google Scholar]
  74. 74.
    Koch M, Baum J. 2016. The mechanics of malaria parasite invasion of the human erythrocyte—towards a reassessment of the host cell contribution. Cell Microbiol 18:3319–29
     [Google Scholar]
  75. 75.
    Koshy AA, Dietrich HK, Christian DA, Melehani JH, Shastri AJ et al. 2012. Toxoplasma co-opts host cells it does not invade. PLOS Pathog 8:7e1002825
     [Google Scholar]
  76. 76.
    Krishnamurthy S, Deng B, del Rio R, Buchholz KR, Treeck M et al. 2016. Not a simple tether: Binding of Toxoplasma gondii AMA1 to RON2 during invasion protects AMA1 from rhomboid-mediated cleavage and leads to dephosphorylation of its cytosolic tail. mBio 7:5e00754–16
     [Google Scholar]
  77. 77.
    Kudryashev M, Lepper S, Stanway R, Bohn S, Baumeister W et al. 2010. Positioning of large organelles by a membrane-associated cytoskeleton in Plasmodium sporozoites. Cell Microbiol 12:3362–71
     [Google Scholar]
  78. 78.
    Lamarque M, Besteiro S, Papoin J, Roques M, Normand BV-L et al. 2011. The RON2-AMA1 interaction is a critical step in moving junction-dependent invasion by apicomplexan parasites. PLOS Pathog 7:2e1001276
     [Google Scholar]
  79. 79.
    Lamarque MH, Roques M, Kong-Hap M, Tonkin ML, Rugarabamu G et al. 2014. Plasticity and redundancy among AMA-RON pairs ensure host cell entry of Toxoplasma parasites. Nat. Commun. 5:14098
     [Google Scholar]
  80. 80.
    Lebrun M, Carrthers VB, Cesbron-Delauw M-F 2020. Toxoplasma secretory proteins and their roles in parasite cell cycle and infection. Toxoplasma gondii: The Model Apicomplexan; Perspectives and Methods LM Weiss, K Kim 607–704 Amsterdam: Elsevier
     [Google Scholar]
  81. 81.
    Lebrun M, Michelin A, El Hajj H, Poncet J, Bradley PJ et al. 2005. The rhoptry neck protein RON4 re-localizes at the moving junction during Toxoplasma gondii invasion. Cell Microbiol 7:121823–33
     [Google Scholar]
  82. 82.
    Lemgruber L, Lupetti P, Souza WD, Vommaro RC. 2011. New details on the fine structure of the rhoptry of Toxoplasma gondii. Microsc. Res. Tech. 74:9812–18
     [Google Scholar]
  83. 83.
    Lentini G, Ben Chaabene R, Vadas O, Ramakrishnan C, Mukherjee B et al. 2021. Structural insights into an atypical secretory pathway kinase crucial for Toxoplasma gondii invasion. Nat. Commun. 12:13788
     [Google Scholar]
  84. 84.
    Lentini G, Dubois DJ, Maco B, Soldati-Favre D, Frénal K. 2019. The roles of Centrin 2 and Dynein Light Chain 8a in apical secretory organelles discharge of Toxoplasma gondii. Traffic 20:8583–600
     [Google Scholar]
  85. 85.
    Leykauf K, Treeck M, Gilson PR, Nebl T, Braulke T et al. 2010. Protein kinase A dependent phosphorylation of apical membrane antigen 1 plays an important role in erythrocyte invasion by the malaria parasite. PLOS Pathog 6:6e1000941
     [Google Scholar]
  86. 86.
    Liffner B, Balbin JM, Wichers JS, Gilberger T-W, Wilson DW. 2021. The ins and outs of Plasmodium rhoptries, focusing on the cytosolic side. Trends Parasitol 37:7638–50
     [Google Scholar]
  87. 87.
    Liffner B, Frölich S, Heinemann GK, Liu B, Ralph SA et al. 2020. PfCERLI1 is a conserved rhoptry associated protein essential for Plasmodium falciparum merozoite invasion of erythrocytes. Nat. Commun. 11:11411
     [Google Scholar]
  88. 88.
    Mageswaran SK, Guérin A, Theveny LM, Chen WD, Martinez M et al. 2021. In situ ultrastructures of two evolutionarily distant apicomplexan rhoptry secretion systems. Nat. Commun. 12:14983 Erratum 2021. Nat. Commun. 12:16203
     [Google Scholar]
  89. 89.
    Manzoni G, Marinach C, Topçu S, Briquet S, Grand M et al. 2017. Plasmodium P36 determines host cell receptor usage during sporozoite invasion. eLife 6:e25903
     [Google Scholar]
  90. 90.
    Martinez M, Chen WD, Cova MM, Molnár P, Mageswaran SK et al. 2022. situ structure and priming mechanism of the rhoptry secretion system in Plasmodium revealed by cryo-electron tomography. bioRxiv 2022.01.11.475861, Jan. 11
  91. 91.
    Mital J, Meissner M, Soldati D, Ward GE. 2005. Conditional expression of Toxoplasma gondii apical membrane antigen-1 (TgAMA1) demonstrates that TgAMA1 plays a critical role in host cell invasion. Mol. Biol. Cell 16:94341–49
     [Google Scholar]
  92. 92.
    Mordue DG, Håkansson S, Niesman I, Sibley LD. 1999. Toxoplasma gondii resides in a vacuole that avoids fusion with host cell endocytic and exocytic vesicular trafficking pathways. Exp. Parasitol. 92:287–99
     [Google Scholar]
  93. 93.
    Morisaki JH, Heuser JE, Sibley LD. 1995. Invasion of Toxoplasma gondii occurs by active penetration of the host cell. J. Cell Sci. 108:Part 62457–64
     [Google Scholar]
  94. 94.
    Nguitragool W, Bokhari AA, Pillai AD, Rayavara K, Sharma P et al. 2011. Malaria parasite clag3 genes determine channel-mediated nutrient uptake by infected red blood cells. Cell 145:5665–77
     [Google Scholar]
  95. 95.
    Nichols BA, Chiappino ML, O'Connor GR. 1983. Secretion from the rhoptries of Toxoplasma gondii during host-cell invasion. J. Ultrastruct. Res. 83:185–98
     [Google Scholar]
  96. 96.
    Nouvian R, Neef J, Bulankina AV, Reisinger E, Pangršič T et al. 2011. Exocytosis at the hair cell ribbon synapse apparently operates without neuronal SNARE proteins. Nat. Neurosci. 14:4411–13
     [Google Scholar]
  97. 97.
    Nozaki M, Baba M, Tachibana M, Tokunaga N, Torii M, Ishino T. 2020. Detection of the rhoptry neck protein complex in Plasmodium sporozoites and its contribution to sporozoite invasion of salivary glands. mSphere 5:4e00325–20
     [Google Scholar]
  98. 98.
    Obrova K, Cyrklaff M, Frank R, Mair GR, Mueller A-K. 2019. Transmission of the malaria parasite requires ferlin for gamete egress from the red blood cell. Cell Microbiol 21:5e12999
     [Google Scholar]
  99. 99.
    Pacheco NDS, Tosetti N, Koreny L, Waller RF, Soldati-Favre D. 2020. Evolution, composition, assembly, and function of the conoid in Apicomplexa. Trends Parasitol 36:8688–704
     [Google Scholar]
  100. 100.
    Paing MM, Tolia NH. 2014. Multimeric assembly of host-pathogen adhesion complexes involved in apicomplexan invasion. PLOS Pathog 10:6e1004120
     [Google Scholar]
  101. 101.
    Paredes-Santos TC, de Souza W, Attias M. 2012. Dynamics and 3D organization of secretory organelles of Toxoplasma gondii. J. Struct. Biol. 177:2420–30
     [Google Scholar]
  102. 102.
    Parker ML, Boulanger MJ. 2015. An extended surface loop on Toxoplasma gondii apical membrane antigen 1 (AMA1) governs ligand binding selectivity. PLOS ONE 10:5e0126206
     [Google Scholar]
  103. 103.
    Parker ML, Penarete-Vargas DM, Hamilton PT, Guérin A, Dubey JP et al. 2016. Dissecting the interface between apicomplexan parasite and host cell: insights from a divergent AMA-RON2 pair. PNAS 113:2398–403
     [Google Scholar]
  104. 104.
    Patel A, Perrin AJ, Flynn HR, Bisson C, Withers-Martinez C et al. 2019. Cyclic AMP signalling controls key components of malaria parasite host cell invasion machinery. PLOS Biol 17:5e3000264
     [Google Scholar]
  105. 105.
    Pinheiro PS, Houy S, Sørensen JB. 2016. C2-domain containing calcium sensors in neuroendocrine secretion. J. Neurochem. 139:6943–58
     [Google Scholar]
  106. 106.
    Pizarro JC, Vulliez-Le Normand B, Chesne-Seck M-L, Collins CR, Withers-Martinez C et al. 2005. Crystal structure of the malaria vaccine candidate apical membrane antigen 1. Science 308:5720408–11
     [Google Scholar]
  107. 107.
    Porchet E, Torpier G. 1977. Etude du germe infectieux de Sarcocystis tenella et Toxoplasma gondii par la technique du cryodécapage [Freeze fracture study of Toxoplasma and Sarcocystis infective stages]. Z. Parasitenkd 54:2101–24
     [Google Scholar]
  108. 108.
    Porchet-Hennere E, Nicolas G 1983. Are rhoptries of Coccidia really extrusomes?. J. Ultrastruct. Res. 84:2194–203
     [Google Scholar]
  109. 109.
    Possenti A, Cristina MD, Nicastro C, Lunghi M, Messina V et al. 2022. Functional characterization of the thrombospondin-related paralogous proteins rhoptry discharge factor 1 and 2 unveils phenotypic plasticity in Toxoplasma gondii rhoptry exocytosis. bioRxiv 2022.03.02.482699, Mar. 2
  110. 110.
    Poukchanski A, Fritz HM, Tonkin ML, Treeck M, Boulanger MJ, Boothroyd JC. 2013. Toxoplasma gondii sporozoites invade host cells using two novel paralogues of RON2 and AMA1. PLOS ONE 8:8e70637
     [Google Scholar]
  111. 111.
    Ragotte RJ, Higgins MK, Draper SJ. 2020. The RH5-CyRPA-Ripr complex as a malaria vaccine target. Trends Parasitol 36:6545–59
     [Google Scholar]
  112. 112.
    Reddy KS, Amlabu E, Pandey AK, Mitra P, Chauhan VS, Gaur D. 2015. Multiprotein complex between the GPI-anchored CyRPA with PfRH5 and PfRipr is crucial for Plasmodium falciparum erythrocyte invasion. PNAS 112:41179–84
     [Google Scholar]
  113. 113.
    Riglar DT, Richard D, Wilson DW, Boyle MJ, Dekiwadia C et al. 2011. Super-resolution dissection of coordinated events during malaria parasite invasion of the human erythrocyte. Cell Host Microbe 9:19–20
     [Google Scholar]
  114. 114.
    Riglar DT, Whitehead L, Cowman AF, Rogers KL, Baum J. 2016. Localisation-based imaging of malarial antigens during erythrocyte entry reaffirms a role for AMA1 but not MTRAP in invasion. J. Cell Sci. 129:1228–42
     [Google Scholar]
  115. 115.
    Risco-Castillo V, Topcu S, Son O, Briquet S, Manzoni G, Silvie O 2014. CD81 is required for rhoptry discharge during host cell invasion by Plasmodium yoelii sporozoites. Cell. Microbiol. 16:101533–48
     [Google Scholar]
  116. 116.
    Rizo J, Xu J. 2015. The synaptic vesicle release machinery. Annu. Rev. Biophys. 44:339–67
     [Google Scholar]
  117. 117.
    Robert-Gangneux F, Dardé M-L. 2012. Epidemiology of and diagnostic strategies for toxoplasmosis. Clin. Microbiol Rev 25:2264–96
     [Google Scholar]
  118. 118.
    Rodriguez M, Lustigman S, Montero E, Oksov Y, Lobo CA. 2008. PfRH5: a novel reticulocyte-binding family homolog of Plasmodium falciparum that binds to the erythrocyte, and an investigation of its receptor. PLOS ONE 3:10e3300
     [Google Scholar]
  119. 119.
    Roger N, Dubremetz JF, Delplace P, Fortier B, Tronchin G, Vernes A. 1988. Characterization of a 225 kilodalton rhoptry protein of Plasmodium falciparum. Mol. Biochem. Parasitol. 27:2–3135–41
     [Google Scholar]
  120. 120.
    Roux I, Safieddine S, Nouvian R, Grati M, Simmler M-C et al. 2006. Otoferlin, defective in a human deafness form, is essential for exocytosis at the auditory ribbon synapse. Cell 127:2277–89
     [Google Scholar]
  121. 121.
    Rugarabamu G, Marq J-B, Guérin A, Lebrun M, Soldati-Favre D. 2015. Distinct contribution of Toxoplasma gondii rhomboid proteases 4 and 5 to micronemal protein protease 1 activity during invasion. Mol. Microbiol. 97:2244–62
     [Google Scholar]
  122. 122.
    Sassmannshausen J, Pradel G, Bennink S. 2020. Perforin-like proteins of apicomplexan parasites. Front. Cell Infect. Microbiol. 10:578883
     [Google Scholar]
  123. 123.
    Schmidt MHH, Chen B, Randazzo LM, Bogler O. 2003. SETA/CIN85/Ruk and its binding partner AIP1 associate with diverse cytoskeletal elements, including FAKs, and modulate cell adhesion. J. Cell Sci. 116:Part 142845–55
     [Google Scholar]
  124. 124.
    Schrevel J, Asfaux-Foucher G, Hopkins JM, Robert V, Bourgouin C et al. 2008. Vesicle trafficking during sporozoite development in Plasmodium berghei: ultrastructural evidence for a novel trafficking mechanism. Parasitology 135:Part 11–12
     [Google Scholar]
  125. 125.
    Segev-Zarko L, Dahlberg PD, Sun S, Pelt DM, Sethian JA et al. 2022. Ionophore-stimulation promotes re-organization of the invasion machinery of Toxoplasma gondii. bioRxiv 2022.01.12.476068, Jan. 12
  126. 126.
    Sheiner L, Santos JM, Klages N, Parussini F, Jemmely N et al. 2010. Toxoplasma gondii transmembrane microneme proteins and their modular design. Mol. Microbiol. 77:4912–29
     [Google Scholar]
  127. 127.
    Shen B, Buguliskis JS, Lee TD, Sibley LD. 2014. Functional analysis of rhomboid proteases during Toxoplasma invasion. mBio 5:5e01795–14
     [Google Scholar]
  128. 128.
    Shen B, Sibley LD. 2012. The moving junction, a key portal to host cell invasion by apicomplexan parasites. Curr. Opin. Microbiol. 15:4449–55
     [Google Scholar]
  129. 129.
    Sherling ES, Perrin AJ, Knuepfer E, Russell MRG, Collinson LM et al. 2019. The Plasmodium falciparum rhoptry bulb protein RAMA plays an essential role in rhoptry neck morphogenesis and host red blood cell invasion. PLOS Pathog 15:9e1008049
     [Google Scholar]
  130. 130.
    Silvie O, Franetich JF, Charrin S, Mueller MS, Siau A et al. 2004. A role for apical membrane antigen 1 during invasion of hepatocytes by Plasmodium falciparum sporozoites. J. Biol. Chem. 279:109490–96
     [Google Scholar]
  131. 131.
    Singer M, Simon K, Forné I, Meissner M. 2022. A central protein complex essential for invasion in Toxoplasma gondii. bioRxiv 2022.02.24.481622, Feb. 24
  132. 132.
    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 6:2e1000746
     [Google Scholar]
  133. 133.
    Sparvoli D, Delabre J, Penarete-Vargas DM, Mageswaran SK, Tsypin LM et al. 2022. An apical membrane complex controls rhoptry exocytosis and invasion in Toxoplasma. bioRxiv 2022.02.25.481937, Feb. 25
  134. 134.
    Sparvoli D, Lebrun M. 2021. Unraveling the elusive rhoptry exocytic mechanism of Apicomplexa. Trends Parasitol 37:7622–37
     [Google Scholar]
  135. 135.
    Srinivasan P, Beatty WL, Diouf A, Herrera R, Ambroggio X et al. 2011. Binding of Plasmodium merozoite proteins RON2 and AMA1 triggers commitment to invasion. PNAS 108:3213275–80
     [Google Scholar]
  136. 136.
    Straub KW, Cheng SJ, Sohn CS, Bradley PJ. 2009. Novel components of the Apicomplexan moving junction reveal conserved and coccidia-restricted elements. Cell Microbiol 11:4590–603
     [Google Scholar]
  137. 137.
    Striepen B. 2013. Parasitic infections: time to tackle cryptosporidiosis. Nature 503:7475189–91
     [Google Scholar]
  138. 138.
    Suarez C, Lentini G, Ramaswamy R, Maynadier M, Aquilini E et al. 2019. A lipid-binding protein mediates rhoptry discharge and invasion in Plasmodium falciparum and Toxoplasma gondii parasites. Nat. Commun. 10:14041
     [Google Scholar]
  139. 139.
    Sun SY, Segev-Zarko L, Chen M, Pintilie GD, Schmid MF et al. 2022. Cryo-ET of Toxoplasma gives subnanometer insight into tubulin-based structures. PNAS 119:6e2111661119
     [Google Scholar]
  140. 140.
    Suss-Toby E, Zimmerberg J, Ward GE. 1996. Toxoplasma invasion: The parasitophorous vacuole is formed from host cell plasma membrane and pinches off via a fission pore. PNAS 93:168413–18
     [Google Scholar]
  141. 141.
    Sweeney KR, Morrissette NS, LaChapelle S, Blader IJ. 2010. Host cell invasion by Toxoplasma gondii is temporally regulated by the host microtubule cytoskeleton. Eukaryot. Cell 9:111680–89
     [Google Scholar]
  142. 142.
    Tagoe DNA, Drozda AA, Coppens I, Coleman BI, Gubbels M-J. 2020. Toxoplasma ferlin1 is a versatile and dynamic mediator of microneme trafficking and secretion. bioRxiv 2020.04.27.063628, Apr. 28
  143. 143.
    Tagoe DNA, Drozda AA, Falco JA, Bechtel TJ, Weerapana E, Gubbels M-J. 2021. Ferlins and TgDOC2 in Toxoplasma microneme, rhoptry and dense granule secretion. Life 11:3217
     [Google Scholar]
  144. 144.
    Takemae H, Sugi T, Kobayashi K, Gong H, Ishiwa A et al. 2013. Characterization of the interaction between Toxoplasma gondii rhoptry neck protein 4 and host cellular beta-tubulin. Sci. Rep. 3:3199
     [Google Scholar]
  145. 145.
    Tokunaga N, Nozaki M, Tachibana M, Baba M, Matsuoka K et al. 2019. Expression and localization profiles of rhoptry proteins in Plasmodium berghei sporozoites. Front. Cell. Infect. Microbiol. 9:316
     [Google Scholar]
  146. 146.
    Tonkin ML, Crawford J, Lebrun ML, Boulanger MJ. 2013. Babesia divergens and Neospora caninum apical membrane antigen 1 structures reveal selectivity and plasticity in apicomplexan parasite host cell invasion. Protein Sci 22:1114–27
     [Google Scholar]
  147. 147.
    Tonkin ML, Roques M, Lamarque MH, Pugnière M, Douguet D et al. 2011. Host cell invasion by apicomplexan parasites: insights from the co-structure of AMA1 with a RON2 peptide. Science 333:6041463–67
     [Google Scholar]
  148. 148.
    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]
  149. 149.
    Treeck M, Zacherl S, Herrmann S, Cabrera A, Kono M et al. 2009. Functional analysis of the leading malaria vaccine candidate AMA-1 reveals an essential role for the cytoplasmic domain in the invasion process. PLOS Pathog 5:3e1000322
     [Google Scholar]
  150. 150.
    Tyler JS, Boothroyd JC. 2011. The C-terminus of Toxoplasma RON2 provides the crucial link between AMA1 and the host-associated invasion complex. PLOS Pathog 7:2e1001282
     [Google Scholar]
  151. 151.
    Uboldi AD, Wilde M-L, McRae EA, Stewart RJ, Dagley LF et al. 2018. Protein kinase A negatively regulates Ca2+ signalling in Toxoplasma gondii. PLOS Biol 16:9e2005642
     [Google Scholar]
  152. 152.
    Volz JC, Yap A, Sisquella X, Thompson JK, Lim NTY et al. 2016. Essential role of the PfRh5/PfRipr/CyRPA complex during Plasmodium falciparum invasion of erythrocytes. Cell Host Microbe 20:160–71
     [Google Scholar]
  153. 153.
    Vulliez-Le Normand B, Saul FA, Hoos S, Faber BW, Bentley GA. 2017. Cross-reactivity between apical membrane antgen 1 and rhoptry neck protein 2 in P. vivax and P. falciparum: a structural and binding study. PLOS ONE 12:8e0183198
     [Google Scholar]
  154. 154.
    Vulliez-Le Normand B, Tonkin ML, Lamarque MH, Langer S, Hoos S et al. 2012. Structural and functional insights into the malaria parasite moving junction complex. PLOS Pathog 8:6e1002755
     [Google Scholar]
  155. 155.
    Wang M, Cao S, Du N, Fu J, Li Z et al. 2017. The moving junction protein RON4, although not critical, facilitates host cell invasion and stabilizes MJ members. Parasitology 144:111490–97
     [Google Scholar]
  156. 156.
    Wang X, Fu Y, Beatty WL, Ma M, Brown A et al. 2021. Cryo-EM structure of cortical microtubules from human parasite Toxoplasma gondii identifies their microtubule inner proteins. Nat. Commun. 12:13065
     [Google Scholar]
  157. 157.
    Weiss GE, Gilson PR, Taechalertpaisarn T, Tham W-H, de Jong NWM et al. 2015. Revealing the sequence and resulting cellular morphology of receptor-ligand interactions during Plasmodium falciparum invasion of erythrocytes. PLOS Pathog 11:2e1004670
     [Google Scholar]
  158. 158.
    Wilde M-L, Triglia T, Marapana D, Thompson JK, Kouzmitchev AA et al. 2021. Protein kinase A is essential for invasion of Plasmodium falciparum into human erythrocytes. mBio 10:5e01972–19
     [Google Scholar]
  159. 159.
    Wilson SK, Heckendorn J, Martorelli Di Genova B, Koch LL, Rooney PJ et al. 2020. A Toxoplasma gondii patatin-like phospholipase contributes to host cell invasion. PLOS Pathog 16:7e1008650
     [Google Scholar]
  160. 160.
    Wong W, Huang R, Menant S, Hong C, Sandow JJ et al. 2019. Structure of Plasmodium falciparum Rh5-CyRPA-Ripr invasion complex. Nature 565:7737118–21
     [Google Scholar]
  161. 161.
    World Health Organ 2020. World Malaria Report 2020: 20 Years of Global Progress and Challenges Geneva: World Health Organ.
  162. 162.
    Wright KE, Hjerrild KA, Bartlett J, Douglas AD, Jin J et al. 2014. Structure of malaria invasion protein RH5 with erythrocyte basigin and blocking antibodies. Nature 515:7527427–30
     [Google Scholar]
  163. 163.
    Yang ASP, Lopaticki S, O'Neill MT, Erickson SM, Douglas DN et al. 2017. AMA1 and MAEBL are important for Plasmodium falciparum sporozoite infection of the liver. Cell. Microbiol. 19:9e12745
     [Google Scholar]
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How Apicomplexa Parasites Secrete and Build Their Invasion Machinery
Annual Review of Microbiology 76, 619 (2022); https://doi.org/10.1146/annurev-micro-041320-021425
/content/journals/10.1146/annurev-micro-041320-021425
/content/journals/10.1146/annurev-micro-041320-021425
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