CoChat
Sign Up
Cited by 254Toxoplasma gondii Research StudiesParasitic Infections and DiagnosticsTrypanosoma species research and implications

Invasion and intracellular survival by protozoan parasites

Open access
David Sibley, L.·2011·Immunological Reviews
DOI 10.1111/j.1600-065x.2010.00990.xPMC PMC3697736
Open this paper in CoChat — free account

Abstract

Summary: Intracellular parasitism has arisen only a few times during the long ancestry of protozoan parasites including in diverse groups such as microsporidians, kinetoplastids, and apicomplexans. Strategies used to gain entry differ widely from injection (e.g. microsporidians), active penetration of the host cell (e.g. Toxoplasma), recruitment of lysosomes to a plasma membrane wound (e.g. Trypanosoma cruzi), to host cell‐mediated phagocytosis (e.g. Leishmania). The resulting range of intracellular niches is equally diverse ranging from cytosolic (e.g. T. cruzi) to residing within a non‐fusigenic vacuole (e.g. Toxoplasma, Encephalitozoon) or a modified phagolysosome (e.g. Leishmania). These lifestyle choices influence access to nutrients, interaction with host cell signaling pathways, and detection by pathogen recognition systems. As such, intracellular life requires a repertoire of adaptations to assure entry–exit from the cell, as well as to thwart innate immune mechanisms and prevent clearance. Elucidating these pathways at the cellular and molecular level may identify key steps that can be targeted to reduce parasite survival or augment immunologic responses and thereby prevent disease.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1111/j.1600-065x.2010.00990.x

Cites

1 of 1 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Both intracellular and extracellular parasites have evolved mechanisms to avoid or survive the immune response and to use it for their own benefit.

    “Both intracellular and extracellular parasites have evolved mechanisms to not only avoid or survive the immune response, but also to use it for their own benefit (93, 94).”

    From Macrophage Cytokines: Involvement in Immunity and Infectious Diseases (2014) · cites this paper as [93]

    The Introduction describes intracellular parasites escaping host defenses, and the Apicomplexans section reports that T. gondii resists immune clearance and alters host immune signaling. These passages support immune evasion and manipulation by intracellular parasites, but the paper does not establish the claim for extracellular parasites. (LLM, conf=0.84)

    Experimental — accuracy not yet measured

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 216

  1. [1]Baldauf SL The deep roots of eukaryotes Science 2003 300 1703 1706 12805537
  2. [2]Shiflett AM Johnson PJ Mitochondrion-related organelles in eukaryotic protists Annu Rev Microbiol 2010 PMC3208401 20528687
  3. [3]Loftus B The genome of the protist parasite Entamoeba histolytica Nature 2005 433 865 868 15729342
  4. [4]Keeling PJ Fast NM Microsporidia: biology and evolution of highly reduced intracellular parasites Annu Rev Microbiol 2002 56 93 116 12142484
  5. [5]Escalante AA Ayala FJ Evolutionary origin of Plasmodium and other Apicomplexa based on rRNA genes Proc Natl Acad Sci USA 1995 92 5793 7597031 PMC41587
  6. [6]Simpson AG Stevens JR Lukes J The evolution and diversity of kinetoplastid flagellates Trends Parasitol 2006 22 168 174 16504583
  7. [7]Haas A Everybody has a home of their own - “The phagosome zoo” Schaible UE Haas A Intracellular Niches of Microbes Weinheim Wiley VCH 2009 159 190
  8. [8]Kennedy AD DeLeo FR Neutrophil apoptosis and the resolution of infection Immunol Res 2009 43 25 61 19066741
  9. [9]Martens S Howard JC The interferon-inducible GTPases Annu Rev Cell Dev Biol 2006 22 559 589 16824009
  10. [11]Takeda K Akira S Toll receptors and pathogen resistance Cellular Mirobiology 2003 5 143 153 12614458
  11. [12]Inohara Chamaillard McDonald C Nunez G NOD-LRR proteins: role in host-microbial interactions and inflammatory disease Annu Rev Biochem 2005 74 355 383 15952891
  12. [13]Didier ES Didier PJ Snowden KF Shadduck JA Microsporidiosis in mammals Microb Infect 2000 2 709 720 10884622
  13. [14]Katinka MD Genome sequence and gene compaction of the eukaryote parasite Encephalitozoon cuniculi Nature 2001 414 450 453 11719806
  14. [15]Keeling PJ Fast NM Law JS Williams BA Slamovits CH Comparative genomics of microsporidia Folia Parasitol (Praha) 2005 52 8 14 16004359
  15. [16]Texier C Vidau C Vigues B El Alaoui H Delbac F Microsporidia: a model for minimal parasite894 host interactions Curr Opin Microbiol 2010 20542726
  16. [17]Bigliardi E Sacchi L Cell biology and invasion of the microsporidia Microb Infect 2001 3 373 379 11369274
  17. [18]Pleshinger J Weidner E The microsporidian spore invasion tube. IV. Discharge activation begins with pH-triggered Ca2+ influx J Cell Biol 1985 100 1834 1838 2581975 PMC2113605
  18. [19]Weidner E The microsporidian spore invasion tube. III. Tube extrusion and assembly J Cell Biol 1982 93 976 979 7119008 PMC2112143
  19. [21]Frixione E Ruiz L Cerbon J Undeen AH Germination of Nosema algerae (Microspora) spores: conditional inhibition by D2O, ethanol and Hg2+ suggests dependence of water influx upon membrane hydration and specific transmembrane pathways J Eukaryot Microbiol 1997 44 109 116 9190262
  20. [22]Xu Y Weiss LM The microsporidian polar tube: a highly specialised invasion organelle Int J Parasitol 2005 35 941 953 16005007 PMC3109658
  21. [23]Weidner E Interactions between Encephalitozoon cuniculi and macrophages. Parasitophorous vacuole growth and absence of lysosomal fusion Z Parasitenk Parasitol Res 1975 47 109 1189574
  22. [24]Couzinet S Cejas E Schittny J Deplazes P Weber R Zimmerli S Phagocytic uptake of Encephalitozoon cuniculi by nonprofessional phagocytes Infect Immun 2000 68 6939 6945 11083817 PMC97802
  23. [25]Leitch GJ Ward TL Shaw AP Newman G Apical spore phagocytosis is not a significant route of infection of differentiated enterocytes by Encephalitozoon intestinalis Infect Immun 2005 73 7697 7704 16239574 PMC1273909
  24. [26]Franzen C Muller A Hartmann P Salzberger B Cell invasion and intracellular fate of Encephalitozoon cuniculi (Microsporidia) Parasitol 205 130 285 292 15796011
  25. [27]Orlik J Bottcher K Gross U Bohne W Germination of phagocytosed E. cuniculi spores does not significantly contribute to parasitophorous vacuole formation in J774 cells Parasitol Res 2010 106 753 755 20107836 PMC2815800
  26. [28]Fasshauer V Gross U Bohne W The parasitophorous vacuole membrane of Encephalitozoon cuniculi lacks host cell membrane proteins immediately after invasion Eukaryot Cell 2005 4 221 224 15643077 PMC544160
  27. [29]Ronnebaumer K Gross U Bohne W The nascent parasitophorous vacuole membrane of Encephalitozoon cuniculi is formed by host cell lipids and contains pores which allow nutrient uptake Eukaryot Cell 2008 7 1001 1008 18408058 PMC2446663
  28. [30]Hayman JR Southern TR Nash TE Role of sulfated glycans in adherence of the microsporidian Encephalitozoon intestinalis to host cells in vitro Infect Immun 2005 73 841 848 15664924 PMC546933
  29. [31]Southern TR Jolly CE Lester ME Hayman JR EnP1, a microsporidian spore wall protein that enables spores to adhere to and infect host cells in vitro Eukaryot Cell 2007 6 1354 1362 17557882 PMC1951136
  30. [32]Keeling PJ The reduced genome of the parasitic microsporidian Enterocytozoon bieneusi lacks genes for core carbon metabolism Genome Biol Evol 2010 2 304 309 20624735 PMC2942035
  31. [33]Tsaousis AD Kunji ER Goldberg AV Lucocq JM Hirt RP Embley TM A novel route for ATP acquisition by the remnant mitochondria of Encephalitozoon cuniculi Nature 2008 453 553 556 18449191
  32. [34]Niederkorn JY Shadduck JA Schmidt EC Susceptibility of selected inbred strains of mice to Encephalitozoon cuniculi J Infect Dis 1981 144 249 253 6792298
  33. [35]Khan IA Moretto M Role of gamma interferon in cellular immune response against murine Encephalitozoon cuniculi infection Infect Immun 1999 67 1887 1893 10085032 PMC96542
  34. [36]Moretto MM Lawlor EM Khan IA Lack of interleukin-12 in p40-deficient mice leads to poor CD8+ T-cell immunity against Encephalitozoon cuniculi infection Infect Immun 2010 78 2505 2511 20308292 PMC2876566
  35. [37]Khan IA Schwartzman JD Kasper LH Moretto M CD8+ CTLs are essential for protective immunity against Encephalitozoon cuniculi infection J Immunol 1999 162 6086 6091 10229850
  36. [38]Moretto M Casciotti L Durell B Khan IA Lack of CD4+ T cells does not affect induction of CD8+ T-cell immunity against Encephalitozoon cuniculi infection Infect Immun 2000 68 6223 6232 11035729 PMC97703
  37. [39]Moretto M Durell B Schwartzman JD Khan IA Gamma delta T cell-deficient mice have a down951 regulated CD8+ T cell immune response against Encephalitozoon cuniculi infection J Immunol 2001 166 7389 7397 11390490
  38. [40]Moretto MM Weiss LM Combe CL Khan IA IFN-gamma-producing dendritic cells are important for priming of gut intraepithelial lymphocyte response against intracellular parasitic infection J Immunol 2007 179 2485 2492 17675510 PMC3109618
  39. [41]Fischer J West J Agochukwu N Suire C Hale-Donze H Induction of host chemotactic response by Encephalitozoon spp Infect Immun 2007 75 1619 1625 17178789 PMC1865724
  40. [42]Fischer J Suire C Hale-Donze H Toll-like receptor 2 recognition of the microsporidia Encephalitozoon spp. induces nuclear translocation of NF-kappaB and subsequent inflammatory responses Infect Immun 2008 76 4737 4744 18678660 PMC2546815
  41. [43]Levine ND The Protozoan Phylum Apicomplexa Boca Raton CRC Press 1988
  42. [44]Leander BS Marine gregarines: evolutionary prelude to the apicomplexan radiation? Trends Parasitol 2008 24 60 67 18226585
  43. [45]Morrissette NS Sibley LD Cytoskeleton of apicomplexan parasites Microbiol Mol Biol Rev 2002 66 21 38 11875126 PMC120781
  44. [46]Sibley LD Invasion strategies of intracellular parasites Science 2004 304 248 253 15073368
  45. [47]Barta JR Phylogenetic analysis of the class sporozoea (Phylum Apicomplexan Levine 1970): evidence for the independent evolution of heteroxenous life cycles J Parasitol 1989 75 195 206 2494316
  46. [48]Tzipori S Widmer G A hundred-year retrospective on cryptosporidiosis Trends Parasitol 2008 24 184 189 18329342 PMC2716703
  47. [49]Homer MJ Aguilar-Delfin I Telford SR 3rd Krause PJ Persing DH Babesiosis Clin Microbiol Rev 2000 13 451 469 10885987 PMC88943
  48. [50]Miller LH Good MF Milon G Malaria pathogenesis Science 1994 264 1878 1883 8009217
  49. [51]Dobbelaere DA Kuenzi P The strategies of the Theileria parasite: a new twist in host-pathogen interactions Curr Opin Immunol 2004 16 524 530 15245750
  50. [52]Dubey JP Toxoplasma, Hammondia, Besniotia, Sarcocystis, and other tissue cyst-forming coccidia of man and animals Kreier JP Parasitic Protozoa New York Academic Press 1977 101 237
  51. [53]Dubey JP Toxoplasmosis of animals and humans Boca Raton CRC Press 2010
  52. [54]Su C Evans D Cole RH Kissinger JC Ajioka JW Sibley LD Recent expansion of Toxoplasma through enhanced oral transmission Science 2003 299 414 416 12532022
  53. [55]Sibley LD Ajioka JW Population structure of Toxoplasma gondii: Clonal expansion driven by infrequent recombination and selective sweeps Ann Rev Microbiol 2008 62 329 351 18544039
  54. [56]McCabe RE Antitoxoplasma chemotherapy Joynson DHM Wreghitt TG Toxoplasmosis: a comprehensive clinical guide Cambridge Cambridge Univ. Press 2001 319 359
  55. [57]Joynson DH Wreghitt TJ Toxoplasmosis: A comprehensive clinical guide Cambridge University Press 2001
  56. [58]Heintzelman MB Cellular and molecular mechanics of gliding locomotion in eukaryotes Int Rev Cytol 2006 251 79 129 16939778
  57. [59]Håkansson S Morisaki H Heuser JE Sibley LD Time-lapse video microscopy of gliding motility in Toxoplasma gondii reveals a novel, biphasic mechanism of cell locomotion Mol Biol Cell 1999 10 3539 3547 10564254 PMC25631
  58. [60]Meissner M Schluter D Soldati D Role of Toxoplasma gondii myosin A in powering parasite gliding and host cell invasion Science 2002 298 837 840 12399593
  59. [61]Sahoo N Beatty WL Heuser JE Sept D Sibley LD Unusual kinetic and structural properties control rapid assembly and turnover of actin in the parasite Toxoplasma gondii Mol Biol Cell 2006 17 895 906 16319175 PMC1356598
  60. [62]Starnes GL Coincon M Sygusch J Sibley LD Aldolase is essential for energy production and bridging adhesin-actin cytoskeletal interactions during parasite invasion of host cells Cell Host Microbe 2009 5 353 364 19380114 PMC2683947
  61. [63]Huynh MH Carruthers VB Toxoplasma MIC2 is a major determinant of invasion and virulence PloS Pathog 2006 2 753 762 PMC1550269 16933991
  62. [64]Dowse T Soldati D Rhomboid-like proteins in Apicomplexa: phylogeny and nomenclature Trends Parastiol 2005 35 747 756 15922242
  63. [65]Buguliskis JS Brossier F Shuman J Sibley LD Rhomboid 4 (ROM4) affects the processing of surface adhesins and facilitates host cell invasion by Toxoplasma gondii PLoS Pathog 2010 6 e1000858 20421941 PMC2858701
  64. [66]Ménard R Gliding motility and cell invasion by Apicomplexa: insights from the Plasmodium sporozoite Cell Micro 2001 3 63 73 11207621
  65. [67]Soldati D Meissner M Toxoplasma as a novel system for motility Curr Opin Cell Biol 2004 16 32 40 15037302
  66. [68]Tardieux I Menard R Migration of Apicomplexa across biological barriers: the Toxoplasma and Plasmodium rides Traffic 2008 9 627 635 18194412 PMC2329915
  67. [69]Baum J Papenfuss AT Baum B Speed TP Cowman AF Regulation of apicomplexan actin-based motility Nat Rev Microbiol 2006 4 621 628 16845432
  68. [70]Dobrowolski JM Sibley LD Toxoplasma invasion of mammalian cells is powered by the actin cytoskeleton of the parasite Cell 1996 84 933 939 8601316
  69. [71]Morisaki JH Heuser JE Sibley LD Invasion of Toxoplasma gondii occurs by active penetration of the host cell J Cell Sci 1995 108 2457 2464 7673360
  70. [72]Gonzalez V Host cell entry by apicomplexa parasites requires actin polymerization in the host cell Cell Host Microbe 2009 5 259 272 19286135
  71. [73]Amino R Host cell traversal is important for progression of the malaria parasite through the dermis to the liver Cell Host Microbe 2008 3 88 96 18312843
  72. [74]Suss-Toby E Zimmerberg J Ward GE Toxoplasma invasion: The parasitophorous vacuole is formed from host cell plasma membrane and pinches off via a fusion pore Proc Natl Acad Sci USA 1996 93 8413 8418 8710885 PMC38685
  73. [75]Charron AJ Sibley LD Molecular partitioning during host cell penetration by Toxoplasma gondii Traffic 2004 5 855 867 15479451
  74. [76]Mordue DG Desai N Dustin M Sibley LD 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 1783 1792 10601353 PMC2195726
  75. [77]Murphy SC Erythrocyte detergent-resistant membrane proteins: their characterization and selective uptake during malarial infection Blood 2004 103 1920 1928 14592818
  76. [78]Mordue D Håkansson S Niesman I Sibley LD Toxoplasma gondii resides in a vacuole that avoids fusion with host cell endocytic and exocytic vesicular trafficking pathways Exp Parasitol 1999 92 87 99 10366534
  77. [79]Mordue DG Sibley LD 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 9379044
  78. [80]Schwab JC Beckers CJM Joiner KA The parasitophorous vacuole membrane surrounding intracellular Toxoplasma gondii functions as a molecular sieve Proc Natl Acad Sci USA 1994 91 509 513 8290555 PMC42978
  79. [81]Carruthers VB Sibley LD Sequential protein secretion from three distinct organelles of Toxoplasma gondii accompanies invasion of human fibroblasts Eur J Cell Biol 1997 73 114 123 9208224 PMC13475723
  80. [82]Carruthers VB Tomley FM Microneme proteins in apicomplexans Subcell Biochem 2008 47 33 45 18512339 PMC2847500
  81. [83]Anantharaman V Iyer LM Balaji S Aravind L Adhesion molecules and other secreted host1051 interaction determinants in Apicomplexa: insights from comparative genomics Int Rev Cytol 2007 262 1 74 17631186
  82. [84]Lourido S Shuman J Zhang C Shokat KM Hui R Sibley LD Calcium-dependent protein kinase 1 is an essential regulator of exocytosis in Toxoplasma Nature 2010 465 359 362 20485436 PMC2874977
  83. [85]Billker O Lourido S Sibley LD Calcium-dependent signaling and kinases in apicomplexan parasites Cell Host Microbe 2009 5 612 622 19527888 PMC2718762
  84. [86]Mital J Meissner M Soldati D Ward GE 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 4341 4349 16000372 PMC1196342
  85. [87]Leykauf K Protein kinase a dependent phosphorylation of apical membrane antigen 1 plays an important role in erythrocyte invasion by the malaria parasite PLoS Pathog 2010 6 e1000941 20532217 PMC2880582
  86. [88]Montero E Rodriguez M Oksov Y Lobo CA Babesia divergens apical membrane antigen 1 and its interaction with the human red blood cell Infect Immun 2009 77 4783 4793 19720759 PMC2772537
  87. [89]Håkansson S Charron AJ Sibley LD Toxoplasma evacuoles: a two-step process of secretion and fusion forms the parasitophorous vacuole EMBO J 2001 20 3132 3144 11406590 PMC150190
  88. [90]Bradley PJ Sibley LD Rhoptries: an arsenal of secreted virulence factors Curr Opin Microbiol 2007 10 582 587 17997128 PMC2682365
  89. [91]Alexander DL Mital J Ward GE Bradley PJ Boothroyd JC Identification of the moving junction complex of Toxoplasma gondii: a collaboration between distinct secretory organelles PLoS Pathog 2005 1 137 149 PMC1262624 16244709
  90. [92]Besteiro S Michelin A Poncet J Dubremetz J Lebrun M Export of a Toxoplasma gondii rhoptry neck protein complex at the host cell membrane to form the moving junction during invasion PLoS Path 2009 5 e1000309 PMC2642630 19247437
  91. [93]Straub KW Cheng SJ Sohn CS Bradley PJ Novel components of the apicomplexan moving junction reveal conserved and coccidia-restricted elements Cell Microbiol 2009 11 590 603 19134112 PMC2798130
  92. [94]Richard D Interaction between Plasmodium falciparum apical membrane antigen 1 and the rhoptry neck protein complex defines a key step in the erythrocyte invasion process of malaria parasites J Biol Chem 2010 285 14812 14822 PMC2863225 20228060
  93. [95]Blackman MJ Malaria proteases and host cell egress: an emerging casade Cell Microbiol 2008 10 1925 1934 18503638 PMC2610400
  94. [96]Roiko MS Carruthers VB New roles for perforins and proteases in apicomplexan egress Cell Microbiol 2009 11 1444 1452 19614666 PMC3953416
  95. [97]Nagamune K Hicks LM Fux B Broissier F Chini EN Sibley LD Abscisic acid controls calcium1086 dependent egress and development in Toxoplasma gondii Nature 2008 451 207 211 18185591 PMC2877910
  96. [98]Kafsack BF Pena JD Coppens I Ravindran S Boothroyd JC Carruthers VB Rapid membrane disruption by a perforin-like protein facilitates parasite exit from host cells Science 2009 323 530 533 19095897 PMC2662845
  97. [99]Glushakova S Humphrey G Leikina E Balaban A Miller J Zimmerberg J New stages in the program of malaria parasite egress imaged in normal and sickle erythrocytes Curr Biol 2010 20 1117 1121 20537541 PMC3541015
  98. [100]Aly AS Matuschewski K A malarial cysteine protease is necessary for Plasmodium sporozoite egress from oocysts J Exp Med 2005 202 225 230 16027235 PMC2213010
  99. [101]Yeoh S Subcellular discharge of a serine protease mediates release of invasive malaria parasites from host erythrocytes Cell 2007 131 1072 1083 18083098
  100. [102]Dvorin JD A plant-like kinase in Plasmodium falciparum regulates parasite egress from erythrocytes Science 2010 328 910 912 20466936 PMC3109083
  101. [103]Sturm A Manipulation of host hepatocytes by the malaria parasite for delivery into liver sinusoids Science 2006 313 1287 1290 16888102
  102. [104]Chandramohanadas R Apicomplexan parasites co-opt host calpains to facilitate their escape from infected cells Science 2009 324 794 797 19342550 PMC3391539
  103. [105]Wilson CB Tsai V Remington JS Failure to trigger the oxidative burst of normal macrophages J Exp Med 1980 151 328 346 7356726 PMC2185778
  104. [106]Adams LB Hibbs JB Taintor RR Krahenbuhl JL Microbiostatic effect of murine-activated macrophages for Toxoplasma gondii: Role for synthesis of inorganic nitrogen oxides from L-arginine J Immunol 1990 144 2725 2729 2319133
  105. [107]Pfefferkorn ER Interferon-γ blocks the growth of Toxoplasma gondii in human fibroblasts by inducing the host to degrade tryptophan Proc Natl Acad Sci USA 1984 81 908 912 6422465 PMC344948
  106. [108]Taylor GA Feng CG Sher A Control of IFN-γ mediated host resistance to intracellular pathogens by immunity-related GTPases (p47 GTPases) Microb Infect 2007 9 1644 1651 18023232
  107. [109]Zhao Z Autophagosome-independent essential function for the autophagy protein Atg5 in cellular immunity to intracellular pathogens Cell Host Microbe 2008 4 458 469 18996346 PMC2682425
  108. [110]Khaminets A Coordinated loading of IRG resistance GTPases on to the Toxoplasma gondii parasitophorous vacuole Cell Microbiol 2010 12 939 961 20109161 PMC2901525
  109. [111]Zhao Y Ferguson DJ Wilson DC Howard JC Sibley LD Yap GS Virulent Toxoplasma gondii evade immunity-related GTPas-mediated parasite vacuole disruption within primed macrophages J Immunol 2009 182 3775 3781 19265156 PMC2848815
  110. [112]Leng J Butcher BA Denkers EY Dysregulation of macrophage signal transduction by Toxoplasma gondii: past progress and recent advances Parasite Immunol 2009 31 717 728 19891610 PMC2774889
  111. [113]Kim SK Fouts AE Boothroyd JC Toxoplasma gondii dysregulates IFN-γ inducible gene expression in human fiboblasts: insights from a genome-wide transcriptional profiling J Immunol 2007 178 5154 5165 17404298
  112. [114]Hippe D Gais A Gross U Luder CG Modulation of caspase activation by Toxoplasma gondii Methods Mol Biol 2009 470 275 288 19089389
  113. [115]Blader I Manger ID Boothroyd JC Microarray analysis reveals previously unknown changes in Toxoplasma gondii infected human cells J Biol Chem 2001 276 24223 24231 11294868
  114. [116]Phelps ED Sweeney KR Blader IJ Toxoplasma gondii rhoptry discharge correlates with activation of the early growth response 2 host cell transcription factor Infect Immun 2008 76 4703 4712 18678671 PMC2546823
  115. [117]Molestina RE Sinai AP Host and parasite-derived IKK activities direct distinct temporal phases of NF-kappaB activation and target gene expression following Toxoplasma gondii infection J Cell Sci 2005 118 5785 5796 16339966
  116. [118]Su C Howe DK Dubey JP Ajioka JW Sibley LD Identification of quantitative trait loci controlling acute virulence in Toxoplasma gondii Proc Natl Acad Sci (USA) 2002 99 10753 10758 12149482 PMC125035
  117. [119]Khan A Composite genome map and recombination parameters derived from three archetypal lineages of Toxoplasma gondii Nuc Acids Res 2005 33 2980 2992 PMC1137028 15911631
  118. [120]Saeij JPJ Coller S Boyle JP Jerome ME White ME Boothroyd JC Toxoplasma co-opts host gene expression by injection of a polymorphic kinase homologue Nature 2007 445 324 327 17183270 PMC2637441
  119. [121]Robben PM Mordue DG Truscott SM Takeda K Akira S Sibley LD Production of IL-12 by macrophages infected with Toxoplasma gondii depends on the parasite genotype J Immunol 2004 172 3686 3694 15004172
  120. [122]Yamamoto M A single polymorphic amino acid on Toxoplasma gondii kinase ROP16 determines the direct and strain-specific activation of Stat3 J Exp Med 2009 206 2747 2760 19901082 PMC2806617
  121. [123]Ong YC Reese ML Boothroyd JC Toxoplasma rhoptry protein 16 (ROP16) subverts host function by direct tyrosine phosphorylation of STAT6 J Biol Chem 2010 PMC2937901 20624917
  122. [124]Taylor S A secreted serine-threonine kinase determines virulence in the eukaryotic pathogen Toxoplasma gondii Science 2006 314 1776 1780 17170305
  123. [125]Saeij JPJ Polymorphic secreted kinases are key virulence factors in toxoplasmosis Science 2006 314 1780 1783 17170306 PMC2646183
  124. [126]Khan A Taylor S Ajioka JW Rosenthal BM Sibley LD Selection at a single locus leads to widespread expansion of Toxoplasma gondii lineages that are virulence in mice PLoS Genetics 2009 5 e1000404 19266027 PMC2644818
  125. [127]Yap GS Sher A Cell-mediated immunity to Toxoplasma gondii: initiation, regulation and effector function Immunobiol 1999 201 240 247 10631573
  126. [128]Mordue DG Sibley LD A novel population of Gr-1+ activated macrophages induced during acute toxoplasmosis J Leukoc Biol 2003 74 1015 1025 12972511
  127. [129]Robben PR LaRegina M Kuziel WA Sibley LD Recruitment of Gr-1+ monocytes is essential for control of acute toxoplasmosis J Exp Med 2005 201 1761 1769 15928200 PMC2213275
  128. [130]Dunay IR Gr1+ inflammatory monocytes are required for mucosal resistance to the pathogen Toxoplasma gondii Immunity 2008 29 306 317 18691912 PMC2605393
  129. [131]Barragan A Sibley LD Migration of Toxoplasma gondii across biological barriers Trends Microbiol 2003 11 426 430 13678858
  130. [132]Courret N Darche S Songio P Milon G Buzoni-Gatel D Tardieux I CD11c and CD11b expressing mouse leukocytes transport single Toxoplasma gondii tachyzoites to the brain Blood 2005 107 309 316 16051744 PMC1895351
  131. [133]Lambert H Barragan A Modelling parasite dissemination: host cell subversion and immune evasion by Toxoplasma gondii Cell Microbiol 2010 12 292 300 19995386
  132. [134]Wetzel DM Schmidt J Kuhlenschmidt M Dubey JP Sibley LD Gliding motility leads to active cellular invasion by Cryptosporidium parvum sporozoites Infect Immun 2005 73 5379 5387 16113253 PMC1231075
  133. [135]Borowski H Clode PL Thompson RC Active invasion and/or encapsulation? A reappraisal of host-cell parasitism by Cryptosporidium Trends Parasitol 2008 24 509 516 18801703
  134. [136]Forney JR DeWald DB Yang S Speer CA Healey MC A role for host phosphoinositide 3-kinase and cytoskeletal remodeling during Cryptosporidium parvum infection Infect Immun 1999 67 844 852 9916099 PMC96395
  135. [137]Shaw MK Cell invasion by Theileria sporozoites Trends Parasitol 2003 19 2 6 12488213
  136. [138]Lodge R Descoteaux A Modulation of phagolysosome biogenesis by the lipophosphoglycan of Leishmania Clin Immunol 2005 114 256 265 15721836
  137. [139]Lodge R Descoteaux A Leishmania invasion and phagosome biogenesis Subcell Biochem 2008 47 174 181 18512351
  138. [140]Holm A Tejle K Magnusson KE Descoteaux A Rasmusson B Leishmania donovani lipophosphoglycan causes periphagosomal actin accumulation: correlation with impaired translocation of PKC-alpha and defective phagosome maturation Cell Microbiol 2001 3 439 447 11437830
  139. [141]Lodge R Descoteaux A Leishmania donovani promastigotes induce periphagosomal F-actin accumulation through retention of the GTPase Cdc42 Cell Microbiol 2005 7 1647 1658 16207251
  140. [142]Lodge R Diallo TO Descoteaux A Leishmania donovani lipophosphoglycan blocks NADPH oxidase assembly at the phagosome membrane Cell Microbiol 2006 8 1922 1931 16848789
  141. [143]Rodriguez NE Gaur U Wilson ME Role of caveolae in Leishmania chagasi phagocytosis and intracellular survival in macrophages Cell Microbiol 2006 8 1106 1120 16819964
  142. [144]Ueno N Bratt CL Rodriguez NE Wilson ME Differences in human macrophage receptor usage, lysosomal fusion kinetics and survival between logarithmic and metacyclic Leishmania infantum chagasi promastigotes Cell Microbiol 2009 11 1827 1841 19702651 PMC2788030
  143. [145]Flannagan RS Cosio G Grinstein S Antimicrobial mechanisms of phagocytes and bacterial evasion strategies Nat Rev Microbiol 2009 7 355 366 19369951
  144. [146]Lodge R Descoteaux A Phagocytosis of Leishmania donovani amastigotes is Rac1 dependent and occurs in the absence of NADPH oxidase activation Eur J Immunol 2006 36 2735 2744 16955522
  145. [147]Wilson J Control of parasitophorous vacuole expansion by LYST/Beige restricts the intracellular growth of Leishmania amazonensis PLoS Pathog 2008 4 e1000179 18927622 PMC2562527
  146. [148]Sacks DL Leishmania-sand fly interactions controlling species-specific vector competence Cell Microbiol 2001 3 189 196 11298643
  147. [149]Desjardins M Descoteaux A Inhibition of phagolysosomal biogenesis by the Leishmania lipophosphoglycan J Exp Med 1997 185 2061 2068 9182677 PMC2196352
  148. [150]Scianimanico S Desrosiers M Dermine JF Meresse S Descoteaux A Desjardins M Impaired recruitment of the small GTPase rab7 correlates with the inhibition of phagosome maturation by Leishmania donovani promastigotes Cell Microbiol 1999 1 19 32 11207538
  149. [151]Dermine JF Scianimanico S Prive C Descoteaux A Desjardins M Leishmania promastigotes require lipophosphoglycan to actively modulate the fusion properties of phagosomes at an early step of phagocytosis Cell Microbiol 2000 2 115 126 11207568
  150. [152]Vinet AF Fukuda M Turco SJ Descoteaux A The Leishmania donovani lipophosphoglycan excludes the vesicular proton-ATPase from phagosomes by impairing the recruitment of synaptotagmin V PLoS Pathog 2009 5 e1000628 19834555 PMC2757729
  151. [153]Ilg T Demar M Harbecke D Phosphoglycan repeat-deficient Leishmania mexicana parasites remain infectious within monocytes J Immunol 2001 276 4988 4997 11071892
  152. [154]Schaible UE Schlesinger PH Steinberg TH Mangel WF Kobayashi T Russell DG Parasitophorous vacuoles of Leishmania mexicana acquire macrophages form the host cell cytosol via two independent routes J Cell Sci 1999 112 681 693 9973603
  153. [155]Huynh C Sacks DL Andrews NW A Leishmania amazonensis ZIP family iron transporter is essential for parasite replication within macrophage phagolysosomes J Exp Med 2006 203 2363 2375 17000865 PMC2118100
  154. [156]Alexander J Satoskar AR Russell DG Leishmania species: models of intracellular parasitism J Cell Sci 1999 112 2993 3002 10462516
  155. [157]Matte C Descoteaux A Leishmania donovani amastigotes impair IFN-gamma-induced STAT1-alpha nuclear translocation by blocking the interaction between STAT1-alpha and importin-alpha5 Infect Immun 2010 PMC2937469 20566692
  156. [158]Peters NC Sacks DL The impact of vector-mediated neutrophil recruitment on cutaneous leishmaniasis Cell Microbiol 2009 11 1290 1296 19545276 PMC3431610
  157. [159]Segal AW How neutrophils kill microbes Annu Rev Immunol 2005 23 197 223 15771570 PMC2092448
  158. [160]Gueirard P Laplante A Rondeau C Milon G Desjardins M Trafficking of Leishmania donovani promastigotes in non-lytic compartments in neutrophils enables the subsequent transfer of parasites to macrophages Cell Microbiol 2008 10 100 111 17651446
  159. [161]Xin L Type I IFN receptor regulates neutrophil functions and innate immunity to Leishmania parasites J Immunol 2010 184 7047 7056 20483775 PMC4159077
  160. [162]Conrad SM Strauss-Ayali D Field AE Mack M Mosser DM Leishmania-derived murine monocyte chemoattractant protein 1 enhances the recruitment of a restrictive population of CC chemokine receptor 2-positive macrophages Infect Immun 2007 75 653 665 17088347 PMC1828528
  161. [163]Bogdan C Mechanisms and consequences of persistence of intracellular pathogens: leishmaniasis as an example Cell Microbiol 2008 10 1221 1234 18363880
  162. [164]Blank C Bogdan C Bauer C Erb K Moll H Murine epidermal Langerhans cells do not express inducible nitric oxide synthase Eur J Immunol 1996 26 792 796 8625969
  163. [165]Bogdan C Donhauser N Doring R Rollinghoff M Diefenbach A Rittig MG Fibroblasts as host cells in latent leishmaniosis J Exp Med 2000 191 2121 2130 10859337 PMC2193203
  164. [166]Milei J Guerri-Guttenberg RA Grana DR Storino R Prognostic impact of Chagas disease in the United States Am Heart J 2009 157 22 29 19081392
  165. [167]Macedo AM Machado CR Oliveira RP Pena SD Trypanosoma cruzi: genetic structure of populations and relevance of genetic variability to the pathogenesis of chagas disease Mem Inst Oswaldo Cruz 2004 99 1 12 15057339
  166. [168]Lescure FX Chagas disease: changes in knowledge and management Lancet Infect Dis 2010 10 556 570 20670903
  167. [169]Bern C Montgomery SP Katz L Caglioti S Stramer SL Chagas disease and the US blood supply Curr Opin Infect Dis 2008 21 476 482 18725796
  168. [170]Epting C Coates BM Engman DM Molecular mechanisms of host cell invasion by Trypanosoma cruzi Exp Parasitol 2010 PMC3443968 20599990
  169. [171]Mortara RA Host cell actin remodeling in response to Trypanosoma cruzi: trypomastigote versus amastigote entry Subcell Biochem 2008 47 101 109 18512345
  170. [172]Barrias ES Reignault LC De Souza W Carvalho TM Dynasore, a dynamin inhibitor, inhibits Trypanosoma cruzi entry into peritoneal macrophages PLoS One 2010 5 e7764 20098746 PMC2808331
  171. [173]Rodriguez A Samoff E Rioult MG Chung A Andrews NW Host cell invasion by trypanosomes requires lysosomes and microtubule/kinesin-mediated transport J Cell Biol 1996 134 349 362 8707821 PMC2120885
  172. [174]Tardieux I Lysosome recruitment and fusion are early events required for trypanosome invasion of mammalian cells Cell 1992 71 1117 1130 1473148
  173. [175]McNeil PL Kirchhausen T An emergency response team for membrane repair Nat Rev Mol Cell Biol 2005 6 499 505 15928713
  174. [176]Caler EV Chakrabarti S Fowler KT Rao S Andrews NW The exocytosis-regulatory protein synaptotagmin VII mediates cell invasion by Trypanosoma cruzi J Exp Med 2001 193 1097 1104 11342594 PMC2193425
  175. [177]Reddy A Caler EV Andrews NW Plasma membrane repair is mediated by Ca(2+)-regulated exocytosis of lysosomes Cell 2001 106 157 169 11511344
  176. [178]Romano PS Arboit MA Vazquez CL Colombo MI The autophagic pathway is a key component in the lysosomal dependent entry of Trypanosoma cruzi into the host cell Autophagy 2009 5 6 18 19115481
  177. [179]Woolsey AM Sunwoo L Petersen CA Brachmann SM Cantley LC Burleigh BA Novel PI 3-kinase-dependent mechanisms of trypanosome invasion and vacuole maturation J Cell Sci 2003 116 3611 3622 12876217
  178. [180]Mott GA Burleigh BA The role of host cell lysosomes in Trypanosoma cruzi invasion Subcell Biochem 2008 47 165 173 18512350
  179. [181]Andrade LO Andrews NW Lysosomal fusion is essential for the retention of Trypanosoma cruzi inside host cells J Exp Med 2004 200 1135 1143 15520245 PMC2211867
  180. [182]Woolsey AM Burleigh BA Host cell actin polymerization is required for cellular retention of Trypanosoma cruzi and early association with endosomal/lysosomal compartments Cell Microbiol 2004 6 829 838 15272864
  181. [183]Scharfstein J Host cell invasion by Trypanosoma cruzi is potentiated by activation of bradykinin B (2) receptors J Exp Med 2000 192 1289 1300 11067878 PMC2193362
  182. [184]Rodriguez A Rioult MG Ora A Andrews NW A trypanosome-soluble factor induces IP3 formation, intracellular Ca2+ mobilization and microfilament rearrangement in host cells J Cell Biol 1995 129 1263 1273 7775573 PMC2120476
  183. [185]Burleigh BA Caler EV Webster P Andrews NW A cytosolic serine endopeptidase from Trypanosoma cruzi is required for the generation of Ca2+ signaling in mammalian cells J Cell Biol 1997 136 609 620 9024691 PMC2134300
  184. [186]Caler EV Vaena de Avalos S Haynes PA Andrews NW Burleigh BA Oligopeptidase B1298 dependent signaling mediates host cell invasion by Trypanosoma cruzi EMBO J 1998 17 4975 4986 9724634 PMC1170826
  185. [187]Rodriguez A Martinez I Chung A Berlot CH Andrews NW cAMP regulates Ca2+-dependent exocytosis of lysosomes and lysosome-mediated cell invasion by trypanosomes J Biol Chem 1999 274 16754 16759 10358016
  186. [188]Andrade LO Andrews NW The Trypanosoma cruzi - host - cell interplay: location, invasion, retention Nat Rev Microbiol 2005 3 819 823 16175174
  187. [189]Andrews NW Abrams CK Slatin SL Griffiths G A T. cruzi secreted protein immunologically related to the complement component C9: evidence for membrane pore-forming activity at low pH Cell 1990 61 1277 1287 2194668
  188. [190]Manning-Cela R Cortes A Gonzalez-Rey E Van Voorhis WC Swindle J Gonzalez A LYT1 protein is required for efficient in vitro infection by Trypanosoma cruzi Infect Immun 2001 69 3916 3923 11349059 PMC98423
  189. [191]Zago MP Barrio AB Cardozo RM Duffy T Schijman AG Basombrio MA Impairment of infectivity and immunoprotective effect of a LYT1 null mutant of Trypanosoma cruzi Infect Immun 2008 76 443 451 17938222 PMC2223657
  190. [192]Rubin-de-Celis SS Uemura H Yoshida N Schenkman S Expression of trypomastigote trans1315 sialidase in metacyclic forms of Trypanosoma cruzi increases parasite escape from its parasitophorous vacuole Cell Microbiol 2006 8 1888 1898 16824037
  191. [193]Hall BF Webster P Ma AK Joiner KA Andrews NW Desialylation of lysosomal membrane glycoproteins by Trypanosoma cruzi: a role for the surface neuraminidase in facilitating parasite entry into the host cell cytoplasm J Exp Med 1992 176 313 325 1500849 PMC2119312
  192. [194]Silber AM Colli W Ulrich H Alves MJ Pereira CA Amino acid metabolic routes in Trypanosoma cruzi: possible therapeutic targets against Chagas’ disease Curr Drug Targets Infect Disord 2005 5 53 64 15777198
  193. [195]Kayama H Takeda K The innate immune response to Trypanosoma cruzi infection Microb Infect 2010 12 511 517 20348008
  194. [196]Tarleton RL Immune system recognition of Trypanosoma cruzi Curr Opin Immunol 2007 19 430 434 17651955
  195. [197]Almeida IC Highly purified glycosylphosphatidylinositols from Trypanosoma cruzi are potent proinflammatory agents EMBO J 2000 19 1476 1485 10747016 PMC310217
  196. [198]Campos MA Activation of Toll-like receptor-2 by glycosylphosphatidylinositol anchors from a protozoan parasite J Immunol 2001 167 416 423 11418678
  197. [199]Bafica A Santiago HC Goldszmid R Ropert C Gazzinelli RT Sher A Cutting edge: TLR9 and TLR2 signaling together account for MyD88-dependent control of parasitemia in Trypanosoma cruzi infection J Immunol 2006 177 3515 3519 16951309
  198. [200]Shoda LK DNA from protozoan parasites Babesia bovis, Trypanosoma cruzi, and T. brucei is mitogenic for B lymphocytes and stimulates macrophage expression of interleukin-12, tumor necrosis factor alpha, and nitric oxide Infect Immun 2001 69 2162 2171 11254571 PMC98143
  199. [201]Koga R TLR-dependent induction of IFN-beta mediates host defense against Trypanosoma cruzi J Immunol 2006 177 7059 7066 17082622
  200. [202]Santiago HC Mice deficient in LRG-47 display enhanced susceptibility to Trypanosoma cruzi infection associated with defective hemopoiesis and intracellular control of parasite growth J Immunol 2005 175 8165 8172 16339555

200 of 216 shown

Cited by

Sorted by citations

Authors
David Sibley, L.
Venue
Immunological Reviews
Publisher
Wiley
Published
2011-02-23
Volume
240
Issue
1
Pages
72-91
ISSN
  • 0105-2896 (ISSN-L)
  • 1600-065X
DOI
10.1111/j.1600-065x.2010.00990.x
PMC
PMC3697736
OpenAlex
W2140990000
Cited by
254
References
1
Citations by year
2026: 4 · 2025: 11 · 2024: 9 · 2023: 32 · 2022: 8 · 2021: 16 · 2020: 13 · 2019: 17 · 2018: 13 · 2017: 19 · 2016: 18 · 2015: 22 · 2014: 28 · 2013: 20 · 2012: 15
FWCI
3.16
Type
journal article
Language
en
Open access
Licence
onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations
  • Immunological Reviews (publishedVersion)
  • PubMed (publishedVersion)
  • Europe PMC (PubMed Central) (acceptedVersion)
  • PubMed Central (acceptedVersion)
Funders
National Institute of Allergy and Infectious Diseases (R01AI059176, R01AI036629, R01AI034036)
Topics
  • Life Sciences › Immunology and Microbiology › Parasitology › Toxoplasma gondii Research Studies
  • Life Sciences › Immunology and Microbiology › Parasitology › Parasitic Infections and Diagnostics
  • Health Sciences › Medicine › Epidemiology › Trypanosoma species research and implications
Keywords
protozoan parasites, intracellular parasitism, host cell invasion, host cell egress, microsporidia, kinetoplastids, Apicomplexa, Toxoplasma, Trypanosoma cruzi, Leishmania, Encephalitozoon, phagolysosomes, host cell signaling, innate immune evasion, host-parasite interactions
MeSH terms
Host-Parasite Interactions, Humans, Phylogeny, Intracellular Space, Eukaryota

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review