Hijacking of host cellular functions by the apicomplexa

Annual Review of Microbiology

Volumn 62, Issue , 2008, Pages 471-487

  Plattner, Fabienne ^a   Soldati Favre, Dominique ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

Author keywords

Apoptosis; Cryptosporidium parvum; Immunity; Invasion; Nutrients; Plasmodium falciparum; Theileria parva; Toxoplasma gondii

Indexed keywords

ANTIGEN PRESENTATION; APICOMPLEXA; APOPTOSIS; CELL INVASION; CELL PROLIFERATION; CELL SURVIVAL; CELL TRANSFORMATION; CELL VACUOLE; CRYPTOSPORIDIUM PARVUM; GENE EXPRESSION REGULATION; HOST CELL; IMMUNOMODULATION; MEMBRANE TRANSPORT; NONHUMAN; PARASITE IMMUNITY; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROTEIN SYNTHESIS; REVIEW; THEILERIA PARVA; TOXOPLASMA GONDII;

ANIMALS; APICOMPLEXA; APOPTOSIS; CRYPTOSPORIDIUM PARVUM; HOST-PATHOGEN INTERACTIONS; HUMANS; MODELS, BIOLOGICAL; ORGANELLES; PLASMODIUM FALCIPARUM; PROTOZOAN INFECTIONS; THEILERIA PARVA; TOXOPLASMA;

APICOMPLEXA; CRYPTOSPORIDIUM PARVUM; PLASMODIUM FALCIPARUM; PROTOZOA; THEILERIA PARVA; TOXOPLASMA GONDII;

EID: 53849111970     PISSN: 00664227     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.micro.62.081307.162802     Document Type: Review

References (102)

1. Abrahamsen MS, Templeton TJ, Enomoto S, Abrahante JE, Zhu G, et al. 2004. Complete genome sequence of the apicomplexan, Cryptosporidium parvum. Science 304:441-45
2. Baum J, Papenfuss AT, Baum B, Speed TP, Cowman AF. 2006. Regulation of apicomplexan actin-based motility. Nat. Rev. Microbiol. 4:621-28
3. Beyer TV, Svezhova NV, Radchenko AI, Sidorenko NV. 2002. Parasitophorous vacuole: morphofunctional diversity in different coccidian genera (a short insight into the problem). Cell Biol. Int. 26:861-71
4. Blader IJ, Manger ID, Boothroyd JC. 2001. Microarray analysis reveals previously unknown changes in Toxoplasma gondii-infected human cells. J. Biol. Chem. 276:24223-31
5. Bonnin A, Lapillonne A, Petrella T, Lopez J, Chaponnier C, et al. 1999. Immunodetection of the microvillous cytoskeleton molecules villin and ezrin in the parasitophorous vacuole wall of Cryptosporidium parvum (Protozoa: Apicomplexa). Eur. J. Cell Biol. 78:794-801
6. Bradley PJ, Sibley LD. 2007. Rhoptries: an arsenal of secreted virulence factors. Curr. Opin. Microbiol. 10:582-87
7. Breman JG. 2001. The ears of the hippopotamus: manifestations, determinants, and estimates of the malaria burden. Am. J. Trop. Med. Hyg. 64:1-11
8. Carmen JC, Hardi L, Sinai AP. 2006. Toxoplasma gondii inhibits UV light-induced apoptosis through multiple interactions with the mitochondrion-dependent programmed cell death pathway. Cell Microbiol. 8:301-15
9. Carmen JC, Sinai AP. 2007. Suicide prevention: disruption of apoptotic pathways by protozoan parasites. Mol. Microbiol. 4:904-16
10. 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
11. Chen XM, Huang BQ, Splinter PL, Cao H, Zhu G, et al. 2003. Cryptosporidium parvum invasion of biliary epithelia requires host cell tyrosine phosphorylation of cortactin via c-Src. Gastroenterology 125:216-28
12. Chen XM, Huang BQ, Splinter PL, Orth JD, Billadeau DD, et al. 2004. Cdc42 and the actin-related protein/neural Wiskott-Aldrich syndrome protein network mediate cellular invasion by Cryptosporidium parvum. Infect. Immun. 72:3011-21
13. Chen XM, O'Hara SP, Huang BQ, Nelson JB, Lin JJ, et al. 2004. Apical organelle discharge by Cryptosporidium parvum is temperature, cytoskeleton, and intracellular calcium dependent and required for host cell invasion. Infect. Immun. 72:6806-16
14. Clough B, Atilola FA, Pasvoi G. 1998. The role of rosetting in the multiplication of Plasmodium falciparum: rosette formation neither enhances nor targets parasite invasion into uninfected red cells. Br. J. Haematol. 100:99-104
15. Coban C, Ishii KJ, Horii T, Akira S. 2007. Manipulation of host innate immune responses by the malaria parasite. Trends Microbiol. 15:271-78
16. Cooke BM, Lingelbach K, Bannister LH, Tilley L. 2004. Protein trafficking in Plasmodium falciparum-infected red blood cells. Trends Parasitol. 20:581-89
17. Coppens I, Dunn JD, Romano JD, Pypaert M, Zhang H, et al. 2006. Toxoplasma gondii sequesters lysosomes from mammalian hosts in the vacuolar space. Cell 125:261-74
18. Coppens I, Sinai AP, Joiner KA. 2000. Toxoplasma gondii exploits host low-density lipoprotein receptor-mediated endocytosis for cholesterol acquisition. J. Cell Biol. 149:167-80
19. Corso PS, Kramer MH, Blair KA, Addiss DG, Davis JP, Haddix AC. 2003. Cost of illness in the 1993 waterborne Cryptosporidium outbreak, Milwaukee, Wisconsin. Emerg. Infect. Dis. 9:426-31
20. Crawford MJ, Thomsen-Zieger N, Ray M, Schachtner J, Roos DS, Seeber F. 2006. Toxoplasma gondii scavenges host-derived lipoic acid despite its de novo synthesis in the apicoplast. EMBO J. 25:3214-22
21. Current WL, Reese NC. 1986. A comparison of endogenous development of three isolates of Cryptosporidium in suckling mice. J. Protozool. 33:98-108
22. de Melo EJ, de Carvalho TU, de Souza W. 1992. Penetration of Toxoplasma gondii into host cells induces changes in the distribution of the mitochondria and the endoplasmic reticulum. Cell Struct. Funct. 17:311-17
23. Decherf G, Egee S, Staines HM, Ellory JC, Thomas SL. 2004. Anionic channels in malaria-infected human red blood cells. Blood Cells Mol. Dis. 32:366-71
24. Deng M, Lancto CA, Abrahamsen MS. 2004. Cryptosporidium parvum regulation of human epithelial cell gene expression. Int. J. Parasitol. 34:73-82
25. Denkers EY, Butcher BA. 2005. Sabotage and exploitation in macrophages parasitized by intracellular protozoans. Trends Parasitol. 21:35-41
26. Desai SA, Bezrukov SM, Zimmerberg J. 2000. A voltage-dependent channel involved in nutrient uptake by red blood cells infected with the malaria parasite. Nature 406:1001-5
27. Desai SA, Rosenberg RL. 1997. Pore size of the malaria parasite's nutrient channel. Proc. Natl. Acad. Sci. USA 94:2045-49
28. Dessauge F, Lizundia R, Baumgartner M, Chaussepied M, Langsley G. 2005. Taking the Myc is bad for Theileria. Trends Parasitol. 21:377-85
29. Dobbelaere DA, Kuenzi P. 2004. The strategies of the Theileria parasite: a new twist in host-pathogen interactions. Curr. Opin. Immunol. 16:524-30
30. Dziadek B, Dziadek J, Dlugonska H. 2007. Identification of Toxoplasma gondii proteins binding human lactoferrin: a new aspect of rhoptry proteins function. Exp. Parasitol. 115:277-82
31. El Hajj H, Lebrun M, Arold ST, Vial H, Labesse G, Dubremetz JF. 2007. ROP18 is a rhoptry kinase controlling the intracellular proliferation of Toxoplasma gondii. PLoS Pathog. 3:e14
32. Elliott DA, Clark DP. 2000. Cryptosporidium parvum induces host cell actin accumulation at the host-parasite interface. Infect. Immun. 68:2315-22
33. Elliott DA, Coleman DJ, Lane MA, May RC, Machesky LM, Clark DP. 2001. Cryptosporidium parvum infection requires host cell actin polymerization. Infect. Immun. 69:5940-42
34. Endo T, Pelster B, Piekarski G. 1981. Infection of murine peritoneal macrophages with Toxoplasma gondii exposed to UV light. Z. Parasitenkd. 65:121-29
35. Forney JR, DeWald DB, Yang S, Speer CA, Healey MC. 1999. A role for host phosphoinositide 3-kinase and cytoskeletal remodeling during Cryptosporidium parvum infection. Infect. Immun. 67:844-52
36. Fox BA, Bzik DJ. 2002. De novo pyrimidine biosynthesis is required for virulence of Toxoplasma gondii. Nature 415:926-29
37. Fox BA, Gigley JP, Bzik DJ. 2004. Toxoplasma gondii lacks the enzymes required for de novo arginine biosynthesis and arginine starvation triggers cyst formation. Int. J. Parasitol. 34:323-31
38. Gao LY, Kwaik YA. 2000. The modulation of host cell apoptosis by intracellular bacterial pathogens. Trends Microbiol. 8:306-13
39. Gero AM, O'Sullivan WJ. 1990. Purines and pyrimidines in malarial parasites. Blood Cells 16:467-84
40. Gowda DC. 2007. TLR-mediated cell signaling by malaria GPIs. Trends Parasitol. 23:596-604
41. Gupta N, Zahn MM, Coppens I, Joiner KA, Voelker DR. 2005. Selective disruption of phosphatidylcholine metabolism of the intracellular parasite Toxoplasma gondii arrests its growth. J. Biol. Chem. 280:16345-53
42. Haeggstrom M, Kironde F, Berzins K, Chen Q, Wahlgren M, Fernandez V. 2004. Common trafficking pathway for variant antigens destined for the surface of the Plasmodium falciparum-infected erythrocyte. Mol. Biochem. Parasitol. 133:1-14
43. 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
44. Halonen SK, Weidner E. 1994. Overcoating of Toxoplasma parasitophorous vacuoles with host cell vimentin type intermediate filaments. J. Eukaryot. Microbiol. 1:65-71
45. Heussler VT, Rottenberg S, Schwab R, Kuenzi P, Fernandez PC, et al. 2002. Hijacking of host cell IKK signalosomes by the transforming parasite Theileria. Science 298:1033-36
46. Jan G, Delorme V, David V, Revenu C, Rebollo A, et al. 2007. The toxofilin-actin-PP2C complex of Toxoplasma: identification of interacting domains. Biochem. J. 401:711-19
47. Joiner KA, Fuhrman SA, Miettinen HM, Kasper LH, Mellman I. 1990. Toxoplasma gondii: fusion competence of parasitophorous vacuoles in Fc receptor-transfected fibroblasts. Science 249:641-46
48. Keeley A, Soldati D. 2004. The glideosome: a molecular machine powering motility and host-cell invasion by Apicomplexa. Trends Cell Biol. 14:528-32
49. Kim L, Denkers EY. 2006. Toxoplasma gondii triggers Gi-dependent PI 3-kinase signaling required for inhibition of host cell apoptosis. J. Cell Sci. 119:2119-26
50. Kim SK, Fouts AE, Boothroyd JC. 2007. Toxoplasma gondii dysregulates IFN-gamma-inducible gene expression in human fibroblasts: insights from a genome-wide transcriptional profiling. J. Immunol. 178:5154-65
51. Kooij TW, Janse CJ, Waters AP. 2006. Plasmodium postgenomics: better the bug you know? Nat. Rev. Microbiol. 4:344-57
52. Kravetz JD, Federman DG. 2005. Toxoplasmosis in pregnancy. Am. J. Med. 118:212-16
53. Krug EC, Marr JJ, Berens RL. 1989. Purine metabolism in Toxoplasma gondii. J. Biol. Chem. 264:10601-7
54. Lacharme L, Villar V, Rojo-Vazquez FA, Suarez S. 2004. Complete development of Cryptosporidium parvum in rabbit chondrocytes (VELI cells). Microbes. Infect. 6:566-71
55. Lambert H, Hitziger N, Dellacasa I, Svensson M, Barragan A. 2006. Induction of dendritic cell migration upon Toxoplasma gondii infection potentiates parasite dissemination. Cell Microbiol. 8:1611-23
56. Lang C, Gross U, Luder CG. 2007. Subversion of innate and adaptive immune responses by Toxoplasma gondii. Parasitol. Res. 100:191-203
57. Lauer SA, Rathod PK, Ghori N, Haldar K. 1997. A membrane network for nutrient import in red cells infected with the malaria parasite. Science 276:1122-25
58. Machado J Jr, Fernandez PC, Baumann I, Dobbelaere DA. 2000. Characterisation of NF-kappa B complexes in Theileria parva-transformed T cells. Microbes Infect. 2:1311-20
59. Martin RE, Kirk K. 2007. Transport of the essential nutrient isoleucine in human erythrocytes infected with the malaria parasite Plasmodium falciparum. Blood 109:2217-24
60. Mazumdar J, Striepen B. 2007. Make it or take it: fatty acid metabolism of apicomplexan parasites. Eukaryot. Cell 6:1727-35
61. Mercier C, Adjogble KD, Daubener W, Delauw MF. 2005. Dense granules: Are they key organelles to help understand the parasitophorous vacuole of all apicomplexa parasites? Int. J. Parasitol. 35:829-49
62. Michel R, Schupp K, Raether W, Bierther FW. 1980. Formation of a close junction during invasion of erythrocytes by Toxoplasma gondii in vitro. Int. J. Parasitol. 10:309-13
63. Mordue DG, Desai N, Dustin M, Sibley LD. 1999. 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. 190:1783-92
64. Mordue DG, Sibley LD. 1997. Intracellular fate of vacuoles containing Toxoplasma gondii is determined at the time of formation and depends on the mechanism of entry. J. Immunol. 159:4452-59
65. Pain A, Renauld H, Berriman M, Murphy L, Yeats CA, et al. 2005. Genome of the host-cell transforming parasite Theileria annulata compared with T. parva. Science 309:131-33
66. Pfefferkorn ER, Eckel M, Rebhun S. 1986. Interferon-gamma suppresses the growth of Toxoplasma gondii in human fibroblasts through starvation for tryptophan. Mol. Biochem. Parasitol. 20:215-24
67. Roos DS, Donald RG, Morrissette NS, Moulton AL. 1994. Molecular tools for genetic dissection of the protozoan parasite Toxoplasma gondii. Methods Cell Biol. 45:27-63
68. Roulston A, Marcellus RC, Branton PE. 1999. Viruses and apoptosis. Annu. Rev. Microbiol. 53:577-628
69. Rowe JA, Obiero J, Marsh K, Raza A. 2002. Short report: positive correlation between rosetting and parasitemia in Plasmodium falciparum clinical isolates. Am. J. Trop. Med. Hyg. 66:458-60
70. Roy CR, Mocarski ES. 2007. Pathogen subversion of cell-intrinsic innate immunity. Nat. Immunol. 8:1179-87
71. Saeij JP, Boyle JP, Coller S, Taylor S, Sibley LD, et al. 2006. Polymorphic secreted kinases are key virulence factors in toxoplasmosis. Science 314:1780-83
72. Saeij JP, Coller S, Boyle JP, Jerome ME, White MW, Boothroyd JC. 2007. Toxoplasma co-opts host gene expression by injection of a polymorphic kinase homologue. Nature 445:324-27
73. Schneider I, Haller D, Kullmann B, Beyer D, Ahmed JS, Seitzer U. 2007. Identification, molecular characterization and subcellular localization of a Theileria annulata parasite protein secreted into the host cell cytoplasm. Parasitol. Res. 101:1471-82
74. Schwab JC, Beckers CJ, Joiner KA. 1994. The parasitophorous vacuole membrane surrounding intracellular Toxoplasma gondii functions as a molecular sieve. Proc. Natl. Acad. Sci. USA 91:509-13
75. Schwartzman JD, Pfefferkorn ER. 1982. Toxoplasma gondii: purine synthesis and salvage in mutant host cells and parasites. Exp. Parasitol. 53:77-86
76. Shaw MK. 2003. Cell invasion by Theileria sporozoites. Trends Parasitol. 19:2-6
77. Shaw MK, Tilney LG, Musoke AJ, Teale AJ. 1995. MHC class I molecules are an essential cell surface component involved in Theileria parva sporozoite binding to bovine lymphocytes. J. Cell Sci. 108(Pt. 4):1587-96
78. Sibley LD, Niesman IR, Parmley SF, Cesbron-Delauw MF. 1995. Regulated secretion of multi-lamellar vesicles leads to formation of a tubulo-vesicular network in host-cell vacuoles occupied by Toxoplasma gondii. J. Cell Sci. 108(Pt. 4):1669-77
79. Sibley LD, Weidner E, Krahenbuhl JL. 1985. Phagosome acidification blocked by intracellular Toxoplasma gondii. Nature 315:416-19
80. Sinai AP, Joiner KA. 2001. The Toxoplasma gondii protein ROP2 mediates host organelle association with the parasitophorous vacuole membrane. J. Cell Biol. 154:95-108
81. Sinai AP, Webster P, Joiner KA. 1997. Association of host cell endoplasmic reticulum and mitochondria with the Toxoplasma gondii parasitophorous vacuole membrane: a high affinity interaction. J. Cell Sci. 110(Pt. 17):2117-28
82. Singh AP, Buscaglia CA, Wang Q, Levay A, Nussenzweig DR, et al. 2007. Plasmodium circumsporozoite protein promotes the development of the liver stages of the parasite. Cell 131:492-504
83. Snow RW, Guerra CA, Noor AM, Myint HY, Hay SI. 2005. The global distribution of clinical episodes of Plasmodium falciparum malaria. Nature 434:214-17
84. Spycher C, Rug M, Klonis N, Ferguson DJ, Cowman AF, et al. 2006. Genesis of and trafficking to the Maurer's clefts of Plasmodium falciparum-infected erythrocytes. Mol. Cell Biol. 26:4074-85
85. Striepen B, Pruijssers AJ, Huang J, Li C, Gubbels MJ, et al. 2004. Gene transfer in the evolution of parasite nucleotide biosynthesis. Proc. Natl. Acad. Sci. USA 101:3154-59
86. Sturm A, Amino R, van de Sand C, Regen T, Retzlaff S, et al. 2006. Manipulation of host hepatocytes by the malaria parasite for delivery into liver sinusoids. Science 313:1287-90
87. Su C, Evans D, Cole RH, Kissinger JC, Ajioka JW, Sibley LD. 2003. Recent expansion of Toxoplasma through enhanced oral transmission. Science 299:414-16
88. 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. Proc. Natl. Acad. Sci. USA 93:8413-18
89. Swan DG, Phillips K, Tait A, Shiels BR. 1999. Evidence for localisation of a Theileria parasite AT hook DNA-binding protein to the nucleus of immortalised bovine host cells. Mol. Biochem. Parasitol. 101:117-29
90. Taylor S, Barragan A, Su C, Fux B, Fentress SJ, et al. 2006. A secreted serine-threonine kinase determines virulence in the eukaryotic pathogen Toxoplasma gondii. Science 314:1776-80
91. Tenter AM, Heckeroth AR, Weiss LM. 2000. Toxoplasma gondii: from animals to humans. Int. J. Parasitol. 30:1217-58
92. Tilley L, Sougrat R, Lithgow T, Hanssen E. 2008. The twists and turns of Maurer's cleft trafficking in P. falciparum-infected erythrocytes. Traffic 9:187-97
93. Travier L, Mondragon R, Dubremetz JF, Musset K, Mondragon M, et al. 2008. Functional domains of the Toxoplasma GRA2 protein in the formation of the membranous nanotubular network of the parasitophorous vacuole. Int. J. Parasitol. 7:757-73
94. Vutova P, Wirth M, Hippe D, Gross U, Schulze-Osthoff K, et al. 2007. Toxoplasma gondii inhibits Fas/CD95-triggered cell death by inducing aberrant processing and degradation of caspase 8. Cell Microbiol. 9:1556-70
95. Ward GE, Miller LH, Dvorak JA. 1993. The origin of parasitophorous vacuole membrane lipids in malaria-infected erythrocytes. J. Cell Sci. 106(Pt. 1):237-48
96. Webster P, Dobbelaere DA, Fawcett DW. 1985. The entry of sporozoites of Theileria parva into bovine lymphocytes in vitro. Immunoelectron microscopic observations. Eur. J. Cell Biol. 36:157-62
97. Wetzel DM, Schmidt J, Kuhlenschmidt MS, Dubey JP, Sibley LD. 2005. Gliding motility leads to active cellular invasion by Cryptosporidium parvum sporozoites. Infect. Immun. 73:5379-87
98. Williams GT. 1994. Programmed cell death: a fundamental protective response to pathogens. Trends Microbiol. 2:463-64
99. Williams RO, Dobbelaere DA. 1993. The molecular basis of transformation of lymphocytes by Theileria parva infection. Semin. Cell Biol. 4:363-71
100. Wong SY, Remington JS. 1994. Toxoplasmosis in pregnancy. Clin. Infect. Dis. 18:853-61
101. Xiao GH, Jeffers M, Bellacosa A, Mitsuuchi Y, Van der Woude GF, Testa JR. 2001. Anti-apoptotic signaling by hepatocyte growth factor/Met via the phosphatidylinositol 3-kinase/Akt and mitogen-activated protein kinase pathways. Proc. Natl. Acad. Sci. USA 98:247-52
102. Zeng B, Zhu G. 2006. Two distinct oxysterol binding protein-related proteins in the parasitic protist Cryptosporidium parvum (Apicomplexa). Biochem. Biophys. Res. Commun. 346:591-99