Infected dendritic cells facilitate systemic dissemination and transplacental passage of the obligate intracellular parasite Neospora caninum in mice

PLoS ONE

Volumn 7, Issue 3, 2012, Pages

  Collantes Fernandez, Esther ^a,b,c   Arrighi, Romanico B G ^a,b   Álvarez García, Gema ^c   Weidner, Jessica M ^a,b   Regidor Cerrillo, Javier ^c   Boothroyd, John C ^d   Ortega Mora, Luis M ^c   Barragan, Antonio ^a,b  

^a KAROLINSKA INSTITUTE   (Sweden)

^b Swedish Institute for Communicable Disease Control   (Sweden)

^c UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^d STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL MIGRATION; CELL POLARITY; CONTROLLED STUDY; DENDRITIC CELL; FEMALE; HOST PARASITE INTERACTION; IN VITRO STUDY; IN VIVO STUDY; INTRACELLULAR TRANSPORT; INTRAUTERINE INFECTION; MALE; MOUSE; NEOSPOROSIS; NEWBORN; NEWBORN MORTALITY; NONHUMAN; PARASITE LOAD; PARASITE LOCALIZATION; PARASITE MIGRATION; PARASITE TRANSMISSION; PARASITE VIRULENCE; PHENOTYPIC VARIATION; PLACENTAL TRANSFER; PROGENY; VERTICAL TRANSMISSION; ANIMAL; CELL LINE; COCCIDIOSIS; CYTOLOGY; DISEASE TRANSMISSION; EXTRACELLULAR SPACE; HUMAN; INTRACELLULAR SPACE; MOVEMENT (PHYSIOLOGY); NEOSPORA; PARASITOLOGY; PATHOGENICITY; PHENOTYPE; PHYSIOLOGY; PLACENTA; PREGNANCY; SPECIES DIFFERENCE; TROPHOBLAST;

COCCIDIA; MUS; NEOSPORA CANINUM;

ANIMALS; CELL LINE; CELL POLARITY; COCCIDIOSIS; DENDRITIC CELLS; EXTRACELLULAR SPACE; FEMALE; HUMANS; INFECTIOUS DISEASE TRANSMISSION, VERTICAL; INTRACELLULAR SPACE; MALE; MICE; MOVEMENT; NEOSPORA; PHENOTYPE; PLACENTA; PREGNANCY; SPECIES SPECIFICITY; TROPHOBLASTS;

EID: 84857778663     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0032123     Document Type: Article

References (44)

1. Dubey JP, Schares G, Ortega-Mora LM, (2007) Epidemiology and control of neosporosis and Neospora caninum. Clin Microbiol Rev 20: 323-367.
2. Williams DJ, Hartley CS, Bjorkman C, Trees AJ, (2009) Endogenous and exogenous transplacental transmission of Neospora caninum- how the route of transmission impacts on epidemiology and control of disease. Parasitology 136: 1895-1900.
3. Buxton D, McAllister MM, Dubey JP, (2002) The comparative pathogenesis of neosporosis. Trends Parasitol 18: 546-552.
4. Innes EA, Andrianarivo AG, Bjorkman C, Williams DJ, Conrad PA, (2002) Immune responses to Neospora caninum and prospects for vaccination. Trends Parasitol 18: 497-504.
5. Dobrowolski JM, Sibley LD, (1996) Toxoplasma invasion of mammalian cells is powered by the actin cytoskeleton of the parasite. Cell 84: 933-939.
6. Barragan A, Sibley LD, (2002) Transepithelial migration of Toxoplasma gondii is linked to parasite motility and virulence. J Exp Med 195: 1625-1633.
7. 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: 1611-1623.
8. Lambert H, Vutova PP, Adams WC, Lore K, Barragan A, (2009) The Toxoplasma gondii-shuttling function of dendritic cells is linked to the parasite genotype. Infect Immun 77: 1679-1688.
9. Lambert H, Barragan A, (2010) Modelling parasite dissemination: host cell subversion and immune evasion by Toxoplasma gondii. Cell Microbiol 12: 292-300.
10. Courret N, Darche S, Sonigo P, Milon G, Buzoni-Gatel D, et al. (2006) CD11c- and CD11b-expressing mouse leukocytes transport single Toxoplasma gondii tachyzoites to the brain. Blood 107: 309-316.
11. Boysen P, Klevar S, Olsen I, Storset AK, (2006) The protozoan Neospora caninum directly triggers bovine NK cells to produce gamma interferon and to kill infected fibroblasts. Infect Immun 74: 953-960.
12. Strohbusch M, Muller N, Hemphill A, Margos M, Grandgirard D, et al. (2009) Neospora caninum and bone marrow-derived dendritic cells: parasite survival, proliferation, and induction of cytokine expression. Parasite Immunol 31: 366-372.
13. Dion S, Germon S, Guiton R, Ducournau C, Dimier-Poisson I, (2011) Functional activation of T cells by dendritic cells and macrophages exposed to the intracellular parasite Neospora caninum. Int J Parasitol 41: 685-695.
14. Sibley LD, (2004) Intracellular parasite invasion strategies. Science 304: 248-253.
15. Mold JE, Michaelsson J, Burt TD, Muench MO, Beckerman KP, et al. (2008) Maternal alloantigens promote the development of tolerogenic fetal regulatory T cells in utero. Science 322: 1562-1565.
16. Gomez-Lopez N, Guilbert LJ, Olson DM, (2010) Invasion of the leukocytes into the fetal-maternal interface during pregnancy. J Leukoc Biol 88: 625-633.
17. Regidor-Cerrillo J, Gomez-Bautista M, Del Pozo I, Jimenez-Ruiz E, Aduriz G, et al. (2010) Influence of Neospora caninum intra-specific variability in the outcome of infection in a pregnant BALB/c mouse model. Vet Res 41: 52.
18. Regidor-Cerrillo J, Gomez-Bautista M, Sodupe I, Aduriz G, Alvarez-Garcia G, et al. (2011) In vitro invasion efficiency and intracellular proliferation rate comprise virulence-related phenotypic traits of Neospora caninum. Vet Res 42: 41.
19. Regidor-Cerrillo J, Pedraza-Diaz S, Gomez-Bautista M, Ortega-Mora LM, (2006) Multilocus microsatellite analysis reveals extensive genetic diversity in Neospora caninum. J Parasitol 92: 517-524.
20. Dubey JP, Hattel AL, Lindsay DS, Topper MJ, (1988) Neonatal Neospora caninum infection in dogs: isolation of the causative agent and experimental transmission. J Am Vet Med Assoc 193: 1259-1263.
21. Barber JS, Holmdahl OJ, Owen MR, Guy F, Uggla A, et al. (1995) Characterization of the first European isolate of Neospora caninum (Dubey, Carpenter, Speer, Topper and Uggla). Parasitology 111 (Pt 5): 563-568.
22. Stenlund S, Bjorkman C, Holmdahl OJ, Kindahl H, Uggla A, (1997) Characterization of a Swedish bovine isolate of Neospora caninum. Parasitol Res 83: 214-219.
23. Regidor-Cerrillo J, Gomez-Bautista M, Pereira-Bueno J, Aduriz G, Navarro-Lozano V, et al. (2008) Isolation and genetic characterization of Neospora caninum from asymptomatic calves in Spain. Parasitology 135: 1651-1659.
24. Kim K, Eaton MS, Schubert W, Wu S, Tang J, (2001) Optimized expression of green flourescent protein in Toxoplasma gondii using thermostable green flourescent protein mutants. Mol Biochem Parasitol 113: 309-313.
25. Wice B, Menton D, Geuze H, Schwartz AL, (1990) Modulators of cyclic AMP metabolism induce syncytiotrophoblast formation in vitro. Exp Cell Res 186: 306-316.
26. Donald RGK, Carter D, Ullman B, Roos DS, (1996) Insertional tagging, cloning, and expression of the Toxoplasma gondii hypoxanthine-xanthine-guanine phosphoribosyltransferase gene. Journal of Biological Chemistry 271: 14010-14019.
27. Saeij JP, Boyle JP, Grigg ME, Arrizabalaga G, Boothroyd JC, (2005) Bioluminescence imaging of Toxoplasma gondii infection in living mice reveals dramatic differences between strains. Infect Immun 73: 695-702.
28. Marugan-Hernandez V, Ortega-Mora LM, Aguado-Martinez A, Alvarez-Garcia G, (2011) Genetic manipulation of Neospora caninum to express the bradyzoite-specific protein NcSAG4 in tachyzoites. Parasitology 138: 472-480.
29. Kim SK, Karasov A, Boothroyd JC, (2007) Bradyzoite-specific surface antigen SRS9 plays a role in maintaining Toxoplasma gondii persistence in the brain and in host control of parasite replication in the intestine. Infect Immun 75: 1626-1634.
30. Norbury CC, Chambers BJ, Prescott AR, Ljunggren HG, Watts C, (1997) Constitutive macropinocytosis allows TAP-dependent major histocompatibility complex class I presentation of exogenous soluble antigen by bone marrow-derived dendritic cells. Eur J Immunol 27: 280-288.
31. Collantes-Fernandez E, Zaballos A, Alvarez-Garcia G, Ortega-Mora LM, (2002) Quantitative detection of Neospora caninum in bovine aborted fetuses and experimentally infected mice by real-time PCR. J Clin Microbiol 40: 1194-1198.
32. Mordue DG, Monroy F, La Regina M, Dinarello CA, Sibley LD, (2001) Acute toxoplasmosis leads to lethal overproduction of Th1 cytokines. J Immunol 167: 4574-4584.
33. Risco-Castillo V, Fernandez-Garcia A, Ortega-Mora LM, (2004) Comparative analysis of stress agents in a simplified in vitro system of Neospora caninum bradyzoite production. J Parasitol 90: 466-470.
34. Hitziger N, Dellacasa I, Albiger B, Barragan A, (2005) Dissemination of Toxoplasma gondii to immunoprivileged organs and role of Toll/interleukin-1 receptor signalling for host resistance assessed by in vivo bioluminescence imaging. Cell Microbiol 7: 837-848.
35. Lopez-Perez IC, Collantes-Fernandez E, Aguado-Martinez A, Rodriguez-Bertos A, Ortega-Mora LM, (2008) Influence of Neospora caninum infection in BALB/c mice during pregnancy in post-natal development. Vet Parasitol 155: 175-183.
36. Morrison DA, (2002) How to improve statistical analysis in parasitology research publications. Int J Parasitol 32: 1065-1070.
37. Barragan A, Brossier F, Sibley LD, (2005) Transepithelial migration of Toxoplasma gondii involves an interaction of intercellular adhesion molecule 1 (ICAM-1) with the parasite adhesin MIC2. Cell Microbiol 7: 561-568.
38. Lopez-Perez IC, Risco-Castillo V, Collantes-Fernandez E, Ortega-Mora LM, (2006) Comparative effect of Neospora caninum infection in BALB/c mice at three different gestation periods. J Parasitol 92: 1286-1291.
39. Mineo TW, Oliveira CJ, Silva DA, Oliveira LL, Abatepaulo AR, et al. (2010) Neospora caninum excreted/secreted antigens trigger CC-chemokine receptor 5-dependent cell migration. Int J Parasitol 40: 797-805.
40. Teixeira L, Botelho AS, Mesquita SD, Correia A, Cerca F, et al. (2010) Plasmacytoid and conventional dendritic cells are early producers of IL-12 in Neospora caninum-infected mice. Immunol Cell Biol 88: 79-86.
41. Hall JM, Lingenfelter P, Adams SL, Lasser D, Hansen JA, et al. (1995) Detection of maternal cells in human umbilical cord blood using fluorescence in situ hybridization. Blood 86: 2829-2832.
42. Suguitan AL Jr, Leke RG, Fouda G, Zhou A, Thuita L, et al. (2003) Changes in the levels of chemokines and cytokines in the placentas of women with Plasmodium falciparum malaria. J Infect Dis 188: 1074-1082.
43. Pfaff AW, Georges S, Abou-Bacar A, Letscher-Bru V, Klein JP, et al. (2005) Toxoplasma gondii regulates ICAM-1 mediated monocyte adhesion to trophoblasts. Immunol Cell Biol 83: 483-489.
44. Sacks D, Sher A, (2002) Evasion of innate immunity by parasitic protozoa. Nat Immunol 3: 1041-1047.