Neutrophil extracellular trap formation as innate immune reactions against the apicomplexan parasite Eimeria bovis

Veterinary Immunology and Immunopathology

Volumn 133, Issue 1, 2010, Pages 1-8

  Behrendt, Jan Hillern ^a   Ruiz, Antonio ^b   Zahner, Horst ^a   Taubert, Anja ^a   Hermosilla, Carlos ^c  

^a JUSTUS LIEBIG UNIVERSITY   (Germany)

^b UNIVERSITY OF LAS PALMAS DE GRAN CANARIA   (Spain)

^c ROYAL VETERINARY COLLEGE   (United Kingdom)

Author keywords

Innate immunity; Neutrophil extracellular traps; PMN; Protozoan parasite

Indexed keywords

CELL DNA; DEOXYRIBONUCLEASE; DIPHENYLIODONIUM SALT; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE;

ANIMAL CELL; APICOMPLEXAN INFECTION; ARTICLE; CATTLE DISEASE; CELL KINETICS; COCULTURE; CONTROLLED STUDY; COW; EIMERIA BOVIS; FEMALE; FLUORESCENCE IMAGING; HOST CELL; HOST PARASITE INTERACTION; IMMOBILIZED CELL; IMMUNE RESPONSE; IN VITRO STUDY; INFECTION RESISTANCE; INNATE IMMUNITY; LEUKOCYTE FUNCTION; MOLECULAR IMAGING; NEUTROPHIL; NEUTROPHIL CHEMOTAXIS; NONHUMAN; QUANTITATIVE ANALYSIS; SCANNING ELECTRON MICROSCOPY; SPOROZOITE;

ANIMALS; CATTLE; CATTLE DISEASES; COCCIDIOSIS; COCULTURE TECHNIQUES; EIMERIA; EXTRACELLULAR SPACE; IMMUNITY, INNATE; MICROSCOPY, ELECTRON, SCANNING; MICROSCOPY, FLUORESCENCE; NEUTROPHILS; ORGANIC CHEMICALS;

BOVINAE; EIMERIA; EIMERIA BOVIS; PROTOZOA;

EID: 71649111077     PISSN: 01652427     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.vetimm.2009.06.012     Document Type: Article

References (39)

1. Alghamdi A.S., and Foster D.N. Seminal DNase frees spermatozoa entangled in neutrophil extracellular traps. Biol. Reprod. 73 (2005) 1174-1181
2. Baker V.S., Imade G.E., Molta N.B., Tawde P., Pam S.D., Obadofin M.O., Sagay S.A., Egah D.Z., Iya D., Afolabi B.B., Baker M., Ford K., Ford R., Roux K.H., and Keller III T.C. Cytokine-associated neutrophil extracellular traps and antinuclear antibodies in Plasmodium falciparum infected children under six years of age. Malar. J. 7 (2008) 41
3. Behrendt J.H., Hermosilla C., Hardt M., Failing K., Zahner H., and Taubert A. PMN-mediated immune reactions against Eimeria bovis. Vet. Parasitol. 151 (2008) 97-109
4. Beiter K., Wartha F., Albiger B., Normark S., Zychlinsky A., and Henriques-Normark B. An endonuclease allows Streptococcus pneumoniae to escape from neutrophil extracellular traps. Curr. Biol. 16 (2006) 401-407
5. Bekhti K., Kazanji M., and Pery P. In vitro interactions between murine neutrophils and Eimeria falciformis sporozoites. Res. Immunol. 143 (1992) 909-917
6. Blagburn B.L., and Todd Jr. K.S. Pathological changes and immunity associated with experimental Eimeria vermiformis infections in Mus musculus. J. Protozool. 31 (1984) 556-561
7. Brinkmann V., Reichard U., Goosmann C., Fauler B., Uhlemann Y., Weiss D.S., Weinrauch Y., and Zychlinsky A. Neutrophil extracellular traps kill bacteria. Science 303 (2004) 1532-1535
8. Brinkmann V., and Zychlinsky A. Beneficial suicide: why neutrophils die to make NETs. Nat. Rev. Microbiol. 5 (2007) 577-582
9. Buchanan J.T., Simpson A.J., Aziz R.K., Liu G.Y., Kristian S.A., Kotb M., Feramisco J., and Nizet V. DNase expression allows the pathogen group A Streptococcus to escape killing in neutrophil extracellular traps. Curr. Biol. 16 (2006) 396-400
10. Cross A.R., and Jones O.T. The effect of the inhibitor diphenylene iodonium on the superoxide-generating system of neutrophils. Specific labelling of a component polypeptide of the oxidase. Biochem. J. 237 (1986) 111-116
11. Daugschies A., Burger H.J., and Akimaru M. Apparent digestibility of nutrients and nitrogen balance during experimental infection of calves with Eimeria bovis. Vet. Parasitol. 77 (1998) 93-102
12. Fiege N., Klatte D., Kollmann D., Zahner H., and Bürger H.-J. Eimeria bovis in cattle: colostral transfer of antibodies and immune response to experimental infections. Parasitol. Res. 78 (1992) 32-38
13. Fitzgerald P.R. The economic impact of coccidiosis in domestic animals. Adv. Vet. Sci. Comp. Med. 24 (1980) 121-143
14. Friend S.C., and Stockdale P.H. Experimental Eimeria bovis infection in calves: a histopathological study. Can. J. Comp. Med. 44 (1980) 129-140
15. Fuchs T.A., Abed U., Goosmann C., Hurwitz R., Schulze I., Wahn V., Weinrauch Y., Brinkmann V., and Zychlinsky A. Novel cell death program leads to neutrophil extracellular traps. J. Cell Biol. 176 (2007) 231-241
16. Gazzinelli R.T., and Denkers E.Y. Protozoan encounters with Toll-like receptor signalling pathways: implications for host parasitism. Nat. Rev. Immunol. 6 (2006) 895-906
17. Gupta A.K., Hasler P., Holzgreve W., Gebhardt S., and Hahn S. Induction of neutrophil extracellular DNA lattices by placental microparticles and IL-8 and their presence in preeclampsia. Hum. Immunol. 66 (2005) 1146-1154
18. Hermosilla C., Bürger H.J., and Zahner H. T cell responses in calves to a primary Eimeria bovis infection: phenotypical and functional changes. Vet. Parasitol. 84 (1999) 49-64
19. Hermosilla C., Barbisch B., Heise A., Kowalik S., and Zahner H. Development of Eimeria bovis in vitro: suitability of several bovine, human and porcine endothelial cell lines, bovine fetal gastrointestinal, Madin-Darby bovine kidney (MDBK) and African green monkey kidney (VERO) cells. Parasitol. Res. 88 (2002) 301-307
20. Hughes H.P., Thomas K.R., and Speer C.A. Antigen-specific lymphocyte transformation induced by oocyst antigens of Eimeria bovis. Infect. Immun. 56 (1988) 1518-1525
21. Hughes H.P., Whitmire W.M., and Speer C.A. Immunity patterns during acute infection by Eimeria bovis. J. Parasitol. 75 (1989) 86-91
22. Lippolis J.D., Reinhardt T.A., Goff J.P., and Horst R.L. Neutrophil extracellular trap formation by bovine neutrophils is not inhibited by milk. Vet. Immunol. Immunopathol. 113 (2006) 248-255
23. MacLaren A., and de Souza W. Further studies on the interaction of Toxoplasma gondii with neutrophils and eosinophils. J. Submicrosc. Cytol. Pathol. 34 (2002) 99-104
24. MacLaren A., Attias M., and de S.W. Aspects of the early moments of interaction between tachyzoites of Toxoplasma gondii with neutrophils. Vet. Parasitol. 125 (2004) 301-312
25. Margraf S., Lögters T., Reipen J., Altrichter J., Scholz M., and Windolf J. Neutrophil-derived circulating free DNA (cf-DNA/NETs), a potential prognostic marker for posttraumatic development of inflammatory second hit and sepsis. Shock 30 (2008) 352-358
26. Martinelli S., Urosevic M., Daryadel A., Oberholzer P.A., Baumann C., Fey M.F., Dummer R., Simon H.U., and Yousefi S. Induction of genes mediating interferon-dependent extracellular trap formation during neutrophil differentiation. J. Biol. Chem. 279 (2004) 44123-44132
27. Mesfin G.M., Bellamy J.E., and Stockdale P.H. The pathological changes caused by Eimeria falciformis var. pragensis in mice. Can. J. Comp. Med. 42 (1978) 496-510
28. Palic D., Ostojic J., Andreasen C.B., and Roth J.A. Fish cast NETs: neutrophil extracellular traps are released from fish neutrophils. Dev. Comp. Immunol. 31 (2007) 805-816
29. Rose M.E., Wakelin D., and Hesketh P. Eimeria vermiformis: differences in the course of primary infection can be correlated with lymphocyte responsiveness in the BALB/c and C57BL/6 mouse, Mus musculus. Exp. Parasitol. 71 (1990) 276-283
30. + T lymphocytes contribute differentially in resistance to primary and secondary infections. Parasitology 105 Pt 3 (1992) 349-354
31. Schito M.L., and Barta J.R. Nonspecific immune responses and mechanisms of resistance to Eimeria papillata infections in mice. Infect. Immun. 65 (1997) 3165-3170
32. Shi M.Q., Hirzmann J., Dafa'alla T.H., and Zahner H. In vivo expression profiles of cytokine and iNOS mRNAs in rats infected with Eimeria separata. Vet. Parasitol. 97 (2001) 131-140
33. Speer C.A., Reduker D.W., Burgess D.E., Whitmire W.M., and Splitter G.A. Lymphokine-induced inhibition of growth of Eimeria bovis and Eimeria papillata (Apicomplexa) in cultured bovine monocytes. Infect. Immun. 50 (1985) 566-571
34. Taubert A., Krüll M., Zahner H., and Hermosilla C. Toxoplasma gondii and Neospora caninum infections of bovine endothelial cells induce endothelial adhesion molecule gene transcription and subsequent PMN adhesion. Vet. Immunol. Immunopathol. 112 (2006) 272-283
35. Taubert A., Hermosilla C., Sühwold A., and Zahner H. Antigen-induced cytokine production in lymphocytes of Eimeria bovis primary and challenge infected calves. Vet. Immunol. Immunopathol. 126 (2008) 309-320
36. Urban C.F., Reichard U., Brinkmann V., and Zychlinsky A. Neutrophil extracellular traps capture and kill Candida albicans yeast and hyphal forms. Cell Microbiol. 8 (2006) 668-676
37. von Köckritz-Blickwede M., Goldmann O., Thulin P., Heinemann K., Norrby-Teglund A., Rohde M., and Medina E. Phagocytosis-independent antimicrobial activity of mast cells by means of extracellular trap formation. Blood 111 (2008) 3070-3080
38. Wartha F., Beiter K., Albiger B., Fernebro J., Zychlinsky A., Normark S., and Henriques-Normark B. Capsule and d-alanylated lipoteichoic acids protect Streptococcus pneumoniae against neutrophil extracellular traps. Cell Microbiol. 9 (2007) 1162-1171
39. Wilson C.B., and Remington J.S. Activity of human blood leukocytes against Toxoplasma gondii. J. Infect. Dis. 140 (1979) 890-895