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Infection and Immunity, April 2007, p. 1954-1963, Vol. 75, No. 4
0019-9567/07/$08.00+0     doi:10.1128/IAI.01034-06
Copyright © 2007, American Society for Microbiology. All Rights Reserved.

Peritoneal Lavage Cells of Indonesian Thin-Tail Sheep Mediate Antibody-Dependent Superoxide Radical Cytotoxicity In Vitro against Newly Excysted Juvenile Fasciola gigantica but Not Juvenile Fasciola hepatica{triangledown}

David Piedrafita,1,2,3* Endah Estuningsih,4 Jill Pleasance,2 Rhoda Prowse,3 Herman W. Raadsma,5 Els N. T. Meeusen,1,2 and Terry W. Spithill3,6

Department of Physiology, Monash University, Clayton, Victoria 3800, Australia,1 School of Veterinary Science, Melbourne University, Victoria 3010, Australia,2 The Cooperative Research Center for Vaccine Technology, The Bancroft Centre, Royal Brisbane Hospital, Brisbane, Queensland 4029, Australia,3 Research Institute for Veterinary Science, Bogor, West Java, Indonesia,4 Faculty of Veterinary Science, University of Sydney, Camden, New South Wales 2570, Australia,5 Institute of Parasitology and Centre for Host-Parasite Interactions, McGill University, Montreal H9X 3V9, Canada6

Received 3 July 2006/ Returned for modification 16 August 2006/ Accepted 2 January 2007

Indonesian thin-tail (ITT) sheep resist infection by Fasciola gigantica by an immunological mechanism within 2 to 4 weeks of infection yet are susceptible to F. hepatica infection. Studies of ITT sheep show that little liver damage occurs following F. gigantica infection, suggesting that the invading parasites are killed within the peritoneum or shortly after reaching the liver. We investigated whether cells isolated from the peritoneums of ITT sheep could kill newly excysted juvenile F. gigantica in vitro and act as a potential mechanism of resistance against F. gigantica infection. Peritoneal cells from F. gigantica-infected sheep, rich in macrophages and eosinophils, mediated antibody-dependent cytotoxicity against juvenile F. gigantica in vitro. Cytotoxicity was dependent on contact between the parasite and effector cells. Isolated mammary gland eosinophils of F. gigantica-infected sheep, or resident peritoneal monocytes/macrophages from uninfected sheep, also killed the juvenile parasites in vitro. By using inhibitors, we show that the molecular mechanism of killing in these assays was dependent on the production of superoxide radicals by macrophages and eosinophils. In contrast, this cytotoxic mechanism was ineffective against juvenile F. hepatica parasites in vitro. Analysis of superoxide dismutase activity and mRNA levels showed that activity and gene expression were higher in F. hepatica than in F. gigantica, suggesting a possible role for this enzyme in the resistance of F. hepatica to superoxide-mediated killing. We suggest that ovine macrophages and eosinophils, acting in concert with a specific antibody, may be important effector cells involved in the resistance of ITT sheep to F. gigantica.

* Corresponding author. Mailing address: Department of Physiology, Monash University, Wellington Road, Clayton, Victoria 3800, Australia. Phone: 61 3 9905 2593. Fax: 61 3 9905 2547. E-mail: david.piedrafita{at}med.monash.edu.au.

{triangledown} Published ahead of print on 8 January 2007.

Editor: J. F. Urban, Jr.

Infection and Immunity, April 2007, p. 1954-1963, Vol. 75, No. 4
0019-9567/07/$08.00+0     doi:10.1128/IAI.01034-06
Copyright © 2007, American Society for Microbiology. All Rights Reserved.





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