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Infection and Immunity, June 2001, p. 4007-4018, Vol. 69, No. 6
0019-9567/01/$04.00+0   DOI: 10.1128/IAI.69.6.4007-4018.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.

Ascaris suum-Derived Products Induce Human Neutrophil Activation via a G Protein-Coupled Receptor That Interacts with the Interleukin-8 Receptor Pathway

Franco H. Falcone,1 Adriano G. Rossi,2 Rose Sharkey,1,dagger Alan P. Brown,3 David I. Pritchard,3 and Rick M. Maizels1,*

Institute of Cell, Animal and Population Biology, University of Edinburgh, Ashworth Laboratories, Edinburgh EH9 3JT,1 Respiratory Medicine Unit, Department of Medicine (RIE), Rayne Laboratory, University of Edinburgh, Edinburgh EH8 9AG,2 and School of Biology, University of Nottingham, University Park, Nottingham NG7 2RD,3 United Kingdom

Received 12 December 2000/Returned for modification 8 February 2001/Accepted 13 March 2001

Infection with tissue-migrating helminths is frequently associated with intense granulocyte infiltrations. Several host-derived factors are known to mediate granulocyte recruitment to the tissues, but less attention has been paid to how parasite-derived products trigger this process. Parasite-derived chemotactic factors which selectively recruit granulocytes have been described, but nothing is known about which cellular receptors respond to these agents. The effect of products from the nematodes Ascaris suum, Toxocara canis, and Anisakis simplex on human neutrophils were studied. We monitored four parameters of activation: chemotaxis, cell polarization, intracellular Ca2+ transients, and priming of superoxide anion production. Body fluids of A. suum (ABF) and T. canis (TcBF) induced strong directional migration, shape change, and intracellular Ca2+ transients. ABF also primed neutrophils for production of superoxide anions. Calcium mobilization in response to A. suum-derived products was completely abrogated by pretreatment with pertussis toxin, implicating a classical G protein-coupled receptor mechanism in the response to ABF. Moreover, pretreatment with interleukin-8 (IL-8) completely abrogated the response to ABF, demonstrating desensitization of a common pathway. However, ABF was unable to fully desensitize the response to IL-8, and binding to CXCR1 or CXCR2 was excluded in experiments using RBL-2H3 cells transfected with the two human IL-8 receptors. Our results provide the first evidence for a direct interaction between a parasite-derived chemotactic factor and the host's chemotactic network, via a novel G protein-coupled receptor which interacts with the IL-8 receptor pathway.

* Corresponding author. Mailing address: Institute of Cell, Animal and Population Biology, University of Edinburgh, Ashworth Laboratories, King's Buildings, Edinburgh EH9 3JT, United Kingdom. Phone: 44 131 650 6763. Fax: 44 131 650 5450. E-mail: r.maizels{at}ed.ac.uk.

dagger Present address: Department of Respiratory Medicine, Altnagelvin Hospital, Londonderry BT47 1SB, United Kingdom.

Infection and Immunity, June 2001, p. 4007-4018, Vol. 69, No. 6
0019-9567/01/$04.00+0   DOI: 10.1128/IAI.69.6.4007-4018.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.


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