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Infection and Immunity, July 2002, p. 3656-3664, Vol. 70, No. 7
0019-9567/02/$04.00+0     DOI: 10.1128/IAI.70.7.3656-3664.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.

Chronic Helminth Infection Induces Alternatively Activated Macrophages Expressing High Levels of CCR5 with Low Interleukin-12 Production and Th2-Biasing Ability

Miriam Rodríguez-Sosa,1,2 Abhay R. Satoskar,2,{dagger} Rodrigo Calderón,1 Lorena Gomez-Garcia,1 Rafael Saavedra,3 Rafael Bojalil,1 and Luis I. Terrazas1,2*

Department of Immunology, Instituto Nacional de Cardiologia "Ignacio Chavez," D.F. Mexico 14080, and,1 Department of Immunology, Instituto de Investigaciones Biomedicas, U.N.A.M., D.F. Mexico 04510, Mexico, and,3 Department of Immunology and Infectious Diseases, Harvard School of Public Health, Boston, Massachusetts 021152

Received 3 December 2001/ Returned for modification 22 February 2002/ Accepted 8 April 2002

Helminth infections induce Th2-type biased immune responses. Although the mechanisms involved in this phenomenon are not yet clearly defined, antigen-presenting cells (APC) could play an important role in this process. Here, we have used peritoneal macrophages (F4/80+) recruited at different times after challenge with Taenia crassiceps as APC and tested their ability to regulate Th1/Th2 differentiation. Macrophages from acute infections produced high levels of interleukin-12 (IL-12) and nitric oxide (NO), paralleled with low levels of IL-6 and prostaglandin E2 (PGE2) and with the ability to induce strong antigen-specific CD4+ T-cell proliferation in response to nonrelated antigens. In contrast, macrophages from chronic infections produced higher levels of IL-6 and PGE2 and had suppressed production of IL-12 and NO, associated with a poor ability to induce antigen-specific proliferation in CD4+ T cells. Failure to induce proliferation was not due to a deficient expression of accessory molecules, since major histocompatibility complex class II, CD40, and B7-2 were up-regulated, together with CD23 and CCR5 as infection progressed. These macrophages from chronic infections were able to bias CD4+ T cells to produce IL-4 but not gamma interferon (IFN-{gamma}), contrary to macrophages from acute infections. Blockade of B7-2 and IL-6 and inhibition of PGE2 failed to restore the proliferative response in CD4+ T cells. Furthermore, studies using STAT6-/- mice revealed that STAT6-mediated signaling was essential for the expansion of these alternatively activated macrophages. These data demonstrate that helminth infections can induce different macrophage populations that have Th2-biasing properties.

* Corresponding author. Mailing address: Department of Immunology, Instituto Nacional de Cardiologia <904>Ignacio Chavez,<905> Juan Badiano #1, Tlalpan, Mexico, D.F. Mexico 14080. Phone: (5255) 5573-2911. Fax: (5255) 5573-0994. E-mail: terlui{at}cardiologia.org.mx.

Editor: J. M. Mansfield

{dagger} Present address: Department of Microbiology, The Ohio State University, Columbus, OH 43210-1292

Infection and Immunity, July 2002, p. 3656-3664, Vol. 70, No. 7
0019-9567/02/$04.00+0     DOI: 10.1128/IAI.70.7.3656-3664.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.



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