J. Exp. Med.
Volume 185, Number 11, June 2, 1997 1959-1968

Impaired Host Defense, Hematopoiesis, Granulomatous Inflammation and Type 1-Type 2 Cytokine Balance in Mice Lacking CC Chemokine Receptor 1

By Ji-Liang Gao,^* Thomas A. Wynn, Yun Chang,^§ Eric J. Lee, Hal E. Broxmeyer,^¶ Scott Cooper,^¶ H. Lee Tiffany,^* Heiner Westphal, June Kwon-Chung,^§ and Philip M. Murphy^*

From the ^* Laboratory of Host Defenses,  Laboratory of Parasitic Diseases, and ^§ Laboratory of Clinical Investigation, National Institute of Allergy and Infectious Diseases,  Laboratory of Mammalian Genes and Development, National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, Maryland 20892; and ^¶ Departments of Microbiology/Immunology and Medicine and the Walther Oncology Center, Indiana University School of Medicine, Indianapolis, Indiana 46202-5121

CC chemokine receptor 1 (CCR1) is expressed in neutrophils, monocytes, lymphocytes, and eosinophils, and binds the leukocyte chemoattractant and hematopoiesis regulator macrophage inflammatory protein (MIP)-1, as well as several related CC chemokines. Four other CCR subtypes are known; their leukocyte and chemokine specificities overlap with, but are not identical to, CCR1, suggesting that CCR1 has both redundant and specific biologic roles. To test this, we have developed CCR1-deficient mice (/) by targeted gene disruption. Although the distribution of mature leukocytes was normal, steady state and induced trafficking and proliferation of myeloid progenitor cells were disordered in / mice. Moreover, mature neutrophils from / mice failed to chemotax in vitro and failed to mobilize into peripheral blood in vivo in response to MIP-1. Consistent with this, / mice had accelerated mortality when challenged with Aspergillus fumigatus, a fungus controlled principally by neutrophils. To test the role of CCR1 in granuloma formation, we injected Schistosoma mansoni eggs intravenously, and observed a 40% reduction in the size of lung granulomas in / mice compared to +/+ littermates. This was associated with increased interferon- and decreased interleukin-4 production in / versus +/+ lung lymph node cells stimulated with egg-specific antigen, suggesting that CCR1 influences the inflammatory response not only through direct effects on leukocyte chemotaxis, but also through effects on the type 1-type 2 cytokine balance. Thus CCR1 has nonredundant functions in hematopoiesis, host defense, and inflammation.

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