J. Exp. Med., Volume 189, Number 1, January 4, 1999 179-186

Modulation of Immune Complex-induced Inflammation In Vivo by the Coordinate Expression of Activation and Inhibitory Fc Receptors

By Raphael Clynes,^* Jay S. Maizes,^* Rodolphe Guinamard,^* Masao Ono,^§ Toshiyuki Takai,^§ and Jeffrey V. Ravetch^*

From the ^* Laboratory of Molecular Genetics and Immunology,  The Rockefeller University, New York 10021; the  Department of Experimental Immunology, Institute of Development, Aging and Cancer, Tohoku University, Sendai 980-8575, Japan; and ^§ Core Research for Evolutional Science and Technology (CREST), Japan Science and Technology Corporation (JST), Tokyo 101-0062, Japan

Autoantibodies and immune complexes are major pathogenic factors in autoimmune injury, responsible for initiation of the inflammatory cascade and its resulting tissue damage. This activation results from the interaction of immunoglobulin (Ig)G Fc receptors containing an activation motif (ITAM) with immune complexes (ICs) and cytotoxic autoantibodies which initiates and propagates an inflammatory response. In vitro, this pathway can be interrupted by coligation to FcRIIB, an IgG Fc receptor containing an inhibitory motif (ITIM). In this report, we describe the in vivo consequences of FcRII deficiency in the inflammatory response using a mouse model of IC alveolitis. At subthreshold concentrations of ICs that fail to elicit inflammatory responses in wild-type mice, FcRII-deficient mice developed robust inflammatory responses characterized by increased hemorrhage, edema, and neutrophil infiltration. Bronchoalveolar fluids from FcRII^/ stimulated mice contain higher levels of tumor necrosis factor and chemotactic activity, suggesting that FcRII deficiency lowers the threshold of IC stimulation of resident cells such as the alveolar macrophage. In contrast, complement- and complement receptor-deficient mice develop normal inflammatory responses to suprathreshold levels of ICs, while FcR^/ mice are completely protected from inflammatory injury. An inhibitory role for FcRII on macrophages is demonstrated by analysis of FcRII^/ macrophages which show greater phagocytic and calcium flux responses upon FcRIII engagement. These data reveal contrasting roles for the cellular receptors for IgG on inflammatory cells, providing a regulatory mechanism for setting thresholds for IC sensitivity based on the ratio of ITIM to ITAM FcR expression. Exploiting the FcRII inhibitory pathway could thus provide a new therapeutic approach for modulating antibody-triggered inflammation.

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