An appropriate balance of matrix synthesis and degradation is required for normal morphogenesis and maintenance of tissue architecture. Extracellular matrix molecules and their receptors, as well as proteinases and their inhibitors, are all involved in matrix remodeling. This report examines the idea that extracellular matrix receptors can regulate matrix remodeling. Rabbit synovial fibroblasts and human embryonic lung fibroblasts (MRC-5) were cultured under two sets of conditions. First, they were plated in serum and allowed to establish an extracellular matrix over a 48 h period. Rat monoclonal antibody to the alpha 5/beta 1 integrin fibronectin receptor or normal rat IgG was added to the medium and the expression of the metalloproteinases was examined. Cells treated with anti-alpha 5/beta 1 expressed procollagenase and prostromelysin, whereas the control cells did not. In both cases the cells were well spread and maintained a well-organized cytoskeleton. In the second condition, cells were plated in serum-free medium on intact fibronectin, anti-alpha 5/beta 1, or fragments of fibronectin that contained the cell-binding domain. Cells attached and spread on all these substrates in a fibronectin receptor-dependent manner. They expressed collagenase and stromelysin on anti-alpha 5/beta 1 and on several fibronectin fragments, but not on intact fibronectin. These data support the hypothesis that the fibronectin receptor can exist in more than one functional state and that these functional states provide information that influences gene expression. Adhesion and spreading are supported by all states, whereas only a subset permits collagenase and stromelysin expression.