Local, synaptic synthesis of new proteins in response to neuronal stimulation plays a key role in regulation of synaptic morphogenesis. Recent studies indicate that matrix metalloproteinase-9 (MMP-9), an endopeptidase that regulates the pericellular environment through cleavage of its protein components, plays a critical role in regulation of spine morphology and synaptic plasticity. Here, we sought to determine whether MMP-9 mRNA is transported to dendrites for local translation and protein release. First, dendritic transport of MMP-9 mRNA was seen in primary hippocampal neuronal cultures treated with glutamate, and in dentate gyrus granule cells in adult anesthetized rats following induction of long-term potentiation. Second, rapid, activity-dependent polyadenylation of MMP-9 mRNA, association of the mRNA with actively translating polysomes, and de novo MMP-9 protein synthesis was obtained in synaptoneurosomes isolated from rat hippocampus. Third, glutamate stimulation of cultured hippocampal neurons evoked rapid (minutes) increase in MMP-9 activity, as measured by cleavage of its native substrate, beta-dystroglycan. This activity was reduced by the polyadenylation inhibitor, thus linking MMP-9 translation with protein function. In aggregate, our findings show that MMP-9 mRNA is transported to dendrites, locally translated and the protein released in an activity-dependent manner. Acting in concert with other dendritically synthesized proteins, locally secreted MMP-9 may contribute to the structural and functional plasticity of the activated synapses.