Regions of tissue that ressemble cartilage develop at the point where tendon wraps under a bone and receives compressive forces in addition to tension. Northern blot analysis was used to assess expression of mRNA for several extracellular matrix constituents in cells immediately after their isolation from tensional and compressive regions of fetal, adult and old adult bovine deep flexor tendon. Messenger RNA for aggrecan and type II collagen, as well as for biglycan and decorin, was highly expressed in cells from the compressed region of adult tendon, indicating that this tissue contains cells with a chondrocytic phenotype. In contrast, only mRNA for decorin was highly expressed in cells from the tensional region of adult tendon. The major developmental changes in mRNA expression in the compressed region of tendon included a approximately 25-fold increase in aggrecan expression between fetal and adult tissue and an increase in type II collagen mRNA from undetectable in fetal tendon to expression in adult tendon that was nearly as high as the level expressed in cells from adult articular cartilage. Developmental changes in the tensional region consisted of a approximately 10-fold decrease in type I collagen expression and a 4-fold increase in decorin expression in cells from adult tissue, as compared to fetal tissue. These observations indicate that levels of gene expression for proteoglycans and collagen in tendon correlate with the mechanical environment in the tissue. The regional distinctions in mRNA expression were lost when cells were grown in monolayer culture for one week.(ABSTRACT TRUNCATED AT 250 WORDS)