The effects of X irradiation on matrix formation by growth-plate and articular chondrocytes, as reflected by metabolism of proteoglycans and type II collagen, were examined in a rabbit chondrocyte culture system. Irradiation with 1 to 10 Gy selectively inhibited synthesis of proteoglycans (incorporation of [35S]sulfate) depending on the stage of differentiation of the irradiated cells; however, synthesis of type II collagen was not affected. Irradiation of an immature culture, in which chondrocytes had just reached confluence, suppressed incorporation of [35S]sulfate into the glycosaminoglycan, 10 Gy inducing approximately 45-50% inhibition. In contrast, the irradiation of mature cultures, in which chondrocytes had already secreted extensive cartilage matrix, did not affect the rate of synthesis of proteoglycans (incorporation of [35S]sulfate). We also found that here irradiation stimulated the degradation of proteoglycans, but with the effect differing in growth-plate chondrocytes and articular chondrocytes. In growth-plate chondrocytes, cleavage from a site close to the G1 globular domain induced by 10 Gy enhanced the release of 35S-labeled proteoglycans into the medium, whereas in articular chondrocytes, irradiation had only marginal effects on the release of 35S-labeled proteoglycans. Our results show that irradiation with 1-10 Gy impaired proteoglycan metabolism in cartilage, with differing effects according to the stage of cell differentiation and the type of chondrocyte.