We have previously characterized a 95-kDa plasma membrane receptor for low and very low density lipoproteins in chicken oocytes (George, R., Barber, D. L., and Schneider, W. J. (1987) J. Biol. Chem. 262, 16838-16847). We now report that somatic cells of chickens, such as fibroblasts, express a different receptor for these lipoproteins. This receptor has a Mr of 130,000 and is part of a regulatory system for cholesterol homeostasis analogous to the low density lipoprotein receptor pathway in mammalian cells. Oocytes produce only the 95-kDa receptor, while fibroblasts synthesize exclusively the 130-kDa receptor. In addition to their different Mr values, another distinctive feature of the two proteins was revealed by ligand blotting experiments: the oocyte receptor bound rabbit beta-VLDL (a class of apolipoprotein-B and -E containing lipoprotein particles), whereas the fibroblast receptor did not. Furthermore, polyclonal rabbit antibodies that recognize the oocyte 95-kDa receptor failed to cross-react with the 130-kDa protein on fibroblasts [corrected]. We suggest that different receptors have evolved in the chicken in order to facilitate the deposition of lipids into oocytes (i.e. yolk formation) with concomitant maintenance of cholesterol homeostasis in extraoocytic tissues.