This study examines the high capacity binding of intact and carboxyl-terminal-truncated alpha A(alpha A) crystallin to two types of lens membrane preparations; membrane stripped of extrinsic protein and some lipid by extraction with urea and alkali and unextracted membrane isolated by centrifugation of total water insoluble protein on a sucrose gradient (native membrane). High capacity binding of alpha A crystallin to the urea-treated membrane was seen once the alpha A substrate concentration reached about 1 mg/ml of media. The membrane bound up to one mg of alpha A per mg of intrinsic protein (MP26) at a concentration of 5 mg alpha A/ml media, binding 5 to 10 times greater than that seen by others at saturation of the high affinity but low capacity binding sites. No apparent differences were seen between high capacity binding of carboxyl terminal-truncated alpha A (by trypsin) and intact alpha A, although each crystalline could antagonize binding of the other. However, once membrane bound, neither crystallin appeared to grossly displace the other. Using the carboxyl terminal-truncated alpha crystallin as a model substrate, native membrane was seen to have a higher capacity to bind the truncated alpha crystallin than urea-extracted membrane and binding was better correlated with the preexisting alpha A content of the native membrane than its MP26 content. An artificial native membrane was prepared by prebinding the truncated alpha A to urea-extracted membrane. This preparation bound more intact alpha A than urea-extracted membrane bearing no prebound crystallin. We conclude that lens native membrane possesses a high capacity to bind alpha crystallins and that this binding could be mediated through protein-protein interactions with alpha crystallin bound in situ to the membrane as extrinsic protein.