J chain is a 137-residue polypeptide that is covalently linked to polymeric immunoglobulins and participates in their synthesis and transport to external secretions. To clarify these roles, the secondary structure of J chain was characterized by computer-assisted analyses of human and mouse sequences and by circular dichroism measurements of the isolated J chain. The secondary-structure profiles obtained were very similar to those of superoxide dismutase or immunoglobulin light chain variable domains, suggesting that the J chain folds into an eight-stranded antiparallel beta-barrel and should contain approximately 37% beta-sheet conformation, with the rest of the structure existing as reverse turns (random coil). The circular dichroism measurements indicated that the conformation of denatured, S-carboxymethylated or S-sulfonated J chain consists of 75% random coil and 25% beta-structure. Upon reformation of disulfide bonds the percentage of beta-structure in the air-oxidized J chain increased to 34%, a value that is in good agreement with the secondary-structure analysis. Two alternative models of J-chain structure, a two-domain model [Cann, G., Zaritsky, A. & Koshland, M.E. (1982) Proc. Natl. Acad. Sci. USA 79, 6656-6660] and a single-domain antiparallel beta-sheet bilayer model (proposed in this paper), are compared.