Zinc uptake and distribution in Xenopus laevis oocytes and embryos

Xenopus laevis vitellogenin contains 2 g-atoms (g-at) of Zn and 3 g-at of Ca/dimer, transports zinc in plasma, and plays a role in its distribution within the oocyte [Montorzi et al. (1994) Biochem. Biophys. Res. Commun. 200, 1407-1413; Montorzi et al. (1995) Biochemistry) 33, 10851-10858]. We here report the dynamics and time course of Zn-65-labeled vitellogenin uptake by and distribution within stages II and IV oocytes, the fate of the metal in oocytes as they progress from stages II to VI, as well as in the first two cleavage blastomeres, the blastula, and subsequent stages of the developing embryo and tadpole. Zn-65 bound to vitellogenin is taken up within less than 30 min by either stage II or IV oocytes incubated under in vitro culture conditions whereas free Zn-65 is not. Once internalized, Zn-65 remains within the cytosol of stage II, whereas in stage IV oocytes, it is transferred within 4 h of its entry from the cytosol into yolk platelets. Nearly all of the transferred Zn-65 is found within yolk platelets and their precursors where it is associated with the vitellogenin cleavage product, lipovitellin. Its distribution within the oocyte organelles differs at each stage of oogenesis. In the early stages (III-IV) most of the oocyte zinc is located first in the small endocytosed vesicles and then in multivesicular bodies. When the zinc transfer process is finalized in the late stages of oogenesis (V-VI), >90% of the total oocyte zinc is within yolk platelets while the remainder is in the cytosol. In embryos and tadpoles, the larger of these two pools remain sequestered in yolk platelets and is inaccessible to cytosolic apoproteins throughout the entire period of embryo formation. Its redistribution to the cytosol does not begin until several days after the tadpole has hatched. The smaller pool, on the other hand, is already present in the cytosol and is, therefore, postulated to constitute the sole source of zinc required for embryogenesis.