Polyadenylation of Na(+)-K(+)-ATPase beta 1-subunit during early development of Xenopus laevis

Am J Physiol. 1994 Jan;266(1 Pt 1):C157-64. doi: 10.1152/ajpcell.1994.266.1.C157.

Abstract

In fully grown Xenopus oocytes, the synthesis of beta-subunits is limiting for the formation of functional Na(+)-K(+)-adenosinetriphosphatase alpha/beta-complexes (Geering, K. FEBS Lett. 285: 189-193, 1991). In the present study, we show that during oocyte growth (from stage I to stage VI) alpha 1-, but not beta 1- or beta 3-isoform, mRNAs accumulate. In addition, beta-mRNAs are apparently sequestered in an untranslated pool in fully grown oocytes (stage VI). From fertilization to morulation, the total pools of alpha 1-, beta 1-, or beta 3-mRNAs vary little. Whereas polyadenylated [poly(A)+] alpha 1- and beta 3-isoform mRNAs did not change significantly, poly(A)+ beta 1-mRNA abundance increased three- to fourfold at morulation, accompanied by a parallel increase in beta 1-protein synthesis. After midblastula transition (i.e., at early gastrula) and during neurulation, poly(A)+ alpha 1- and beta 3-mRNAs accumulated rapidly, whereas poly(A)+ beta 1-mRNA accumulation was delayed by approximately 2 h, beginning only at early neurula. Our results indicate that 1) the abundance of poly(A)+ beta 1-mRNA is rate limiting during embryonic development for the assembly of alpha 1/beta 1-heterodimers, shown to be involved in the vectorial transport of sodium in kidney cells, and 2) the polyadenylation of beta 1-mRNA is a rate-limiting factor during morulation for the synthesis and assembly of new sodium pumps at the time of blastocoel fluid formation. The 3'-untranslated region of beta 1-mRNA (but not of alpha 1-mRNA) expresses cytoplasmic polyadenylation elements (CPEs) with the consensus sequence AXX-AUUUU(A/U)(A/U)(A/U). A role of CPE in the differential polyadenylation of alpha 1- and beta 1-mRNA is proposed.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Aging / metabolism
  • Amino Acid Sequence
  • Animals
  • Brain / enzymology
  • Embryo, Nonmammalian / metabolism*
  • Embryo, Nonmammalian / physiology
  • Embryonic and Fetal Development*
  • Female
  • Male
  • Molecular Sequence Data
  • Nucleic Acid Hybridization
  • Oocytes / metabolism
  • Oocytes / physiology
  • Poly A / metabolism*
  • Protein Biosynthesis
  • RNA, Messenger / metabolism
  • Ribonuclease H
  • Sodium-Potassium-Exchanging ATPase / chemistry
  • Sodium-Potassium-Exchanging ATPase / metabolism*
  • Xenopus laevis

Substances

  • RNA, Messenger
  • Poly A
  • Ribonuclease H
  • Sodium-Potassium-Exchanging ATPase