Molecular identification and characterization of Xenopus egg uroplakin III, an egg raft-associated transmembrane protein that is tyrosine-phosphorylated upon fertilization

J Biol Chem. 2005 Apr 15;280(15):15029-37. doi: 10.1074/jbc.M410538200. Epub 2005 Feb 7.

Abstract

Here we describe mass spectrometric identification, molecular cloning, and biochemical characterization of a lipid/membrane raft-associated protein that is tyrosine-phosphorylated upon Xenopus egg fertilization. This protein is homologous to mammalian uroplakin III, a member of the uroplakin family proteins (UPs) that constitute asymmetric unit membranes in the mammalian urothelial tissues, thus termed Xenopus uroplakin III (xUPIII). xUPIII contains N-linked sugars and is highly expressed in Xenopus eggs, ovary, urinary tract, and kidney. In unfertilized eggs, xUPIII is predominantly localized to the lipid/membrane rafts and exposed on the cell surface, as judged by surface biotinylation experiments and indirect immunofluorescent studies. After fertilization or hydrogen peroxide-induced egg activation, xUPIII becomes rapidly phosphorylated on tyrosine residue-249, which locates in the carboxyl-terminal cytoplasmic tail of the molecule. Raft localization and tyrosine phosphorylation of xUPIII can be reconstituted in HEK293 cells by coexpression of xUPIII, and Xenopus c-Src, a tyrosine kinase whose fertilization-induced activation in egg rafts is required for initiation of development. In mammals, UPIII is forming a complex with a tetraspanin molecule uroplakin Ib. As another tetraspanin, CD9, is known to be a critical component for sperm-egg fusion in the mouse, we have assumed that xUPIII is involved in sperm-egg interaction. An antibody against the extracellular domain of xUPIII blocks sperm-egg interaction, as judged by the occurrence of egg activation and first cell cleavage. Thus, xUPIII represents an egg raft-associated protein that is likely involved in sperm-egg interaction as well as subsequent Src-dependent intracellular events of egg activation in Xenopus.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Antigens, CD / chemistry
  • Biotinylation
  • CSK Tyrosine-Protein Kinase
  • Cell Line
  • Cell Membrane / metabolism
  • Centrifugation, Density Gradient
  • Cloning, Molecular
  • Cytoplasm / metabolism
  • DNA, Complementary / metabolism
  • Electrophoresis, Polyacrylamide Gel
  • Expressed Sequence Tags
  • Female
  • Fertilization
  • Fluorescent Antibody Technique, Indirect
  • Glutathione Transferase / metabolism
  • Humans
  • Hydrogen Peroxide / chemistry
  • Immunoblotting
  • Immunohistochemistry
  • Immunoprecipitation
  • Lipid Metabolism
  • Male
  • Mass Spectrometry
  • Membrane Glycoproteins / chemistry
  • Membrane Glycoproteins / metabolism*
  • Membrane Microdomains / metabolism
  • Molecular Sequence Data
  • Phosphorylation
  • Protein Binding
  • Protein Structure, Tertiary
  • Protein-Tyrosine Kinases / metabolism
  • Recombinant Fusion Proteins / chemistry
  • Sequence Analysis, DNA
  • Sequence Homology, Amino Acid
  • Sperm-Ovum Interactions
  • Tetraspanin 29
  • Tissue Distribution
  • Tyrosine / chemistry*
  • Uroplakin III
  • Uroplakin Ib
  • Xenopus
  • src-Family Kinases

Substances

  • Antigens, CD
  • CD9 protein, human
  • Cd9 protein, mouse
  • DNA, Complementary
  • Membrane Glycoproteins
  • Recombinant Fusion Proteins
  • Tetraspanin 29
  • UPK1B protein, human
  • UPK3A protein, human
  • Upk3a protein, mouse
  • Uroplakin III
  • Uroplakin Ib
  • Tyrosine
  • Hydrogen Peroxide
  • Glutathione Transferase
  • Protein-Tyrosine Kinases
  • CSK Tyrosine-Protein Kinase
  • src-Family Kinases
  • CSK protein, human

Associated data

  • GENBANK/AB122061
  • GENBANK/BAC99015
  • GENBANK/BC043899