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Physiological Reviews, Vol. 79, No. 2, April 1999, pp. 361-385
Copyright ©1999 by the American Physiological Society
Department of Biochemistry, Faculty of Life Sciences, Tel Aviv University, Tel Aviv, Israel; and Whitney Laboratory, University of Florida, St. Augustine, Florida
Nelson, Nathan and
William R. Harvey.
The vacuolar H+-ATPase (V-ATPase)
is one of the most fundamental enzymes in nature. It functions in
almost every eukaryotic cell and energizes a wide variety of organelles
and membranes. V-ATPases have similar structure and mechanism of
action with F-ATPase and several of their subunits evolved from
common ancestors. In eukaryotic cells, F-ATPases are confined to
the semi-autonomous organelles, chloroplasts, and mitochondria,
which contain their own genes that encode some of the F-ATPase
subunits. In contrast to F-ATPases, whose primary function in
eukaryotic cells is to form ATP at the expense of the proton-motive
force (pmf), V-ATPases function exclusively as ATP-dependent
proton pumps. The pmf generated by V-ATPases in organelles and
membranes of eukaryotic cells is utilized as a driving force for
numerous secondary transport processes. The mechanistic and structural
relations between the two enzymes prompted us to suggest similar
functional units in V-ATPase as was proposed to F-ATPase and to
assign some of the V-ATPase subunit to one of four parts of a
mechanochemical machine: a catalytic unit, a shaft, a hook, and a
proton turbine. It was the yeast genetics that allowed the
identification of special properties of individual subunits and the
discovery of factors that are involved in the enzyme biogenesis and
assembly. The V-ATPases play a major role as energizers of animal
plasma membranes, especially apical plasma membranes of epithelial
cells. This role was first recognized in plasma membranes of
lepidopteran midgut and vertebrate kidney. The list of animals with
plasma membranes that are energized by V-ATPases now includes
members of most, if not all, animal phyla. This includes the classical
Na+ absorption by frog skin, male fertility through
acidification of the sperm acrosome and the male reproductive tract,
bone resorption by mammalian osteoclasts, and regulation of eye
pressure. V-ATPase may function in Na+ uptake by trout
gills and energizes water secretion by contractile vacuoles in
Dictyostelium. V-ATPase was first detected in organelles connected with the vacuolar system. It is the main if not the only
primary energy source for numerous transport systems in these organelles. The driving force for the accumulation of neurotransmitters into synaptic vesicles is pmf generated by V-ATPase. The
acidification of lysosomes, which are required for the proper function
of most of their enzymes, is provided by V-ATPase. The enzyme is
also vital for the proper function of endosomes and the Golgi
apparatus. In contrast to yeast vacuoles that maintain an internal pH
of ~5.5, it is believed that the vacuoles of lemon fruit may have a
pH as low as 2. Similarly, some brown and red alga maintain internal pH
as low as 0.1 in their vacuoles. One of the outstanding questions in
the field is how such a conserved enzyme as the V-ATPase can
fulfill such diverse functions.
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