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Journal of Experimental Biology, Vol 200, Issue 2 203-216, Copyright © 1997 by Company of Biologists
JOURNAL ARTICLES |
WR Harvey and H Wieczorek
Department of Biology, Temple University, Philadelphia, PA 19122, USA. lem@icbr.ifas.ufl.edu
Proton-motive forces are thought to be less important than sodium-motive forces in energizing animal membranes. On the supply side, proton-motive forces across mitochondrial inner membranes are well-known energizers of ATP synthesis, catalyzed by F-type ATP synthases. However, on the demand side, proton-motive forces, generated from ATP by V-ATPases, are not widely accepted as energizers of animal membranes; instead, sodium-motive forces, generated by P-ATPases, are thought to predominate. During the 1980s, Anraku, Nelson, Forgac and others showed that proton-motive forces from H+ V-ATPases energize endomembranes of all eukaryotic cells; in most cases, chloride ions accompany the protons and the output compartment is acidified. Unexpectedly, numerous examples of animal plasma membrane energization by proton-motive forces are now appearing. In many insect epithelia, H+ V-ATPases generate transmembrane voltages which secondarily drive sensory signalling, fluid secretion and even alkalization, rather than acidification. Plasma membranes of phagocytes and osteoclasts as well as polarized membranes of epithelia in vertebrate kidney, bladder and epididymis, even apical membranes of frog skin epithelial cells, are now known to be energized by proton-motive forces. The list of proton-energized animal plasma membranes grows daily and includes cancer cells. The localization of H+ V-ATPases either on endomembranes or on plasma membranes may reflect a key event in their evolution. Proton-motive ATPases, like the H+ A-ATPases in present-day archaebacteria, appear to be ancestors of both H+ F-ATP synthases and H+ V-ATPases. On the basis of a greater than 25% overall sequence identity and much higher identity in the nucleotide-binding and regulatory sites, Nelson and others have argued that the A and B subunits of V-ATPases, like the corresponding beta and alpha subunits of F-ATP synthases, derive from common 'A-ATPase-like' ancestral subunits. They postulate that oxygen, introduced into the earth's atmosphere by cyanobacteria, was a selective agent as these key subunits diverged during evolution. Forgac has focused the issue more sharply by showing that the catalytic 'A' subunit of H+ V-ATPases has tow key sulfhydryl residues that are proximal to each other in the tertiary structure; these residues form a disulfide bond under oxidizing conditions, thereby inactivating the enzyme. The corresponding beta subunit of H+ F-ATPases lacks such sulfhydryl residues. Perhaps because their plasma membranes are the site of oxygen-dependent ATP synthesis, which would select against their sulfhydryl-containing regulatory sites, eubacterial cells lack H+ V-ATPases. This retention of the regulatory cysteine residue in the active sites during evolution may explain why H+ V-ATPases. are commonly found in the reducing atmosphere of the cytoplasm, where they would be active, rather than in the putatively oxidizing atmosphere of many plasma membranes, where they would be inactive. It may also explain why animal plasma membrane H+ V-ATPases are commonly found in 'mitochondria-rich' cells. We suggest that the high oxygen affinity of cytochrome oxidase leads to localized reducing conditions near mitochondria which would allow H+ V-ATPases to remain active in plasma membranes of such cells. Moreover, this 'redox modulation mechanism' may obviate the need to evoke two types of enzyme to explain selective targeting of H+ V-ATPases to plasma membranes or endomembranes: membrane that contains a single form of H+ V-ATPase may cycle between the membranes of the cytoplasmic organelles and the cell surface, the enzyme being active only when reducing conditions remove the disulfide bonding restraint.
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