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Transcript
Physiol Rev
84: 1479, 2004; 10.1152/physrev.00010.2004.
CORRIGENDA
Volume 83, April 2003
Downloaded from http://physrev.physiology.org/ by 10.220.33.2 on July 4, 2017
Pages 475–579: DeCoursey, Thomas E. “Voltage-Gated Proton Channels and Other
Proton Transfer Pathways” (http://physrev.physiology.org/cgi/content/full/83/
2/475). It has recently come to the review author’s attention that solid evidence
(albeit not voltage-clamp proof) existed that voltage-gated proton channels were
present in the dinoflagellate Noctiluca miliaris well before their “discovery” in
snail neurons in 1982 by Thomas and Meech (9). In 1972, Fogel and Hastings (3)
postulated membrane potential-regulated proton flux, and Hastings (4) illustrated
this mechanism explicitly as a cartoon proton channel in 1978. Bioluminescent
marine creatures like Noctiluca emit light when stimulated, producing nocturnal
luminescence (5). This light is emitted from numerous small luciferin- and luciferase-containing organelles called “scintillons” (5, 8) and is triggered by an action
potential in the vacuolar membrane (1). The action potential reflects decreased
impedance (2) that ion substitution experiments reveal to be mediated by a proton
conductance (6). Protons flow from the vacuole at pH 3.5 (6) into the scintillon,
where they trigger bioluminescence via luciferase. Thus the action potential opens
voltage-gated proton channels (5). The regulation of these vacuolar H⫹ channels
by voltage and pH appears to differ markedly from the votage-gated proton
channels described in my review, all of which occur in plasma membranes. In
contrast to plasma membrane proton channels that open to allow proton efflux,
dinoflagellate proton channels open to allow proton influx from the vacuole
(topologically outside) into the cytoplasm (specifically the scintillon compartment). Viewed from this perspective, the tonoplast action potential has normal
polarity, the depolarization reflecting cation (proton) influx, just as in excitable
cells in multicellular organisms. Whether the inferred properties of these channels
are truly distinct from the relatively uniform assortment of channels described in
my review, necessitating the designation of a new class, awaits voltage-clamp
confirmation. In summary, strong evidence exists for the presence of voltage-gated
proton channels in Noctiluca and other dinoflagellates. These primordial H⫹
channels may mediate a proton action potential that triggers bioluminescence.
REFERENCES
1. Eckert R and Reynolds GT. The subcellular origin of bioluminescence in Noctiluca miliaris. J Gen
Physiol 50: 1429 –1458, 1967.
2. Eckert R and Sibaoka T. The flash-triggering action potential of the luminescent dinoflagellate
Noctiluca. J Gen Physiol 52: 258 –282, 1968.
3. Fogel M and Hastings JW. Bioluminescence: mechanism and mode of control of scintillon activity.
Proc Natl Acad Sci USA 69: 690 – 693, 1972.
4. Hastings JW. Bacterial and dinoflagellate luminescent systems. In: Bioluminescence in Action,
edited by Herring P. London: Academic, 1978, p. 129 –170.
5. Hastings JW. Bioluminescence. In: Cell Physiology Sourcebook. A Molecular Approach (3rd ed.),
edited by N. Sperelakis. San Diego, CA: Academic, 2001, p. 1115–1131.
6. Nawata T and Sibaoka T. Ionic composition and pH of the vacuolar sap in marine dinoflagellate
Noctiluca. Plant Cell Physiol 17: 265–272, 1976.
7. Nawata T and Sibaoka T. Coupling between action potential and bioluminescnece in Noctiluca:
effects of inorganic ions and pH in vacuolar sap. J Comp Physiol 134: 137–149, 1979.
8. Schmitter RE, Njus D, Sulzman FM, Gooch VD, and Hastings JW. Dinoflagellate bioluminescence: a comparative study of in vitro components. J Cell Physiol 87: 123–134, 1976.
9. Thomas RC and Meech RW. Hydrogen ion currents and intracellular pH in depolarized voltageclamped snail neurones. Nature 299: 826 – 828, 1982.
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0031-9333/04 $15.00 Copyright © 2004 the American Physiological Society
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