Abstract
We made simultaneous measurements of light-induced changes in the rate of oxygen consumption (QO2) and transmembrane current of single salamander rod photoreceptors. Since the change of PO2 was suppressed by 2 mM Amytal, an inhibitor of mitochondrial respiration, we conclude that it is mitochondrial in origin. To identify the cause of the change of QO2, we measured, in batches of rods, the concentrations of ATP and phosphocreatine (PCr). After 3 min of illumination, when the QO2 had decreased approximately 25%, ATP levels did not change significantly; in contrast, the amount of PCr had decreased approximately 40%. We conclude that either the light-induced decrease of QO2 is not caused by an increase in [ATP] or [PCr], or that the light-induced change of [PCr] is highly heterogeneous in the rod cell.
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Selected References
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- Ahmed J., Braun R. D., Dunn R., Jr, Linsenmeier R. A. Oxygen distribution in the macaque retina. Invest Ophthalmol Vis Sci. 1993 Mar;34(3):516–521. [PubMed] [Google Scholar]
- Ames A., 3rd, Li Y. Y., Heher E. C., Kimble C. R. Energy metabolism of rabbit retina as related to function: high cost of Na+ transport. J Neurosci. 1992 Mar;12(3):840–853. doi: 10.1523/JNEUROSCI.12-03-00840.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Biernbaum M. S., Bownds M. D. Light-induced changes in GTP and ATP in frog rod photoreceptors. Comparison with recovery of dark current and light sensitivity during dark adaptation. J Gen Physiol. 1985 Jan;85(1):107–121. doi: 10.1085/jgp.85.1.107. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cervetto L., Lagnado L., Perry R. J., Robinson D. W., McNaughton P. A. Extrusion of calcium from rod outer segments is driven by both sodium and potassium gradients. Nature. 1989 Feb 23;337(6209):740–743. doi: 10.1038/337740a0. [DOI] [PubMed] [Google Scholar]
- Cornwall M. C., Fein A., MacNichol E. F., Jr Cellular mechanisms that underlie bleaching and background adaptation. J Gen Physiol. 1990 Aug;96(2):345–372. doi: 10.1085/jgp.96.2.345. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Denton R. M., McCormack J. G. Ca2+ as a second messenger within mitochondria of the heart and other tissues. Annu Rev Physiol. 1990;52:451–466. doi: 10.1146/annurev.ph.52.030190.002315. [DOI] [PubMed] [Google Scholar]
- Fein A., Tsacopoulos M. Activation of mitochondrial oxidative metabolism by calcium ions in Limulus ventral photoreceptor. Nature. 1988 Feb 4;331(6155):437–440. doi: 10.1038/331437a0. [DOI] [PubMed] [Google Scholar]
- Fein A., Tsacopoulos M. Light-induced oxygen consumption in Limulus ventral photoreceptors does not result from a rise in the intracellular sodium concentration. J Gen Physiol. 1988 Apr;91(4):515–527. doi: 10.1085/jgp.91.4.515. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hansford R. G. Relation between mitochondrial calcium transport and control of energy metabolism. Rev Physiol Biochem Pharmacol. 1985;102:1–72. doi: 10.1007/BFb0034084. [DOI] [PubMed] [Google Scholar]
- Haugh L. M., Linsenmeier R. A., Goldstick T. K. Mathematical models of the spatial distribution of retinal oxygen tension and consumption, including changes upon illumination. Ann Biomed Eng. 1990;18(1):19–36. doi: 10.1007/BF02368415. [DOI] [PubMed] [Google Scholar]
- Hemmer W., Riesinger I., Wallimann T., Eppenberger H. M., Quest A. F. Brain-type creatine kinase in photoreceptor cell outer segments: role of a phosphocreatine circuit in outer segment energy metabolism and phototransduction. J Cell Sci. 1993 Oct;106(Pt 2):671–683. doi: 10.1242/jcs.106.2.671. [DOI] [PubMed] [Google Scholar]
- Kaupp U. B., Koch K. W. Role of cGMP and Ca2+ in vertebrate photoreceptor excitation and adaptation. Annu Rev Physiol. 1992;54:153–175. doi: 10.1146/annurev.ph.54.030192.001101. [DOI] [PubMed] [Google Scholar]
- Lawson J. W., Veech R. L. Effects of pH and free Mg2+ on the Keq of the creatine kinase reaction and other phosphate hydrolyses and phosphate transfer reactions. J Biol Chem. 1979 Jul 25;254(14):6528–6537. [PubMed] [Google Scholar]
- Linsenmeier R. A., Braun R. D. Oxygen distribution and consumption in the cat retina during normoxia and hypoxemia. J Gen Physiol. 1992 Feb;99(2):177–197. doi: 10.1085/jgp.99.2.177. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Linsenmeier R. A. Effects of light and darkness on oxygen distribution and consumption in the cat retina. J Gen Physiol. 1986 Oct;88(4):521–542. doi: 10.1085/jgp.88.4.521. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lundin A., Hasenson M., Persson J., Pousette A. Estimation of biomass in growing cell lines by adenosine triphosphate assay. Methods Enzymol. 1986;133:27–42. doi: 10.1016/0076-6879(86)33053-2. [DOI] [PubMed] [Google Scholar]
- Lust W. D., Feussner G. K., Barbehenn E. K., Passonneau J. V. The enzymatic measurement of adenine nucleotides and P-creatine in picomole amounts. Anal Biochem. 1981 Jan 15;110(2):258–266. doi: 10.1016/0003-2697(81)90144-5. [DOI] [PubMed] [Google Scholar]
- Mahler M. First-order kinetics of muscle oxygen consumption, and an equivalent proportionality between QO2 and phosphorylcreatine level. Implications for the control of respiration. J Gen Physiol. 1985 Jul;86(1):135–165. doi: 10.1085/jgp.86.1.135. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mahler M. Kinetics of oxygen consumption after a single isometric tetanus of frog sartorius muscle at 20 degrees C. J Gen Physiol. 1978 May;71(5):559–580. doi: 10.1085/jgp.71.5.559. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Matthews P. M., Bland J. L., Gadian D. G., Radda G. K. A 31P-NMR saturation transfer study of the regulation of creatine kinase in the rat heart. Biochim Biophys Acta. 1982 Nov 17;721(3):312–320. doi: 10.1016/0167-4889(82)90084-2. [DOI] [PubMed] [Google Scholar]
- McCormack J. G., Denton R. M. Mitochondrial Ca2+ transport and the role of intramitochondrial Ca2+ in the regulation of energy metabolism. Dev Neurosci. 1993;15(3-5):165–173. doi: 10.1159/000111332. [DOI] [PubMed] [Google Scholar]
- Medrano C. J., Fox D. A. Substrate-dependent effects of calcium on rat retinal mitochondrial respiration: physiological and toxicological studies. Toxicol Appl Pharmacol. 1994 Apr;125(2):309–321. doi: 10.1006/taap.1994.1077. [DOI] [PubMed] [Google Scholar]
- Ratto G. M., Payne R., Owen W. G., Tsien R. Y. The concentration of cytosolic free calcium in vertebrate rod outer segments measured with fura-2. J Neurosci. 1988 Sep;8(9):3240–3246. doi: 10.1523/JNEUROSCI.08-09-03240.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schnetkamp P. P. Sodium-calcium exchange in the outer segments of bovine rod photoreceptors. J Physiol. 1986 Apr;373:25–45. doi: 10.1113/jphysiol.1986.sp016033. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Townes-Anderson E. Intersegmental fusion in vertebrate rod photoreceptors. Rod cell structure revisited. Invest Ophthalmol Vis Sci. 1995 Aug;36(9):1918–1933. [PubMed] [Google Scholar]
- Townes-Anderson E., MacLeish P. R., Raviola E. Rod cells dissociated from mature salamander retina: ultrastructure and uptake of horseradish peroxidase. J Cell Biol. 1985 Jan;100(1):175–188. doi: 10.1083/jcb.100.1.175. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tsacopoulos M., Orkand R. K., Coles J. A., Levy S., Poitry S. Oxygen uptake occurs faster than sodium pumping in bee retina after a light flash. Nature. 1983 Feb 17;301(5901):604–606. doi: 10.1038/301604a0. [DOI] [PubMed] [Google Scholar]
- Tsacopoulos M., Poitry S., Borsellino A. Diffusion and consumption of oxygen in the superfused retina of the drone (Apis mellifera) in darkness. J Gen Physiol. 1981 Jun;77(6):601–628. doi: 10.1085/jgp.77.6.601. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tsacopoulos M., Poitry S. Kinetics of oxygen consumption after a single flash of light in photoreceptors of the drone (Apis mellifera). J Gen Physiol. 1982 Jul;80(1):19–55. doi: 10.1085/jgp.80.1.19. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wallimann T., Wegmann G., Moser H., Huber R., Eppenberger H. M. High content of creatine kinase in chicken retina: compartmentalized localization of creatine kinase isoenzymes in photoreceptor cells. Proc Natl Acad Sci U S A. 1986 Jun;83(11):3816–3819. doi: 10.1073/pnas.83.11.3816. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Widmer H., Poitry S., Tsacopoulos M. The increase of oxygen consumption after a flash of light is tightly coupled to sodium pumping in the lateral ocellus of barnacle. J Gen Physiol. 1990 Jul;96(1):83–108. doi: 10.1085/jgp.96.1.83. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Yau K. W., McNaughton P. A., Hodgkin A. L. Effect of ions on the light-sensitive current in retinal rods. Nature. 1981 Aug 6;292(5823):502–505. doi: 10.1038/292502a0. [DOI] [PubMed] [Google Scholar]
- Yau K. W., Nakatani K. Electrogenic Na-Ca exchange in retinal rod outer segment. Nature. 1984 Oct 18;311(5987):661–663. doi: 10.1038/311661a0. [DOI] [PubMed] [Google Scholar]
- de Azeredo F. A., Lust W. D., Passonneau J. V. Light-induced changes in energy metabolites, guanine nucleotides, and guanylate cyclase within frog retinal layers. J Biol Chem. 1981 Mar 25;256(6):2731–2735. [PubMed] [Google Scholar]
