Abstract
We previously showed that gonadotropin increases the K+ activity in Xenopus oocytes and that this is a signal for increased translation. However, K+ need not act to control synthesis directly but may act through an unidentified downstream effector. Using microinjection to vary the salt content of oocytes and concomitantly measuring [3H]leucine incorporation, we found that small changes in Mg2+ greatly affect translation rates. (Ca2+ had little influence.) By measuring intracellular ion activities, we found that oocyte cations existed in a buffer-like (ion-exchange) equilibrium in which K+ and Mg2+ are the preponderant monovalent and divalent cations. Hence, increasing cellular K+ activity might increase translation by causing Mg2+ activity to rise. If so, the increased translation rates produced by hormone treatment or K+ injection would be prevented by EDTA, a Mg2+ chelating agent. This prediction was tested and confirmed. We conclude that, when gonadotropin increases K+ activity, the cell's internal ion-exchange equilibrium is altered thereby increasing Mg2+ activity and this up-regulates translation.
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Selected References
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- Alvarez-Leefmans F. J., Gamiño S. M., Giraldez F., González-Serratos H. Intracellular free magnesium in frog skeletal muscle fibres measured with ion-selective micro-electrodes. J Physiol. 1986 Sep;378:461–483. doi: 10.1113/jphysiol.1986.sp016230. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Berridge M. J., Irvine R. F. Inositol trisphosphate, a novel second messenger in cellular signal transduction. Nature. 1984 Nov 22;312(5992):315–321. doi: 10.1038/312315a0. [DOI] [PubMed] [Google Scholar]
- Botts J., Chashin A., Schmidt L. Computation of metal binding in bi-metal--bi-chelate systems. Biochemistry. 1966 Apr;5(4):1360–1364. doi: 10.1021/bi00868a032. [DOI] [PubMed] [Google Scholar]
- Brendler T., Godefroy-Colburn T., Yu S., Thach R. E. The role of mRNA competition in regulating translation. III. Comparison of in vitro and in vivo results. J Biol Chem. 1981 Nov 25;256(22):11755–11761. [PubMed] [Google Scholar]
- Brennan J. K., Lichtman M. A. The effect of extracellular calcium and magnesium on the proliferation of murine lymphoblasts. J Cell Physiol. 1973 Aug;82(1):101–112. doi: 10.1002/jcp.1040820112. [DOI] [PubMed] [Google Scholar]
- Busa W. B., Ferguson J. E., Joseph S. K., Williamson J. R., Nuccitelli R. Activation of frog (Xenopus laevis) eggs by inositol trisphosphate. I. Characterization of Ca2+ release from intracellular stores. J Cell Biol. 1985 Aug;101(2):677–682. doi: 10.1083/jcb.101.2.677. [DOI] [PMC free article] [PubMed] [Google Scholar]
- CARVALHO A. P., SANUI H., PACE N. CALCIUM AND MAGNESIUM BINDING PROPERTIES OF CELL MEMBRANE MATERIALS. J Cell Physiol. 1963 Dec;62:311–317. doi: 10.1002/jcp.1030620311. [DOI] [PubMed] [Google Scholar]
- Cochran B. H., Lillquist J. S., Stiles C. D. Post-transcriptional control of protein synthesis in Balb/c-3T3 cells by platelet-derived growth factor and platelet-poor plasma. J Cell Physiol. 1981 Dec;109(3):429–438. doi: 10.1002/jcp.1041090308. [DOI] [PubMed] [Google Scholar]
- Dumont J. N. Oogenesis in Xenopus laevis (Daudin). I. Stages of oocyte development in laboratory maintained animals. J Morphol. 1972 Feb;136(2):153–179. doi: 10.1002/jmor.1051360203. [DOI] [PubMed] [Google Scholar]
- Flatman P. W., Lew V. L. Magnesium buffering in intact human red blood cells measured using the ionophore A23187. J Physiol. 1980 Aug;305:13–30. doi: 10.1113/jphysiol.1980.sp013346. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Flatman P. W. Magnesium transport across cell membranes. J Membr Biol. 1984;80(1):1–14. doi: 10.1007/BF01868686. [DOI] [PubMed] [Google Scholar]
- Hallberg R. L., Smith D. C. In vivo and in vitro hormonal effects on the metabolism of immature oocytes of Xenopus laevis. Dev Biol. 1976 Feb;48(2):308–316. doi: 10.1016/0012-1606(76)90092-0. [DOI] [PubMed] [Google Scholar]
- Horowitz S. B., Lau Y. T. A function that relates protein synthetic rates to potassium activity in vivo. J Cell Physiol. 1988 Jun;135(3):425–434. doi: 10.1002/jcp.1041350309. [DOI] [PubMed] [Google Scholar]
- Horowitz S. B., Paine P. L., Tluczek L., Reynhout J. K. Reference phase analysis of free and bound intracellular solutes. I. Sodium and potassium in amphibian oocytes. Biophys J. 1979 Jan;25(1):33–44. doi: 10.1016/S0006-3495(79)85276-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ilan J., Ilan J. Translation of maternal messenger ribonucleoprotein particles from sea urchin in a cell-free system from unfertilized eggs and product analysis. Dev Biol. 1978 Oct;66(2):375–385. doi: 10.1016/0012-1606(78)90246-4. [DOI] [PubMed] [Google Scholar]
- LUBIN M., ENNIS H. L. ON THE ROLE OF INTRACELLULAR POTASSIUM IN PROTEIN SYNTHESIS. Biochim Biophys Acta. 1964 Apr 27;80:614–631. doi: 10.1016/0926-6550(64)90306-8. [DOI] [PubMed] [Google Scholar]
- Lau Y. T., Yassin R. R., Horowitz S. B. Potassium salt microinjection into Xenopus oocytes mimics gonadotropin treatment. Science. 1988 Jun 3;240(4857):1321–1323. doi: 10.1126/science.3375816. [DOI] [PubMed] [Google Scholar]
- Lee G. T., Engelhardt D. L. Growth-related fluctuation in messenger RNA utilization in animal cells. J Cell Biol. 1978 Oct;79(1):85–86. doi: 10.1083/jcb.79.1.85. [DOI] [PMC free article] [PubMed] [Google Scholar]
- McKeehan W. L., Ham R. G. Calcium and magnesium ions and the regulation of multiplication in normal and transformed cells. Nature. 1978 Oct 26;275(5682):756–758. doi: 10.1038/275756a0. [DOI] [PubMed] [Google Scholar]
- Miller D. S., Lau Y. T., Horowitz S. B. Artifacts caused by cell microinjection. Proc Natl Acad Sci U S A. 1984 Mar;81(5):1426–1430. doi: 10.1073/pnas.81.5.1426. [DOI] [PMC free article] [PubMed] [Google Scholar]
- NANNINGA L. B. Calculation of free magnesium, calcium and potassium in muscle. Biochim Biophys Acta. 1961 Dec 9;54:338–344. doi: 10.1016/0006-3002(61)90374-2. [DOI] [PubMed] [Google Scholar]
- Roberts B. E., Paterson B. M. Efficient translation of tobacco mosaic virus RNA and rabbit globin 9S RNA in a cell-free system from commercial wheat germ. Proc Natl Acad Sci U S A. 1973 Aug;70(8):2330–2334. doi: 10.1073/pnas.70.8.2330. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Robinson K. R. Maturation of Xenopus oocytes is not accompanied by electrode-detectable calcium changes. Dev Biol. 1985 Jun;109(2):504–508. doi: 10.1016/0012-1606(85)90475-0. [DOI] [PubMed] [Google Scholar]
- Rose I. A. The state of magnesium in cells as estimated from the adenylate kinase equilibrium. Proc Natl Acad Sci U S A. 1968 Nov;61(3):1079–1086. doi: 10.1073/pnas.61.3.1079. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rozengurt E. Early signals in the mitogenic response. Science. 1986 Oct 10;234(4773):161–166. doi: 10.1126/science.3018928. [DOI] [PubMed] [Google Scholar]
- Rubin A. H., Terasaki M., Sanui H. Major intracellular cations and growth control: correspondence among magnesium content, protein synthesis, and the onset of DNA synthesis in BALB/c3T3 cells. Proc Natl Acad Sci U S A. 1979 Aug;76(8):3917–3921. doi: 10.1073/pnas.76.8.3917. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rubin H. Central role for magnesium in coordinate control of metabolism and growth in animal cells. Proc Natl Acad Sci U S A. 1975 Sep;72(9):3551–3555. doi: 10.1073/pnas.72.9.3551. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rubin H. Magnesium deprivation reproduces the coordinate effects of serum removal or cortisol addition on transport and metabolism in chick embryo fibroblasts. J Cell Physiol. 1976 Dec;89(4):613–625. doi: 10.1002/jcp.1040890418. [DOI] [PubMed] [Google Scholar]
- SACHS H. A stabilized enzyme system for amino acid incorporation. J Biol Chem. 1957 Sep;228(1):23–39. [PubMed] [Google Scholar]
- Smith G. L. Increased ouabain-sensitive 86Rubidium uptake after mitogenic stimulation of quiescent chicken embryo fibroblasts with purified multiplication-stimulating activity. J Cell Biol. 1977 Jun;73(3):761–767. doi: 10.1083/jcb.73.3.761. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Soltoff S. P., Cantley L. C. Mitogens and ion fluxes. Annu Rev Physiol. 1988;50:207–223. doi: 10.1146/annurev.ph.50.030188.001231. [DOI] [PubMed] [Google Scholar]
- Stanners C. P., Becker H. Control of macromolecular synthesis in proliferating and resting Syrian hamster cells in monolayer culture. I. Ribosome function. J Cell Physiol. 1971 Feb;77(1):31–42. doi: 10.1002/jcp.1040770105. [DOI] [PubMed] [Google Scholar]
- Terasaki M., Rubin H. Evidence that intracellular magnesium is present in cells at a regulatory concentration for protein synthesis. Proc Natl Acad Sci U S A. 1985 Nov;82(21):7324–7326. doi: 10.1073/pnas.82.21.7324. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Thomas G., Gordon J. Regulation of protein synthesis during the shift of quiescent animal cells into the proliferative state. Cell Biol Int Rep. 1979 Jul;3(4):307–320. doi: 10.1016/s0309-1651(79)80001-6. [DOI] [PubMed] [Google Scholar]
- Tluczek L., Lau Y. T., Horowitz S. B. Water, potassium, and sodium during amphibian oocyte development. Dev Biol. 1984 Jul;104(1):97–105. doi: 10.1016/0012-1606(84)90039-3. [DOI] [PubMed] [Google Scholar]
- Tupper J. T., Zorgniotti F., Mills B. Potassium transport and content during G1 and S phase following serum stimulation of 3T3 cells. J Cell Physiol. 1977 Jun;91(3):429–440. doi: 10.1002/jcp.1040910313. [DOI] [PubMed] [Google Scholar]
- Wallace R. A., Jared D. W., Dumont J. N., Sega M. W. Protein incorporation by isolated amphibian oocytes. 3. Optimum incubation conditions. J Exp Zool. 1973 Jun;184(3):321–333. doi: 10.1002/jez.1401840305. [DOI] [PubMed] [Google Scholar]