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Modulation of duodenal iron uptake by hypoxia and fasting in the rat

Published online by Cambridge University Press:  09 March 2007

E. M. Taylor ,
K. B. Raja ,
R. J. Simpson  and
T. J. Peters
E. M. Taylor
Affiliation:
Department of Clinical Biochemistry, King's College School of Medicine and Dentistry, Bessemer Rd, London SE5 9PJ
K. B. Raja
Affiliation:
Department of Clinical Biochemistry, King's College School of Medicine and Dentistry, Bessemer Rd, London SE5 9PJ
R. J. Simpson
Affiliation:
Department of Clinical Biochemistry, King's College School of Medicine and Dentistry, Bessemer Rd, London SE5 9PJ
T. J. Peters
Affiliation:
Department of Clinical Biochemistry, King's College School of Medicine and Dentistry, Bessemer Rd, London SE5 9PJ
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Abstract

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The effect of hypoxic exposure on in vitro duodenal Fe uptake kinetics was studied in tissue fragments from rats that were fed or fasted overnight before study. Hypoxic exposure was for 3 d at 0·5 atm and fasting was for the last 18-24 h before Fe uptake determinations. The non-permeable Fe2+ chelator 3-(2-pyridyl)-5,6-bis-(4-phenyl-sulphonic acid)-l,2,4-triazine (ferrozine), and medium deoxygenation inhibited uptake in all experimental groups. Ferrozine sensitivity and mucosal Fe3+ reductase activity were greatest in hypoxic animals. Fe uptake was inhibited by membrane depolarization only after fasting or hypoxic exposure of the rats. The data demonstrated that Fe uptake by rat duodenal fragments involves at least two mechanisms: a membrane-potentialindependent mechanism which is not responsive to hypoxia and a second mechanism, induced by fasting or hypoxia, which is inhibited by membrane depolarization. Uptake is partially dependent on reduction of Fe3+ to Fe2+ and this is primarily associated with the second mechanism for uptake. These properties have been reported also in mouse and human Fe uptake, suggesting that the rat is a useful model for the study of basic mechanisms of Fe absorption

Keywords

IronIntestineMembrane potential
Type
General Nutrition
Information
British Journal of Nutrition , Volume 77 , Issue 3 , March 1997 , pp. 459 - 473
Copyright
Copyright © The Nutrition Society 1997

References

REFERENCES

Alcorn, C. J., Simpson, R. J., Leahy, D. & Peters, T. J. (1991). In vitro studies of intestinal drug absorption. Determination of partition and distribution coefficients with bush border membrane vesicles. Biochemical Pharmacology 42, 2259–2264.Google Scholar
Barrand, M. A., Hider, R. C. & Callingham, B. A. (1990). The importance of reductive mechanisms for intestinal uptake from ferric maltol and ferric nitrilotriacetic acid (NTA). Journal of Pharmacy and Pharmacology 42, 279–282.CrossRefGoogle ScholarPubMed
Batey, R. & Gallacher, N. (1977). Effect of iron stores and hysterectomy on iron absorption and distribution in pregnant mice. American Journal of Physiology 232, E57–E61.Google Scholar
Bienfait, H. F. (1985). Regulated redox processes at the plasmalemma of plant-root cells and their function in iron uptake. Journal of Bioenergetics and Biomembranes 17, 73–83.CrossRefGoogle ScholarPubMed
Bihler, I. & Crane, R. K. (1962). Studies on the mechanism of intestinal absorption of sugars. V. Influence of several cations and anions on the active transport of sugars in vitro by various preparations of hamster small intestine. Biochimica et Biophysica Acta 59, 78–93.Google Scholar
Bothwell, T. H., Pirzio-Biroli, G. & Finch, C. A. (1958). Iron absorption. I. Factors influencing absorption. Journal of Laboratory and Clinical Medicine 51, 24–36.Google ScholarPubMed
Conrad, M. E., Foy, A. L., Williams, H. L. & Knospe, W. H. (1967). Effect of starvation and protein depletion on femokinetics and iron absorption. American Journal of Physiology 213, 557–565.CrossRefGoogle ScholarPubMed
Cox, T. M. & Peters, T. J. (1979). Cellular mechanisms in the regulation of iron absorption: studies in deficiency before and after treatment. Journal of Physiology 289, 469–478.CrossRefGoogle Scholar
Cox, T. M. & Peters, T. J. (1980). In vitro studies of duodenal iron uptake in patients with primary and secondary iron storage disease. Quarterly Journal of Medicine 49, 249–257.Google Scholar
Dancis, A., Roman, D. G., Anderson, G. J., Hinnesbusch, A. G. & Klausner, R. D. (1992). Ferric reductase of Saccharomyces cerevisiae: molecular characterisation, role in iron uptake, and transcriptional control by iron. Proceedings of the National Academy of Sciences USA 89, 3869–3873.Google Scholar
Debnam, E. S. & Thompson, C. S. (1984). The effect of fasting on the potential difference across the brushborder membrane of enterocytes in rat small intestine. Journal of Physiology 355, 449–456.CrossRefGoogle ScholarPubMed
Donati, R. M., Chapman, C. W., Warnecke, M. A. & Gallacher, N. I. (1964). Iron metabolism in acute starvation. Proceedings of the Society for Experimental Biology and Medicine 117, 50–53.Google Scholar
Drabkin, D. L. & Austin, J. H. (1932). Spectrophotometric studies. I. Spectrophotometric constants for common haemoglobin derivatives in human, dog and rabbit blood. Journal of Biological Chemistry 98, 719–733.CrossRefGoogle Scholar
Eisenthal, R. & Cornish-Bowden, A. (1974). The direct linear plot. A new graphical procedure for estimating enzyme kinetic parameters. Biochemical Journal 139, 715–720.Google Scholar
Fairweather-Tait, S. J. & Wright, A. J. A. (1984). The influence of previous iron intake on the estimation of bioavailability of Fe from a test meal given to rats. British Journal of Nutrition 51, 185–191.CrossRefGoogle ScholarPubMed
Falholt, K., Lund, B. & Falholt, W. (1973). An easy colorimetric micromethod for routine determination of free fatty acids in plasma. Clinica Chimica Acta 46, 105–111.CrossRefGoogle ScholarPubMed
Flanagan, P. R., Haist, J. & Valberg, L. S. (1980). Comparative effects of iron deficiency induced by bleeding and a low-iron diet on the intestinal absorptive interactions of iron, cobalt, manganese, zinc, lead and cadmium. Journal of Nutrition 110, 1754–1763.CrossRefGoogle Scholar
Forrester, R. H., Conrad, M. E. & Crosby, W. H. (1962). Measurement of total body iron59 in animals using whole body liquid scintillation detectors. Proceedings of the Society for Experimental Biology and Medicine 111, 115–119.Google Scholar
Foy, A. L., Williams, H. L., Cortell, S. & Conrad, M. E. (1967). A modified procedure for the determination of non heme iron in tissue. Analytical Biochemistry 18, 559–563.CrossRefGoogle Scholar
Glantz, S. A. & Slinker, B. K. (1990). Primer of Applied Regression and Analysis of Variance. New York: McGraw-Hill Inc.Google Scholar
Hodgson, L. L., Quail, E. A. & Morgan, E. H. (1994). Receptor-independent uptake of transferrin-bound iron by reticulocytes. Archives of Biochemistry and Biophysics 308, 318–326.CrossRefGoogle ScholarPubMed
Minitab Inc. (1992). Minitab Version 7.2. Philadelphia, PA: State College.Google Scholar
Murray, M. J. & Stein, N. (1967). Effects of intestinal contents on uptake of radioiron by everted rat gut sacs. Proceedings of the Society for Experimental Biology and Medicine 125, 411–413.Google Scholar
Murray, M. J. & Stein, N. (1972). The effect of injected iron on the absorption of iron in iron deficiency. British Journal of Haematology 23, 13–16.CrossRefGoogle ScholarPubMed
Nunez, M. T., Alvarez, X., Smith, M., Tapia, V. & Glass, J. (1994). Role of redox systems on Fe3+ uptake by transformed human intestinal epithelial (Caco-2) cells. American Journal of Physiology 267, C1582–C1588.Google Scholar
O'Riordan, D. K., Sharp, P. A., Epstein, O., Srai, S. K. S. & Debnam, E. S. (1994). Increased iron transfer in overnight fasted rats. Gut 35, S52.Google Scholar
Osterloh, K. R. S., Simpson, R. J., Snape, S. & Peters, T. J. (1987). Intestinal iron absorption and mucosal transferrin in rats subjected to hypoxia. Blut 55, 421–431.CrossRefGoogle ScholarPubMed
Pearson, W. N., Reich, M., Frank, H. & Salamat, L. (1967). Effect of dietary iron level on gut iron levels and iron absorption in the rat. Journal of Nutrition 92, 53–65.Google Scholar
Raja, K. B., Bjamason, I., Simpson, R. I. & Peters, T. J. (1987 a). In vitro measurement and adaptive response of Fe3+ uptake by mouse intestine. Cell Biochemistry and Function 5, 69–76.Google Scholar
Raja, K. B., Duane, P. E., Ward, R. J., Iancu, T. C., Simpson, R. J. & Peters, T. J. (1990). In vitro and in vivo studies on Fe3+ absorption by mouse duodenum. Effect of iron loading on adaptive response to chronic hypoxia. Biochemical Pharmacology 9, 107–117.Google Scholar
Raja, K. B., Pountney, D. J., Bomford, A., Przemioslo, R., Sherman, D., Simpson, R. J., Williams, R. & Peters, T. J. (1996). A duodenal mucosal abnormality in the reduction of Fe(III) in patients with genetic haemochromatosis. Gut 38, 765–769.CrossRefGoogle ScholarPubMed
Raja, K. B., Simpson, R. J. & Peters, T. J. (1987 b). Comparison of 59Fe3+ uptake in vitro and in vivo by mouse duodenum. Biochimica et Biophysica Acta 901, 52–60.CrossRefGoogle ScholarPubMed
Raja, K. B., Simpson, R. J. & Peters, T. J. (1987 c). Effect of Ca2+ and Mg2+ on the uptake of Fe3+ by mouse intestinal mucosa. Biochimica et Biophysica Acta 923, 46–51.CrossRefGoogle ScholarPubMed
Raja, K. B., Simpson, R. J. & Peters, T. J. (1989). Membrane potential dependence of Fe(III) uptake by mouse duodenum. Biochimica et Biophysica Acfa 984, 262–266.Google Scholar
Raja, K. B., Simpson, R. J. & Peters, T. J. (1992). Investigation of a role for reduction in ferric iron uptake by mouse duodenum. Biochimica et Biophysica Acta 1135, 141–146.CrossRefGoogle ScholarPubMed
Raja, K. B., Simpson, R. J., Pippard, M. J. & Peters, T. J. (1988). In vivo studies on the relationship between intestinal iron (Fe3+) absorption, hypoxia and erythropoiesis in the mouse. British Journal of Haematology 68, 373–378.Google Scholar
Schümann, K., Elsenhans, B., Ehtechami, C. & Forth, W. (1990). Increased intestinal iron absorption in rats with normal hepatic iron stores. Kinetic aspects of the adaptive response to parenteral iron repletion in dietary iron deficiency. Biochimica et Biophysica Acta 1033, 277–281.CrossRefGoogle ScholarPubMed
Schümann, K., Elsenhans, B., Hunder, G., Strugala, G. & Forth, W. (1989). Increase of the intestinal iron absorption in growing rats and mice after 8 days of iron-deficient feeding. Zeitschrift für Versuchstierkunde 32, 261–267.Google Scholar
Simpson, R. J. (1992). Effect of hypoxic exposure on iron absorption in heterozygous hypotransferrinaemic mice. Annals of Haematology 65, 260–264.Google Scholar
Simpson, R. J. (1996). Dietary iron levels and hypoxia independently affect iron absorption in mice. Journal of Nutrition 126, 1858–1864.Google ScholarPubMed
Simpson, R. J., Venkatesan, S. & Peters, T. J. (1989). Brush border membrane non-esterified fatty acids. Physiological levels and significance for mucosal iron uptake in mouse proximal intestine. Cell Biochemistry and Function 7, 165–171.Google Scholar
Southon, S., Wright, A. J. & Fairweatha-Tait, S. J. (1989). The effect of differences in dietary iron intake on 59Fe absorption and duodenal morphology in pregnant rats. British Journal of Nutrition 62, 707–717.Google Scholar
Turnbull, A. (1974). Iron absorption. In Iron in Biochemistry and Medicine, pp. 369–402 [Jacobs, A. and Worwood, M., editors]. London: Academic Press.Google Scholar
Wien, E. M. & Van Campen, D. R. (1991). Femc iron absorption in rats: relationship to iron status, endogenous sulfhydryl and other redox components in the intestinal lumen. Journal of Nutrition 121, 825–831.Google Scholar
Wien, E. M. & Van Campen, D. R. (1994). Enhanced Fe3+-reducing capacity does not seem to play a major role in increasing iron absorption in rion-deficient rats. Journal of Nutrition 124, 2006–2015.CrossRefGoogle Scholar
Wollenberg, P. & Rummel, W. (1987). Dependence of intestinal iron absorption on the valency state of iron. Archives of Pharmacology 336, 578–582.CrossRefGoogle Scholar