Hostname: page-component-78c5997874-8bhkd Total loading time: 0 Render date: 2024-11-10T16:40:56.379Z Has data issue: false hasContentIssue false
  • English
  • Français

Increased phagocytosis and production of reactive oxygen species by neutrophils during magnesium deficiency in rats and inhibition by high magnesium concentration

Published online by Cambridge University Press:  09 March 2007

Françoise I. Bussière ,
Elyett Gueux ,
Edmond Rock ,
Jean-Pierre Girardeau ,
Arlette Tridon ,
Andrzej Mazur  and
Yves Rayssiguier
Françoise I. Bussière
Affiliation:
Centre de Recherches en Nutrition Humaine d'Auvergne, Unité Maladies Métaboliques et Micronutriments, INRA, Theix, 63122 St-Genès-Champanelle, France
Elyett Gueux
Affiliation:
Centre de Recherches en Nutrition Humaine d'Auvergne, Unité Maladies Métaboliques et Micronutriments, INRA, Theix, 63122 St-Genès-Champanelle, France
Edmond Rock
Affiliation:
Centre de Recherches en Nutrition Humaine d'Auvergne, Unité Maladies Métaboliques et Micronutriments, INRA, Theix, 63122 St-Genès-Champanelle, France
Jean-Pierre Girardeau
Affiliation:
Laboratoire de Microbiologie, INRA, Theix, 63122 St-Genès-Champanelle, France
Arlette Tridon
Affiliation:
Laboratoire d'Immunologie, CHRU Clermont-Ferrand, France
Andrzej Mazur
Affiliation:
Centre de Recherches en Nutrition Humaine d'Auvergne, Unité Maladies Métaboliques et Micronutriments, INRA, Theix, 63122 St-Genès-Champanelle, France
Yves Rayssiguier*
Affiliation:
Centre de Recherches en Nutrition Humaine d'Auvergne, Unité Maladies Métaboliques et Micronutriments, INRA, Theix, 63122 St-Genès-Champanelle, France
*
*Corresponding author: Dr Y Rayssiguier, fax + 33 473 62 46 38, email yves.rayssiguier@clermont.inra.fr
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

Recent studies underline the importance of the immunoinflammatory processes in the pathology of Mg deficiency. Neutrophils possess a superoxide anion-generating NADPH oxidase and its inappropriate activation may result in tissue damage. The aim of the present study was to assess the effect of experimental Mg deficiency in the rat on polymorphonuclear leucocytes (PMN) activity and the role of increasing extracellular Mg. Weaning male Wistar rats were fed either a Mg-deficient or a control diet for 8 d. In Mg-deficient rats, the characteristic inflammatory response was accompanied by a marked increase in the number of PMN. Higher plasma interleukin 6 and NO concentrations and increased lipid peroxidation in the heart were found in Mg-deficient rats as compared with control rats. As shown by chemiluminescence studies, basal neutrophil activity from Mg-deficient rats was significantly elevated when compared with neutrophils from control rats. Moreover, the chemiluminescence of PMN from Mg-deficient rats was significantly higher than that of control rats following phorbol myristate acetate or opsonized zymosan activation. PMN from Mg-deficient rats also showed an increased activity of phagocytosis in comparison with neutrophils from control animals. Increasing extracellular Mg concentration in the incubating medium of PMN (0·8 v. 8·0 mM) decreased the chemiluminescence activity of PMN from control rats following opsonized zymosan activation. Chemiluminescence activities of PMN from Mg-deficient rats following phorbol myristate acetate or opsonized zymosan challenge were also decreased by high extracellular Mg concentration. From this work, it appears that PMN activation is an early consequence of Mg deficiency and that high extracellular Mg concentration inhibits free radicals generation.

Keywords

MagnesiumInflammationPolymorphonuclear leucocytes
Type
Research Article
Information
British Journal of Nutrition , Volume 87 , Issue 2 , February 2002 , pp. 107 - 113
Copyright
Copyright © The Nutrition Society 2002

References

Babior, BM (1984) The respiratory burst of phagocytes. Journal of Clinical Investigation 73, 599–601.CrossRefGoogle ScholarPubMed
Bois, P, Gascon, A & Beaulnes, A (1963) Histamine-liberating effect of magnesium deficiency in the rat. Nature 187, 501–502.CrossRefGoogle Scholar
Cassatella, MA (1995) The production of cytokines by polymorphonuclear neutrophils. Immunology Today 16, 21–26.CrossRefGoogle ScholarPubMed
Classen, UG, Seitz, G, Grimm, P & Classen, HG (1994) Influence of high and low dietary magnesium levels on functional, chemical and morphological parameters of old rats. Magnesium Research 7, 233–243.Google ScholarPubMed
Edwards, SW (1991) Regulation of neutrophil oxidant production. In Calcium, Oxygen Radicals and Cellular Damage, pp. 35–75 [Duncan, CJ, editor]. Cambridge: University Press.CrossRefGoogle Scholar
Freedman, AM, Atrakchi, AH, Cassidy, MM, Muesing, RA & Weglicki, WB (1990) Magnesium deficiency-induced cardiomyopathy: protection by vitamin E. Biochemical Biophysical Research Communication 170, 1102–1106.CrossRefGoogle ScholarPubMed
Galan, P, Preziosi, P, Durlach, V, Valeix, P, Ribas, L, Bouzid, D, Favier, A & Hercberg, S (1997) Dietary magnesium intake in a French adult population. Magnesium Research 10, 321–328.Google Scholar
Givalois, L, Dornand, J, Mekaouche, M, Solier, MD, Bristow, AF, Ixart, G, Siaud, P, Assenmacher, I & Barbanel, G (1994) Temporal cascade of plasma level surges in ACTH, corticosterone, and cytokines in endotoxin-challenged rats. American Journal of Physiology 276, R164–R170.Google Scholar
Gueux, E, Bussière, F & Rayssiguier, Y (2001) Magnesium content of polymorphonuclear blood cells is not an indicator of magnesium status. In Advances in Magnesium Research: Nutrition and Health [Rayssiguier, Y, Mazur, A and Durlach, J, editors]. London: John Libbey & Co Ltd (In the Press).Google Scholar
Hasegawa, H, Suzuki, K, Nakaji, S & Sugawara, K (1997) Analysis and assessment of the capacity of neutrophils to produce reactive oxygen species in a 96-well microplate format using lucigenin- and luminol-dependent chemiluminescence. Journal of Immunological Methods 210, 1–10.CrossRefGoogle Scholar
Iseri, LT & French, JH (1984) Magnesium: nature's physiologic calcium blocker. American Heart Journal 108, 188–193.CrossRefGoogle ScholarPubMed
Kruse, HD, Orent, ER & McCollum, EV (1932) Studies on magnesium deficiency in animals. I. Symptomatology resulting from magnesium deprivation. Journal of Biological Chemistry 96, 519–539.CrossRefGoogle Scholar
Kurantsin-Mills, J, Cassidy, MM, Stanfford, RE & Weglicki, WB (1997) Marked alterations in circulating inflammatory cells during cardiomyopathy development in a magnesium-deficient rat model. British Journal of Nutrition 78, 845–855.CrossRefGoogle Scholar
McCreary, PA, Battifora, H, Hahneman, BM, Laing, GH & Hass, GM (1967) Leukocytosis, bone marrow hyperplasia and leukemia in chronic magnesium deficiency in the rat. Blood 29, 683–690.CrossRefGoogle ScholarPubMed
Mak, IT, Dickens, BF, Komarov, AM, Wagner, TL, Phillips, TM & Weglicki, WB (1997) Activation of the neutrophil and loss of plasma glutathione during Mg-deficiency modulation by nitric oxide synthase inhibition. Molecular and Cellular Biochemistry 176, 35–39.CrossRefGoogle ScholarPubMed
Mak, IT, Komarov, AM, Wagner, TL, Stafford, RE, Dickens, BF & Weglicki, WB (1996) Enhanced NO production during Mg deficiency and its role in mediating red blood glutathione loss. American Journal of Physiology 271, C385–C390.CrossRefGoogle ScholarPubMed
Malpuech-Brugère, C, Kuryszko, J, Nowacki, W, Rock, E, Rayssiguier, Y & Mazur, A (1998) Early morphological and immunological alterations in the spleen during magnesium deficiency in the rat. Magnesium Research 11, 161–169.Google ScholarPubMed
Malpuech-Brugère, C, Nowacki, W, Daveau, M, Gueux, E, Linard, C, Rock, E, Lebreton, J-PMazur, A & Rayssiguier, Y (2000) Inflammatory response following acute magnesium deficiency in the rat. Biochimica et Biophysica Acta 1501, 91–98.CrossRefGoogle ScholarPubMed
Malpuech-Brugère, C, Nowacki, W, Rock, E, Gueux, E, Mazur, A & Rayssiguier, Y (1999) Enhanced tumor necrosis factor-α production following endotoxin challenge in rats is an early event during magnesium deficiency. Biochimica et Biophysica Acta 1453, 35–40.CrossRefGoogle ScholarPubMed
Nishio, A, Ishiguro, S, Ikegaki, I, Matsumoto, S, Yoshimitsu, F & Miyazaki, A (1988) Histamine metabolism and pinnal hyperaemia during magnesium deficiency in rats. Magnesium Research 1, 155–161.Google ScholarPubMed
Nishio, A, Kikuchi, K, Miyamoto, A & Ishiguro, (2001) Phagocytosis by alveolar macrophages during dietary magnesium deficiency in adult rats. Magnesium Research 14, 120–121. Abstr.Google Scholar
Rayssiguier, Y, Bussière, FI, Gueux, E, Rock, E & Mazur, A (2001) Acute phase response in magnesium deficiency: possible relevance to atherosclerosis. In Advances in Magnesium Research: Nutrition and Health [Rayssiguier, Y, Mazur, A and Durlach, J, editors] London: John Libbey & Co. Ltd (In the Press).Google Scholar
Rayssiguier, Y, Gueux, E, Bussière, L, Durlach, J & Mazur, A (1993) Dietary magnesium affects susceptibility of lipoproteins and tissues to peroxidation in rats. Journal of American College of Nutrition 12, 133–137.CrossRefGoogle ScholarPubMed
Rayssiguier, Y, Malpuech, C, Nowacki, W, Rock, E, Gueux, E & Mazur, A (1997) Inflammatory response in magnesium deficiency. In Advances in Magnesium Research: 1. Magnesium in Cardiology, Suppl. 1, Magnesium Research, pp. 415–421 [Smetana, R, editor]. London: John Libbey & Co Ltd.Google Scholar
Rayssiguier, Y, Thomasset, M, Garel, J-M & Barlet, J-P (1982) Plasma parathyroid hormone levels and intestinal calcium binding protein in magnesium deficient rats. Hormone and Metabolic Research 14, 379–382.CrossRefGoogle ScholarPubMed
Rock, E, Astier, C, Lab, C, Nowacki, W, Gueux, E, Mazur, A & Rayssiguier, Y (1995 a) Magnesium deficiency in rats induces a rise in plasma nitric oxide. Magnesium Research 8, 237–242.Google ScholarPubMed
Rock, E, Astier, C, Lab, C, Vignon, X, Gueux, E, Motta, C & Rayssiguier, Y (1995 b) Dietary magnesium deficiency in rats enhances free radical production in skeletal muscle. Journal of Nutrition 125, 1205–1210.Google ScholarPubMed
Seelig, M (1989) Cardiovascular consequences of magnesium deficiency and loss: Pathogenesis, prevalence and manifestations-magnesium and chloride loss in refractory potassium repletion. American Journal of Cardiology 63, 4G–21G.CrossRefGoogle ScholarPubMed
Sethi, S, Songh, MP & Dikshit, M (1999) Nitric oxide-mediated augmentation of polymorphonuclear free radical generation after hypoxia-reoxygenation. Blood 93, 333–340.CrossRefGoogle ScholarPubMed
Shibata, M, Ueshima, K, Harada, M, Nakamura, M, Hiramori, K, Endo, S, Sato, N, Mukaida, H, Suzuki, T, Suzuki, T & Inada, K (1999) Effect of magnesium sulfate pretreatment and significance of matrix metalloproteinase-1 and interleukin-6 levels in coronary reperfusion therapy for patients with acute myocardial infarction. Angiology 50, 573–582.CrossRefGoogle ScholarPubMed
Shils, ME (1994) Magnesium. In Modern Nutrition in Health and Disease, pp. 164–184 [Shils, ME, Olson, JA and Shike, M, editors]. Malvern: Lea and Febiger.Google Scholar
Simchovitz, L, Foy, MA & Cragoe, EJ (1990) A role for Na+/Ca2+ exchange in the generation of superoxide radicals by human neutrophils. Journal of Biological Chemistry 265, 13449–13456.CrossRefGoogle Scholar
Snyderman, R & Uhing, RJ (1992) Chemoattractant Stimulus–Response Coupling. In Inflammation: Basic Principles and Clinical Correlates, pp. 421–439 [Gallin, JI, Goldstein, IM and Snyderman, R, editors]. New York, NY: Raven Press.Google Scholar
Vormann, J, Günther, T, Höllriegl, V & Schümann, K (1997) Pathobiochemical effects of graded magnesium deficiency in rats. In Advances in Magnesium Research: Magnesium in Cardiology, pp. 422–434 [Smetana, R, editor]. London: John Libbey & Co Ltd.Google Scholar
Wang, J-F, Komarov, P & de Groot, H (1993) Luminol chemiluminescence in rat macrophages and granulocytes: The role of NO, O2-H2O2, and HOCl. Archives of Biochemistry and Biophysics 304, 189–196.CrossRefGoogle ScholarPubMed
Weglicki, WB & Phillips, TM (1992) Pathobiology of magnesium deficiency: a cytokine/neurogenic inflammation hypothesis. American Journal of Physiology 263, R734–R737.Google ScholarPubMed
Zimmermann, P, Weiss, U, Classen, HG, Wendt, B, Epple, A, Zollner, H, Temmel, W, Weger, M & Porta, S (2000) The impact of diets with different magnesium contents on magnesium and calcium in serum and tissues of the rat. Life Science 67, 949–958.CrossRefGoogle ScholarPubMed