Manganese supplementation reduces high glucose-induced monocyte adhesion to endothelial cells and endothelial dysfunction in zucker diabetic fatty rats

Journal of Biological Chemistry

Volumn 288, Issue 9, 2013, Pages 6409-6416

  Burlet, Elodie ^a   Jain, Sushil K ^a  

^a LOUISIANA STATE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AORTIC TISSUE; BLOOD LEVELS; BODY WEIGHT; DIABETIC PATIENT; DYSLIPIDEMIAS; ENDOTHELIAL DYSFUNCTION; EXPOSED TO; HIGH GLUCOSE; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; ICAM-1 EXPRESSION; IN-VITRO; IN-VIVO; MONOCYTE ADHESION; TYPE-2 DIABETES; UP-REGULATION;

ADHESION; BODY FLUIDS; DISEASES; ENDOTHELIAL CELLS; GLUCOSE; MANGANESE COMPOUNDS; RATS;

MANGANESE;

CHOLESTEROL; GLUCOSE; INTERCELLULAR ADHESION MOLECULE 1; MANGANESE; MANGANESE CHLORIDE; MANGANESE SUPEROXIDE DISMUTASE; MONOCYTE CHEMOTACTIC PROTEIN 1; PLACEBO; REACTIVE OXYGEN METABOLITE; SMALL INTERFERING RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ADHESION; CELL CULTURE; CHOLESTEROL BLOOD LEVEL; CONTROLLED STUDY; DIABETES MELLITUS; DRUG EFFECT; ENDOTHELIAL DYSFUNCTION; GENE SILENCING; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MALE; MONOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN SECRETION; RAT; SUPPLEMENTATION; UMBILICAL VEIN ENDOTHELIAL CELL; UPREGULATION;

ANIMALS; CELL ADHESION; CHEMOKINE CCL2; GENE EXPRESSION REGULATION; GENE KNOCKDOWN TECHNIQUES; GLUCOSE; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; INTERCELLULAR ADHESION MOLECULE-1; MANGANESE; MONOCYTES; RATS; RATS, ZUCKER; REACTIVE OXYGEN SPECIES; SUPEROXIDE DISMUTASE; SWEETENING AGENTS;

EID: 84874762640     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.447805     Document Type: Article

References (38)

1. Fridovich, I. (1997) Superoxide anion radical (O2 .) , superoxide dismutases, and related matters. J. Biol. Chem. 272, 18515-18517
2. Anetor, J. I., Asiribo, O. A., Adedapo, K. S., Akingbola, T. S., Olorunnisola, O. S., and Adeniyi, F. A. (2007) Increased plasma manganese, partially reduced ascorbate,1 and absence of mitochondrial oxidative stress in type 2 diabetes mellitus: implications for the superoxide uncoupling protein 2 (UCP-2) pathway. Biol. Trace Elem. Res. 120, 19-27
3. Hussain, S., and Ali, S. F. (1999) Manganese scavenges superoxide and hydroxyl radicals: an in vitro study in rats. Neurosci. Lett. 261, 21-24
4. Paynter, D. I. (1980) Changes in activity of the manganese superoxide dismutase enzyme in tissues of the rat with changes in dietary manganese. J. Nutr. 110, 437-447
5. Davis, C. D., Ney, D. M., and Greger, J. L. (1990) Manganese, iron, and lipid interactions in rats. J. Nutr. 120, 507-513
6. Zidenberg-Cherr, S., Keen, C. L., Lönnerdal, B., and Hurley, L. S. (1983) Superoxide dismutase activity and lipid peroxidation in the rat: developmental correlations affected by manganese deficiency. J. Nutr. 113, 2498-2504
7. Ekmekcioglu, C., Prohaska, C., Pomazal, K., Steffan, I., Schernthaner, G., and Marktl, W. (2001) Concentrations of seven trace elements in different hematological matrices in patients with type 2 diabetes as compared to healthy controls. Biol. Trace Elem. Res. 79, 205-219
8. Kazi, T. G., Afridi, H. I., Kazi, N., Jamali, M. K., Arain, M. B., Jalbani, N., and Kandhro, G. A. (2008) Copper, chromium, manganese, iron, nickel, and zinc levels in biological samples of diabetes mellitus patients. Biol. Trace Elem. Res. 122, 1-18
9. Volkov, N. F. (1963) Cobalt, manganese, and zinc content in the blood of atherosclerosis patients. Fed. Proc. Transl. Suppl. 22, 897-899
10. Bomb, B. S., Kumawat, D. C., Bomb, P., Taly, A. B., Bedi, T., and Bedi, H. K. (1988) Effect of manganese on regression of atherosclerosis in cholesterol fed rabbits. J. Assoc. Physicians India 36, 149-150
11. Peluso, I., Morabito, G., Urban, L., Ioannone, F., and Serafini, M. (2012) Oxidative stress in atherosclerosis development: the central role of LDL and oxidative burst. Endocr. Metab. Immune Disord. Drug Targets 12, 351-360
12. Panee, J. (2012) Monocyte chemoattractant protein 1 (MCP-1) in obesity and diabetes. Cytokine 60, 1-12
13. Rains, J. L., Kanikarla-Marie, P., and Jain, S. K. (2012) Hyperketonemia induces upregulation of LFA-1 in monocytes, which is mediated by ROS and p38 MAPK activation. Can. J. Physiol. Pharmacol. 90, 1642-1646
14. Malthankar, G. V., White, B. K., Bhushan, A., Daniels, C. K., Rodnick, K. J., and Lai, J. C. (2004) Differential lowering by manganese treatment of activities of glycolytic and tricarboxylic acid (TCA) cycle enzymes investigated in neuroblastoma and astrocytoma cells is associated with manganese- induced cell death. Neurochem. Res. 29, 709-717
15. Isaac, A. O., Kawikova, I., Bothwell, A. L., Daniels, C. K., and Lai, J. C. (2006) Manganese treatment modulates the expression of peroxisome proliferator-activated receptors in astrocytoma and neuroblastoma cells. Neurochem. Res. 31, 1305-1316
16. Sun, Y., Oberley, L. W., and Li, Y. (1988)Asimple method for clinical assay of superoxide dismutase. Clin. Chem. 34, 497-500
17. Rains, J. L., and Jain, S. K. (2011) Hyperketonemia increases monocyte adhesion to endothelial cells and is mediated by LFA-1 expression in monocytes and ICAM-1 expression in endothelial cells. Am. J. Physiol. Endocrinol. Metab. 301, E298-306
18. Manna, P., and Jain, S. K. (2011) Hydrogen sulfide and L-cysteine increase phosphatidylinositol 3,4,5-trisphosphate (PIP3) and glucose utilization by inhibiting phosphatase and tensin homolog (PTEN) protein and activating phosphoinositide 3-kinase (PI3K)/serine/threonine protein kinase (AKT)/protein kinase Cζ/λ (PKCζ/λ) in 3T3l1 adipocytes. J. Biol. Chem. 286, 39848-39859
19. Son, E. W., Lee, S. R., Choi, H. S., Koo, H. J., Huh, J. E., Kim, M. H., and Pyo, S. (2007) Effects of supplementation with higher levels of manganese and magnesium on immune function. Arch. Pharm. Res. 30, 743-749
20. Bae, Y. J., Choi, M. K., and Kim, M. H. (2011) Manganese supplementation reduces the blood cholesterol levels in ca-deficient ovariectomized rats. Biol. Trace Elem. Res. 141, 224-231
21. Metais, C., Forcheron, F., Abdallah, P., Basset, A., Del Carmine, P., Bricca, G., and Beylot, M. (2008) Adiponectin receptors: expression in Zucker diabetic rats and effects of fenofibrate and metformin. Metabolism 57, 946-953
22. Forcheron, F., Basset, A., Abdallah, P., Del Carmine, P., Gadot, N., and Beylot, M. (2009) Diabetic cardiomyopathy: effects of fenofibrate and metformin in an experimental model - the Zucker diabetic rat. Cardiovasc. Diabetol. 8, 16
23. Holm, A. M., Johansen, P. B., Ahnfelt-Rønne, I., and Rømer, J. (2004) Adipogenic and orexigenic effects of the ghrelin-receptor ligand tabimorelin are diminished in leptin-signalling-deficient ZDF rats. Eur. J. Endocrinol. 150, 893-904
24. Beckman, J. A., Creager, M. A., and Libby, P. (2002) Diabetes and atherosclerosis: epidemiology, pathophysiology, and management. JAMA 287, 2570-2581
25. Faxon, D. P., Creager, M. A., Smith, S. C., Jr., Pasternak, R. C., Olin, J. W., Bettmann, M. A., Criqui, M. H., Milani, R. V., Loscalzo, J., Kaufman, J. A., Jones, D. W., and Pearce, W. H. (2004) Atherosclerotic Vascular Disease Conference: Executive Summary: Atherosclerotic Vascular Disease Conference proceeding for healthcare professionals from a special writing group of the American Heart Association. Circulation 109, 2595-2604
26. Walter, R. M., Jr., Uriu-Hare, J. Y., Olin, K. L., Oster, M. H., Anawalt, B. D., Critchfield, J. W., and Keen, C. L. (1991) Copper, zinc, manganese, and magnesium status and complications of diabetes mellitus. Diabetes Care 14, 1050-1056
27. Nahar, Z., Azad, M. A., Rahman, M. A., Rahman, M. A., Bari, W., Islam, S. N., Islam, M. S., and Hasnat, A. (2010) Comparative analysis of serum manganese, zinc, calcium, copper, and magnesium level in panic disorder patients. Biol. Trace Elem. Res. 133, 284-290
28. Rollins, B. J. (1997) Chemokines. Blood 90, 909-928
29. Xing, L., and Remick, D. G. (2007) Promoter elements responsible for antioxidant regulation of MCP-1 gene expression. Antioxid. Redox. Signal. 9, 1979-1989
30. Lefer, D. J., and Granger, D. N. (1999) Monocyte rolling in early atherogenesis: Vital role in lesion development. Circ. Res. 84, 1353-1355
31. Egashira, K. (2003) Molecular mechanisms mediating inflammation in vascular disease: Special reference to monocyte chemoattractant protein-1. Hypertension 41, 834-841
32. Jain, S. K., McVie, R., Duett, J., and Herbst, J. J. (1989) Erythrocyte membrane lipid peroxidation and glycosylated hemoglobin in diabetes. Diabetes 38, 1539-1543
33. Jain, S. K. (1989) Hyperglycemia can cause membrane lipid peroxidation and osmotic fragility in human red blood cells. J. Biol. Chem. 264, 21340-21345
34. Jain, S. K., and Palmer, M. (1997) The effect of oxygen radicals metabolites and vitamin E on glycosylation of proteins. Free Radic. Biol. Med. 22, 593-596
35. Bonazzi, M., and Cossart, P. (2011) Impenetrable barriers or entry portals? The role of cell-cell adhesion during infection. J. Cell Biol. 195, 349-358
36. Golias, C., Batistatou, A., Bablekos, G., Charalabopoulos, A., Peschos, D., Mitsopoulos, P., and Charalabopoulos, K. (2011) Physiology and pathophysiology of selectins, integrins, and IgSF cell adhesion molecules focusing on inflammation. A paradigm model on infectious endocarditis. Cell Commun. Adhes. 18, 19-32
37. Khan, A. G., Pickl-Herk, A., Gajdzik, L., Marlovits, T. C., Fuchs, R., and Blaas, D. (2010) Human rhinovirus 14 enters rhabdomyosarcoma cells expressing ICAM-1 by a clathrin-, caveolin-, and flotillin-independent pathway. J. Virol. 84, 3984-3992
38. Mukhopadhyay, S., and Linstedt, A. D. (2012) Manganese blocks intracellular trafficking of shiga toxin and protects against Shiga toxicosis. Science 335, 332-335