Insulin-induced NADPH oxidase activation promotes proliferation and matrix metalloproteinase activation in monocytes/macrophages

Free Radical Biology and Medicine

Volumn 46, Issue 8, 2009, Pages 1058-1067

  San José, Gorka ^a   Bidegain, Julen ^a   Robador, Pablo A ^a   Díez, Javier ^a,b   Fortuño, Ana ^a   Zalba, Guillermo ^a  

^a UNIVERSITY OF NAVARRA   (Spain)

^b UNIVERSITY CLINIC OF NAVARRA   (Spain)

Author keywords

Insulin; Matrix metalloproteinase; Monocyte macrophage; NADPH oxidase; Superoxide

Indexed keywords

GELATINASE B; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INSULIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE C; PROTEIN P47; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; SMALL INTERFERING RNA; SOMATOMEDIN C; SUPEROXIDE;

ANIMAL CELL; ARTICLE; CELL MEMBRANE; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME ACTIVATION; GENE SILENCING; HUMAN; HUMAN CELL; MACROPHAGE; MONOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; CELL LINE; CELL PROLIFERATION; CELLS, CULTURED; ENZYME ACTIVATION; ENZYME INHIBITORS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HUMANS; INSULIN; MACROPHAGES; MATRIX METALLOPROTEINASE 9; MEMBRANE GLYCOPROTEINS; MICE; MONOCYTES; NADPH OXIDASE; NF-KAPPA B; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PROTEIN KINASE C; PROTEIN TRANSPORT; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; SUPEROXIDES;

MURINAE;

EID: 63049123598     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2009.01.009     Document Type: Article

References (44)

1. Griendling K.K., Sorescu D., and Ushio Fukai M. NAD(P)H oxidase: role in cardiovascular biology and disease. Circ. Res. 86 (2000) 494-501
2. Nishikawa T., Edelstein D., Du X.L., Yamagishi S., Matsumura T., Kaneda Y., Yorek M.A., Beebe D., Oates P.J., Hammes H.P., Giardino I., and Brownlee M. Normalizing mitochondrial superoxide production blocks three pathways of hyperglycaemic damage. Nature 404 (2000) 787-790
3. Bokoch M., and Knaus U.G. NADPH oxidases: not just for leukocytes anymore!. Trends Biochem. Sci. 28 (2003) 502-508
4. Brandes R.P., and Kreuzer J. Vascular NADPH oxidases: molecular mechanisms of activation. Cardiovasc. Res. 65 (2005) 16-27
5. Sorescu D., Weiss D., Lassegue B., Clempus R.E., Szocs K., Sorescu G.P., Valppu L., Quinn M.T., Lambeth J.D., Vega J.D., Taylor W.R., and Griendling K.K. Superoxide production and expression of nox family proteins in human atherosclerosis. Circulation 105 (2002) 1429-1435
6. Azumi H., Inoue N., Ohashi Y., Terashima M., Mori T., Fujita H., Awano K., Kobayashi K., Maeda K., Hata K., Shinke T., Kobayashi S., Hirata K., Kawashima S., Itabe H., Hayashi Y., Imajoh-Ohmi S., Itoh H., and Yokoyama M. Superoxide generation in directional coronary atherectomy specimens of patients with angina pectoris: important role of NAD(P)H oxidase. Arterioscler. Thromb. Vasc. Biol. 22 (2002) 1838-1844
7. Zalba G., Beloqui O., San José G., Moreno M.U., Fortuño A., and Díez J. NADPH oxidase-dependent superoxide production is associated with carotid intima-media thickness in subjects free of clinical atherosclerotic disease. Arterioscler. Thromb. Vasc. Biol. 25 (2005) 1452-1457
8. Delbosc S., Paizanis E., Magous R., Araiz C., Dimo T., Cristol J.P., Cros G., and Azay J. Involvement of oxidative stress and NADPH oxidase activation in the development of cardiovascular complications in a model of insulin resistance, the fructose-fed rat. Atherosclerosis 179 (2005) 43-49
9. Sonta T., Inoguchi T., Tsubouchi H., Sekiguchi N., Kobayashi K., Matsumoto S., Utsumi H., and Nawata H. Evidence for contribution of vascular NAD(P)H oxidase to increased oxidative stress in animal models of diabetes and obesity. Free Radic. Biol. Med. 37 (2004) 115-123
10. Fortuño A., San José G., Moreno M.U., Beloqui O., Díez J., and Zalba G. Phagocytic NADPH oxidase overactivity underlies oxidative stress in metabolic syndrome. Diabetes 55 (2006) 209-215
11. Ceolotto G., Bevilacqua M., Papparella I., Baritono E., Franco L., Corvaja C., Mazzoni M., Semplicini A., and Avogaro A. Insulin generates free radicals by an NAD(P)H, phosphatidylinositol 3′-kinase-dependent mechanism in human skin fibroblasts ex vivo. Diabetes 53 (2004) 1344-1351
12. Zhuang D., Ceacareanu A.C., Lin Y., Ceacareanu B., Dixit M., Chapman K.E., Waters C.M., Rao G.N., and Hassid A. Nitric oxide attenuates insulin- or IGF-I-stimulated aortic smooth muscle cell motility by decreasing H2O2 levels: essential role of cGMP. Am. J. Physiol. Heart Circ. Physiol. 286 (2004) H2103-H2112
13. Krieger-Brauer H.I., and Kather H. Human fat cells possess a plasma membrane-bound H2O2-generating system that is activated by insulin via a mechanism bypassing the receptor kinase. J. Clin. Invest. 89 (1992) 1006-1013
14. 2 and plays an integral role in insulin signal transduction. Mol. Cell. Biol. 24 (2004) 1844-1854
15. Ross R. Atherosclerosis is an inflammatory disease. Am. Heart J. 138 (1999) S419-S420
16. Fortuño A., Oliván S., Beloqui O., San José G., Moreno M.U., Díez J., and Zalba G. Association of increased phagocytic NADPH oxidase-dependent superoxide production with diminished nitric oxide generation in essential hypertension. J. Hypertens. 22 (2004) 2169-2175
17. Zalba G., Fortuño A., Orbe J., San José G., Moreno M.U., Belzunce M., Rodríguez J.A., Beloqui O., Páramo J.A., and Díez J. Phagocytic NADPH oxidase-dependent superoxide production stimulates matrix metalloproteinase-9: implications for human atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 27 (2007) 587-593
18. Facchini F.S., Hua N.W., Reaven G.M., and Stoohs R.A. Hyperinsulinemia: the missing link among oxidative stress and age-related diseases?. Free Radic. Biol. Med. 29 (2000) 1302-1306
19. Furukawa S., Fujita T., Shimabukuro M., Iwaki M., Yamada Y., Nakajima Y., Nakayama O., Makishima M., Matsuda M., and Shimomura I. Increased oxidative stress in obesity and its impact on metabolic syndrome. J. Clin. Invest. 114 (2004) 1752-1761
20. Hoyal C.R., Gutierrez A., Young B.M., Catz S.D., Lin J.H., Tsichlis P.N., and Babior B.M. Modulation of p47PHOX activity by site-specific phosphorylation: Akt-dependent activation of the NADPH oxidase. Proc. Natl. Acad. Sci. USA 100 (2003) 5130-5135
21. Zhan Y., Virbasius J.V., Song X., Pomerleau D.P., and Zhou G.W. The p40phox and p47phox PX domains of NADPH oxidase target cell membranes via direct and indirect recruitment by phosphoinositides. J. Biol. Chem. 277 (2002) 4512-4518
22. Cathcart M.K. Regulation of superoxide anion production by NADPH oxidase in monocytes/macrophages: contributions to atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 24 (2004) 23-28
23. Standaert M.L., Galloway L., Karnam P., Bandyopadhyay G., Moscat J., and Farese R.V. Protein kinase C-zeta as a downstream effector of phosphatidylinositol 3-kinase during insulin stimulation in rat adipocytes. Potential role in glucose transport. J. Biol. Chem. 272 (1997) 30075-30082
24. Frey R.S., Gao X., Javaid K., Siddiqui S.S., Rahman A., and Malik A.B. Phosphatidylinositol 3-kinase gamma signaling through protein kinase Czeta induces NADPH oxidase-mediated oxidant generation and NF-kappaB activation in endothelial cells. J. Biol. Chem. 281 (2006) 16128-16138
25. Droge W. Free radicals in the physiological control of cell function. Physiol. Rev. 82 (2002) 47-95
26. Zhang H.S., and Wang S.Q. Notoginsenoside R1 inhibits TNF-alpha-induced fibronectin production in smooth muscle cells via the ROS/ERK pathway. Free Radic. Biol. Med. 40 (2006) 1664-1674
27. Wang Y., Zeigler M.M., Lam G.K., Hunter M.G., Eubank T.D., Khramtsov V.V., Tridandapani S., Sen C.K., and Marsh C.B. The role of the NADPH oxidase complex, p38 MAPK, and Akt in regulating human monocyte/macrophage survival. Am. J. Respir. Cell Mol. Biol. 36 (2007) 68-77
28. Kefaloyianni E., Gaitanaki C., and Beis I. ERK1/2 and p38-MAPK signalling pathways, through MSK1, are involved in NF-kappaB transactivation during oxidative stress in skeletal myoblasts. Cell Signal. 18 (2006) 2238-2251
29. Li L., Mamputu J.C., Wiernsperger N., and Renier G. Signaling pathways involved in human vascular smooth muscle cell proliferation and matrix metalloproteinase-2 expression induced by leptin: inhibitory effect of metformin. Diabetes 54 (2005) 2227-2234
30. Dong F., Zhang X., Wold L.E., Ren Q., Zhang Z., and Ren J. Endothelin-1 enhances oxidative stress, cell proliferation and reduces apoptosis in human umbilical vein endothelial cells: role of ETB receptor, NADPH oxidase and caveolin-1. Br. J. Pharmacol. 145 (2005) 323-333
31. Iida K.T., Suzuki H., Sone H., Shimano H., Toyoshima H., Yatoh S., Asano T., Okuda Y., and Yamada N. Insulin inhibits apoptosis of macrophage cell line, THP-1 cells, via phosphatidylinositol-3-kinase-dependent pathway. Arterioscler. Thromb. Vasc. Biol. 22 (2002) 380-386
32. Senokuchi T., Matsumura T., Sakai M., Matsuo T., Yano M., Kiritoshi S., Sonoda K., Kukidome D., Nishikawa T., and Araki E. Extracellular signal-regulated kinase and p38 mitogen-activated protein kinase mediate macrophage proliferation induced by oxidized low-density lipoprotein. Atherosclerosis 176 (2004) 233-245
33. Fischoeder A., Meyborg H., Stibenz D., Fleck E., Graf K., and Stawowy P. Insulin augments matrix metalloproteinase-9 expression in monocytes. Cardiovasc. Res. 73 (2007) 841-848
34. Djordjevic T., Pogrebniak A., BelAiba R.S., Bonello S., Wolzlaw C., Acker H., Hess J., and Görlach A. The expression of the NADPH oxidase subunit p22phox is regulated by a redox-sensitive pathway in endothelail cells. Free Radic. Biol. Med. 38 (2005) 616-630
35. Reaven G.M. Insulin resistance/compensatory hyperinsulinemia, essential hypertension, and cardiovascular disease. J. Clin. Endocrinol. Metab. 88 (2003) 2399-2403
36. Ceriello A., and Motz E. Is oxidative stress the pathogenic mechanism underlying insulin resistance, diabetes, and cardiovascular disease? The common soil hypothesis revisited. Arterioscler. Thromb. Vasc. Biol. 24 (2004) 816-823
37. Spagnoli L.G., Orlandi A., and Santeusanio G. Foam cells of the rabbit atherosclerotic plaque arrested in metaphase by colchicine show a macrophage phenotype. Atherosclerosis 88 (1991) 87-92
38. Galis Z.S., and Khatri J.J. Matrix metalloproteinases in vascular remodeling and atherogenesis: the good, the bad, and the ugly. Circ. Res. 90 (2002) 251-262
39. Bendeck M.P., Irvin C., Reidy M., Smith L., Mulholland D., Horton M., and Giachelli C.M. Smooth muscle cell matrix metalloproteinase production is stimulated via alpha(v)beta(3) integrin. Arterioscler. Thromb. Vasc. Biol. 20 (2000) 1467-1472
40. Blankenberg S., Rupprecht H.J., Poirier O., Bickel C., Smieja M., Hafner G., Meyer J., Cambien F., and Tiret L. Plasma concentrations and genetic variation of matrix metalloproteinase 9 and prognosis of patients with cardiovascular disease. Circulation 107 (2003) 1579-1585
41. Dandona P., Aljada A., Mohanty P., Ghanim H., Hamouda W., Assian E., and Ahmad S. Insulin inhibits intranuclear nuclear factor kappaB and stimulates IkappaB in mononuclear cells in obese subjects: evidence for an anti-inflammatory effect?. J. Clin. Endocrinol. Metab. 86 (2001) 3257-3265
42. Mohanty P., Hamouda W., Garg R., Aljada A., Ghanim H., and Dandona P. Glucose challenge stimulates reactive oxygen species (ROS) generation by leucocytes. J. Clin. Endocrinol. Metab. 85 (2000) 2970-2973
43. Touyz R.M. Apocynin, NADPH oxidase, and vascular cells: a complex matter. Hypertension 51 (2008) 172-174
44. Heumüller S., Wind S., Barbosa-Sicard E., Schmidt H.H., Busse R., Schröder K., and Brandes R.P. Apocynin is not an inhibitor of vascular NADPH oxidases but an antioxidant. Hypertension 51 (2008) 211-217