The nitroxide radical TEMPOL prevents obesity, hyperlipidaemia, elevation of inflammatory cytokines, and modulates atherosclerotic plaque composition in apoE-/- mice

Atherosclerosis

Volumn 240, Issue 1, 2015, Pages 234-241

  Kim, Christine H J ^a,b   Mitchell, James B ^c   Bursill, Christina A ^a,b   Sowers, Anastasia L ^c   Thetford, Angela ^c   Cook, John A ^c   van Reyk, David M ^d   Davies, Michael J ^a,b,e  

^a HEART RESEARCH INSTITUTE   (Australia)

^b University of Sydney   (Australia)

^c NATIONAL CANCER INSTITUTE   (United States)

^d UNIVERSITY OF TECHNOLOGY SYDNEY   (Australia)

^e UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

Adipokines; Atherosclerosis; Cardiovascular disease; Inflammatory cytokines; Lipid; Nitroxide; TEMPOL

Indexed keywords

ADIPONECTIN; COLLAGEN; CYTOKINE; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; INTERLEUKIN 6; LEPTIN; LOW DENSITY LIPOPROTEIN CHOLESTEROL; MONOCYTE CHEMOTACTIC PROTEIN 1; MYELOPEROXIDASE; NITROXIDE; RADICAL; SERUM AMYLOID A; TEMPOL; TRIACYLGLYCEROL; AMINE OXIDE; ANTIINFECTIVE AGENT; ANTILIPEMIC AGENT; ANTIOBESITY AGENT; ANTIOXIDANT; APOLIPOPROTEIN E; AUTACOID; BIOLOGICAL MARKER; CHOLESTEROL; SPIN LABELING;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AORTA SINUS; ARTICLE; ATHEROSCLEROTIC PLAQUE; BODY MASS; CONTROLLED STUDY; FAT INTAKE; FEMALE; HYPERLIPIDEMIA; LIPID BLOOD LEVEL; LIPID DIET; MACROPHAGE; MOUSE; NONHUMAN; OBESITY; PRIORITY JOURNAL; SMOOTH MUSCLE FIBER; TRIACYLGLYCEROL BLOOD LEVEL; ANIMAL; AORTA; AORTIC DISEASES; ATHEROSCLEROSIS; BLOOD; BODY WEIGHT; DEFICIENCY; DISEASE MODEL; DRUG EFFECTS; GENETICS; HYPERLIPIDEMIAS; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; SPIN LABELING; TIME;

ANIMALS; ANTI-INFECTIVE AGENTS; ANTI-OBESITY AGENTS; ANTIOXIDANTS; AORTA; AORTIC DISEASES; APOLIPOPROTEINS E; ATHEROSCLEROSIS; BIOMARKERS; BODY WEIGHT; CHOLESTEROL; CYCLIC N-OXIDES; CYTOKINES; DISEASE MODELS, ANIMAL; HYPERLIPIDEMIAS; HYPOLIPIDEMIC AGENTS; INFLAMMATION MEDIATORS; MICE, KNOCKOUT; OBESITY; PLAQUE, ATHEROSCLEROTIC; SPIN LABELS; TIME FACTORS; TRIGLYCERIDES;

EID: 84925358212     PISSN: 00219150     EISSN: 18791484     Source Type: Journal    
DOI: 10.1016/j.atherosclerosis.2015.03.012     Document Type: Article

References (50)

1. Graham I., Cooney M.-T., Bradley D., et al. Dyslipidemias in the prevention of cardiovascular disease: risks and causality. Curr. Cardiol. Rep. 2012, 14:709-720.
2. Mitchell J.B., Xavier S., DeLuca A.M., et al. Alow molecular weight antioxidant decreases weight and lowers tumor incidence. Free Radic. Biol. Med. 2003, 34:93-102.
3. Soule B.P., Hyodo F., Matsumoto K., et al. The chemistry and biology of nitroxide compounds. Free Radic. Biol. Med. 2007, 42:1632-1650.
4. Soule B.P., Hyodo F., Matsumoto K., et al. Therapeutic and clinical applications of nitroxide compounds. Antioxid. Redox Signal 2007, 9:1731-1743.
5. Samuni A., Mitchell J.B., DeGraff W., et al. Nitroxide SOD-mimics: modes of action. Free Radic. Res. Commun. 1991, 12-13:187-194.
6. Krishna C.M., Samuni A. Nitroxides as antioxidants. Meth. Enzymol. 1994, 234:580-589.
7. Lam M.A., Pattison D.I., Bottle S.E., et al. Nitric oxide and nitroxides can act as efficient scavengers of protein-derived free radicals. Chem. Res. Toxicol. 2008, 21:2111-2119.
8. Pattison D.I., Lam M., Shinde S.S., et al. The nitroxide TEMPO is an efficient scavenger of protein radicals: cellular and kinetic studies. Free Radic. Biol. Med. 2012, 53:1664-1674.
9. Krishna C.M., Samuni A., Taira J., et al. Stimulation by nitroxides of catalase-like activity of heme proteins; kinetics and mechanism. J.Biol. Chem. 1996, 271:26018-26025.
10. Vaz S.M., Augusto O. Inhibition of myeloperoxidase-mediated protein nitration by tempol: kinetics, mechanism, and implications. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:8191-8196.
11. Rees M.D., Bottle S.E., Fairfull-Smith K.E., et al. Inhibition of myeloperoxidase-mediated hypochlorous acid production by nitroxides. Biochem. J. 2009, 421:79-86.
12. Queiroz R.F., Vaz S.M., Augusto O. Inhibition of the chlorinating activity of myeloperoxidase by tempol: revisiting the kinetics and mechanisms. Biochem. J. 2011, 439:423-431.
13. Li F., Jiang C., Krausz K.W., et al. Microbiome remodelling leads to inhibition of intestinal farnesoid X receptor signalling and decreased obesity. Nat. Commun. 2013, 4:1-10.
14. Frances D.E., Ronco M.T., Ingaramo P.I., et al. Role of reactive oxygen species in the early stages of liver regeneration in streptozotocin-induced diabetic rats. Free Radic. Res. 2011, 45:1143-1153.
15. Wilcox C.S., Pearlman A. Chemistry and antihypertensive effects of Tempol and other nitroxides. Pharmacol. Rev. 2008, 60:418-469.
16. Patel K., Chen Y.F., Dennehy K., et al. Acute antihypertensive action of nitroxides in the spontaneously hypertensive rat. Am. J. Physiol. 2006, 290:R37-R43.
17. Cannizzo B., Quesada I., Militello R., et al. Tempol attenuates atherosclerosis associated with metabolic syndrome via decreased vascular inflammation and NADPH-2 oxidase expression. Free Radic. Res. 2014, 48:684-693.
18. Brown B.E., Kim C.H., Torpy F.R., et al. Supplementation with carnosine decreases plasma triglycerides and modulates atherosclerotic plaque composition in diabetic apo E(-/-) mice. Atherosclerosis 2014, 232:403-409.
19. Bursill C.A., Choudhury R.P., Ali Z., et al. Broad-spectrum CC-chemokine blockade by gene transfer inhibits macrophage recruitment and atherosclerotic plaque formation in apolipoprotein E-knockout mice. Circulation 2004, 110:2460-2466.
20. Allen J.K., Hensley W.J., Nicholls A.V., et al. An enzymic and centrifugal method for estimating high-density lipoprotein cholesterol. Clin. Chem. 1979, 25:325-327.
21. Di Bartolo B.A., Vanags L.Z., Tan J.T., et al. The apolipoprotein A-I mimetic peptide, ETC-642, reduces chronic vascular inflammation in the rabbit. Lipids Health Dis. 2011, 10:224.
22. Ankel E.G., Lai C.S., Hopwood L.E., et al. Cytotoxicity of commonly used nitroxide radical spin probes. Life Sci. 1987, 40:495-498.
23. Mitchell J.B., Anver M.R., Sowers A.L., et al. The antioxidant Tempol reduces carcinogenesis and enhances survival in mice when administered after nonlethal total body radiation. Cancer Res. 2012, 72:4846-4855.
24. Finn A.V., Nakano M., Narula J., et al. Concept of vulnerable/unstable plaque. Arterioscler. Thromb. Vasc. Biol. 2010, 30:1282-1292.
25. Dandona P., Aljada A., Chaudhuri A., et al. Metabolic syndrome - a comprehensive perspective based on interactions between obesity, diabetes, and inflammation. Circulation 2005, 111:1448-1454.
26. Hotamisligil G.S., Shargill N.S., Spiegelman B.M. Adipose expression of tumor-necrosis-factor-alpha - direct role in obesity-linked insulin resistance. Science 1993, 259:87-91.
27. Knight S.F., Yuan J.H., Roy S., et al. Simvastatin and tempol protect against endothelial dysfunction and renal injury in a model of obesity and hypertension. Am. J. Physiol. 2010, 298:F86-F94.
28. Virdis A., Santini F., Colucci R., et al. Vascular generation of tumor necrosis factor-alpha reduces nitric oxide availability in small arteries from visceral fat of obese patients. J.Am. Coll. Cardiol. 2011, 58:238-247.
29. Queiroz R.F., Jordao A.K., Cunha A.C., et al. Nitroxides attenuate carrageenan-induced inflammation in rat paws by reducing neutrophil infiltration and the resulting myeloperoxidase-mediated damage. Free Radic. Biol. Med. 2012, 53:1942-1953.
30. Baetta R., Corsini A. Role of polymorphonuclear neutrophils in atherosclerosis: current state and future perspectives. Atherosclerosis 2010, 210:1-13.
31. van Leeuwen M., Gijbels M.J., Duijvestijn A., et al. Accumulation of myeloperoxidase-positive neutrophils in atherosclerotic lesions in LDLR-/- mice. Arterioscler. Thromb. Vasc. Biol. 2008, 28:84-89.
32. Daugherty A., Dunn J.L., Rateri D.L., et al. Myeloperoxidase, a catalyst for lipoprotein oxidation, is expressed in human atherosclerotic lesions. J.Clin. Invest. 1994, 94:437-444.
33. Sugiyama S., Okada Y., Sukhova G.K., et al. Macrophage myeloperoxidase regulation by granulocyte macrophage colony- stimulating factor in human atherosclerosis and implications in acute coronary syndromes. Am. J. Pathol. 2001, 158:879-891.
34. Tang W.H., Wu Y., Nicholls S.J., et al. Plasma myeloperoxidase predicts incident cardiovascular risks in stable patients undergoing medical management for coronary artery disease. Clin. Chem. 2011, 57:33-39.
35. Nicholls S.J., Hazen S.L. Myeloperoxidase and cardiovascular disease. Arterioscler. Thromb. Vasc. Biol. 2005, 25:1102-1111.
36. Kajer T.B., Fairfull-Smith K.E., Y T., et al. Inhibition of myeloperoxidase- and neutrophil-mediated oxidant production by tetraethyl- and tetramethyl-nitroxides. Free Radic. Biol. Med. 2014, 70:96-105.
37. Small D.M., Shipley G.G. Physical-chemical basis of lipid deposition in atherosclerosis. Science 1974, 185:222-229.
38. Libby P. Inflammation in atherosclerosis. Nature 2002, 420:868-874.
39. Menini S., Iacobini C., Ricci C., et al. D-carnosine octylester attenuates atherosclerosis and renal disease in ApoE null mice fed a western diet through reduction of carbonyl stress and inflammation. Br. J. Pharmacol. 2012, 166:1344-1356.
40. Ebenezer P.J., Mariappan N., Elks C.M., et al. Diet-induced renal changes in Zucker rats are ameliorated by the superoxide dismutase mimetic TEMPOL. Obesity 2009, 17:1994-2002.
41. Asghar M., Lokhandwala M.F. Antioxidant Tempol lowers age-related increases in insulin resistance in Fischer 344 rats. Clin. Exp. Hypertens. 2006, 28:533-541.
42. Jernas M., Palming J., Sjoholm K., et al. Separation of human adipocytes by size: hypertrophic fat cells display distinct gene expression. Faseb J. 2006, 20:1540-1542.
43. Kumon Y., Suehiro T., Hashimoto K., et al. Local expression of acute phase serum amyloid A mRNA in rheumatoid arthritis synovial tissue and cells. J.Rheumatol. 1999, 26:785-790.
44. Poitou C., Viguerie N., Cancello R., et al. Serum amyloid A: production by human white adipocyte and regulation by obesity and nutrition. Diabetologia 2005, 48:519-528.
45. Meek R.L., Urielishoval S., Benditt E.P. Expression of apolipoprotein serum amyloid-a messenger-rna in human atherosclerotic lesions and cultured vascular cells - implications for serum amyloid-A function. Proc. Natl. Acad. Sci. U. S. A. 1994, 91:3186-3190.
46. Hattori Y., Akimoto K., Gross S.S., et al. Angiotensin-II-induced oxidative stress elicits hypoadiponectinaemia rats. Diabetologia 2005, 48:1066-1074.
47. Villarreal-Molina M.T., Antuna-Puente B. Adiponectin: anti-inflammatory and cardioprotective effects. Biochimie 2012, 94:2143-2149.
48. Al-Daghri N.M., Al-Attas O.S., Alokail M.S., et al. Visceral adiposity index is highly associated with adiponectin values and glycaemic disturbances. Eur. J. Clin. Invest. 2013, 43:183-189.
49. Enos R.T., Davis J.M., Velazquez K.T., et al. Influence of dietary saturated fat content on adiposity, macrophage behavior, inflammation, and metabolism: composition matters. J.Lipid Res. 2013, 54:152-163.
50. Samuni Y., Cook J.A., Choudhuri R., et al. Inhibition of adipogenesis by Tempol in 3T3-L1 cells. Free Radic. Biol. Med. 2010, 49:667-673.