Impact of the carotenoid astaxanthin on phagocytic capacity and ROS/RNS production of human neutrophils treated with free fatty acids and high glucose

International Immunopharmacology

Volumn 11, Issue 12, 2011, Pages 2220-2226

  Guerra, Beatriz Alves ^a   Otton, Rosemari ^a  

^a UNIVERSIDADE CRUZEIRO DO SUL   (Brazil)

Author keywords

Astaxanthin; Free radicals; Hyperglycemia; Hyperlipidemia; Leukocytes; Oxidative stress

Indexed keywords

ASTAXANTHIN; FATTY ACID; GLUCOSE; GLUCOSE 6 PHOSPHATE DEHYDROGENASE; HYDROGEN PEROXIDE; LUCIGENIN; NITRIC OXIDE; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; SUPEROXIDE; ZYMOSAN;

ADULT; ARTICLE; CELL FUNCTION; ENZYME ACTIVITY; FEMALE; HUMAN; HUMAN CELL; MALE; METABOLITE; NEUTROPHIL; NORMAL HUMAN; PARAMETER; PHAGOCYTOSIS; PRIORITY JOURNAL;

ADULT; FATTY ACIDS, NONESTERIFIED; FEMALE; GLUCOSE; GLUCOSEPHOSPHATE DEHYDROGENASE; HUMANS; MALE; NEUTROPHILS; PHAGOCYTOSIS; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN SPECIES; XANTHOPHYLLS; YOUNG ADULT;

EID: 81855176007     PISSN: 15675769     EISSN: 18781705     Source Type: Journal    
DOI: 10.1016/j.intimp.2011.10.004     Document Type: Article

References (68)

1. J.V. Hunt, R.T. Dean, and S.P. Wolff Hydroxyl radical production and autoxidative glycosylation. Glucose autoxidation as the cause of protein damage in the experimental glycation model of diabetes mellitus and ageing Biochem J 256 1988 205 212
2. P.J. Thornalley, and N.J. Dodd Free radical production from normal and adriamycin-treated rat cardiac sarcosomes Biochem Pharmacol 34 1985 669 674 (Pubitemid 15110183)
3. S. Pennathur, and J.W. Heinecke Mechanisms of oxidative stress in diabetes: implications for the pathogenesis of vascular disease and antioxidant therapy Front Biosci 9 2004 565 574 (Pubitemid 39043735)
4. M. Brownlee The pathobiology of diabetic complications: a unifying mechanism Diabetes 54 2005 1615 1625 (Pubitemid 40770750)
5. E.P. Haber, J. Procopio, C.R. Carvalho, A.R. Carpinelli, P. Newsholme, and R. Curi New insights into fatty acid modulation of pancreatic beta-cell function Int Rev Cytol 248 2006 1 41 (Pubitemid 43238169)
6. P. Newsholme, E.P. Haber, S.M. Hirabara, E.L. Rebelato, J. Procopio, and D. Morgan Diabetes associated cell stress and dysfunction: role of mitochondrial and non-mitochondrial ROS production and activity J Physiol 583 2007 9 24 (Pubitemid 47244241)
7. M. Lodovici, S. Caldini, L. Morbidelli, V. Akpan, M. Ziche, and P. Dolara Protective effect of 4-coumaric acid from UVB ray damage in the rabbit eye Toxicology 255 2009 1 5
8. B. Tesfamariam, and R.A. Cohen Free radicals mediate endothelial cell dysfunction caused by elevated glucose Am J Physiol 263 1992 H321 H326
9. S.K. Jain, R. McVie, R. Jackson, S.N. Levine, and G. Lim Effect of hyperketonemia on plasma lipid peroxidation levels in diabetic patients Diabetes Care 22 1999 1171 1175 (Pubitemid 29293972)
10. S.E. Kahn The relative contributions of insulin resistance and beta-cell dysfunction to the pathophysiology of Type 2 diabetes Diabetologia 46 2003 3 19 (Pubitemid 36237741)
11. Y. Kajimoto, and H. Kaneto Role of oxidative stress in pancreatic beta-cell dysfunction Ann N Y Acad Sci 1011 2004 168 176 (Pubitemid 38608402)
12. W. Droge Free radicals in the physiological control of cell function Physiol Rev 82 2002 47 95 (Pubitemid 34654215)
13. J.F. Turrens Mitochondrial formation of reactive oxygen species J Physiol 552 2003 335 344 (Pubitemid 37321833)
14. L.E. Fridlyand, and L.H. Philipson Oxidative reactive species in cell injury: mechanisms in diabetes mellitus and therapeutic approaches Ann N Y Acad Sci 1066 2005 136 151
15. L. Fialkow, Y. Wang, and G.P. Downey Reactive oxygen and nitrogen species as signaling molecules regulating neutrophil function Free Radic Biol Med 42 2007 153 164 (Pubitemid 46001554)
16. F.R. Sheppard, M.R. Kelher, E.E. Moore, N.J. McLaughlin, A. Banerjee, and C.C. Silliman Structural organization of the neutrophil NADPH oxidase: phosphorylation and translocation during priming and activation J Leukoc Biol 78 2005 1025 1042 (Pubitemid 41572466)
17. H. Ishii, M.R. Jirousek, D. Koya, C. Takagi, P. Xia, and A. Clermont Amelioration of vascular dysfunctions in diabetic rats by an oral PKC beta inhibitor Science 272 1996 728 731 (Pubitemid 26000279)
18. G.L. King, H. Ishii, and D. Koya Diabetic vascular dysfunctions: a model of excessive activation of protein kinase C Kidney Int Suppl 60 1997 S77 S85
19. C.R. Cavaglieri, A. Nishiyama, L.C. Fernandes, R. Curi, E.A. Miles, and P.C. Calder Differential effects of short-chain fatty acids on proliferation and production of pro- and anti-inflammatory cytokines by cultured lymphocytes Life Sci 73 2003 1683 1690 (Pubitemid 36859872)
20. P.C. Calder The relationship between the fatty acid composition of immune cells and their function Prostaglandins Leukot Essent Fatty Acids 79 2008 101 108
21. B. Halliwell Reactive oxygen species in living systems: source, biochemistry, and role in human disease Am J Med 91 1991 14S 22S
22. J.P. Yuan, J. Peng, K. Yin, and J.H. Wang Potential health-promoting effects of astaxanthin: a high-value carotenoid mostly from microalgae Mol Nutr Food Res 55 2011 150 165
23. R.T. Lorenz, and G.R. Cysewski Commercial potential for Haematococcus microalgae as a natural source of astaxanthin Trends Biotechnol 18 2000 160 167 (Pubitemid 30171334)
24. E.A. Johnson, and G.H. An Astaxanthin from microbial sources Crit Rev Biotechnol 11 1991 297 326
25. G. Hussein, U. Sankawa, H. Goto, K. Matsumoto, and H. Watanabe Astaxanthin, a carotenoid with potential in human health and nutrition J Nat Prod 69 2006 443 449
26. A. Ranga Rao, R.L. Raghunath Reddy, V. Baskaran, R. Sarada, and G.A. Ravishankar Characterization of microalgal carotenoids by mass spectrometry and their bioavailability and antioxidant properties elucidated in rat model J Agric Food Chem 58 2010 8553 8559
27. W. Miki Biological functions and activities of animal carotenoids Pure Appl Chem 63 1991 141 146
28. P. Palozza, and N.I. Krinsky Astaxanthin and canthaxanthin are potent antioxidants in a membrane model Arch Biochem Biophys 297 1992 291 295 (Pubitemid 23282883)
29. A.P. Bolin, R.C. Macedo, D.P. Marin, M.P. Barros, and R. Otton Astaxanthin prevents in vitro auto-oxidative injury in human lymphocytes Cell Biol Toxicol 26 2010 457 467
30. R.C. Macedo, A.P. Bolin, D.P. Marin, and R. Otton Astaxanthin addition improves human neutrophils function: in vitro study Eur J Nutr 49 2010 447 457
31. F.J. Pashkow, D.G. Watumull, and C.L. Campbell Astaxanthin: a novel potential treatment for oxidative stress and inflammation in cardiovascular disease Am J Cardiol 101 2008 58D 68D
32. R. Otton, and R. Curi Toxicity of a mixture of fatty acids on human blood lymphocytes and leukaemia cell lines Toxicol In Vitro 19 2005 749 755 (Pubitemid 40828770)
33. T.R. Campoio, F.A. Oliveira, and R. Otton Oxidative stress in human lymphocytes treated with fatty acid mixture: role of carotenoid astaxanthin Toxicol In Vitro 25 7 2011 1448 1456
34. G.A. Spiller, and A. Dewell Safety of an astaxanthin-rich Haematococcus pluvialis algal extract: a randomized clinical trial J Med Food 6 2003 51 56 (Pubitemid 36576614)
35. E. Pick, and D. Mizel Rapid microassays for the measurement of superoxide and hydrogen peroxide production by macrophages in culture using an automatic enzyme immunoassay reader J Immunol Methods 46 1981 211 226 (Pubitemid 11020859)
36. A.H. Ding, C.F. Nathan, and D.J. Stuehr Release of reactive nitrogen intermediates and reactive oxygen intermediates from mouse peritoneal macrophages. Comparison of activating cytokines and evidence for independent production J Immunol 141 1988 2407 2412
37. L.F. Costa Rosa, R. Curi, C. Murphy, and P. Newsholme Effect of adrenaline and phorbol myristate acetate or bacterial lipopolysaccharide on stimulation of pathways of macrophage glucose, glutamine and O2 metabolism. Evidence for cyclic AMP-dependent protein kinase mediated inhibition of glucose-6-phosphate dehydrogenase and activation of NADP+-dependent 'malic' enzyme Biochem J 310 Pt 2 1995 709 714
38. H.U. Bergmeyer, E. Bernt, F. Schmidt, and H. Stork d-glucose determination with hexokinase and glucose-6-phosphate dehydrogenase H.U. Bergmeyer, Methods of enzymatic analysis 1974 Academic New York 1196 1201
39. M.M. Bradford A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Anal Biochem 72 1976 248 254
40. C.J. Mullarkey, D. Edelstein, and M. Brownlee Free radical generation by early glycation products: a mechanism for accelerated atherogenesis in diabetes Biochem Biophys Res Commun 173 1990 932 939
41. J.W. Baynes Role of oxidative stress in development of complications in diabetes Diabetes 40 1991 405 412
42. J.L. Evans, I.D. Goldfine, B.A. Maddux, and G.M. Grodsky Are oxidative stress-activated signaling pathways mediators of insulin resistance and beta-cell dysfunction? Diabetes 52 2003 1 8 (Pubitemid 36042100)
43. K.P. Bouter, F.H. Meyling, J.B. Hoekstra, N. Masurel, D.W. Erkelens, and R.J. Diepersloot Influence of blood glucose levels on peripheral lymphocytes in patients with diabetes mellitus Diabetes Res 19 1992 77 80
44. C.P. Nielson, and D.A. Hindson Inhibition of polymorphonuclear leukocyte respiratory burst by elevated glucose concentrations in vitro Diabetes 38 1989 1031 1035 (Pubitemid 20015054)
45. J.D. Bagdade, K.L. Nielson, and R.J. Bulger Reversible abnormalities in phagocytic function in poorly controlled diabetic patients Am J Med Sci 263 1972 451 456
46. J. Jakelic, S. Kokic, I. Hozo, J. Maras, and D. Fabijanic Nonspecific immunity in diabetes: hyperglycemia decreases phagocytic activity of leukocytes in diabetic patients Med Arh 49 1995 9 12
47. P. Schonfeld, and L. Wojtczak Fatty acids as modulators of the cellular production of reactive oxygen species Free Radic Biol Med 45 2008 231 241
48. J.T. Curnutte, J.A. Badwey, J.M. Robinson, M.J. Karnovsky, and M.L. Karnovsky Studies on the mechanism of superoxide release from human neutrophils stimulated with arachidonate J Biol Chem 259 1984 11851 11857 (Pubitemid 14022110)
49. M.A. Myers, L.C. McPhail, and R. Snyderman Redistribution of protein kinase C activity in human monocytes: correlation with activation of the respiratory burst J Immunol 135 1985 3411 3416 (Pubitemid 16250609)
50. S.J. Corley, and P.M. Rosoff Unsaturated fatty acids and lipoxygenase products regulate phagocytic NADPH oxidase activity by a nondetergent mechanism J Lab Clin Med 118 1991 343 351
51. S.J. Hardy, A. Ferrante, A. Poulos, B.S. Robinson, D.W. Johnson, and A.W. Murray Effect of exogenous fatty acids with greater than 22 carbon atoms (very long chain fatty acids) on superoxide production by human neutrophils J Immunol 153 1994 1754 1761 (Pubitemid 24251120)
52. K. Kakinuma, and S. Minakami Effects of fatty acids on superoxide radical generation in leukocytes Biochim Biophys Acta 538 1978 50 59 (Pubitemid 8235925)
53. T. Inoguchi, P. Li, F. Umeda, H.Y. Yu, M. Kakimoto, and M. Imamura High glucose level and free fatty acid stimulate reactive oxygen species production through protein kinase C-dependent activation of NAD(P)H oxidase in cultured vascular cells Diabetes 49 2000 1939 1945
54. M. Karima, A. Kantarci, T. Ohira, H. Hasturk, V.L. Jones, and B.H. Nam Enhanced superoxide release and elevated protein kinase C activity in neutrophils from diabetic patients: association with periodontitis J Leukoc Biol 78 2005 862 870 (Pubitemid 41384402)
55. R. Gyurko, C.C. Siqueira, N. Caldon, L. Gao, A. Kantarci, and T.E. Van Dyke Chronic hyperglycemia predisposes to exaggerated inflammatory response and leukocyte dysfunction in Akita mice J Immunol 177 2006 7250 7256 (Pubitemid 44715094)
56. 2-generation by mononuclear phagocytes in diabetes J Leukoc Biol 81 2007 520 527 (Pubitemid 46198404)
57. K. Omori, T. Ohira, Y. Uchida, S. Ayilavarapu, E.L. Batista Jr., and M. Yagi Priming of neutrophil oxidative burst in diabetes requires preassembly of the NADPH oxidase J Leukoc Biol 84 2008 292 301 (Pubitemid 351960304)
58. N.D. Burg, and M.H. Pillinger The neutrophil: function and regulation in innate and humoral immunity Clin Immunol 99 2001 7 17
59. B. Halliwell, and J.M. Gutteridge Free radicals in medicine and biology 2nd ed. 1999 Clarendon Press Oxford
60. A.D. McCarthy, S.B. Etcheverry, and A.M. Cortizo Effect of advanced glycation endproducts on the secretion of insulin-like growth factor-I and its binding proteins: role in osteoblast development Acta Diabetol 38 2001 113 122 (Pubitemid 34042074)
61. J.W. Baynes, and S.R. Thorpe Role of oxidative stress in diabetic complications: a new perspective on an old paradigm Diabetes 48 1999 1 9 (Pubitemid 29019345)
62. J.L. Wautier, M.P. Wautier, A.M. Schmidt, G.M. Anderson, O. Hori, and C. Zoukourian Advanced glycation end products (AGEs) on the surface of diabetic erythrocytes bind to the vessel wall via a specific receptor inducing oxidant stress in the vasculature: a link between surface-associated AGEs and diabetic complications Proc Natl Acad Sci U S A 91 1994 7742 7746
63. H. Vlassara, W. Cai, J. Crandall, T. Goldberg, R. Oberstein, and V. Dardaine Inflammatory mediators are induced by dietary glycotoxins, a major risk factor for diabetic angiopathy Proc Natl Acad Sci U S A 99 2002 15596 15601 (Pubitemid 35403978)
64. A.K. Mohamed, A. Bierhaus, S. Schiekofer, H. Tritschler, R. Ziegler, and P.P. Nawroth The role of oxidative stress and NF-kappaB activation in late diabetic complications Biofactors 10 1999 157 167 (Pubitemid 29533824)
65. C. Nacci, M. Tarquinio, and M. Montagnani Molecular and clinical aspects of endothelial dysfunction in diabetes Intern Emerg Med 4 2009 107 116
66. A.C. Maritim, R.A. Sanders, and J.B. Watkins III Diabetes, oxidative stress, and antioxidants: a review J Biochem Mol Toxicol 17 2003 24 38 (Pubitemid 36410972)
67. S.J. Kim, Z. Zhang, A. Saha, C. Sarkar, Z. Zhao, Y. Xu, and A.B. Mukherjee Omega-3 and omega-6 fatty acids suppress ER- and oxidative stress in cultured neurons and neuronal progenitor cells from mice lacking PPT1 Neurosci Lett 479 2010 292 296
68. M. Valko, C.J. Rhodes, J. Moncol, M. Izakovic, and M. Mazur Free radicals, metals and antioxidants in oxidative stress-induced cancer Chem Biol Interact 160 2006 1 40 (Pubitemid 43227479)