nach oben

European Journal of Nutrition

Erschienen in:

01.04.2014 | Original Contribution

Fucoxanthin in association with Vitamin c acts as modulators of human neutrophil function

verfasst von: A. C. Morandi, N. Molina, B. A. Guerra, A. P. Bolin, R. Otton

Erschienen in: European Journal of Nutrition | Ausgabe 3/2014

Einloggen, um Zugang zu erhalten

Abstract

Introduction

Neutrophils provide the first line of defense of the innate immune system by phagocytosing, killing and digesting bacteria and fungi. During this process, neutrophils produce reactive oxygen species (ROS), which in excess, can damage the cells themselves and surrounding tissues. The carotenoid fucoxanthin (Fc) has been studied concerning its antioxidant and anti-inflammatory actions. Vitamin c (Vc) also demonstrates potent antioxidant action. This study aimed to evaluate the effect of Fc (2 μM) in association with Vc (100 μM) on functional parameters of human neutrophils in vitro.

Materials and methods

We evaluated the migration and phagocytic capacity, intracellular calcium mobilization, ROS production (O ₂ ^·− , H₂O₂, HOCl), myeloperoxidase activity, profile of antioxidant enzymes, phosphorylation of p38 MAPK and p65 NFκB subunit, GSH/GSSG ratio and release of pro-inflammatory cytokines (TNF-α and IL-6) in neutrophils under different stimuli.

Results

We verified an increase in phagocytic capacity for all treatments, together with an increase in intracellular calcium only in cells treated with Fc and Fc + Vc. ROS production was reduced by all treatments, although Vc was a better antioxidant than Fc. Phosphorylation of the p-65 subunit of NFκB was reduced in cells treated with Fc + Vc and release of TNF-α and IL-6 was reduced by all treatments. These findings indicate that the regulation of inflammatory cytokines by neutrophils is not exclusively under the control of the NFκB pathway. Fc reduced the activity of some antioxidant enzymes, whereas Vc increased GR activity and the GSH/GSSG ratio.

Conclusion

In conclusion, the results presented in this study clearly show an immunomodulatory effect of the carotenoid fc alone or in combination with Vc on the function of human neutrophils.

Nathan C (2006) Neutrophils and immunity: challenges and opportunities. Nat Rev Immunol 6(3):173–182. doi:10.1038/nri1785 CrossRef

Mayer-Scholl A, Averhoff P, Zychlinsky A (2004) How do neutrophils and pathogens interact? Curr Opin Microbiol 7(1):62–66. doi:10.1016/j.mib.2003.12.004 CrossRef

Babior BM (1999) NADPH oxidase: an update. Blood 93(5):1464–1476

Chapman AL, Hampton MB, Senthilmohan R, Winterbourn CC, Kettle AJ (2002) Chlorination of bacterial and neutrophil proteins during phagocytosis and killing of Staphylococcus aureus. J Biol Chem 277(12):9757–9762. doi:10.1074/jbc.M106134200 CrossRef

Halliwell B (2001) Role of free radicals in the neurodegenerative diseases: therapeutic implications for antioxidant treatment. Drugs Aging 18(9):685–716CrossRef

Jakus Z, Simon E, Frommhold D, Sperandio M, Mocsai A (2009) Critical role of phospholipase Cgamma2 in integrin and Fc receptor-mediated neutrophil functions and the effector phase of autoimmune arthritis. J Exp Med 206(3):577–593. doi:10.1084/jem.20081859 CrossRef

Jones DP (2006) Redefining oxidative stress. Antioxid Redox Signal 8(9–10):1865–1879. doi:10.1089/ars.2006.8.1865 CrossRef

Biasi D, Carletto A, Caramaschi P, Bonella F, Bambara V, Pacor ML, Bambara LM (2003) Neutrophils in rheumatoid inflammation. Recenti Prog Med 94(1):25–30

Henson PM (2005) Dampening inflammation. Nat Immunol 6(12):1179–1181. doi:10.1038/ni1205-1179 CrossRef

10.

Serhan CN, Savill J (2005) Resolution of inflammation: the beginning programs the end. Nat Immunol 6(12):1191–1197. doi:10.1038/ni1276 CrossRef

11.

Ames BN, Shigenaga MK, Hagen TM (1993) Oxidants, antioxidants, and the degenerative diseases of aging. Proc Natl Acad Sci USA 90(17):7915–7922CrossRef

12.

Fitch PM, Roghanian A, Howie SE, Sallenave JM (2006) Human neutrophil elastase inhibitors in innate and adaptive immunity. Biochem Soc Trans 34(Pt 2):279–282. doi:10.1042/BST20060279

13.

Duarte TL, Lunec J (2005) Review: when is an antioxidant not an antioxidant? A review of novel actions and reactions of vitamin C. Free Radic Res 39(7):671–686. doi:10.1080/10715760500104025 CrossRef

14.

Sachindra NM, Sato E, Maeda H, Hosokawa M, Niwano Y, Kohno M, Miyashita K (2007) Radical scavenging and singlet oxygen quenching activity of marine carotenoid fucoxanthin and its metabolites. J Agric Food Chem 55(21):8516–8522. doi:10.1021/jf071848a CrossRef

15.

Urikura I, Sugawara T, Hirata T (2011) Protective effect of Fucoxanthin against UVB-induced skin photoaging in hairless mice. Biosci Biotechnol Biochem 75(4):757–760CrossRef

16.

Liu CL, Liang AL, Hu ML (2011) Protective effects of fucoxanthin against ferric nitrilotriacetate-induced oxidative stress in murine hepatic BNL CL.2 cells. Toxicol In Vitro 25(7):1314–1319. doi:10.1016/j.tiv.2011.04.023 CrossRef

17.

Hu T, Liu D, Chen Y, Wu J, Wang S (2010) Antioxidant activity of sulfated polysaccharide fractions extracted from Undaria pinnitafida in vitro. Int J Biol Macromol 46(2):193–198. doi:10.1016/j.ijbiomac.2009.12.004 CrossRef

18.

Riccioni G, D’Orazio N, Franceschelli S, Speranza L (2011) Marine carotenoids and cardiovascular risk markers. Mar Drugs 9(7):1166–1175. doi:10.3390/md9071166 CrossRef

19.

Guerra BA, Bolin AP, Morandi AC, Otton R (2012) Glycolaldehyde impairs neutrophil biochemical parameters by an oxidative and calcium-dependent mechanism–protective role of antioxidants astaxanthin and vitamin C. Diabetes Res Clin Pract 98(1):108–118. doi:10.1016/j.diabres.2012.07.004 CrossRef

20.

Hatanaka E, Monteagudo PT, Marrocos MS, Campa A (2007) Interaction between serum amyloid A and leukocytes—a possible role in the progression of vascular complications in diabetes. Immunol Lett 108(2):160–166. doi:10.1016/j.imlet.2006.12.005 CrossRef

21.

Sampaio SC, Sousa-e-Silva MC, Borelli P, Curi R, Cury Y (2001) Crotalus durissus terrificus snake venom regulates macrophage metabolism and function. J Leukoc Biol 70(4):551–558

22.

Hatanaka E, Levada-Pires AC, Pithon-Curi TC, Curi R (2006) Systematic study on ROS production induced by oleic, linoleic, and gamma-linolenic acids in human and rat neutrophils. Free Radic Biol Med 41(7):1124–1132. doi:10.1016/j.freeradbiomed.2006.06.014 CrossRef

23.

Dypbukt JM, Bishop C, Brooks WM, Thong B, Eriksson H, Kettle AJ (2005) A sensitive and selective assay for chloramine production by myeloperoxidase. Free Radic Biol Med 39(11):1468–1477. doi:10.1016/j.freeradbiomed.2005.07.008 CrossRef

24.

Grynkiewicz G, Poenie M, Tsien RY (1985) A new generation of Ca2 + indicators with greatly improved fluorescence properties. J Biol Chem 260(6):3440–3450

25.

Pick E, Mizel D (1981) 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(2):211–226CrossRef

26.

Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126CrossRef

27.

Ewing JF, Janero DR (1995) Microplate superoxide dismutase assay employing a nonenzymatic superoxide generator. Anal Biochem 232(2):243–248. doi:10.1006/abio.1995.0014 CrossRef

28.

Mannervik B (1985) Glutathione peroxidase. Methods Enzymol 113:490–495CrossRef

29.

Carlberg I, Mannervik B (1985) Glutathione reductase. Methods Enzymol 113:484–490CrossRef

30.

Rahman I, Kode A, Biswas SK (2006) Assay for quantitative determination of glutathione and glutathione disulfide levels using enzymatic recycling method. Nat Protoc 1(6):3159–3165. doi:10.1038/nprot.2006.378 CrossRef

31.

Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254CrossRef

32.

Bokoch GM (1995) Chemoattractant signaling and leukocyte activation. Blood 86(5):1649–1660

33.

Underhill DM, Ozinsky A (2002) Phagocytosis of microbes: complexity in action. Annu Rev Immunol 20:825–852. doi:103001.114744 CrossRef

34.

Macedo RC, Bolin AP, Marin DP, Otton R (2010) Astaxanthin addition improves human neutrophils function: in vitro study. Eur J Nutr 49(8):447–457. doi:10.1007/s00394-010-0103-1 CrossRef

35.

Guerra BA, Otton R (2011) Impact of the carotenoid astaxanthin on phagocytic capacity and ROS/RNS production of human neutrophils treated with free fatty acids and high glucose. Int Immunopharmacol 11(12):2220–2226. doi:10.1016/j.intimp.2011.10.004 CrossRef

36.

Fassett RG, Coombes JS (2009) Astaxanthin, oxidative stress, inflammation and cardiovascular disease. Future Cardiol 5(4):333–342. doi:10.2217/fca.09.19 CrossRef

37.

Babior BM (2000) Phagocytes and oxidative stress. Am J Med 109(1):33–44CrossRef

38.

Kettle AJ, Gedye CA, Winterbourn CC (1993) Superoxide is an antagonist of antiinflammatory drugs that inhibit hypochlorous acid production by myeloperoxidase. Biochem Pharmacol 45(10):2003–2010CrossRef

39.

Guilpain P, Servettaz A, Batteux F, Guillevin L, Mouthon L (2008) Natural and disease associated anti-myeloperoxidase (MPO) autoantibodies. Autoimmun Rev 7(6):421–425. doi:10.1016/j.autrev.2008.03.009 CrossRef

40.

Pullar JM, Vissers MC, Winterbourn CC (2000) Living with a killer: the effects of hypochlorous acid on mammalian cells. IUBMB Life 50(4–5):259–266. doi:10.1080/713803731 CrossRef

41.

Malech HL, Gallin JI (1987) Current concepts: immunology. Neutrophils in human diseases. N Engl J Med 317(11):687–694. doi:10.1056/NEJM198709103171107 CrossRef

42.

Shao B, Oda MN, Bergt C, Fu X, Green PS, Brot N, Oram JF, Heinecke JW (2006) Myeloperoxidase impairs ABCA1-dependent cholesterol efflux through methionine oxidation and site-specific tyrosine chlorination of apolipoprotein A-I. J Biol Chem 281(14):9001–9004. doi:10.1074/jbc.C600011200 CrossRef

43.

Cuddihy SL, Parker A, Harwood DT, Vissers MC, Winterbourn CC (2008) Ascorbate interacts with reduced glutathione to scavenge phenoxyl radicals in HL60 cells. Free Radic Biol Med 44(8):1637–1644. doi:10.1016/j.freeradbiomed.2008.01.021 CrossRef

44.

Hsuanyu Y, Dunford HB (1999) Oxidation of clozapine and ascorbate by myeloperoxidase. Arch Biochem Biophys 368(2):413–420. doi:10.1006/abbi.1999.1328 CrossRef

45.

Marquez LA, Dunford HB, Van Wart H (1990) Kinetic studies on the reaction of compound II of myeloperoxidase with ascorbic acid. Role of ascorbic acid in myeloperoxidase function. J Biol Chem 265(10):5666–5670

46.

Marquez LA, Dunford HB (1990) Reaction of compound III of myeloperoxidase with ascorbic acid. J Biol Chem 265(11):6074–6078

47.

Parker A, Cuddihy SL, Son TG, Vissers MC, Winterbourn CC (2011) Roles of superoxide and myeloperoxidase in ascorbate oxidation in stimulated neutrophils and H2O2-treated HL60 cells. Free Radic Biol Med 51(7):1399–1405. doi:10.1016/j.freeradbiomed.2011.06.029 CrossRef

48.

Niggli V (2003) Signaling to migration in neutrophils: importance of localized pathways. Int J Biochem Cell Biol 35(12):1619–1638CrossRef

49.

Niggli V (2003) Microtubule-disruption-induced and chemotactic-peptide-induced migration of human neutrophils: implications for differential sets of signalling pathways. J Cell Sci 116(Pt 5):813–822CrossRef

50.

Kim KN, Heo SJ, Kang SM, Ahn G, Jeon YJ (2010) Fucoxanthin induces apoptosis in human leukemia HL-60 cells through a ROS-mediated Bcl-xL pathway. Toxicol In Vitro 24(6):1648–1654. doi:10.1016/j.tiv.2010.05.023 CrossRef

51.

Vernooy JH, Kucukaycan M, Jacobs JA, Chavannes NH, Buurman WA, Dentener MA, Wouters EF (2002) Local and systemic inflammation in patients with chronic obstructive pulmonary disease: soluble tumor necrosis factor receptors are increased in sputum. Am J Respir Crit Care Med 166(9):1218–1224CrossRef

52.

Midwinter RG, Cheah FC, Moskovitz J, Vissers MC, Winterbourn CC (2006) IkappaB is a sensitive target for oxidation by cell-permeable chloramines: inhibition of NF-kappaB activity by glycine chloramine through methionine oxidation. Biochem J 396(1):71–78. doi:10.1042/BJ20052026 CrossRef

53.

Kim KN, Heo SJ, Yoon WJ, Kang SM, Ahn G, Yi TH, Jeon YJ (2010) Fucoxanthin inhibits the inflammatory response by suppressing the activation of NF-kappaB and MAPKs in lipopolysaccharide-induced RAW 264.7 macrophages. Eur J Pharmacol 649(1–3):369–375. doi:10.1016/j.ejphar.2010.09.032 CrossRef

54.

Clive DR, Greene JJ (1996) Cooperation of protein disulfide isomerase and redox environment in the regulation of NF-kappaB and AP1 binding to DNA. Cell Biochem Funct 14(1):49–55. doi:10.1002/cbf.638 CrossRef

55.

Krump E, Sanghera JS, Pelech SL, Furuya W, Grinstein S (1997) Chemotactic peptide N-formyl-met-leu-phe activation of p38 mitogen-activated protein kinase (MAPK) and MAPK-activated protein kinase-2 in human neutrophils. J Biol Chem 272(2):937–944CrossRef

56.

Heo SJ, Jeon YJ (2009) Protective effect of fucoxanthin isolated from Sargassum siliquastrum on UV-B induced cell damage. J Photochem Photobiol B 95(2):101–107. doi:10.1016/j.jphotobiol.2008.11.011 CrossRef

57.

D’Orazio N, Gemello E, Gammone MA, de Girolamo M, Ficoneri C, Riccioni G (2012) Fucoxanthin: a treasure from the sea. Mar drugs 10(3):604–616. doi:10.3390/md10030604 CrossRef

58.

Socaciu C, Jessel R, Diehl HA (2000) Carotenoid incorporation into microsomes: yields, stability and membrane dynamics. Spectrochim Acta A Mol Biomol Spectrosc 56(14):2799–2809CrossRef

59.

Landrum JT, Bone RA (2001) Lutein, zeaxanthin, and the macular pigment. Arch Biochem Biophys 385(1):28–40. doi:10.1006/abbi.2000.2171 CrossRef

60.

Gruszecki WI (1023) Sielewiesiuk J (1990) Orientation of xanthophylls in phosphatidylcholine multibilayers. Biochim Biophys Acta 3:405–412

61.

Goto S, Kogure K, Abe K, Kimata Y, Kitahama K, Yamashita E, Terada H (2001) Efficient radical trapping at the surface and inside the phospholipid membrane is responsible for highly potent antiperoxidative activity of the carotenoid astaxanthin. Biochim Biophys Acta 1512(2):251–258CrossRef

62.

Barros MP, Pinto E, Colepicolo P, Pedersen M (2001) Astaxanthin and peridinin inhibit oxidative damage in Fe(2+)-loaded liposomes: scavenging oxyradicals or changing membrane permeability? Biochem Biophys Res Commun 288(1):225–232. doi:10.1006/bbrc.2001.5765 CrossRef

63.

Matsumoto M, Hosokawa M, Matsukawa N, Hagio M, Shinoki A, Nishimukai M, Miyashita K, Yajima T, Hara H (2010) Suppressive effects of the marine carotenoids, fucoxanthin and fucoxanthinol on triglyceride absorption in lymph duct-cannulated rats. Eur J Nutr 49(4):243–249. doi:10.1007/s00394-009-0078-y CrossRef

64.

Hashimoto T, Ozaki Y, Mizuno M, Yoshida M, Nishitani Y, Azuma T, Komoto A, Maoka T, Tanino Y, Kanazawa K (2012) Pharmacokinetics of fucoxanthinol in human plasma after the oral administration of kombu extract. Br J Nutr 107(11):1566–1569. doi:10.1017/S0007114511004879 CrossRef

65.

Asai A, Yonekura L, Nagao A (2008) Low bioavailability of dietary epoxyxanthophylls in humans. Br J Nutr 100(2):273–277. doi:10.1017/S0007114507895468 CrossRef

66.

Bigley R, Wirth M, Layman D, Riddle M, Stankova L (1983) Interaction between glucose and dehydroascorbate transport in human neutrophils and fibroblasts. Diabetes 32(6):545–548CrossRef

67.

Stankova L, Bigley R, Ingermann RL (1991) The effect of cyanide on vitamin C uptake by human polymorphonuclear leukocytes. Gen Pharmacol 22(5):903–905CrossRef

68.

Wang Y, Russo TA, Kwon O, Chanock S, Rumsey SC, Levine M (1997) Ascorbate recycling in human neutrophils: induction by bacteria. Proc Natl Acad Sci USA 94(25):13816–13819CrossRef

69.

Wolf G (1993) Uptake of ascorbic acid by human neutrophils. Nutr Rev 51(11):337–338CrossRef

70.

Gotoh N, Niki E (1992) Rates of interactions of superoxide with vitamin E, vitamin C and related compounds as measured by chemiluminescence. Biochim Biophys Acta 1115(3):201–207CrossRef

71.

Guaiquil VH, Vera JC, Golde DW (2001) Mechanism of vitamin C inhibition of cell death induced by oxidative stress in glutathione-depleted HL-60 cells. J Biol Chem 276(44):40955–40961. doi:10.1074/jbc.M106878200 CrossRef

Titel: Fucoxanthin in association with Vitamin c acts as modulators of human neutrophil function
verfasst von: A. C. Morandi
N. Molina
B. A. Guerra
A. P. Bolin
R. Otton
Publikationsdatum: 01.04.2014
Verlag: Springer Berlin Heidelberg
Erschienen in: European Journal of Nutrition / Ausgabe 3/2014
Print ISSN: 1436-6207
Elektronische ISSN: 1436-6215
DOI: https://doi.org/10.1007/s00394-013-0582-y

Leitlinien kompakt für die Innere Medizin

Mit medbee Pocketcards sicher entscheiden.

^{Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag}

Kostenlos registrieren

Neu im Fachgebiet Innere Medizin

24.04.2024 | DGIM 2024 | Kongressbericht | Nachrichten

Update Innere Medizin

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.

Newsletter bestellen

Springer Medizin

Fucoxanthin in association with Vitamin c acts as modulators of human neutrophil function

Abstract

Introduction

Materials and methods

Results

Conclusion

Leitlinien kompakt für die Innere Medizin

Neu im Fachgebiet Innere Medizin

Metformin rückt in den Hintergrund

Myokarditis nach Infekt – richtig schwierig wird es bei Profisportlern

Thrombophiliescreening – Wenn, dann richtig und nur bei therapeutischer Konsequenz

Bei Senioren mit Prostatakarzinom auf Anämie achten!

Update Innere Medizin

Springer Medizin

Abstract

Introduction

Materials and methods

Results

Conclusion

Bitte loggen Sie sich ein, um Zugang zu diesem Inhalt zu erhalten

Weitere Artikel der Ausgabe 3/2014

Molecular pathology of acute kidney injury in a choline-deficient model and fish oil protective effect

Low dietary calcium and obesity: a comparative study in genetically obese and normal rats during early growth

Effect of dietary fatty acid composition on substrate utilization and body weight maintenance in humans

Dietary conjugated α-linolenic acid did not improve glucose tolerance in a neonatal pig model

Long-term cysteine fortification impacts cysteine/glutathione homeostasis and food intake in ageing rats

Incorporation of conjugated linoleic acid isomers into porcine erythrocytes

Leitlinien kompakt für die Innere Medizin

Neu im Fachgebiet Innere Medizin

Metformin rückt in den Hintergrund

Myokarditis nach Infekt – richtig schwierig wird es bei Profisportlern

Thrombophiliescreening – Wenn, dann richtig und nur bei therapeutischer Konsequenz

Bei Senioren mit Prostatakarzinom auf Anämie achten!

Update Innere Medizin