Advertisement

Analytical and Bioanalytical Chemistry

, Volume 408, Issue 1, pp 265–270 | Cite as

Rapid assessment of singlet oxygen-induced plasma lipid oxidation and its inhibition by antioxidants with diphenyl-1-pyrenylphosphine (DPPP)

  • Mayuko Morita
  • Yuji Naito
  • Toshikazu Yoshikawa
  • Etsuo NikiEmail author
Research Paper

Abstract

Recent studies suggesting the involvement of singlet oxygen in the pathogenesis of multiple diseases have attracted renewed attention to lipid oxidation mediated by singlet oxygen. Although the rate constants for singlet oxygen quenching by antioxidants have been measured extensively, the inhibition of lipid oxidation mediated by singlet oxygen has received relatively less attention, partly because a convenient method for measuring the rate of lipid oxidation is not available. The objective of this study was to develop a convenient method to measure plasma lipid oxidation mediated by singlet oxygen which may be applied to a rapid assessment of the antioxidant capacity to inhibit this oxidation using a conventional microplate reader. Singlet oxygen was produced from naphthalene endoperoxide, and lipid hydroperoxide production was followed by using diphenyl-1-pyrenylphosphine (DPPP). Non-fluorescent DPPP reacts stoichiometrically with lipid hydroperoxides to give highly fluorescent DPPP oxide. It was found that plasma oxidation by singlet oxygen increased the fluorescence intensity of DPPP oxide, which was suppressed by antioxidants. Fucoxanthin suppressed the oxidation more efficiently than β-carotene and α-tocopherol, while ascorbic acid and Trolox were not effective. The present method may be useful for monitoring lipid oxidation and also for rapid screening of the capacity of dietary antioxidants and natural products to inhibit lipid oxidation in a biologically relevant system.

Keywords

Antioxidant Carotenoid Diphenyl-1-pyrenylphosphine Plasma lipid oxidation Singlet oxygen 

Notes

Acknowledgments

The kind gift of α-tocopherol from Tama Biochemical Co. Ltd. is highly acknowledged.

Compliance with ethical standards

The animal experiments and care were approved by the Institutional Animal Care and Use Committee of Kyoto Prefectural University of Medicine, approved on March 31, 2015, as No. M25-163.

Conflict of interest

The authors declare that they have no competing interests.

References

  1. 1.
    Niki E (2009) Lipid peroxidation: physiological levels and dual biological effects. Free Radic Biol Med 47:469–484CrossRefGoogle Scholar
  2. 2.
    Foote CS (1976) Photosensitized oxidation and singlet oxygen: consequences in biological systems. In: Pryor WA (ed) Free radicals in biology, vol. 2. Academic, New York, pp 85–133Google Scholar
  3. 3.
    Ogilby PR (2010) Singlet oxygen: there is indeed something new under the sun. Chem Soc Rev 39:3181–3209CrossRefGoogle Scholar
  4. 4.
    Miyamoto S, Martinez GR, Medeiros MH, Di Mascio P (2014) Singlet molecular oxygen generated by biological hydroperoxides. J Photochem Photobiol B 139:24–33CrossRefGoogle Scholar
  5. 5.
    Korytowski W, Bachowski GJ, Girotti AW (1992) Photoperoxidation of cholesterol in homogeneous solution, isolated membranes, and cells: comparison of the 5 alpha- and 6 beta-hydroperoxides as indicators of singlet oxygen intermediacy. Photochem Photobiol 56:1–8CrossRefGoogle Scholar
  6. 6.
    Wentworth P Jr, Nieva J, Takeuchi C, Galve R, Wentworth AD, Dilley RB, DeLaria GA, Saven A, Babior BM, Janda KD, Eschenmoser A, Lerner RA (2003) Evidence for ozone formation in human atherosclerotic arteries. Science 302:1053–1056CrossRefGoogle Scholar
  7. 7.
    Uemi M, Ronsein GE, Miyamoto S, Medeiros MH, Di Mascio P (2009) Generation of cholesterol carboxyaldehyde by the reaction of singlet molecular oxygen as well as ozone with cholesterol. Chem Res Toxicol 22:875–884CrossRefGoogle Scholar
  8. 8.
    Tomono S, Miyoshi N, Shiokawa H, Iwabuchi T, Aratani Y, Higashi T, Nukaya H, Ohshima H (2011) Formation of cholesterol ozonolysis products in vitro and in vivo through a myeloperoxidase-dependent pathway. J Lipid Res 52:87–97CrossRefGoogle Scholar
  9. 9.
    Zhang Q, Powers ET, Nieva J, Huff ME, Dendle MA, Bieschke J, Glabe CG, Eschenmoser A, Wentworth P, Lerner RA, Kelly JW (2004) Metabolite-initiated protein misfolding may trigger Alzheimer’s disease. Proc Natl Acad Sci U S A 101:4752–4757CrossRefGoogle Scholar
  10. 10.
    Umeno A, Shichiri M, Ishida N, Hashimoto Y, Abe K, Kataoka M, Yoshino K, Hagihara Y, Aki N, Funaki M, Asada Y, Yoshida Y (2013) Singlet oxygen induced products of linoleates, 10- and 12-(Z, E)-hydroxyoctadecadienoic acids (HODE), can be potential biomarkers for early detection of type 2 diabetes. PLoS One 8, e63542CrossRefGoogle Scholar
  11. 11.
    Murotomi K, Umeno A, Yasunaga M, Shichiri M, Ishida N, Abe H, Yoshida Y, Nakajima Y (2015) Switching from singlet-oxygen-mediated oxidation to free-radical-mediated oxidation in the pathogenesis of type 2 diabetes in model mouse. Free Radic Res 49:133–138CrossRefGoogle Scholar
  12. 12.
    Minami Y, Yokoyama K, Bando N, Kawai Y, Terao J (2008) Occurrence of singlet oxygen oxygenation of oleic acid and linoleic acid in the skin of live mice. Free Radic Res 42:197–204CrossRefGoogle Scholar
  13. 13.
    Niki E (2015) Lipid oxidation in the skin. Free Radic Res 49:827–834CrossRefGoogle Scholar
  14. 14.
    Davies MJ, Truscott RJ (2001) Photo-oxidation of proteins and its role in cataractogenesis. J Photochem Photobiol B 63:114–125CrossRefGoogle Scholar
  15. 15.
    Choe E, Min DB (2006) Chemistry and reactions of reactive oxygen species in foods. Crit Rev Food Sci Nutr 46:1–22CrossRefGoogle Scholar
  16. 16.
    Di Mascio P, Murphy ME, Sies H (1991) Antioxidant defense systems: the role of carotenoids, tocopherols, and thiols. Am J Clin Nutr 53:194S–200SGoogle Scholar
  17. 17.
    Ouchi A, Aizawa K, Iwasaki Y, Inakuma T, Terao J, Nagaoka S, Mukai K (2010) Kinetic study of the quenching reaction of singlet oxygen by carotenoids and food extracts in solution. Development of a singlet oxygen absorption capacity (SOAC) assay method. J Agric Food Chem 58:9967–9978CrossRefGoogle Scholar
  18. 18.
    Terao J, Matsushita S (1977) Products formed by photosensitized oxidation of unsaturated fatty acid esters. J Am Oil Chem Soc 54:234–238CrossRefGoogle Scholar
  19. 19.
    Niki E (2010) Assessment of antioxidant capacity in vitro and in vivo. Free Radic Biol Med 49:503–515CrossRefGoogle Scholar
  20. 20.
    Niki E (2014) Role of vitamin E as a lipid-soluble peroxyl radical scavenger: in vitro and in vivo evidence. Free Radic Biol Med 66:3–12CrossRefGoogle Scholar
  21. 21.
    Wagner JR, Motchnik PA, Stocker R, Sies H, Ames BN (1993) The oxidation of blood plasma and low density lipoprotein components by chemically generated singlet oxygen. J Biol Chem 268:18502–18506Google Scholar
  22. 22.
    Ojima F, Sakamoto H, Ishiguro Y, Terao J (1993) Consumption of carotenoids in photosensitized oxidation of human plasma and plasma low-density lipoprotein. Free Radic Biol Med 15:377–384CrossRefGoogle Scholar
  23. 23.
    Akasaka K, Ohrui H, Meguro H, Tamura M (1993) Determination of triacylglycerol and cholesterol ester hydroperoxides in human plasma by high-performance liquid chromatography with fluorometric postcolumn detection. J Chromatogr 617:205–211CrossRefGoogle Scholar
  24. 24.
    Akasaka K, Ohrui H (2000) Development of phosphine reagents for the high-performance liquid chromatographic-fluorometric determination of lipid hydroperoxides. J Chromatogr A 881:159–170CrossRefGoogle Scholar
  25. 25.
    Saito I, Matsuura T, Inoue K (1981) Formation of superoxide ion from singlet oxygen. Use of a water-soluble singlet oxygen source. J Am Chem Soc 103:188–190CrossRefGoogle Scholar
  26. 26.
    Costa D, Fernandes E, Santos JL, Pinto DC, Silva AM, Lima JL (2007) New noncellular fluorescence microplate screening assay for scavenging activity against singlet oxygen. Anal Bioanal Chem 387:2071–2081CrossRefGoogle Scholar
  27. 27.
    Iwasaki Y, Takahashi S, Aizawa K, Mukai K (2015) Development of singlet oxygen absorption capacity (SOAC) assay method. 4. Measurements of the SOAC values for vegetable and fruit extracts. Biosci Biotechnol Biochem 79:280–291, and previous papers of this series CrossRefGoogle Scholar
  28. 28.
    Morita M, Naito Y, Yoshikawa T, Niki E (2015) Assessment of radical scavenging capacity of antioxidants contained in foods and beverages in plasma solution. Food Funct 6:1591–1599CrossRefGoogle Scholar
  29. 29.
    Okimoto Y, Watanabe A, Niki E, Yamashita T, Noguchi N (2000) A novel fluorescent probe diphenyl-1-pyrenylphosphine to follow lipid peroxidation in cell membranes. FEBS Lett 474:137–140CrossRefGoogle Scholar
  30. 30.
    Takahashi M, Shibata M, Niki E (2001) Estimation of lipid peroxidation of live cells using a fluorescent probe, diphenyl-1-pyrenylphosphine. Free Radic Biol Med 31:164–174CrossRefGoogle Scholar
  31. 31.
    Nagano T, Tanaka T, Mizuki H, Hirobe M (1994) Toxicity of singlet oxygen generated thermolytically in Escherichia coli. Chem Pharm Bull 42:883–887CrossRefGoogle Scholar
  32. 32.
    Terao J, Minami Y, Bando N (2011) Singlet molecular oxygen-quenching activity of carotenoids: relevance to protection of the skin from photoaging. J Clin Biochem Nutr 48:57–62CrossRefGoogle Scholar
  33. 33.
    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 55:8516–8522CrossRefGoogle Scholar
  34. 34.
    Takashima M, Shichiri M, Hagihara Y, Yoshida Y, Niki E (2012) Capacity of fucoxanthin for scavenging peroxyl radicals and inhibition of lipid peroxidation in model systems. Free Radic Res 46:1406–1412CrossRefGoogle Scholar
  35. 35.
    Sugawara T, Baskaran V, Tsuzuki W, Nagao A (2002) Brown algae fucoxanthin is hydrolyzed to fucoxanthinol during absorption by Caco-2 human intestinal cells and mice. J Nutr 132:946–951Google Scholar
  36. 36.
    Tsuchihashi H, Kigoshi M, Iwatsuki M, Niki E (1995) Action of β-carotene as an antioxidant against lipid peroxidation. Arch Biochem Biophys 323:137–147CrossRefGoogle Scholar
  37. 37.
    Nakagawa K, Kiko T, Hatade K, Sookwong P, Arai H, Miyazawa T (2009) Antioxidant effect of lutein towards phospholipid hydroperoxidation in human erythrocytes. Br J Nutr 102:1280–1284CrossRefGoogle Scholar
  38. 38.
    Santas J, Guardiola F, Rafecas M, Bou R (2013) Determination of total plasma hydroperoxides using a diphenyl-1-pyrenylphosphine fluorescent probe. Anal Biochem 434:172–177CrossRefGoogle Scholar
  39. 39.
    Ohshima T, Hopia A, German JB, Frankel EN (1996) Determination of hydroperoxides and structures by high-performance liquid chromatography with post-column detection with diphenyl-1-pyrenylphosphine. Lipids 31:1091–1096CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Mayuko Morita
    • 1
    • 2
  • Yuji Naito
    • 1
  • Toshikazu Yoshikawa
    • 2
  • Etsuo Niki
    • 1
    • 3
    Email author
  1. 1.Department of Molecular Gastroenterology and HepatologyKyoto Prefectural University of MedicineKyotoJapan
  2. 2.Department of Gastrointestinal ImmunologyKyoto Prefectural University of MedicineKyotoJapan
  3. 3.Health Research InstituteNational Institute of Advanced Industrial Science and TechnologyTakamatsuJapan

Personalised recommendations