11-Hydroperoxide eicosanoid-mediated 2(E),4(E)-decadienal production from arachidonic acid in the brown algae, Saccharina angustata

  • Kangsadan BoonprabEmail author
  • Kenji Matsui
  • Yoshihiko Akakabe
  • Norishige Yotsukura
  • Tadahiko Kajiwara


This work aims to propose a pathway for the production of 2(E),4(E)-decadienal from arachidonic acid (ARA) via 11-hydroperoxide eicosanoid (11 hydroperoxyeicosatetraenoic acid, 11-HPETE) through lipoxygenase (LOX) and hydroperoxide lyase (HPL) in the brown alga, Saccharina angustata, by identifying pathway intermediates through three studies. The first study investigated the biogeneration of 2(E),4(E)-decadienal in crude homogenates of fronds (CHF), while the second and third investigated whether ARA is the precursor of the pathway and if 11-HPETE is produced from ARA as an intermediate in 2(E),4(E)-decadienal generation, respectively. The results showed that 2(E),4(E)-decadienal was formed in CHF and its concentration increased after incubation. This finding led to the hypothesis that 2(E),4(E)-decadienal is formed enzymatically via LOX-HPL and consequently its biogeneration was determined. ARA was indicated to be a precursor of the pathway since, after CHF was incubated with ARA as a substrate, the amount of aldehyde increased significantly compared with that produced by CHF without ARA and without incubation. The production of 11-HPETE from ARA was also demonstrated as an intermediate reaction in 2(E),4(E)-decadienal formation via the LOX-HPL pathway. The hydroxy isomer of 11-HPETE was produced, and ARA was incubated with homogenated fronds in combination with glutathione peroxidase and glutathione to control its stability during identification. The compound was identified as 11-HPETE because the purified isomer showed the same retention time when co-injected with the standard using an HPLC technique; moreover, the same indicated mass spectrum was obtained as that of the standard via a GC/GCMS technique. The indicated pathway and the pathway for the production of short chain aldehydes [n-hexanal, 2(E),3(Z)-nonenal and 2(E),4(E)-decadienal] from ARA and linoleic acid through theirs hydroperoxides are proposed.


Phaeophyta Saccharina angustata 2(E),4(E)-Decadienal 11 Hydroperoxyeicosatetraenoic acid Lipoxygenase Hydroperoxide lyase 


Funding information

This work was performed as part of the JSPS-NRCT Core University Program on the “Development of thermotolerant microbial resources and their applications”, with the cooperation of Japanese and Thai scientists and in association with Kasetsart University in Thailand and Yamaguchi University in Japan (1999-2010).

Supplementary material

10811_2019_1776_MOESM1_ESM.pdf (38 kb)
ESM 1 (PDF 37 kb)
10811_2019_1776_MOESM2_ESM.pdf (312 kb)
ESM 2 (PDF 312 kb)
10811_2019_1776_MOESM3_ESM.pdf (117 kb)
ESM 3 (PDF 116 kb)
10811_2019_1776_MOESM4_ESM.pdf (84 kb)
ESM 4 (PDF 83 kb)
10811_2019_1776_MOESM5_ESM.pdf (43 kb)
ESM 5 (PDF 42 kb)
10811_2019_1776_MOESM6_ESM.pdf (208 kb)
ESM 6 (PDF 207 kb)


  1. Akakabe Y, Matsui K, Kajiwara T (2003) 2,4-Decadienals are produced via (R)-11-HPITE from arachidonic acid in marine green alga Ulva conglobata. Bioorg Med Chem 11:3607–3609CrossRefGoogle Scholar
  2. Andreou A, Brodhun F, Feussner I (2009) Biosynthesis of oxylipins in non-mammals. Prog Lipid Res 48:148–170CrossRefGoogle Scholar
  3. Barbosa M, Collado-González J, Andrade PB, Ferreres F, Valentão P, Galano JM, Durand T, Gil-Izquierdo Á (2015) Nonenzymatic α-linolenic acid derivatives from the sea: macroalgae as novel sources of phytoprostanes. J Agric Food Chem 63:6466–6474CrossRefGoogle Scholar
  4. Barbosa M, Valentão P, Andrade PB (2016) Biologically active oxylipins from enzymatic and nonenzymatic routes in macroalgae. Mar Drugs 14:23CrossRefGoogle Scholar
  5. Blée E (1998) Phytooxylipins and plant defense reactions. Prog Lipid Res 37:33–72CrossRefGoogle Scholar
  6. Boeynaems JM, Brash AR, Oates JA, Hubbard WC (1980) Preparation and assay of monohydroxy-eicosatetraenoic acids. Anal Biochem 104:259–267CrossRefGoogle Scholar
  7. Boonprab K, Matsui K, Akakabe Y, Yotsukura N, Kajiwara T (2003a) Hydroperoxy-arachidonic acid mediated n-hexanal and (Z)-3- and (E)-2-nonenal formation in Laminaria angustata. Phytochemistry 63:669–678CrossRefGoogle Scholar
  8. Boonprab K, Matsui K, Yoshida M, Akakabe Y, Chirapart A, Kajiwara T (2003b) C6-aldehyde formation by fatty acid hydroperoxide lyase in the brown alga, Laminaria angustatata. Z Naturforsch 58c:207–214CrossRefGoogle Scholar
  9. Boonprab K, Matsui K, Akakabe Y, Yotsukura N, Kajiwara T (2004) Arachidonic conversion by lipoxygenase in the brown alga, Laminaria angustata. Kasetsart J (Nat Sci) 38:72–77Google Scholar
  10. Boonprab K, Matsui K, Akkabe Y, Yoshida M, Yotsukura N, Chirapat A, Kajiwara T (2006) Formation of aldehyde flavor (n-hexanal, 3Z-nonenal and 2E-nonenal) in the brown alga, Laminaria angustata. J Appl Phycol 18:409–412CrossRefGoogle Scholar
  11. Brodowsky ID, Hamberg M, Oliw EH (1992) A linoleic acid (8R)-dioxygenase and hydroperoxide isomerase of the fungus Gaeumannomyces graminis. Biosynthesis of (8R)-hydroxylinoleic acid and (7S,8S)-dihydroxylinoleic acid from (8R)-hydroperoxylinoleic acid. J Biol Chem 267:14738–14745Google Scholar
  12. Bryant RW, Simon TC, Bailey JM (1982) Role of glutathione peroxidase and hexose monophosphate shunt in the platelet lipoxygenase pathway. J Biol Chem 257:14937–14943Google Scholar
  13. Cadwallader KR (2000) Enzymes and flavor biogenesis in fish. In: Haard NF, Simpson BK (eds) Seafood enzymes: utilization and influence on postharvest seafood quality. Marcel Dekker, Inc., New York, pp 365–383Google Scholar
  14. Dulley JR, Grieve PA (1975) Simple technique for eliminating interference by detergents in the Lowry method of protein determination. Anal Biochem 64:136–141CrossRefGoogle Scholar
  15. Fujimura T, Kawai T (2000) Enzymes and seaweed flavor. In: Haard NF, Simpson BK (eds) Seafood enzymes: utilization and influence on postharvest seafood quality. Marcel Dekker, Inc., New York, pp 385–407Google Scholar
  16. Gerwick WH (1994) Structure and biosynthesis of marine algal oxylipins. Biochim Biophys Acta 1211:243–255CrossRefGoogle Scholar
  17. Gerwick WH, Proteau PJ, Nagle DG, Wise ML, Jiang ZD, Bernart MW, Hamberg M (1993) Biologically active oxylipins from seaweeds. Hydrobiologia 260/261:653–665CrossRefGoogle Scholar
  18. Graff G, Anderson LA, Jaques LW (1990) Preparation and purification of soybean lipoxygenase-derived unsaturated hydroperoxy and hydroxy fatty acids and determination of molar absorptivities of hydroxy fatty acids. Anal Biochem 188:38–47CrossRefGoogle Scholar
  19. Grechkin AN (2002) Hydroperoxide lyase and divinyl ether synthase. Prostaglandins Other Lipid Mediat 68-69:457–470CrossRefGoogle Scholar
  20. Hamberg M, Gerwick WH (1993) Biosynthesis of vicinal dihydroxy fatty acids in the red alga Gracilariopsis lemaneiformis: identification a sodium-dependent 12-lipoxygenase and a hydroperoxide isomerase. Arch Biochem Biophys 305:115–122CrossRefGoogle Scholar
  21. Hamberg M, Herman CA, Herman RP (1986) Novel biological transformations of 15-Ls-hydroperoxy-5,8,11,13-eicosatetraenoic acid. Biochim Biophys Acta 877:447–457CrossRefGoogle Scholar
  22. Hamberg M, Su C, Oliw E (1998) Manganese lipoxygenase. Discovery of a bis-allylic hydroperoxide as product and intermediate in a lipoxygenase reaction. J Biol Chem 273:13080–13088CrossRefGoogle Scholar
  23. Hatanaka A (1996) The fresh green odor emitted by plants. Food Rev Int 12:303–350CrossRefGoogle Scholar
  24. Hatanaka A (2003) So-called “green odor” as plant origin--chemistry and biochemistry. Seikagaku 75:1414–1428Google Scholar
  25. Hatzelmann A, Schatz M, Ullrich V (1989) Involvement of glutathione peroxidase activity in the stimulation of 5-lipoxygenase activity by glutathione-depleting agents in human polymorphonuclear leukocytes. Eur J Biochem 180:527–533CrossRefGoogle Scholar
  26. Hombeck M, Pohnert G, Boland W (1999) Biosynthesis of dictyopterene A: stereoselectivity of a lipoxygenase/hydroperoxide lyase from Gomphonema parvulum (Bacillariophyceae). Chem Commun 3:243–244CrossRefGoogle Scholar
  27. Jayasena DD, Ahn DU, Nam KC, Jo C (2013) Flavour chemistry of chicken meat: a review. Asian-Australas J Anim Sci 26:732–742CrossRefGoogle Scholar
  28. Kajiwara T (1997) Dynamic studies on bioflavor of seaweed. Koryo No 196:61–70. (in Japanese with English summary)Google Scholar
  29. Kajiwara T, Hatanaka A, Kawai T, Ishihara M, Tsuneya T (1988) Study of flavor compounds of essential oil extracts from edible Japanese kelps. J Food Sci 53:960–962CrossRefGoogle Scholar
  30. Kajiwara T, Kodama K, Hatanaka A, Matsui K (1993a) Volatile compounds from Japanese marine brown algae. In: Teranishi R, Buttery RG, Sugisawa H (eds) Bioactive volatile compounds from plants. Am Chem Soc Symp series, vol 525, Washington, DC, pp 104–120Google Scholar
  31. Kajiwara T, Matsui K, Hatanaka A, Tomoi T, Fujimura T, Kawai T (1993b) Distribution of an enzyme system producing seaweed flavor: conversion of fatty acids to long-chain aldehydes in seaweeds. J Appl Phycol 5:225–230CrossRefGoogle Scholar
  32. Kajiwara T, Matsui K, Akakabe Y (1996) Biogeneration of volatile compounds via oxylipins in edible seaweeds. In: Takeoka GR, Teranishi R, Williams PJ, Kobayashi A (eds) Biotechnology for improved foods and flavors. Am Chem Soc Symp series, vol 637, Washington, DC, pp 146–166Google Scholar
  33. Katayama T (1958) Chemical studies on volatile constituents of seaweed. J Fac Fish Anim Husb Hiroshima Univ 2:67–77Google Scholar
  34. Kuhn H (2000) Structural basis for the positional specificity of lipoxygenases. Prostaglandins Other Lipid Mediat 62:255–270CrossRefGoogle Scholar
  35. Kuhn H, Banthiya S, van Leyen K (2015) Mammalian lipoxygenases and their biological relevance. Biochim Biophys Acta 1851:308–330CrossRefGoogle Scholar
  36. Lehmann WD, Stephan M, Fürstenberger G (1992) Profiling assay for lipoxygenase products of linoleic and arachidonic acid by gas chromatography-mass spectrometry. Anal Biochem 204:158–170CrossRefGoogle Scholar
  37. Matsui K (2006) Green leaf volatiles: hydroperoxide lyase pathway of oxylipin metabolism. Curr Opin Plant Biol 9:274–280CrossRefGoogle Scholar
  38. Mosblech A, Feussner I, Heilmann I (2009) Oxylipins: structurally diverse metabolites from fatty acid oxidation. Plant Physiol Biochem 47:511–517CrossRefGoogle Scholar
  39. Noordermeer MA, Veldink GA, Vliegenthart JF (2001) Fatty acid hydroperoxide lyase: a plant cytochrome p450 enzyme involved in wound healing and pest resistance. Chembiochem 2:494–504CrossRefGoogle Scholar
  40. Pohnert G (2002) Phospholipase A2 activity triggers the wound-activated chemical defense in the diatom Thalassiosira rotula. Plant Physiol 129:103–111CrossRefGoogle Scholar
  41. Qi J, Liu DY, Zhou GH, Xu XL (2017) Characteristic flavor of traditional soup made by stewing Chinese yellow-feather chickens. J Food Sci 82:2031–2040CrossRefGoogle Scholar
  42. Schnurr K, Belkner J, Ursini F, Schewe T, Kuhn H (1996) The selenoenzyme phospholipid hydroperoxide glutathione peroxidase controls the activity of the 15-lipoxygenase with complex substrates and preserves the specificity of the oxygenation products. J Biol Chem 271:4653–4658CrossRefGoogle Scholar
  43. Sekiya J, Kajiwara T, Hatanaka A (1984) Seasonal change in activities of enzymes responsible for the formation of C6-aldehydes and C6-alcohols in tea leaves, and the effects of environmental temperatures on the enzyme activities. Plant Cell Physiol 25:269–280Google Scholar
  44. Sutherland M, Shankaranarayanan P, Schewe T, Nigam S (2001) Evidence for the presence of phospholipid hydroperoxide glutathione peroxidase in human platelets: implications for its involvement in the regulatory network of the 12-lipoxygenase pathway of arachidonic acid metabolism. Biochem J 353:91–100CrossRefGoogle Scholar
  45. Takakura Y, Mizushima M, Hayashi K, Masuzawa T, Nishimura T (2014) Characterization of the key aroma compounds in chicken soup stock using aroma extract dilution analysis. Food Sci Technol Res 20:109–113CrossRefGoogle Scholar
  46. Weitzel F, Wendel A (1993) Selenoenzymes regulate the activity of leukocyte 5-lipoxygenase via the peroxide tone. J Biol Chem 268:6288–6292Google Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Department of Fishery Products, Faculty of FisheriesKasetsart UniversityBangkokThailand
  2. 2.Department of Biological Chemistry, Faculty of AgricultureYamaguchi UniversityYamaguchiJapan
  3. 3.Field Science Center for Northern BiosphereHokkaido UniversitySapporoJapan

Personalised recommendations