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In vitro antioxidant, anti-glycation and immunomodulation activities of fermented blue-green algae Aphanizomenon flos-aquae

  • Miyu Taniguchi
  • Takashi KudaEmail author
  • Junna Shibayama
  • Tetsuya Sasaki
  • Toshihide Michihata
  • Hajime Takahashi
  • Bon Kimura
Original Article
  • 32 Downloads

Abstract

To clarify the antioxidant, anti-glycation and immunomodulatory capacities of fermented blue-green algae Aphanizomenon flos-aquae (AFA), hot aqueous extract suspensions made from 10% AFA were fermented by Lactobacillus plantarum AN7 and Lactococcus lactis subsp. lactis Kushiro-L2 strains isolated from a coastal region of Japan. The DPPH and O2 radical scavenging capacities and Fe-reducing power were increased in the fermented AFA. The increased DPPH radical scavenging capacity of the fermented AFA was fractionated to mainly < 3 kDa and 30–100 kDa. The increased O2 radical scavenging capacities were fractionated to mainly < 3 kDa. Anti-glycation activity in BSA-fructose model rather than BSA-methylglyoxal model was increased by the fermentation. The increased anti-glycation activity was fractionated to mainly 30–100 kDa. The NO concentration in the murine macrophage RAW264.7 culture media was high with the fermented AFA. The increased immunomodulation capacity was also fractionated to mainly 30–100 kDa. These results suggest that the fermented AFA is a more useful material for health foods and supplements.

Keywords

Blue-green algae Aphanizomenon flos-aquae Fermentation Antioxidant Anti-glycation RAW264.7 cells 

Notes

Acknowledgements

This work was partially supported by the Japan Health & Research Institute, Tokyo, Japan; Suzuki Nori Co., Choshi, Japan; and Dr’s Choice, Tokyo, Japan.

Compliance with ethical standards

Conflict of interest

The authors do not declare any conflicts of interest.

References

  1. 1.
    Parker CH, Stutts WL, Degrasse SL (2015) Development and validation of a liquid chromatography-tandem mass spectrometry method for the quantitation of microcystins in blue-green algal dietary supplements. J Agric Food Chem 63:10303–10312CrossRefGoogle Scholar
  2. 2.
    Bishop WM, Zubeck M (2012) Evaluation of microalgae for use as nutraceuticals and nutritional supplements. Nutr Food Sci 2:1000147CrossRefGoogle Scholar
  3. 3.
    Kushak C, Drapeau EM, Van Cott HH (2000) Winter, favorable effects of blue-green algae Aphanizomenon flos-aquae on rat plasma lipids. J Am Nutr Assoc 2:59–65Google Scholar
  4. 4.
    Carmichael WW, Drapeau C, Anderson DM (2000) Harvesting of Aphanizomenon flosaquae Ralfs ex Born. & Flah. var. flosaquae (Cyanobacteria) from Klamath Lake for human dietary use. J Appl Phycol 12:585–595CrossRefGoogle Scholar
  5. 5.
    Taveme YJ, Merkus D, Bogers AJ, Halliwell B, Duncker DJ, Lyons TW (2018) Reactive oxygen species: Radical factors in the evolution of animal life: a molecular timescale from earth’s earliest history to the rise of complex life. Bioessays 40: https://doi.org/10.1002/bies.201700158
  6. 6.
    He LL, Wang X, Wu XX, Wang XX, Kong YM, Wang X et al (2015) Protein damage and reactive oxygen species generation induced by the synergistic effects of ultrasound and methylene blue. Spectrochim Acta A 134:361–366CrossRefGoogle Scholar
  7. 7.
    Nissanka N, Moraes CT (2018) Mitochondrial DNA damage and reactive oxygen species in neurodegenerative disease. FEBS Lett 592:728–742CrossRefGoogle Scholar
  8. 8.
    Birnbaum JH, Wanner D, Gietl AF, Saake A, Kündig TM, Hock C et al (2018) Oxidative stress and altered mitochondrial protein expression in the absence of amyloid-β and tau pathology in iPSC-derived neurons from sporadic Alzheimer’s disease patients. Stem Cell Res 27:121–130CrossRefGoogle Scholar
  9. 9.
    Forrester SJ, Kikuchi DS, Hernandes MS, Xu Q, Griendling KK (2018) Reactive oxygen species in metabolic and inflammatory signalling. Circ Res 122:877–902CrossRefGoogle Scholar
  10. 10.
    Franco R, Martinez-Soccio E (2017) Chemical rules on the assessment of antioxidant potential in food and food additives aimed at reducing oxidative stress and neurodegeneration. Food Chem 235:318–323CrossRefGoogle Scholar
  11. 11.
    Kuda T, Yano T (2014) Mineral composition of seawater bittern nigari products and their effects on changing of browning and antioxidant activity in the glucose/lysine Maillard reaction. Appl Biochem Biotechnol 172:2989–2997CrossRefGoogle Scholar
  12. 12.
    Roohk HV, Zaidi AR, Patel D (2018) Glycated albumin (GA) and inflammation: role of GA as a potential marker of inflammation. Inflamm Res 67:21–30CrossRefGoogle Scholar
  13. 13.
    Rabbani N, Ashour A, Thornalley PJ (2016) Mass spectrometric determination of early and advanced glycation in biology. Glycoconjugate J 33:553–568CrossRefGoogle Scholar
  14. 14.
    Neves D (2013) Advanced glycation end-products: a common pathway in diabetes and age-related erectile dysfunction. Free Radical Res 47:49–69CrossRefGoogle Scholar
  15. 15.
    Crasci L, Lauro MR, Puglisi G, Panico A (2018) Natural antioxidant polyphenols on inflammation management: Anti-glycation activity vs metalloproteinases inhibition. Crit Rev Food Sci Nutr 58:893–904CrossRefGoogle Scholar
  16. 16.
    Chinta KC, Saini V, Glasgaow JN, Mazorodze JH, Rahman MA, Reddy D et al (2016) The emerging role of gasotransmitters in the pathogenesis of tuberculosis. Nitric Oxide 59:28–41CrossRefGoogle Scholar
  17. 17.
    Knott AB, Bossy-Wetzel E (2010) Impact of nitric oxide on metabolism in health and age-related disease. Diab Obes Metab 12:126–133CrossRefGoogle Scholar
  18. 18.
    Ghasemi M, Mayasi Y, Hannoun A, Eslami SM, Carandang R (2018) Nitric oxide and mitochondrial function in neurological diseases. Neurosci 376:48–71CrossRefGoogle Scholar
  19. 19.
    Kawahara M, Nemoto M, Nakata T, Kondo S, Takahashi H, Kimura B et al (2015) Anti-inflammatory properties of fermented soy milk with Lactococcus lactis subsp. lactis S-SU2 in murine macrophage RAW264.7 cells and DSS-induced IBD model mice. Int Immunopharm 26:295–303CrossRefGoogle Scholar
  20. 20.
    Hirano S, Yokota Y, Eda M, Kuda T, Shikano A, Takahashi H et al (2017) Effect of Lactobacillus plantarum Tennozu-SU2 on Salmonella Typhimurium infection in human enterocyte-like HT-29-Luc cells and BALB/c mice. Probiotics Antimicro Prot 9:64–70CrossRefGoogle Scholar
  21. 21.
    Han L, Yu J, Chen Y, Cheng D, Wang X, Wang C (2018) Immunomodulatory activity of docosahexenoic acid on RAW264.7 cells activation through GPR120-mediated signalling pathway. J Agric Food Chem 66:926–934CrossRefGoogle Scholar
  22. 22.
    Shikano A, Kuda T, Takahashi H, Kimura B (2018) Effects of fermented green-loofah and green-papaya on nitric oxide secretion from murine macrophage RAW264.7 cells. Mol Biol Rep 45:1013–1021CrossRefGoogle Scholar
  23. 23.
    Benedetti S, Benvenuti F, Pagliarani S, Francogli S, Scoglio S, Canestrari F (2004) Antioxidant properties of a novel phycocyanin extract from the blue-green alga Aphanizomenon flos-aquae. Life Sci 75:2353–2362CrossRefGoogle Scholar
  24. 24.
    Benedetti S, Benvenuti F, Scoglio S, Canestrari F (2010) Oxygen radical absorbance capacity of phycocyanin and phycocyanobilin from the food supplement Aphanizomenon flos-aquae. J Med Food 13:223–227CrossRefGoogle Scholar
  25. 25.
    Nuzzo D, Presti G, Picone P, Galizzi G, Gulotta E, Giuliano S et al (2018) Effects of the Aphanizomenon flos-aquae extract (Klamin®) on a neurodegeneration cellular model. Oxid Med Cell Longev. 9089016,  https://doi.org/10.1155/2018/9089016
  26. 26.
    Hart AN, Zaske LA, Patterson KM, Drapeau C, Jensen GS (2007) Natural killer cell activation and modulation of chemokine receptor profile in vitro by an extract from the cyanophyta Aphanizomenon flos-aquae. J Med Food 10:435–441CrossRefGoogle Scholar
  27. 27.
    Mohammed SA, Abdelhafez HM, Eid FA, Abdel-Raouf OM, Ibrahim RM (2016) The possible anti-inflammatory role of the blue green algae, Aphanizomenon flos-aquae on liver of adult male rats. J Biosci Appl Res 2:414–425Google Scholar
  28. 28.
    Eda M, Kuda T, Kataoka M, Takahashi H, Kimura B (2016) Anti-glycation properties of the aqueous extract solutions of dried algae products harvested and made in the Miura Peninsula, Japan, and effect of lactic acid fermentation on the properties. J Appl Phycol 28:3617–3624CrossRefGoogle Scholar
  29. 29.
    Kuda T, Eda M, Kataoka M, Nemoto M, Kawahara M, Oshio S et al (2016) Anti-glycation properties of the aqueous extract solutions of dried algae products and effect of lactic acid fermentation on the proper. Food Chem 192:1109–1115CrossRefGoogle Scholar
  30. 30.
    Nemoto M, Kuda T, Eda M, Yamakawa H, Takahashi H, Kimura B (2017) Protective effects of mekabu aqueous solution fermented by Lactobacillus plantarum Sanriku-SU7 on human enterocyte-like HT-29-luc cells and DSS-induced murine IBD model. Probiotics Antimicro Prot 9:48–55CrossRefGoogle Scholar
  31. 31.
    Takei M, Kuda T, Eda M, Shikano A, Takahashi H, Kimura B (2017) Antioxidant and fermentation properties of aqueous solutions of dried algal products from the Boso Peninsula, Japan. Food Biosci 19:85–91CrossRefGoogle Scholar
  32. 32.
    Kuda T, Yazaki T, Ono M, Takahashi H, Kimura B (2013) In vitro cholesterol-lowering properties of Lactobacillus plantarum AN6 isolated from aji-narezushi. Lett Appl Microbiol 57:187–192CrossRefGoogle Scholar
  33. 33.
    Kuda T, Kataoka M, Nemoto M, Kawahara M, Takahashi H, Kimura B (2016) Isolation of lactic acid bacteria from plants of the coastal Satoumi regions for use as starter cultures in fermented milk and soymilk production. LWT—Food Sci Technol 68:202–207Google Scholar
  34. 34.
    Sasaki T, Koshi E, Take H, Michihata T, Maruya M, Enomoto T (2017) Characterisation of odorants in roasted stem tea using gas chromatography–mass spectrometry and gas chromatography-olfactometry analysis. Food Chem 220:177–183CrossRefGoogle Scholar
  35. 35.
    Wang W, Yagiz Y, Buran TJ, Nunes CN, Gu L (2011) Phytochemicals from berries and grapes inhibited the formation of advanced glycation end-products by scavenging reactive carbonyls. Food Res Int 44:2666–2673CrossRefGoogle Scholar
  36. 36.
    Yokota Y, Shikano A, Kuda T, Takei M, Takahashi H, Kimura B (2018) Lactobacillus plantarum AN1 cells increase caecal L. reuteri in an ICR mouse model of dextran sodium sulphate-induced inflammatory bowel disease. Int Immunpharm 56:119–127CrossRefGoogle Scholar
  37. 37.
    Campana R, Martinelli V, Scoglio S, Colombo E, Benedetti S, Baffone W (2017) Influence of Aphanizomenon flos-aquae and two of its extracts on growth ability and antimicrobial properties of Lactobacillus acidophilus DDS-1. LWT—Food Sci Technol 81:291–298Google Scholar
  38. 38.
    McDonough AA, Veiras LC, Guevara CA, Ralph DL (2017) Cardiovascular benefits associated with higher dietary K+ versus lower dietary Na+: evidence from population and mechanistic studies. Am J Physiol Endocrinol Metab 312:E348–E356CrossRefGoogle Scholar
  39. 39.
    Kamel KS, Schreiber M, Halperin ML (2018) Renal potassium physiology: integration of the renal response to dietary potassium depletion. Kidney Int 93:41–53CrossRefGoogle Scholar
  40. 40.
    Oulhote Y, Mergler D, Barbeau B, Bellinger DC, Bouffard T, Brodeur M et al (2014) Neurobehavioral function in school-age children exposed to manganese in drinking water. Environ Health Perspect 122:12CrossRefGoogle Scholar
  41. 41.
    Tallino S, Duffy M, Ralle M, Cortés MP, Latorre M, Burkhead JL (2015) Nutrigenomics analysis reveals that copper deficiency and dietary sucrose up-regulate inflammation, fibrosis and lipogenic pathways in a mature rat model of nonalcoholic fatty liver disease. J Nutr Biochem 26:996–1006CrossRefGoogle Scholar
  42. 42.
    Yumol JL, Wakefield CB, Sacco SE, Sullivan PJ, Comelli EM (2018) Bone development in growing female mice fed calcium and vitamin D at lower levels than is present in the AIN-93G reference diet. Bone Rep 8:229–238CrossRefGoogle Scholar
  43. 43.
    Ishizaki-Koizumi S, Sonaka I, Fujitani S, Nishiguchi S (2002) Mechanisms of the protective effect of L-alanine to D-galactosamine-induced hepatocellular injury: Comparative studies of L-alanine and pyruvate. Biochem Biophys Res Commun 291:738–743CrossRefGoogle Scholar
  44. 44.
    Brosnan JT, Brosnan ME (2013) Glutamate: a truly functional amino acid. Amino Acid 45:413–418CrossRefGoogle Scholar
  45. 45.
    Poolman B, Driessen AJ, Konings WN (1988) Regulation of arginine-ornithine exchange and the arginine deiminase pathway in Streptococcus lactis. J Bacteriol 169:5597–5604CrossRefGoogle Scholar
  46. 46.
    Cynober L (1994) Can arginine and omithine support gut functions? Gut 35(1):S42-S45Google Scholar
  47. 47.
    Goh ET, Stokes CS, Sidhu SS, Vilstrup H, Gluud LL, Morgan YY (2018) L-Ornithine L-aspartate for prevention and treatment of hepatic encephalopathy in people with cirrhosis. Cochrane Database Syst Rev 5:CD012410Google Scholar
  48. 48.
    Grosser N, Oberle S, Berndt G, Erdmann K, Hemmerle A, Schröder H (2004) Antioxidant action of L-alanine: heme oxygenase-1 and ferritin as possible mediators. Biochem Biophys Res Commun 314:351–355CrossRefGoogle Scholar
  49. 49.
    Kawano T, Kagenishi T, Kadono T, Bouteau F, Hiramatsu T, Lin C et al (2015) Production and removal of superoxide anion radical by artificial metalloenzymes and redox-active metals. Commun Integr Biol 8:e1000710CrossRefGoogle Scholar
  50. 50.
    Pisoschi AM, Pop A (2015) The role of antioxidants in the chemistry of oxidative stress: a review. Eur J Med Chem 97:55–74CrossRefGoogle Scholar
  51. 51.
    Kim YH, Keeton JT, Smith SB, Maxim JE, Yang HS, Savell JW (2009) Evaluation of antioxidant capacity and colour stability of calcium lactate enhancement on fresh beef under highly oxidising conditions. Food Chem 115:272–278CrossRefGoogle Scholar
  52. 52.
    Groussard C, Morel I, Chevanne M, Monnier M, Josianne C, Delamarche A (2000) Free radical scavenging and antioxidant effects of lactate ion: an in vitro study. J Appl Physiol 89:169–175CrossRefGoogle Scholar
  53. 53.
    Lobo A, Patil A, Phatak N (2010) Chandra, Free radicals, antioxidants and functional foods: impact on human health. Pharmacol Rev 4:118–126CrossRefGoogle Scholar
  54. 54.
    Pugh N, Ross SA, ElSohly HN, ElSohly MA, Pasco DS (2001) Isolation of three high molecular weight polysaccharide preparations with potent immunostimulatory activity from Spirulina platensis, Aphanizomenon flos-aquae and Chlorella pyrenoidosa. Planta Med 67:737–742CrossRefGoogle Scholar
  55. 55.
    Aaron NH, Zasuke LA, Patterson KM, Drapeau C, Jensen GS (2007) Natural killer cell activation and modulation of chemokine receptor profile in vitro by an extract from the Cyanophyta Aphanizomenon flos-aquae. J Med Food 10:435–441CrossRefGoogle Scholar
  56. 56.
    Mysliwa KB, Solymosi K (2017) Phycobilins and phycobiliproteins used in food industry and medicine. J Mini-Rev Med Chem 17:1173–1193Google Scholar
  57. 57.
    Kondo S, Kuda T, Nemoto M, Usami Y, Takahashi H, Kimura B (2016) Protective effects of rice bran fermented by Saccharomyces cerevisiae Misaki-1 and Lactobacillus plantarum Sanriki-SU8 in dextran sodium sulphate-induced inflammatory bowel disease model mice. Food Biosci 16:44–49CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  • Miyu Taniguchi
    • 1
  • Takashi Kuda
    • 1
    Email author
  • Junna Shibayama
    • 1
  • Tetsuya Sasaki
    • 2
  • Toshihide Michihata
    • 2
  • Hajime Takahashi
    • 1
  • Bon Kimura
    • 1
  1. 1.Department of Food Science and TechnologyTokyo University of Marine Science and TechnologyMinato-cityJapan
  2. 2.Chemistry and Food DepartmentIndustrial Research Institute of IshikawaKanazawaJapan

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