Location via proxy:   [ UP ]  
[Report a bug]   [Manage cookies]                
Skip to main content

Advertisement

Springer Nature Link
Log in

Inhibitory activities of microalgal fucoxanthin against α-amylase, α-glucosidase, and glucose oxidase in 3T3-L1 cells linked to type 2 diabetes

  • Published:
Journal of Oceanology and Limnology Aims and scope Submit manuscript

Abstract

Postprandial hyperglycemia is an early indication of type 2 diabetes and the target of many anti-diabetic and anti-obesity studies. α-Glucosidase and α-amylase are the crucial factors in regulating starch digestion and glucose absorption, making them key targets for many studies to treat postprandial hyperglycemia. We studied the inhibitory activities of microalgal fucoxanthin against rat-intestinal α-glucosidase and pancreatic α-amylase along with the antidiabetic effect to induce differentiation in 3T3-L1 pre-adipocytes using Oil Red-O staining. Fucoxanthin displayed strong hindrance activities toward α-amylase in a concentration-dependent manner, with an IC50 value of 0.68 mmol/L, whereas weak inhibitory activity against α-glucosidase, with an IC50 value of 4.75 mmol/L. Fucoxanthin also considerably elevated glucose oxidase activity in 3T3-L1 cells by 31.3% at 5 µmol/L. During adipocyte differentiation, fucoxanthin showed lipid accumulation in 3T3-L1 cells with no cytotoxicity up to 20 µmol/L. However, fucoxanthin had no inhibitory activity on glucose-6-phosphate dehydrogenase. These results suggest that fucoxanthin might be useful for the prevention of obesity or diabetes by inhibiting carbohydrate-hydrolyzing enzymes and lipid accumulation and be utilized as an ingredient for a functional food or dietary supplement.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Baron A D. 1998. Postprandial hyperglycaemia and α-glucosidase inhibitors. Diabetes Res. Clin. Pract., 40(S1): S51–S55.

    Article  Google Scholar 

  • Bernfeld P. 1955. Amylases, alpha and beta. In: Colowick S P, Kaplan N O eds. Methods in Enzymology. Academic Press, New York. p.149–158.

    Chapter  Google Scholar 

  • Chang Y H, Chen Y L, Huang W C, Liou C J. 2018. Fucoxanthin attenuates fatty acid-induced lipid accumulation in FL83B hepatocytes through regulated Sirt1/AMPK signaling pathway. Biochem. Biophys. Res. Commun., 495(1): 197–203.

    Article  Google Scholar 

  • Chethan S, Sreerama Y N, Malleshi N G. 2008. Mode of inhibition of finger millet malt amylases by the millet phenolics. Food Chem, 111(1): 187–191.

    Article  Google Scholar 

  • Dixon M. 1953. The determination of enzyme inhibitor constants. Biochem. J., 55(1): 170–171.

    Article  Google Scholar 

  • García López P M, de la Mora P G, Wysocka W, Maiztegui B, Alzugaray M E, Del Zotto H, Borelli M I. 2004. Quinolizidine alkaloids isolated from Lupinus species enhance insulin secretion. Eur. J. Pharmacol., 504(1–2): 139–142.

    Article  Google Scholar 

  • Giugliano D, Ceriello A, Paolisso G. 1996. Oxidative stress and diabetic vascular complications. Diabetes Care, 19(3): 257–267.

    Article  Google Scholar 

  • Gumucio D L, Wiebauer K, Caldwell R M, Samuelson L C, Meisler M H. 1988. Concerted evolution of human amylase genes. Mol. Cell. Biol, 8(3): 1 197–1 205.

    Article  Google Scholar 

  • Guyton A C, Hall J E. 2015. Insulin, glucagon, and diabetes mellitus. In: Hall J E. Textbook of Medical Physiology. 13th edn. Saunders, Philadelphia. p.961–978.

    Google Scholar 

  • Haugan J A, Aakermann R, Liaaen-Jensen S. 1992. Isolation of fucoxanthin and peridinin. Meth. Enzymol. 213: 231–245.

    Article  Google Scholar 

  • Heo S J, Hwang J Y, Choi J I, Han J S, Kim H J, Jeon Y J. 2009. Diphlorethohydroxycarmalol isolated from Ishige okamurae, a brown algae, a potent α-glucosidase and α-amylase inhibitor, alleviates postprandial hyperglycemia in diabetic mice. Eur. J. Pharmacol. 615(1–3): 252–256.

    Article  Google Scholar 

  • Hii C S T, Howell S L. 1985. Effects of flavonoids on insulin secretion and 45Ca2+ handling in rat islets of Langerhans. J. Endocrinol., 107(1): 1–8.

    Article  Google Scholar 

  • Horii S, Fukase H, Matsuo T, Kameda Y, Asano N, Matsui K. 1986. Synthesis and α-D-glucosidase inhibitory activity of N-substituted valiolamine derivatives as potential oral antidiabetic agents. J. Med. Chem., 29(6): 1 038–1 046.

    Article  Google Scholar 

  • Jung H A, Islam N, Lee C M, Jeong H O, Chung H Y, Woo H C, Choi J S. 2012. Promising antidiabetic potential of fucoxanthin isolated from the edible brown algae Eisenia bicyclis and Undaria pinnatifida. Fish Sci, 78(6): 1 321–1 329.

    Article  Google Scholar 

  • Kang S I, Ko H C, Shin H S, Kim H M, Hong Y S, Lee N H, Kim S J. 2011. Fucoxanthin exerts differing effects on 3T3-L1 cells according to differentiation stage and inhibits glucose uptake in mature adipocytes. Biochem. Biophys. Res. Commun., 409(4): 769–774.

    Article  Google Scholar 

  • Kawamura-Konishi Y, Watanabe N, Saito M, Nakajima N, Sakaki T, Katayama T, Enomoto T. 2012. Isolation of a new phlorotannin, a potent inhibitor of carbohydrate-hydrolyzing enzymes, from the brown alga Sargassum patens. J. Agric. Food Chem., 60(22): 5 565–5 570.

    Article  Google Scholar 

  • Kawee-Ai A, Kim S M. 2014. Application of microalgal fucoxanthin for the reduction of colon cancer risk: inhibitory activity of fucoxanthin against β-glucuronidase and DLD-1 cancer cells. Nat. Prod. Commun., 9(7): 921–924.

    Google Scholar 

  • Kawee-Ai A, Kuntiya A, Kim S M. 2013. Anticholinesterase and antioxidant activities of fucoxanthin purified from the microalga Phaeodactylum tricornutum. Nat. Prod. Commun, 8(10): 1 381–1 386.

    Google Scholar 

  • Kim K Y, Choi K S, Kurihara H, Kim S M. 2008. β-Glucuronidase inhibitory activity of bromophenols purified from Grateloupia elliptica. Food Sci. Biotechnol., 17(5): 1 110–1 114.

    Google Scholar 

  • Kim S M, Kang S W, Kwon O N, Chung D, Pan C H. 2012. Fucoxanthin as a major carotenoid in Isochrysis aff. Galbana: characterization of extraction for commercial application. J. Korean Soc. Appl. Biol. Chem., 55(4): 477–483.

    Article  Google Scholar 

  • King G L, Kunisaki M, Nishio Y, Inoguchi T, Shiba T, Xia P. 1996. Biochemical and molecular mechanisms in the development of diabetic vascular complications. Diabetes, 45(S3): S105–S108.

    Article  Google Scholar 

  • Kurihara H, Mitani T, Kawabata J, Takahashi K. 1999. Inhibitory potencies of bromophenols from Rhodomelaceae algae against α-glucosidase activity. Fish Sci., 65(2): 300–303.

    Article  Google Scholar 

  • Lam S H, Chen J M, Kang C J, Chen C H, Lee S H. 2008. α-glucosidase inhibitors from the seeds of Syagrus romanzoffiana. Phytochemistry, 69(5): 1 173–1 178.

    Article  Google Scholar 

  • Li B, Huang Y, Paskewitz S M. 2006. Hen egg white lysozyme as an inhibitor of mushroom tyrosinase. FEBS Lett., 580(7): 1 877–1 882.

    Article  Google Scholar 

  • Li Y Y, Wu H S, Tang L, Feng C R, Yu J H, Li Y, Yang Y S, Yang B, He Q J. 2007. The potential insulin sensitizing and glucose lowering effects of a novel indole derivative in vitro and in vivo. Pharmacol. Res, 56(4): 335–343.

    Article  Google Scholar 

  • Lineweaver H, Burk D. 1934. The determination of enzyme dissociation constants. J. Am. Chem. Soc., 56(3): 658–666.

    Article  Google Scholar 

  • Lo Piparo E, Scheib H, Frei N, Williamson G, Grigorov M, Chou C J. 2008. Flavonoids for controlling starch digestion: structural requirements for inhibiting human α-amylase. J. Med. Chem., 51(12): 3 555–3 561.

    Article  Google Scholar 

  • Maeda H, Hosokawa M, Sashima T, Funayama K, Miyashita K. 2005. Fucoxanthin from edible seaweed, Undaria pinnatifida, shows antiobesity effect through UCP1 expression in white adipose tissues. Biochem. Biophys. Res. Commun, 332(2): 392–397.

    Article  Google Scholar 

  • Maeda H, Hosokawa M, Sashima T, Miyashita K. 2007. Dietary combination of fucoxanthin and fish oil attenuates the weight gain of white adipose tissue and decreases blood glucose in obese/diabetic KK-A y mice. J. Agric. Food Chem., 55(19): 7 701–7 706.

    Article  Google Scholar 

  • Maeda H, Hosokawa M, Sashima T, Murakami-Funayama K, Miyashita K. 2009. Anti-obesity and anti-diabetic effects of fucoxanthin on diet-induced obesity conditions in a murine model. Mol. Med. Rep., 2(6): 897–902.

    Article  Google Scholar 

  • Maeda H, Hosokawa M, Sashima T, Takahashi N, Kawada T, Miyashita K. 2006. Fucoxanthin and its metabolite, fucoxanthinol, suppress adipocyte differentiation in 3T3-L1 cells. Int. J. Mol. Med., 18: 147–152.

    Google Scholar 

  • Maeda H, Kanno S, Kodate M, Hosokawa M, Miyashita K. 2015. Fucoxanthinol, metabolite of fucoxanthin, improves obesity-induced inflammation in adipocyte cells. Mar. Drugs, 13(8): 4 799–4 813.

    Article  Google Scholar 

  • Marshall J J, Lauda C M. 1975. Purification and properties of phaseolamin, an inhibitor of alpha-amylase, from the kidney bean, Phaseolus vulgaris. J. Biol. Chem., 250(20): 8 030–8 037.

    Google Scholar 

  • Mikami D, Kurihara H, Kim S M, Takahashi K. 2013. Red algal bromophenols as glucose 6-phosphate dehydrogenase inhibitors. Mar. Drugs, 11(10): 4 050–4 057.

    Article  Google Scholar 

  • Molinski T F, Dalisay D S, Lievens S L, Saludes J P. 2009. Drug development from marine natural products. Nat. Rev. Drug Discov., 8(1): 69–85.

    Article  Google Scholar 

  • Mori K, Ooi T, Hiraoka M, Oka N, Hamada H, Tamura M, Kusumi T. 2004. Fucoxanthin and its metabolites in edible brown algae cultivated in deep seawater. Mar. Drugs, 2(2): 63–72.

    Article  Google Scholar 

  • Okada Y, Ishimaru A, Suzuki R, Okuyama T. 2004. A new phloroglucinol derivative from the brown alga Eisenia bicyclis: potential for the effective treatment of diabetic complications. J. Nat. Prod., 67(1): 103–105.

    Article  Google Scholar 

  • Olive C, Geroch M E, Levy H R. 1971. Glucose 6-phosphate dehydrogenase from Leuconostoc mesenteroides. J. Biol. Chem., 246: 2 047–2 057.

    Google Scholar 

  • Petrushkina M, Gusev E, Sorokin B, Zotko N, Mamaeva A, Filimonova A, Kulikovskiy M, Maltsev Y, Yampolsky I, Guglya E, Vinokurov V, Namsaraev Z, Kuzmin D. 2017. Fucoxanthin production by heterokont microalgae. Algal Res., 24: 387–393.

    Article  Google Scholar 

  • Priya S, Kaur N, GuptaA K. 2010. Purification, characterization and inhibition studies of α-amylase of Rhyzopertha dominica. Pestic. Biochem. Physiol., 98(2): 231–237.

    Article  Google Scholar 

  • Shin E S, Park J, Shin J M, Cho D, Cho S Y, Shin D W, Ham M, Kim J B, Lee T R. 2008. Catechin gallates are NADP+-competitive inhibitors of glucose-6-phosphate dehydrogenase and other enzymes that employ NADP+ as a coenzyme. Bioorg. Med. Chem., 16(7): 3 580–3 586.

    Article  Google Scholar 

  • Shobana S, Sreerama Y N, Malleshi N G. 2009. Composition and enzyme inhibitory properties of finger millet (Eleusine coracana L.) seed coat phenolics: mode of inhibition of α-glucosidase and pancreatic amylase. Food Chem., 115(4): 1 268–1 273.

    Article  Google Scholar 

  • Tadera K, Minami Y, Takamatsu K, Matsuoka T. 2006. Inhibition of α-glucosidase and α-amylase by flavonoids. J. Nutr. Sci. Vitaminol., 52(2): 149–153.

    Article  Google Scholar 

  • Terasaki M, Hirose A, Narayan B, Baba Y, Kawagoe C, Yasui H, Saga N, Hosokawa M, Miyashita K. 2009. Evaluation of recoverable functional lipid components of several brown seaweeds (Phaeophyta) from Japan with special reference to fucoxanthin and fucosterol contents. J. Phycol., 45(4): 974–980.

    Article  Google Scholar 

  • Tewari N, Tiwari V K, Mishra R C, Tripathi R P, Srivastava A K, Ahmad R, Srivastava R, Srivastava B S. 2003. Synthesis and bioevaluation of glycosyl ureas asα-glucosidase inhibitors and their effect on mycobacterium. Bioorg. Med. Chem., 11(13): 2 911–2 922.

    Article  Google Scholar 

  • Xia S, Wang K, Wan L L, Li A F, Hu Q, Zhang C W. 2013. Production, characterization, and antioxidant activity of fucoxanthin from the marine diatom Odontella aurita. Mar. Drugs, 11(7): 2 667–2 681.

    Article  Google Scholar 

  • Yan X J, Chuda Y, Suzuki M, Nagata T. 1999. Fucoxanthin as the major antioxidant in Hijikia fusiformis, a common edible seaweed. Biosci., Biotechnol., Biochem., 63(3): 605–607.

    Article  Google Scholar 

Download references

Acknowledgment

This research was a part of the project titled ‘Future Marine Technology Development’ funded by the Ministry of Oceans and Fisheries, Republic of Korea.

Author information

Authors and Affiliations

  1. Department of Marine Food Science and Technology, Gangneung-Wonju National University, Gangneung, 25457, Republic of Korea

    Arthitaya Kawee-Ai & Sang Moo Kim

  2. Department of Biotechnology, Chiang Mai University, Chiang Mai, 50200, Thailand

    Arthitaya Kawee-Ai

  3. Department of Food Science and Biotechnology, Kyung Hee University, Yongin, 17104, Republic of Korea

    Aaron Taehwan Kim

Authors
  1. Arthitaya Kawee-Ai
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Aaron Taehwan Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sang Moo Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sang Moo Kim.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kawee-Ai, A., Kim, A.T. & Kim, S.M. Inhibitory activities of microalgal fucoxanthin against α-amylase, α-glucosidase, and glucose oxidase in 3T3-L1 cells linked to type 2 diabetes. J. Ocean. Limnol. 37, 928–937 (2019). https://doi.org/10.1007/s00343-019-8098-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00343-019-8098-9

Keyword

Search

Navigation