Dual antidiabetic and antihypertensive activity of fucoxanthin isolated from <i>Sargassum wightii</i> Greville in <i>in vivo</i> rat model

Vijayan Raji; Chitra Loganathan; Thiyagarajan Ramesh; Palvannan Thayumanavan

doi:10.1016/j.fshw.2023.02.037

Food Science and Human Wellness 2023, 12(5): 1693-1700 https://doi.org/10.1016/j.fshw.2023.02.037

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Open Access | Issue | Published: 21 March 2023

Dual antidiabetic and antihypertensive activity of fucoxanthin isolated from Sargassum wightii Greville in in vivo rat model

Show Author's Information Hide Author's Information Vijayan Raji^{^a}, Chitra Loganathan^{^a}, Thiyagarajan Ramesh^{^b}, Palvannan Thayumanavan^{^a}(

)

Department of Biochemistry, Periyar University, Salem, Tamil Nadu 636011, India

Department of Basic Medical Sciences, College of Medicine, Prince Sattam Bin Abdulaziz University, Al-Kharj 11942, Kingdom of Saudi Arabia

Peer review under responsibility of KeAi Communications Co., Ltd.

Keywords:

Hypertension, Diabetes, Oxidative stress, Fucoxanthin, Angiotensin-I-converting enzyme

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Raji V, Loganathan C, Ramesh T, et al. Dual antidiabetic and antihypertensive activity of fucoxanthin isolated from Sargassum wightii Greville in in vivo rat model. Food Science and Human Wellness, 2023, 12(5): 1693-1700. https://doi.org/10.1016/j.fshw.2023.02.037

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Abstract

In a previous study from our laboratory, fucoxanthin purified from brown algae, Sargassum wightii Greville has found to exhibit antioxidant activity and inhibition of angiotensin-I-converting enzyme (ACE) in vitro. The present study aims in understanding the protective effect of fucoxanthin purified from S. wightii against diabetes with hypertension in in vivo. Diabetes and hypertension were induced in rat by streptozotocin and sodium chloride treatment, respectively. In diabetes with hypertension rat, the blood pressure was increased along with hyperglycemia. Administration of fucoxanthin significantly reduced the blood pressure and ACE activity in diabetes with hypertension rat. Furthermore, administration of fucoxanthin significantly reduced the hyperglycemic state. The activity of various enzymes in the liver (hexokinase, glucose-6-phosphate dehydrogenase, glucose-6-phosphatase and fructose-1, 6-phosphatase) and serum (creatine kinase) were normalized to that of control level. The level of glycogen, glycoprotein component and lipid profile were equivalent to control level by fucoxanthin administration in diabetes with hypertension rats. Fucoxanthin ameliorated the oxidative stress by preserving the endogenous antioxidant levels in diabetes with hypertension rats. Also, the pancreatic histological integrity was similar to that of control level in diabetes with hypertension rats by fucoxanthin treatment. Altogether, fucoxanthin showed dual antidiabetic and antihypertensive activity in vivo.

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Dual antidiabetic and antihypertensive activity of fucoxanthin isolated from Sargassum wightii Greville in in vivo rat model

Show Author's information Hide Author's Information Vijayan Raji^{^a}, Chitra Loganathan^{^a}, Thiyagarajan Ramesh^{^b}, Palvannan Thayumanavan^{^a}(

)

Department of Biochemistry, Periyar University, Salem, Tamil Nadu 636011, India

Department of Basic Medical Sciences, College of Medicine, Prince Sattam Bin Abdulaziz University, Al-Kharj 11942, Kingdom of Saudi Arabia

Peer review under responsibility of KeAi Communications Co., Ltd.

Abstract

Keywords: Hypertension, Diabetes, Oxidative stress, Fucoxanthin, Angiotensin-I-converting enzyme

References(50)

[1]

C. Lourenço-Lopes, P. Garcia-Oliveira, M. Carpena, et al., Scientific approaches on extraction, purification and stability for the commercialization of fucoxanthin recovered from brown algae, Foods 9 (2020) 1113. https://doi.org/10.3390/foods9081113.

DOI Google Scholar

[2]

Y. Zhang, W. Xu, X. Huang, et al., Fucoxanthin ameliorates hyperglycemia, hyperlipidemia and insulin resistance in diabetic mice partially through IRS-1/PI3K/Akt and AMPK pathways, J. Funct. Foods 48 (2018) 515-524. https://doi.org/10.1016/j.jff.2018.07.048.

DOI Google Scholar

[3]

M. Bilal, H.M. Iqbal, Biologically active macromolecules: extraction strategies, therapeutic potential and biomedical perspective, Int. J. Biol. Macromol. 151 (2020) 1-18. https://doi.org/10.1016/j.ijbiomac.2020.02.037.

DOI Google Scholar

[4]

M.C. Kang, S.H. Lee, W.W. Lee, et al., Protective effect of fucoxanthin isolated from Ishige okamurae against high-glucose induced oxidative stress in human umbilical vein endothelial cells and zebrafish model, J. Funct. Foods 11 (2014) 304-312. https://doi.org/10.1016/j.jff.2014.09.007.

DOI Google Scholar

[5]

M. Ohishi, Hypertension with diabetes mellitus: physiology and pathology, Hypertens. Res. 41 (2018) 389-393. https://doi.org/10.1038/s41440-018-0034-4.

DOI Google Scholar

[6]

J.R. Sowers, M. Epstein, E.D. Frohlich, Diabetes, hypertension, and cardiovascular disease: an update, Hypertension 37 (2001) 1053-1059. https://doi.org/10.1161/01.HYP.37.4.1053.

DOI Google Scholar

[7]

G. Govindarajan, J.R. Sowers, C.S. Stump, Hypertension and diabetes mellitus, European Cardiology 2 (2006) 1-7.

DOI Google Scholar

[8]

J.R. Petrie, T.J. Guzik, R.M. Touyz, Diabetes, hypertension, and cardiovascular disease: clinical insights and vascular mechanisms, Can. J. Cardiol. 34 (2018) 575-584. https://doi.org/10.1016/j.cjca.2017.12.005.

DOI Google Scholar

[9]

V. Raji, C. Loganathan, G. Sadhasivam, et al., Purification of fucoxanthin from Sargassum wightii Greville and understanding the inhibition of angiotensin 1-converting enzyme: an in vitro and in silico studies, Int. J. Biol. Macromol. 148 (2020) 696-703. https://doi.org/10.1016/j.ijbiomac.2020.01.140.

DOI Google Scholar

[10]

N. Orie, N. Anyaegbu, Nifedipine effectively lowers salt-induced high blood pressure in diabetic rats, General Pharmacology: The Vascular System 32 (1999) 471-474. https://doi.org/10.1016/S0306-3623(98)00244-4.

DOI Google Scholar

[11]

S. Parasuraman, R. Raveendran, Measurement of invasive blood pressure in rats, J. Pharmacol. Pharmacother. 3 (2012) 172. https://doi.org/10.4103/0976-500X.95521.

DOI Google Scholar

[12]

N. Brandstrup, J. Kirk, C. Bruni, The hexokinase and phosphoglucoisomerase activities of aortic and pulmonary artery tissue in individuals of various ages, J. Gerontol. 12 (1957) 166-171. https://doi.org/10.1093/geronj/12.2.166.

DOI Google Scholar

[13]

K. Hikaru, O. Toshitsugu, Pathological occurrence of glucose-6-phosphatase in serum in liver diseases, Clin. Chim. Acta 4 (1959) 554-561. https://doi.org/10.1016/0009-8981(59)90165-2.

DOI Google Scholar

[14]

H.A. Ells, H. Kirkman, A colorimetric method for assay of erythrocytic glucose-6-phosphate dehydrogenase, P. Soc. Exp. Biol. Med. 106 (1961) 607-609. https://doi.org/10.3181/00379727-106-26418.

DOI Google Scholar

[15]

J.M. Gancedo, C. Gancedo, Fructose-1, 6-diphosphatase, phosphofructokinase and glucose-6-phosphate dehydrogenase from fermenting and non fermenting yeasts, Archiv für Mikrobiologie 76 (1971) 132-138. https://doi.org/10.1007/BF00411787.

DOI Google Scholar

[16]

S. Seifter, S. Dayton, B. Novic, et al., The estimation of glycogen with the anthrone reagent, Arch. Biochem. 25 (1950) 191-200.

Google Scholar

[17]

P. Niebes, Determination of enzymes and degradation products of glycosaminoglycan metabolism in the serum of healthy and varicose subjects, Clin. Chim. Acta 42 (1972) 399-408. https://doi.org/10.1016/0009-8981(72)90105-2.

DOI Google Scholar

[18]

S.T. Omaye, J.D. Turnbull, H.E. Sauberlich, Selected methods for the determination of ascorbic acid in animal cells, tissues, and fluids, Methods Enzymol. 62 (1979) 3-11. https://doi.org/10.1016/0076-6879(79)62181-x.

DOI Google Scholar

[19]

G.L. Ellman, Tissue sulfhydryl groups, Arch. Biochem. Biophys. 82 (1959) 70-77. https://doi.org/10.1016/0003-9861(59)90090-6.

DOI Google Scholar

[20]

P. Kakkar, B. Das, P. Viswanathan, A modified spectrophotometric assay of superoxide dismutase, Indian J. Biochem. Biophys. 21 (1984) 130-132.

Google Scholar

[21]

M.H. Hadwan, New method for assessment of serum catalase activity, Indian J. Sci. Techn. 9 (2016) 1-5. https://doi.org/10.17485/ijst/2016/v9i4/80499.

DOI Google Scholar

[22]

J.T. Rotruck, A.L. Pope, H.E. Ganther, et al., Selenium: biochemical role as a component of glutathione peroxidase, Science 179 (1973) 588-590. https://doi.org/10.1126/science.179.4073.588.

DOI Google Scholar

[23]

S. Al-Quraishy, M.A. Dkhil, A.E.A. Moneim, Anti-hyperglycemic activity of selenium nanoparticles in streptozotocin-induced diabetic rats, Int. J. Nanomed. 10 (2015) 6741. https://doi.org/10.2147/IJN.S91377.

DOI Google Scholar

[24]

M.M. Rahman, H.S. Kwon, M.J. Kim, et al., Melatonin supplementation plus exercise behavior ameliorate insulin resistance, hypertension and fatigue in a rat model of type 2 diabetes mellitus, BioMed. Pharmacother. 92 (2017) 606-614. https://doi.org/10.1016/j.biopha.2017.05.035.

DOI Google Scholar

[25]

F.C. Luft, L.I. Rankin, A.P. Evan, et al., Blood pressure of alloxan diabetic rats at regular and high salt intake, Clin. Exp. Hypertens. 3 (1981) 509-522. https://doi.org/10.3109/10641968109033679.

DOI Google Scholar

[26]

H. Salahdeen, A. Alada, Cardiovascular response to angiotensin Ⅱ and captopril in normal and diabetic rats loaded with salt, J. Med. Sci. 7 (2007) 187-194. https://doi.org/10.3923/JMS.2007.187.194.

DOI Google Scholar

[27]

Y. Takagi, H. Kadowaki, I. Kobayashi, et al., Effects of high-sodium intake on systemic blood pressure and vascular responses in spontaneously diabetic WBN/Kob-Lepr^fa/fa rats, Clin. Exp. Pharmacol. Physiol. 44 (2017) 305-312. https://doi.org/10.1111/1440-1681.12700.

DOI Google Scholar

[28]

K. Ikeda, A. Kitamura, H. Machida, et al., Effect of Undaria pinnatifida (Wakame) on the development of cerebrovascular diseases in stroke-prone spontaneously hypertensive rats, Clin. Exp. Pharmacol. Physiol. 30 (2003) 44-48. https://doi.org/10.1046/j.1440-1681.2003.03786.x.

DOI Google Scholar

[29]

M.H. Shishavan, R.H. Henning, A. van Buiten, et al., Metformin improves endothelial function and reduces blood pressure in diabetic spontaneously hypertensive rats independent from glycemia control: comparison to vildagliptin, Sci. Rep. 7 (2017) 1-12. https://doi.org/10.1038/s41598-017-11430-7.

DOI Google Scholar

[30]

H.C. Ou, W.C. Chou, P.M. Chu, et al., Fucoxanthin protects against oxLDL‐induced endothelial damage via activating the AMPK‐Akt‐CREB‐PGC1α pathway, Mol. Nutr. Food Res. 63 (2019) 1801353. https://doi.org/10.1002/mnfr.201801353.

DOI Google Scholar

[31]

Y.Q. Zhao, L. Zhang, G.X. Zhao, et al., Fucoxanthin attenuates doxorubicin-induced cardiotoxicity via anti-oxidant and anti-apoptotic mechanisms associated with p38, JNK and p53 pathways, J. Funct. Foods 62 (2019) 103542. https://doi.org/10.1016/j.jff.2019.103542.

DOI Google Scholar

[32]

V. Ramachandran, R. Saravanan, P. Senthilraja, Antidiabetic and antihyperlipidemic activity of asiatic acid in diabetic rats, role of HMG CoA: in vivo and in silico approaches, Phytomed. 21 (2014) 225-232. https://doi.org/10.1016/j.phymed.2013.08.027.

DOI Google Scholar

[33]

S. Penislusshiyan, L. Chitra, I. Ancy, et al., Novel antioxidant astaxanthin-S-allyl cysteine biconjugate diminished oxidative stress and mitochondrial dysfunction to triumph diabetes in rat model, Life Sci. 245 (2020) 117367. https://doi.org/10.1016/j.lfs.2020.117367.

DOI Google Scholar

[34]

H. Park, M. Lee, Y. Park, et al., Beneficial effects of Undaria pinnatifida ethanol extract on diet-induced-insulin resistance in C57BL/6J mice, Food Chem. Toxicol. 49 (2011) 727-733. https://doi.org/10.1016/j.fct.2010.11.032.

DOI Google Scholar

[35]

L. Cohen-Forterre, J. Andre, G. Mozere, et al., Kidney sialidase and sialyltransferase activities in spontaneously and experimentally diabetic rats: influence of insulin and sorbinil treatments, Biochem. Pharmacol. 40 (1990) 507-513. https://doi.org/10.1016/0006-2952(90)90549-z.

DOI Google Scholar

[36]

Z. Wang, J.M. do Carmo, N. Aberdein, et al., Synergistic interaction of hypertension and diabetes in promoting kidney injury and the role of endoplasmic reticulum stress, Hypertension 69 (2017) 879-891. https://doi.org/10.1161/HYPERTENSIONAHA.116.08560.

DOI Google Scholar

[37]

T. Tsukui, K. Konno, M. Hosokawa, et al., Fucoxanthin and fucoxanthinol enhance the amount of docosahexaenoic acid in the liver of KKAy obese/diabetic mice, J. Agric. Food Chem. 55 (2007) 5025-5029. https://doi.org/10.1021/jf070110q.

DOI Google Scholar

[38]

H. Maeda, T. Tsukui, T. Sashima, et al., Seaweed carotenoid, fucoxanthin, as a multi-functional nutrient, Asia Pac. J. Clin. Nutr. 17 (2008).

Google Scholar

[39]

H. Maeda, M. Hosokawa, T. Sashima, et al., Anti-obesity and anti-diabetic effects of fucoxanthin on diet-induced obesity conditions in a murine model, Mol. Med. Rep. 2 (2009) 897-902. https://doi.org/10.3892/mmr_00000189.

DOI Google Scholar

[40]

J. Peng, J.P. Yuan, C.F. Wu, et al., Fucoxanthin, a marine carotenoid present in brown seaweeds and diatoms: metabolism and bioactivities relevant to human health, Marine Drugs 9 (2011) 1806-1828. https://doi.org/10.3390/md9101806.

DOI Google Scholar

[41]

H. Nishino, Cancer prevention by carotenoids, Mutat. Res. 402 (1998) 159-163. https://doi.org/10.1016/s0027-5107(97)00293-5.

DOI Google Scholar

[42]

R. Sangeetha, N. Bhaskar, V. Baskaran, Comparative effects of β-carotene and fucoxanthin on retinol deficiency induced oxidative stress in rats, Mol. Cell. Biochem. 331 (2009) 59. https://doi.org/10.1007/s11010-009-0145-y.

DOI Google Scholar

[43]

R.K. Sangeetha, N. Bhaskar, V. Baskaran, Fucoxanthin restrains oxidative stress induced by retinol deficiency through modulation of Na⁺ Ka⁺-ATPase and antioxidant enzyme activities in rats, Eur. J. Nutr. 47 (2008) 432-441. https://doi.org/10.1007/s00394-008-0745-4.

DOI Google Scholar

[44]

M. Abidov, Z. Ramazanov, R. Seifulla, et al., The effects of Xanthigen^TM in the weight management of obese premenopausal women with non-alcoholic fatty liver disease and normal liver fat, Diabetes Obes. Metab. 12 (2010) 72-81. https://doi.org/10.1111/j.1463-1326.2009.01132.x.

DOI Google Scholar

[45]

Y.C. Chen, C.Y. Cheng, C.T. Liu, et al., Alleviative effect of fucoxanthin-containing extract from brown seaweed Laminaria japonica on renal tubular cell apoptosis through upregulating Na⁺/H⁺ exchanger NHE1 in chronic kidney disease mice, J. Ethnopharmacol. 224 (2018) 391-399. https://doi.org/10.1016/j.jep.2018.06.023.

DOI Google Scholar

[46]

C.L. Liu, Y.T. Chiu, M.L. Hu, Fucoxanthin enhances HO-1 and NQO1 expression in murine hepatic BNL CL. 2 cells through activation of the Nrf2/ARE system partially by its pro-oxidant activity, J. Agric. Food Chem. 59 (2011) 11344-11351. https://doi.org/10.1021/jf2029785.

DOI Google Scholar

[47]

T. Nomura, M. Kikuchi, A. Kubodera, et al., Proton-donative antioxidant activity of fucoxanthin with 1, 1-diphenyl-2-picrylhydrazyl (DPPH), IUBMB Life 42 (1997) 361-370. https://doi.org/10.1080/15216549700202761.

DOI Google Scholar

[48]

X. Yan, Y. Chuda, M. Suzuki, et al., Fucoxanthin as the major antioxidant in Hijikia fusiformis, a common edible seaweed, Biosci. Biotechnol. Biochem. 63 (1999) 605-607. https://doi.org/10.1271/bbb.63.605.

DOI Google Scholar

[49]

N.M. Sachindra, E. Sato, H. Maeda, et al., Radical scavenging and singlet oxygen quenching activity of marine carotenoid fucoxanthin and its metabolites, J. Agric. Food Chem. 55 (2007) 8516-8522. https://doi.org/10.1021/jf071848a.

DOI Google Scholar

[50]

C.I. Chukwuma, M.G. Matsabisa, M.A. Ibrahim, et al., Medicinal plants with concomitant anti-diabetic and anti-hypertensive effects as potential sources of dual acting therapies against diabetes and hypertension: a review, J. Ethnopharmacol. 235 (2019) 329-360. https://doi.org/10.1016/j.jep.2019.02.024.

DOI Google Scholar

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Publication history

Received: 26 June 2021

Revised: 07 July 2021

Accepted: 06 August 2021

Published: 21 March 2023

Issue date: September 2023

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Acknowledgements

Mr. R. Vijayan acknowledges University Grants Commission, New Delhi, India for the award of Rajiv Gandhi National Fellowship (RGNF-2015-17-SC-TAM-20532) to carry out this study. Dr. L. Chitra acknowledges University Grants Commission, India for the award of Dr. D.S. Kothari Post-Doctoral Fellowship (F.4-2/2006 (BSR)/BL/17-18/0313).

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This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).