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http://dx.doi.org/10.4162/nrp.2020.14.3.175

Skate cartilage extracts containing chondroitin sulfate ameliorates hyperlipidemia-induced inflammation and oxidative stress in high cholesterol diet-fed LDL receptor knockout mice in comparison with shark chondroitin sulfate  

Seol, Bo Gyeong (Department of Food Science and Nutrition & Kimchi Research Institute, Pusan National University)
Kim, Ji Hyun (Department of Food Science and Nutrition & Kimchi Research Institute, Pusan National University)
Woo, Minji (Department of Food Science and Nutrition & Kimchi Research Institute, Pusan National University)
Song, Yeong Ok (Department of Food Science and Nutrition & Kimchi Research Institute, Pusan National University)
Choi, Yung Hyun (Anti-Aging Research Center, Dong-eui University)
Noh, Jeong Sook (Department of of Food Science and Nutrition, Tongmyong University)
Cho, Eun Ju (Department of Food Science and Nutrition & Kimchi Research Institute, Pusan National University)
Publication Information
Nutrition Research and Practice / v.14, no.3, 2020 , pp. 175-187 More about this Journal
Abstract
BACKGROUND/OBJECTIVES: In this study, we investigated the beneficial effects of skate cartilage extracts containing chondroitin sulfate (SCS) on hyperlipidemia-induced inflammation and oxidative stress in high cholesterol diet (HCD)-fed mice in comparison with the effects of shark cartilage-derived chondroitin sulfate (CS). MATERIALS/METHODS: Low-density lipoprotein receptor knockout (LDLR-KO) mice were fed HCD with an oral administration of CS (50 and 100 mg/kg BW/day), SCS (100 and 200 mg/kg BW/day), or water, respectively, for ten weeks. RESULTS: The administration of CS or SCS reduced the levels of serum triglyceride (TG), total cholesterol (TC), and LDL cholesterol and elevated the levels of high-density lipoprotein cholesterol, compared with those of the control group (P < 0.05). Furthermore, CS or SCS significantly attenuated inflammation by reducing the serum levels of interleukin (IL)-1β and hepatic protein expression levels of nuclear factor kappa B, inducible nitric oxide synthase, cyclooxygenase-2, and IL-1beta (P < 0.05). In particular, the serum level of tumor necrosis factor-alpha was reduced only in the 100 mg/kg BW/day of SCS-fed group, whereas the IL-6 level was reduced in the 100 and 200 mg/kg BW/day of SCS-fed groups (P < 0.05). In addition, lipid peroxidation and nitric oxide production were attenuated in the livers of the CS and SCS groups mediated by the upregulation of hepatic proteins of antioxidant enzymes, such as superoxide dismutase, catalase, and glutathione peroxidase (P < 0.05). CONCLUSIONS: These results suggest that the biological effects of SCS, similar to those of CS, are attributed to improved lipid profiles as well as suppressed inflammation and oxidative stress induced by the intake of HCD.
Keywords
Chondroitin sulfates; cartilage; hyperlipidemias; inflammation; oxidative stress;
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1 Hu SW, Tian YY, Chang YG, Li ZJ, Xue CH, Wang YM. Fucosylated chondroitin sulfate from sea cucumber improves glucose metabolism and activates insulin signaling in the liver of insulin-resistant mice. J Med Food 2014;17:749-57.   DOI
2 Kim BH, Ahn SH, Choi BD, Kang SJ, Kim YL, Lee HJ, Oh MJ, Jung TS. In vivo evaluation of chondroitin sulfates from midduk (Styela clava) and munggae tunics (Halocynthia roretzi) as a cosmetic material. J Korean Soc Food Sci Nutr 2004;33:641-5.   DOI
3 da Cunha AL, Aguiar JA, Correa da Silva FS, Michelacci YM. Do chondroitin sulfates with different structures have different activities on chondrocytes and macrophages? Int J Biol Macromol 2017;103:1019-31.   DOI
4 Baek JM, Kang KH, Kim SH, Noh JS, Jeong KS. A study on development of high functional materials producing technique using by-products from skate processing (1)-development of chondroitin sulfate materials using skate cartilages. J Environ Sci Int 2016;25:645-54.   DOI
5 Friedewald WT, Levy RI, Fredrickson DS. Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clin Chem 1972;18:499-502.   DOI
6 Ohkawa H, Ohishi N, Yagi K. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 1979;95:351-8.   DOI
7 Schmidt HH, Warner TD, Nakane M, Forstermann U, Murad F. Regulation and subcellular location of nitrogen oxide synthases in RAW264.7 macrophages. Mol Pharmacol 1992;41:615-24.
8 Dietschy JM. Dietary fatty acids and the regulation of plasma low density lipoprotein cholesterol concentrations. J Nutr 1998;128 2 Suppl:444S-448S.   DOI
9 Ichimura M, Kawase M, Masuzumi M, Sakaki M, Nagata Y, Tanaka K, Suruga K, Tamaru S, Kato S, Tsuneyama K, Omagari K. High-fat and high-cholesterol diet rapidly induces non-alcoholic steatohepatitis with advanced fibrosis in Sprague-Dawley rats. Hepatol Res 2015;45:458-69.   DOI
10 Kainuma M, Fujimoto M, Sekiya N, Tsuneyama K, Cheng C, Takano Y, Terasawa K, Shimada Y. Cholesterol-fed rabbit as a unique model of nonalcoholic, nonobese, non-insulin-resistant fatty liver disease with characteristic fibrosis. J Gastroenterol 2006;41:971-80.   DOI
11 Bieghs V, Van Gorp PJ, Wouters K, Hendrikx T, Gijbels MJ, van Bilsen M, Bakker J, Binder CJ, Lutjohann D, Staels B, Hofker MH, Shiri-Sverdlov R. LDL receptor knock-out mice are a physiological model particularly vulnerable to study the onset of inflammation in non-alcoholic fatty liver disease. PLoS One 2012;7:e30668.   DOI
12 Subramanian S, Goodspeed L, Wang S, Kim J, Zeng L, Ioannou GN, Haigh WG, Yeh MM, Kowdley KV, O'Brien KD, Pennathur S, Chait A. Dietary cholesterol exacerbates hepatic steatosis and inflammation in obese LDL receptor-deficient mice. J Lipid Res 2011;52:1626-35.   DOI
13 Han LK, Sumiyoshi M, Takeda T, Chihara H, Nishikiori T, Tsujita T, Kimura Y, Okuda H. Inhibitory effects of chondroitin sulfate prepared from salmon nasal cartilage on fat storage in mice fed a high-fat diet. Int J Obes Relat Metab Disord 2000;24:1131-8.   DOI
14 Wang J, Mazza G. Effects of anthocyanins and other phenolic compounds on the production of tumor necrosis factor ${\alpha}$ in LPS/IFN-${\gamma}$-activated RAW 264.7 macrophages. J Agric Food Chem 2002;50:4183-9.   DOI
15 Kleemann R, Zadelaar S, Kooistra T. Cytokines and atherosclerosis: a comprehensive review of studies in mice. Cardiovasc Res 2008;79:360-76.   DOI
16 Angeli JK, Cruz Pereira CA, de Oliveira Faria T, Stefanon I, Padilha AS, Vassallo DV. Cadmium exposure induces vascular injury due to endothelial oxidative stress: the role of local angiotensin II and COX-2. Free Radic Biol Med 2013;65:838-48.   DOI
17 Gil-Cardoso K, Gines I, Pinent M, Ardevol A, Blay M, Terra X. Effects of flavonoids on intestinal inflammation, barrier integrity and changes in gut microbiota during diet-induced obesity. Nutr Res Rev 2016;29:234-48.   DOI
18 Yuan Y, Naito H, Jia X, Kitamori K, Nakajima T. Combination of hypertension along with a high fat and cholesterol diet induces severe hepatic inflammation in rats via a signaling network comprising $NF-{\kappa}B$, MAPK, and Nrf2 pathways. Nutrients 2017;9:1018.   DOI
19 Anavi S, Eisenberg-Bord M, Hahn-Obercyger M, Genin O, Pines M, Tirosh O. The role of iNOS in cholesterol-induced liver fibrosis. Lab Invest 2015;95:914-24.   DOI
20 Stabler TV, Montell E, Verges J, Huebner JL, Kraus VB. Chondroitin sulfate inhibits monocyte chemoattractant protein-1 release from 3T3-L1 adipocytes: a new treatment opportunity for obesityrelated inflammation? Biomark Insights 2017;12:1177271917726964.
21 Jomphe C, Gabriac M, Hale TM, Heroux L, Trudeau LE, Deblois D, Montell E, Verges J, du Souich P. Chondroitin sulfate inhibits the nuclear translocation of nuclear factor-kappaB in interleukin-$1{\beta}$-stimulated chondrocytes. Basic Clin Pharmacol Toxicol 2008;102:59-65.   DOI
22 Furukawa S, Fujita T, Shimabukuro M, Iwaki M, Yamada Y, Nakajima Y, Nakayama O, Makishima M, Matsuda M, Shimomura I. Increased oxidative stress in obesity and its impact on metabolic syndrome. J Clin Invest 2004;114:1752-61.   DOI
23 Kim HJ, Hwangbo MH, Lee JW, Im HG, Lee IS. Antioxidant effects of red ginseng powder on liver of benzo(${\alpha}$)pyrene-treated mice. Korean J Food Sci Technol 2007;39:217-21.
24 Lovlin R, Cottle W, Pyke I, Kavanagh M, Belcastro AN. Are indices of free radical damage related to exercise intensity. Eur J Appl Physiol Occup Physiol 1987;56:313-6.   DOI
25 Niess AM, Dickhuth HH, Northoff H, Fehrenbach E. Free radicals and oxidative stress in exercise--immunological aspects. Exerc Immunol Rev 1999;5:22-56.
26 Carr AC, McCall MR, Frei B. Oxidation of LDL by myeloperoxidase and reactive nitrogen species: reaction pathways and antioxidant protection. Arterioscler Thromb Vasc Biol 2000;20:1716-23.   DOI
27 Dahech I, Harrabi B, Hamden K, Feki A, Mejdoub H, Belghith H, Belghith KS. Antioxidant effect of nondigestible levan and its impact on cardiovascular disease and atherosclerosis. Int J Biol Macromol 2013;58:281-6.   DOI
28 Lee JY, Lee SH, Kim HJ, Ha JM, Lee SH, Lee JH, Ha BJ. The preventive inhibition of chondroitin sulfate against the CCl4-induced oxidative stress of subcellular level. Arch Pharm Res 2004;27:340-5.   DOI
29 Tomizawa M, Kawanabe Y, Shinozaki F, Sato S, Motoyoshi Y, Sugiyama T, Yamamoto S, Sueishi M. Triglyceride is strongly associated with nonalcoholic fatty liver disease among markers of hyperlipidemia and diabetes. Biomed Rep 2014;2:633-6.   DOI
30 Tannock LR. Advances in the management of hyperlipidemia-induced atherosclerosis. Expert Rev Cardiovasc Ther 2008;6:369-83.   DOI
31 Wouters K, van Gorp PJ, Bieghs V, Gijbels MJ, Duimel H, Lutjohann D, Kerksiek A, van Kruchten R, Maeda N, Staels B, van Bilsen M, Shiri-Sverdlov R, Hofker MH. Dietary cholesterol, rather than liver steatosis, leads to hepatic inflammation in hyperlipidemic mouse models of nonalcoholic steatohepatitis. Hepatology 2008;48:474-86.   DOI
32 Onody A, Csonka C, Giricz Z, Ferdinandy P. Hyperlipidemia induced by a cholesterol-rich diet leads to enhanced peroxynitrite formation in rat hearts. Cardiovasc Res 2003;58:663-70.   DOI
33 Czako L, Szabolcs A, Vajda A, Csati S, Venglovecz V, Rakonczay Z Jr, Hegyi P, Tiszlavicz L, Csont T, Posa A, Berko A, Varga C, Varga Ilona S, Boros I, Lonovics J. Hyperlipidemia induced by a cholesterol-rich diet aggravates necrotizing pancreatitis in rats. Eur J Pharmacol 2007;572:74-81.   DOI
34 Puskas LG, Nagy ZB, Giricz Z, Onody A, Csonka C, Kitajka K, Hackler L Jr, Zvara A, Ferdinandy P. Cholesterol diet-induced hyperlipidemia influences gene expression pattern of rat hearts: a DNA microarray study. FEBS Lett 2004;562:99-104.   DOI
35 Lee LC, Wei L, Huang WC, Hsu YJ, Chen YM, Huang CC. Hypolipidemic effect of tomato juice in hamsters in high cholesterol diet-induced hyperlipidemia. Nutrients 2015;7:10525-37.   DOI
36 Bondia-Pons I, Ryan L, Martinez JA. Oxidative stress and inflammation interactions in human obesity. J Physiol Biochem 2012;68:701-11.   DOI
37 Madamanchi NR, Vendrov A, Runge MS. Oxidative stress and vascular disease. Arterioscler Thromb Vasc Biol 2005;25:29-38.   DOI
38 Nelson RH. Hyperlipidemia as a risk factor for cardiovascular disease. Prim Care 2013;40:195-211.   DOI
39 Harmon RC, Tiniakos DG, Argo CK. Inflammation in nonalcoholic steatohepatitis. Expert Rev Gastroenterol Hepatol 2011;5:189-200.   DOI
40 Muniandy K, Gothai S, Badran KM, Suresh Kumar S, Esa NM, Arulselvan P. Suppression of proinflammatory cytokines and mediators in LPS-Induced RAW 264.7 macrophages by stem extract of alternanthera sessilis via the inhibition of the $NF-{\kappa}B$ pathway. J Immunol Res 2018;2018:3430684.   DOI
41 Ho FM, Liu SH, Liau CS, Huang PJ, Lin-Shiau SY. High glucose-induced apoptosis in human endothelial cells is mediated by sequential activations of c-Jun NH(2)-terminal kinase and caspase-3. Circulation 2000;101:2618-24.   DOI
42 Abe S, Obata Y, Oka S, Koji T, Nishino T, Izumikawa K. Chondroitin sulfate prevents peritoneal fibrosis in mice by suppressing $NF-{\kappa}B$ activation. Med Mol Morphol 2016;49:144-53.   DOI
43 Bauerova K, Ponist S, Kuncirova V, Mihalova D, Paulovicova E, Volpi N. Chondroitin sulfate effect on induced arthritis in rats. Osteoarthritis Cartilage 2011;19:1373-9.   DOI
44 Melgar-Lesmes P, Garcia-Polite F, Del-Rey-Puech P, Rosas E, Dreyfuss JL, Montell E, Verges J, Edelman ER, Balcells M. Treatment with chondroitin sulfate to modulate inflammation and atherogenesis in obesity. Atherosclerosis 2016;245:82-7.   DOI
45 Song YO, Kim M, Woo M, Baek JM, Kang KH, Kim SH, Roh SS, Park CH, Jeong KS, Noh JS. Chondroitin sulfate-rich extract of skate cartilage attenuates lipopolysaccharide-induced liver damage in mice. Mar Drugs 2017;15:E178.
46 Canas N, Valero T, Villarroya M, Montell E, Verges J, Garcia AG, Lopez MG. Chondroitin sulfate protects SH-SY5Y cells from oxidative stress by inducing heme oxygenase-1 via phosphatidylinositol 3-kinase/Akt. J Pharmacol Exp Ther 2007;323:946-53.   DOI