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Studies on the partial characterization of extracted glycosaminoglycans from fish waste and its potentiality in modulating obesity through in-vitro and in-vivo

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Abstract

Glycosaminoglycans (GAGs) are bioactive polysaccharides or glycoconjugates found in the fish waste having significant health impacts. In the present study it has been attempted to extract GAGs from mackerel fish waste through chemical and enzymatic methods. Further, the extracted GAGs (e-GAGs) were analyzed for their composition (uronic acid, total sugar & sulfate), chemical characterization was carried out through techniques of scanning electron microscopy (SEM) and Fourier transform infrared spectroscopy (FTIR) & Proton NMR. Further, probable major GAGs present was identified by enzymatic digestion. The biological potential of the extracted glycoconjugate was assessed further through in-vitro and in-vivo studies. In-vitro biological activity showed good lipase inhibition (IC50, 2.6 mg/mL) and bile acid binding properties (dose-dependent). Lipid accumulation lowered in the e-GAGs differentiated 3T3L1 preadipocyte cells have also been observed. The high fat fed animal (in-vivo) study showed ameliorative effect via reducing blood sugar∼1.28↓, lipid profile↓, plasma insulin∼3.5↓, improved glucose tolerance, and homeostatic model assessment for insulin resistance (HOMA-IR, ∼3.0↓). Furthermore, elimination of bile acid (BA) due to GAG-BA binding properties resultant in removal of elevated fecal triglyceride and cholesterol suggesting its lipid lowering activity. Regulation of various proteins linked to carbohydrate and lipid metabolism including fatty acid synthase (FAS), low density lipoproteins receptor (LDL-R), 7α-hydroxylase, glucose transporter-4 (GLUT4) and Peroxisome proliferator- activated receptor gamma (PPAR-γ) were significant (p < 0.05) with e-GAGs treatment when compared to HFD group. Thus, the e-GAGs showed potential hypolipidemic activity through elimination of bile acid binding property together with regulating the specific protein related to obesity and its associated complications.

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Data Availability

The authors declare that the data supporting the findings of this study are available within the article and in supplementary information files.

References

  1. Ghaly, A.E., Ramakrishnan, V.V., Brooks, M.S., Budge, S.M., Dave, D.: Fish processing wastes as a potential source of proteins. Amino acids and oils: a critical review. J. Microb. Biochem. Technol. 5(4), 107–129 (2013). https://doi.org/10.4172/1948-5948.1000110

    Article  CAS  Google Scholar 

  2. Menon, V.V., Lele, S.S.: Nutraceuticals and bioactive compounds from seafood processing waste. In: Springer handbook of marine biotechnology, pp. 1405–1425. Springer, Berlin, Heidelberg (2015)

    Chapter  Google Scholar 

  3. Kumar, S.G., Rahman, M.A., Lee, S.H., Hwang, H.S., Kim, H.A., Yun, J.W.: Plasma proteome analysis for anti-obesity and anti‐diabetic potentials of chitosan oligosaccharides in ob/ob mice. Proteomics. 9(8), 2149–2162 (2009). https://doi.org/10.1002/pmic.200800571

    Article  CAS  PubMed  Google Scholar 

  4. Lindahl, U., Li, J.P.: Interactions between heparan sulfate and proteins—design and functional implications. Int. Rev. Cell. Mol. Biol. 276, 105–159 (2009). https://doi.org/10.1016/S1937-6448(09)76003-4

    Article  CAS  PubMed  Google Scholar 

  5. Yamada, S., Sugahara, K.: Potential therapeutic application of chondroitin sulfate/dermatan sulfate. Curr. Drug Discov Technol. 5(4), 289–301 (2008). https://doi.org/10.2174/157016308786733564

    Article  CAS  PubMed  Google Scholar 

  6. Arpicco, S., Milla, P., Stella, B., Dosio, F.: Hyaluronic acid conjugates as vectors for the active targeting of drugs, genes and nanocomposites in cancer treatment. Molecules. 19(3), 3193–3230 (2014). https://doi.org/10.3390/molecules19033193

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Trigkilidas, D., Anand, A.: The effectiveness of hyaluronic acid intra-articular injections in managing osteoarthritic knee pain. Ann. R Coll. Surg. Engl. 95(8), 545–551 (2013). https://doi.org/10.1308/003588413X13629960049432

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Kinoshita-Toyoda, A., Yamada, S., Haslam, S.M., Khoo, K.H., Sugiura, M., Morris, H.R., Dell, A., Sugahara, K.: Structural determination of five novel tetrasaccharides containing 3-O-sulfated D-glucuronic acid and two rare oligosaccharides containing a β-D-glucose branch isolated from squid cartilage chondroitin sulfate E. Biochemistry. 43(34), 11063–11074 (2004). https://doi.org/10.1021/bi049622d

    Article  CAS  PubMed  Google Scholar 

  9. Ahn, M.Y., Kim, B.J., Kim, H.J., Yoon, H.J., Jee, S.D., Hwang, J.S., Park, K.K.: Anti-obesity effect of Bombus ignitus queen glycosaminoglycans in rats on a high-fat diet. Int. J. Mol. Sci. 18(3), 681 (2017). https://doi.org/10.3390/ijms18030681

    Article  CAS  PubMed Central  Google Scholar 

  10. Nelson, F.R., Zvirbulis, R.A., Zonca, B., Li, K.W., Turner, S.M., Pasierb, M., Wilton, P., Martinez-Puiz, D., Wu, W.: The effects of an oral preparation containing hyaluronic acid (Oralvisc®) on obese knee osteoarthritis patients determined by pain, function, bradykinin, leptin, inflammatory cytokines, and heavy water analyses. Rheumatol. Int. 35(1), 43–52 (2015). https://doi.org/10.1007/s00296-014-3047-6

    Article  CAS  PubMed  Google Scholar 

  11. Association Official Analytical Chemist [AOAC]: Official methods of analysis,18th Edition. Pub AOAC International Maryland (2005)

  12. Kumar, G.S., Vijayalakshmi, B., Salimath, P.V.: Effect of bitter gourd and spent turmeric on constituents of glycosaminoglycans in different tissues in streptozotocin induced diabetic rats. Mol. Cell. Biochem. 286(1), 53–58 (2006). https://doi.org/10.1007/s11010-005-9086-2

    Article  CAS  PubMed  Google Scholar 

  13. Allalouf, D., Ber, A., Sharon, N.: Acid mucopolysaccharides in rat kidneys. Biochimica et Biophysica Acta (BBA)-Specialized Section on Mucoproteins and Mucopolysaccharides. 83(3),278–287(1964). https://doi.org/10.1016/0926-6526(64)90005-9

  14. McKelvy, J.F., Lee, Y.C.: Microheterogeneity of the carbohydrate group of Aspergillus oryzae α-amylase. Arch. Biochem. Biophys. 132(1), 99–110 (1969). https://doi.org/10.1016/0003-9861(69)90341-5

    Article  CAS  PubMed  Google Scholar 

  15. Dische, Z.: A new specific color reaction of hexuronic acids. J. Biol. Chem. 167(1), 189–198 (1947)

    Article  CAS  Google Scholar 

  16. Kumar, G.S., Salimath, P.V.: Effect of spent turmeric on kidney glycoconjugates in streptozotocin-induced diabetic rats. J. Diabetes Metab. Disord. 13(1), 1–9 (2014). https://doi.org/10.1186/2251-6581-13-78

    Article  Google Scholar 

  17. Kumar, G.S., Shetty, A.K., Sambaiah, K., Salimath, P.V.: Antidiabetic property of fenugreek seed mucilage and spent turmeric in streptozotocin-induced diabetic rats. Nutr. Res. 25(11), 1021–1028 (2005). https://doi.org/10.1016/j.nutres.2005.09.012

    Article  CAS  Google Scholar 

  18. Lowry, O., Rosebrough, N., Farr, A.L., Randall, R.: Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193(1), 265–275 (1951)

    Article  CAS  Google Scholar 

  19. Farndale, R.W., Buttle, D.J., Barrett, A.J.: Improved quantitation and discrimination of sulphated glycosaminoglycans by use of dimethylmethylene blue. Biochim. Biophys. Acta. 883(2), 173–177 (1986). https://doi.org/10.1016/0304-4165(86)90306-5

    Article  CAS  PubMed  Google Scholar 

  20. Krichen, F., Bougatef, H., Capitani, F., Amor, I.B., Koubaa, I., Gargouri, J., Francesca, M., Veronica, M., Fabio, G., Nicola, V., Bougatef, A.: Purification and structural elucidation of chondroitin sulfate/dermatan sulfate from Atlantic bluefin tuna (Thunnus thynnus) skins and their anticoagulant and ACE inhibitory activities. RSC Adv. 8(66), 37965–37975 (2018). https://doi.org/10.1039/c8ra06704j

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Lemmnitzer, K., Schiller, J., Becher, J., Möller, S., Schnabelrauch, M.: Improvement of the digestibility of sulfated hyaluronans by bovine testicular hyaluronidase: a UV spectroscopic and mass spectrometric study. BioMed. Res. Int. (2014). https://doi.org/10.1155/2014/986594

    Article  PubMed  PubMed Central  Google Scholar 

  22. Satyendra, R.V., Vishnumurthy, K.A., Vagdevi, H.M., Rajesh, K.P., Manjunatha, H., Shruthi, A.: Synthesis, in vitro antioxidant, anthelmintic and molecular docking studies of novel dichloro substituted benzoxazole-triazolo-thione derivatives. Eur. J. Med. Chem. 46(7), 3078–3084 (2011). https://doi.org/10.1016/j.ejmech.2011.03.017

    Article  CAS  PubMed  Google Scholar 

  23. Weibel, E.K., Hadvary, P., Hochuli, E., Kupfer, E., Lengsfeld, H.: Lipstatin, an inhibitor of pancreatic lipase, produced by Streptomyces toxytricini I. Producing organism, fermentation, isolation and biological activity. J. Antibiot. 40(8), 1081–1085 (1987). https://doi.org/10.7164/antibiotics.40.1081

    Article  CAS  Google Scholar 

  24. Camire, M.E., Dougherty, M.P.: Raisin dietary fiber composition and in vitro bile acid binding. J. Agric. Food Chem. 51(3), 834–837 (2003). https://doi.org/10.1021/jf025923n

    Article  CAS  PubMed  Google Scholar 

  25. Jones, M.L., Chen, H., Ouyang, W., Metz, T., Prakash, S.: Method for bile acid determination by high performance liquid chromatography. J. Med. Sciences-Taipei. 23(5), 277–280 (2003)

    Google Scholar 

  26. Rahman, M.A., Kumar, S.G., Kim, S.W., Hwang, H.J., Baek, Y.M., Lee, S.H., Hwang, H.S., Shon, Y.H., Nam, K.S., Yun, J.W.: Proteomic analysis for inhibitory effect of chitosan oligosaccharides on 3T3-L1 adipocyte differentiation. Proteomics. 8(3), 569–581 (2008). https://doi.org/10.1002/pmic.200700888

    Article  CAS  PubMed  Google Scholar 

  27. Andrikopoulos, S., Blair, A.R., Deluca, N., Fam, B.C., Proietto, J.: Evaluating the glucose tolerance test in mice. Am. J. Physiol. Endocrinol. Metab. 295(6), E1323–E1332 (2008). https://doi.org/10.1152/ajpendo.90617.2008

    Article  CAS  PubMed  Google Scholar 

  28. Iranloye, B.: Anti-diabetic and antioxidant effects of virgin coconut oil in alloxan induced diabetic male Sprague Dawley rats. J. Diabetes Mellitus. 3(04), 221 (2013)

    Article  Google Scholar 

  29. Reynés, B., Serrano, A., Petrov, P.D., Ribot, J., Chetrit, C., Martínez-Puig, D., Bonet, M.L., Palou, A.: Anti-obesity and insulin-sensitising effects of a glycosaminoglycan mix. J. Funct. Foods. 26, 350–362 (2016). https://doi.org/10.1016/j.jff.2016.07.022

    Article  CAS  Google Scholar 

  30. Talawar, S.T., Gangappa, K., Gurunathan, S., Mayookha, V.P., Gurusiddaiah, S.K.: Sterol Ferulate Rich Wheat Bran Oil Concentrate Prevents Liver Damage in MAFLD Mouse Model by Modulating FAS and PCSK9. ACS Food Sci. Technol. 1(4), 644–652 (2021). https://doi.org/10.1021/acsfoodscitech.0c00156

    Article  CAS  Google Scholar 

  31. Folch, J., Lees, M., Stanley, G.S.: A simple method for the isolation and purification of total lipides from animal tissues. J. Biol. Chem. 226(1), 497–509 (1957)

    Article  CAS  Google Scholar 

  32. Zak, B., Moss, N., Boyle, A.J., Zlatkis, A.: Reactions of certain unsaturated steroids with acid iron reagent. Anal. Chem. 26(4), 776–777 (1954). https://doi.org/10.1021/ac60088a058

    Article  CAS  Google Scholar 

  33. Irvin, J.L., Johnston, C.G., Kopala, J.: A photometric method for the determination of cholates in bile and blood. J. Biol. Chem. 153(2), 439–457 (1944)

    Article  CAS  Google Scholar 

  34. Bhaskaragoud, G., Geetha, V., Sharanappa, T., Kumar, A.S.M., Kumar, C.H., Kumar, G.S.: Hypolipidemic and Antioxidant Properties of Oryzanol Concentrate in Reducing Diabetic Nephropathy via SREBP1 Downregulation Rather than β-Oxidation. Mol. Nutr. Food Res. 62(8), e1700511–e1700511 (2018). https://doi.org/10.1002/mnfr.201700511

    Article  CAS  Google Scholar 

  35. de Barddal, O., Gracher, H.P., Simas-Tosin, A.H.P., Iacomini, F.F., Cipriani, M.: Anticoagulant activity of native and partially degraded glycoglucuronomannan after chemical sulfation. Int. J. Biol. Macromol. 80, 328–333 (2015). https://doi.org/10.1016/j.ijbiomac.2015.06.051

    Article  CAS  Google Scholar 

  36. Kumar, G.S., Shetty, A.K., Salimath, P.V.: Modulatory effect of bitter gourd (Momordica charantia LINN.) on alterations in kidney heparan sulfate in streptozotocin-induced diabetic rats. J. Ethnopharmacol. 115(2), 276–283 (2008). https://doi.org/10.1016/j.jep.2007.10.002

    Article  CAS  PubMed  Google Scholar 

  37. Gao, X., Zhang, Z., Sheng, W., Xue, C.: Determination of glycosaminoglycan in sea cucumber by HPLC with post column derivatization. Math. Phys. Fish. Sci. 9, 105–115 (2011)

    Google Scholar 

  38. Krichen, F., Karaoud, W., Sayari, N., Sila, A., Kallel, F., Ellouz-Chaabouni, S., Bougatef, A.: Sulfated Polysaccharides from Tunisian Fish Skins: Antioxidant, DNA Damage Protective Effect and Antihypertensive Activities. J. Polym. Environ. 24(2), 166–175 (2016). https://doi.org/10.1007/s10924-016-0759-6

    Article  CAS  Google Scholar 

  39. Puri, S., Coulson-Thomas, Y.M., Gesteira, T.F., Coulson-Thomas, V.J.: Distribution and function of glycosaminoglycans and proteoglycans in the development, homeostasis and pathology of the ocular surface. Front. Cell. Dev. Biol. 8, 731 (2020). https://doi.org/10.3389/fcell.2020.00731

    Article  PubMed  PubMed Central  Google Scholar 

  40. Vázquez, J.A., Rodríguez-Amado, I., Montemayor, M.I., Fraguas, J., González, M.D.P., Murado, M.A.: Chondroitin sulfate, hyaluronic acid and chitin/chitosan production using marine waste sources: Characteristics, applications and eco-friendly processes: A review. Mar. Drugs. 11(3), 747–774 (2013). https://doi.org/10.3390/md11030747

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Walsh, A.M., Sweeney, T., Bahar, B., O’Doherty, J.V.: Multi-functional roles of chitosan as a potential protective agent against obesity. PLOS one. 8(1) (2013). https://doi.org/10.1371/journal.pone.0053828 e53828

  42. Zhu, Z., Zhu, B., Sun, Y., Ai, C., Wang, L., Wen, C., Yang, J., Song, S., Liu, X.: Sulfated polysaccharide from sea cucumber and its depolymerized derivative prevent obesity in association with modification of gut microbiota in high-fat diet‐fed mice. Mol. Nutr. Food Res. 62(23), 1800446 (2018). https://doi.org/10.1002/mnfr.201800446

    Article  CAS  Google Scholar 

  43. Punarvasu, T.P., Prashanth, K.V.H.: Self-assembled chitosan derived microparticles inhibit tumor angiogenesis and induce apoptosis in Ehrlich-ascites-tumor bearing mice. Carbohydr. Polym. 278, 118941 (2022). https://doi.org/10.1016/j.carbpol.2021.118941

    Article  CAS  PubMed  Google Scholar 

  44. Zhang, Z., Zhou, Z., Li, Y., Zhou, L., Ding, Q., Xu, L.: Isolated exopolysaccharides from Lactobacillus rhamnosus GG alleviated adipogenesis mediated by TLR2 in mice. Sci. Rep. 6(1), 1–14 (2016). https://doi.org/10.1038/srep36083

    Article  CAS  Google Scholar 

  45. Park, M.K., Jung, U., Roh, C.: Fucoidan from marine brown algae inhibits lipid accumulation. Mar. Drugs. 9(8), 1359–1367 (2011). https://doi.org/10.3390/md9081359

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Gong, L., Zhang, H., Niu, Y., Chen, L., Liu, J., Alaxi, S., Shang, P., Yu, W., Yu, L.: A novel alkali extractable polysaccharide from Plantago asiatic L. seeds and its radical-scavenging and bile acid-binding activities. J. Agric. Food Chem. 63(2), 569–577 (2015). https://doi.org/10.1021/jf505909k

    Article  CAS  PubMed  Google Scholar 

  47. Shiming, H., Daorui, P., Xiong, L., Lijun, Y., Zhengang, Z., Peter, C.C., Mingwei, Z., Dong, L.: A sulfated polysaccharide from GracilariaLemaneiformis regulates cholesterol and bile acid metabolism in high-fat diet mice. Food Funct. 19(10), 3224–3236 (2019). https://doi.org/10.1039/C9FO00263D

    Article  Google Scholar 

  48. Kumar, A.M., Geetha, V., Kumar, G.S.: Impact of phenolic concentrate from tender coconut water and coconut testa on high fat cholesterol fed C57BL6 mice. J. Food Sci. Technol. 1–8 (2021). https://doi.org/10.1007/s13197-021-05138-w

  49. Priyadarshini, M., Wicksteed, B., Schiltz, G.E., Gilchrist, A., Layden, B.T.: SCFA receptors in pancreatic β cells: novel diabetes targets? Trends Endocrinol. Metab. 27(9), 653–664 (2016). https://doi.org/10.1016/j.tem.2016.03.011

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Sumiyoshi, M., Kimura, Y.: Low molecular weight chitosan inhibits obesity induced by feeding a high-fat diet long‐term in mice. J. Pharm. Pharmacol. 58(2), 201–207 (2006). https://doi.org/10.1211/jpp.58.2.0007

    Article  CAS  PubMed  Google Scholar 

  51. Lairon, D., Lafont, H., Vigne, J.L., Nalbone, G., Léonardi, J., Hauton, J.C.: Effects of dietary fibers and cholestyramine on the activity of pancreatic lipase in vitro. Am. J. Clin. Nutr. 42(4), 629–638 (1985). https://doi.org/10.1093/ajcn/42.4.629

    Article  CAS  PubMed  Google Scholar 

  52. Houghton, D., Wilcox, M.D., Chater, P.I., Brownlee, I.A., Seal, C.J., Pearson, J.P.: Biological activity of alginate and its effect on pancreatic lipase inhibition as a potential treatment for obesity. Food Hydrocoll. 49, 18–24 (2015). https://doi.org/10.1016/j.foodhyd.2015.02.019

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Aguilera-Angel, E.Y., Espinal-Ruiz, M., Narváez-Cuenca, C.E.: Pectic polysaccharides with different structural characteristics as inhibitors of pancreatic lipase. Food Hydrocoll. 83, 229–238 (2018). https://doi.org/10.1016/j.foodhyd.2018.05.009

    Article  CAS  Google Scholar 

  54. Gao, J., Lin, L., Sun, B., Zhao, M.: Comparison study on polysaccharide fractions from Laminaria japonica: Structural characterization and bile acid binding capacity. J. Agric. Food Chem. 65(44), 9790–9798 (2017). https://doi.org/10.1021/acs.jafc.7b04033

    Article  CAS  PubMed  Google Scholar 

  55. Long, H., Gu, X., Zhou, N., Zhu, Z., Wang, C., Liu, X., Zhao, M.: Physicochemical characterization and bile acid-binding capacity of water-extract polysaccharides fractionated by stepwise ethanol precipitation from Caulerpa lentillifera. Int. J. Biol. Macromol. 150, 654–661 (2020). https://doi.org/10.1016/j.ijbiomac.2020.02.121

    Article  CAS  PubMed  Google Scholar 

  56. Yang, Y., Zhao, M., Lin, L.: Effects of extraction methods on structural characteristics and bile acid-binding capacities of Moringa oleifera leaf polysaccharide fractions. Int. J. Food Sci. Technol. 55(4), 1539–1546 (2020). https://doi.org/10.1111/ijfs.14430

    Article  CAS  Google Scholar 

  57. Ohtomo, T.: Interaction between bile acids and staphylococcal polysaccharide: inhibition of capsule formation in encapsulated mutant strains (taurine+, taurine–) of Staphylococcus aureus. Can. J. Microbiol. 29(12), 1653–1660 (1983)

    Article  CAS  Google Scholar 

  58. Yu, G., Yue, C., Zang, X., Chen, C., Dong, L., Liu, Y.: Purification, characterization and in vitro bile salt-binding capacity of polysaccharides from Armillaria mellea mushroom. Czech J. Food Sci. 37(1), 51–56 (2019). https://doi.org/10.17221/182/2018-CJFS

    Article  CAS  Google Scholar 

  59. Song, G., Huang, Y., Xiong, M., Yang, Z., Liu, Q., Shen, J., Zhao, P., Yang, X.: Aloperine relieves Type 2 diabetes mellitus via enhancing GLUT4 expression and translocation. Front. Pharmacol. 11, 2267 (2021). https://doi.org/10.3389/fphar.2020.561956

    Article  CAS  Google Scholar 

  60. Chen, Y., Liu, Y., Sarker, M.M.R., Yan, X., Yang, C., Zhao, L., Lv, X., Liu, B., Zhao, C.: Structural characterization and antidiabetic potential of a novel heteropolysaccharide from Grifola frondosa via IRS1/PI3K-JNK signaling pathways. Carbohydr. Polym. 198, 452–461 (2018). https://doi.org/10.1016/j.carbpol.2018.06.077

    Article  CAS  PubMed  Google Scholar 

  61. Shang, Q., Saumoy, M., Holst, J.J., Salen, G., Xu, G.: Colesevelam improves insulin resistance in a diet-induced obesity (F-DIO) rat model by increasing the release of GLP-1. Am. J. Physiol. Gastrointest. Liver Physiol. 298(3), G419–G424 (2010). https://doi.org/10.1152/ajpgi.00362.2009

    Article  CAS  Google Scholar 

  62. Prawitt, J., Staels, B.: Bile acid sequestrants: glucose-lowering mechanisms. Metab Syndr Relat Disord. 8(S1), S-3 (2010). https://doi.org/10.1089/met.2010.0096

  63. Kobayashi, M., Ikegami, H., Fujisawa, T., Nojima, K., Kawabata, Y., Noso, S., Naru, B., Michiko, I., Kaori, Y., Yoshihisa, H., Masao, S., Ogihara, T.: Prevention and treatment of obesity, insulin resistance, and diabetes by bile acid–binding resin. Diabetes. 56(1), 239–247 (2007). https://doi.org/10.2337/db06-0353

    Article  CAS  PubMed  Google Scholar 

  64. Huang, X., Tang, J., Zhou, Q., Lu, H., Wu, Y., Wu, W.: Polysaccharide from fuzi (FPS) prevents hypercholesterolemia in rats. Lipids Health Dis. 9(1), 1–7 (2010). https://doi.org/10.1186/1476-511X-9-9

    Article  CAS  Google Scholar 

  65. Cheng, Y., Tang, K., Wu, S., Liu, L., Qiang, C., Lin, X., Liu, B.: Astragalus polysaccharides lowers plasma cholesterol through mechanisms distinct from statins. PloS one. 6(11), e27437 (2011). https://doi.org/10.1371/journal.pone.0027437

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Duan, Y., Chen, Y., Hu, W., Li, X., Yang, X., Zhou, X., Zhinan, Y., Deling, K., Yao, Z., Hajjar, D.P., Liu, L., Liu, Q., Han, J.: Peroxisome proliferator-activated receptor γ activation by ligands and dephosphorylation induces proprotein convertase subtilisin kexin type 9 and low density lipoprotein receptor expression. J. Biol. Chem. 287(28), 23667–23677 (2012). https://doi.org/10.1074/jbc.M112.350181

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Chiang, J.Y.L., Ferrell, J.M.: Bile acid receptors FXR and TGR5 signaling in fatty liver diseases and therapy. Am. J. Physiol. Gastrointest. Liver Physiol. 318(3), G554–G573 (2020). https://doi.org/10.1152/ajpgi.00223.2019

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

The authors would like to thank the Director, CSIR-Central Food Technological Research Institute, Mysuru, India, for constant support and encourage, also acknowledgement goes to Vijnana Bhavana-a central instrumentation facility as Institution of Excellence (IOE) of University of Mysore, Mysuru for the Scanning Electron Microscopy facility.

Funding

Author Geetha V would like to thank Indian Council of Medical Research, New Delhi for ICMR-SRF Fellowship (Grant # 3/1/2/94/2018-Nut). Fund for the work is supported by the MLP-245 and GAP-561.

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Animal experiment was conducted in male C57BL/6 mice (20-22 g). The animal studies had the Institutional Animal Ethics committee clearance (IAEC #150/2019), it was cleared from CSIR-CFTRI, Mysuru. Animal procedures were performed in compliance with 3R’s ethical rules which are followed in animal experimentation. Sincere efforts were made to minimize the suffering, and the numbers of animals were maintained to get the statistical data comparisons.

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V, G., Das, M., Zarei, M. et al. Studies on the partial characterization of extracted glycosaminoglycans from fish waste and its potentiality in modulating obesity through in-vitro and in-vivo. Glycoconj J 39, 525–542 (2022). https://doi.org/10.1007/s10719-022-10077-5

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