Fisheries and Aquatic Sciences

The Korean Society of Fisheries and Aquatic Science (한국수산과학회)
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Extracts of abalone intestine regulates fat metabolism in 3T3-L1 adipocytes and high fat diet-induced zebrafish larvae

  • Laxmi Sen Thakuri (Department of Nutrapharmaceutical Resources, Mokpo National University) ;
  • Chul Min Park (Department of Nutrapharmaceutical Resources, Mokpo National University) ;
  • Jin Yeong Choi (Department of Biomedicine, Health & Life Convergence Sciences, BK21 FOUR, Mokpo National University) ;
  • Hyeon-A Kim (Department of Food and Nutrition, Mokpo National University) ;
  • Han Kyu Lim (Department of Biomedicine, Health & Life Convergence Sciences, BK21 FOUR, Mokpo National University) ;
  • Jin Woo Park (Department of Biomedicine, Health & Life Convergence Sciences, BK21 FOUR, Mokpo National University) ;
  • Dong Wook Kim (Department of Nutrapharmaceutical Resources, Mokpo National University) ;
  • Dong Young Rhyu (Department of Nutrapharmaceutical Resources, Mokpo National University)
  • Received : 2023.12.03
  • Accepted : 2024.01.24
  • Published : 2024.02.29
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Abstract

Obesity is a disease involving mechanisms of fat accumulation, low-grade inflammatory cytokine release, and mitochondrial dysfunction. The aim of the current study was to investigate the effects of abalone intestine extract on fat metabolism in 3T3-L1 adipocytes and high fat diet-induced zebrafish larvae. The total phenol content was highest in subcritical water extract at 210℃ (SW210) among hot water, ethanol, and subcritical water extracts of abalone intestine. In addition, SW210 of male abalone intestine (MASW210) most effectively controlled the lipid accumulation and expression of adipogenic or lipogenic regulators (PPAR-γ, C/EBPα, SREBP-1c, and FAS) in 3T3-L1 adipocytes. Likewise, in zebrafish larvae fed high fat, MASW210 significantly suppressed body weight, glucose levels, and lipid accumulation. The mRNA expression related to adipogenesis (PPAR-γ and C/EBPα), lipogenesis (SREBP-1c and FAS), inflammatory cytokines (TNF-α and IL-6), energy m/;.etabolism (AMPK, lepr, SIRT1, and adiponectin), and mitochondrial biogenesis (PGC-1α and CPT-1) were significantly regulated by treatment with MASW210. These results suggest that abalone intestine extract such as MASW210, are useful biomaterials for improving obesity and metabolic diseases.

Keywords

Acknowledgement

This work was supported by Research Funds of Sabbatical Year of Mokpo National University in 2022.

References

  1. Achari AE, Jain SK. Adiponectin, a therapeutic target for obesity, diabetes, and endothelial dysfunction. Int J Mol Sci. 2017;18:1321.
  2. Alkhatib A, Tsang C, Tiss A, Bahorun T, Arefanian H, Barake R, et al. Functional foods and lifestyle approaches for diabetes prevention and management. Nutrients. 2017;9:1310.
  3. Bullon N, Seyfoddin A, Alfaro AC. The role of aquafeeds in abalone nutrition and health: a comprehensive review. J World Aquac Soc. 2022;54:7-31. https://doi.org/10.1111/jwas.12883
  4. Cheng M, Liu M, Chang L, Liu Q, Wang C, Hu L, et al. Overview of structure, function and integrated utilization of marine shell. Sci Total Environ. 2023;870:161950.
  5. Cheng Y, Xue F, Yu S, Du S, Yang Y. Subcritical water extraction of natural products. Molecules. 2021;26:4004.
  6. Cook PA. The international abalone market. Dev Aquac Fisher Sci. 2023;42:373-82. https://doi.org/10.1016/B978-0-12-814938-6.00013-0
  7. De Zoysa M. Nutritional value, bioactive compounds, and health promoting properties of abalone. In: Kim SK, editor. Marine nutraceuticals: prospects and perspectives. Boca Raton, FL, CRC Press; 2013. p. 57-70.
  8. Den Broeder MJ, Moester MJB, Kamstra JH, Cenijn PH, Davidoiu V, Kamminga LM, et al. Altered adipogenesis in zebrafish larvae following high fat diet and chemical exposure is visualised by stimulated Raman scattering microscopy. Int J Mol Sci. 2017;18:894.
  9. Du J, Zhao L, Kang Q, He Y, Bi Y. An optimized method for Oil Red O staining with the salicylic acid ethanol solution. Adipocyte. 2023;12:2179334.
  10. Fontecha-Barriuso M, Martin-Sanchez D, Martinez-Moreno JM, Monsalve M, Ramos AM, Sanchez-Nino MD, et al. The role of PGC-1α and mitochondrial biogenesis in kidney diseases. Biomolecules. 2020;10:347.
  11. Goransson O, Kopietz F, Rider MH. Metabolic control by AMPK in white adipose tissue. Trends Endocrinol Metab. 2023;34(11):704-17. https://doi.org/10.1016/j.tem.2023.08.011
  12. Grahame Hardie D, Ross FA, Hawley SA. AMPK: a nutrient and energy sensor that maintains energy homeostasis. Nat Rev Mol Cell Biol. 2012;13:251-62.
  13. Green M, Arora K, Prakash S. Microbial medicine: prebiotic and probiotic functional foods to target obesity and metabolic syndrome. Int J Mol Sci. 2020;21:2890.
  14. Jakab J, Miskic B, Miksic S, Juranic B, Cosic V, Schwarz D, et al. Adipogenesis as a potential anti-obesity target: a review of pharmacological treatment and natural products. Diabetes Metab Syndr Obes. 2021;14:67-83. https://doi.org/10.2147/DMSO.S281186
  15. Kang NH, Mukherjee S, Min T, Kang SC, Yun JW. Trans-anethole ameliorates obesity via induction of browning in white adipocytes and activation of brown adipocytes. Biochimie. 2018;151:1-13. https://doi.org/10.1016/j.biochi.2018.05.009
  16. Khan BM, Liu Y. Marine mollusks: food with benefits. Compr Rev Food Sci Food Saf. 2019;18:548-64. https://doi.org/10.1111/1541-4337.12429
  17. Kojta I, Chacinska M, Blachnio-Zabielska A. Obesity, bioactive lipids, and adipose tissue inflammation in insulin resistance. Nutrients. 2020;12:1305.
  18. Kwon J, Kim B, Lee C, Joung H, Kim BK, Choi IS, et al. Comprehensive amelioration of high-fat diet-induced metabolic dysfunctions through activation of the PGC-1α pathway by probiotics treatment in mice. PLOS ONE. 2020;15:e0228932.
  19. Lee H, Zandkarimi F, Zhang Y, Meena JK, Kim J, Zhuang L, et al. Energy-stress-mediated AMPK activation inhibits ferroptosis. Nat Cell Biol. 2020;22:225-34. https://doi.org/10.1038/s41556-020-0461-8
  20. Lee HB, Jang HS, Oh YD, Lee YH, Lim HK. Analysis of the physiological responses of Pacific abalone (Haliotis discus hannai) to various stressors to identify a suitable stress indicator. J World Aquac Soc. 2023;54:1407-26. https://doi.org/10.1111/jwas.12969
  21. Li H, Ren J, Li Y, Wu Q, Wei J. Oxidative stress: the nexus of obesity and cognitive dysfunction in diabetes. Front Endocrinol. 2023;14:1134025.
  22. Lin D, Xiao M, Zhao J, Li Z, Xing B, Li X, et al. An overview of plant phenolic compounds and their importance in human nutrition and management of type 2 diabetes. Molecules. 2016;21:1374.
  23. Long YC, Zierath JR. AMP-activated protein kinase signaling in metabolic regulation. J Clin Invest. 2006;116:1776-83. https://doi.org/10.1172/JCI29044
  24. Mariani S, Di Giorgio MR, Rossi E, Tozzi R, Contini S, Bauleo L, et al. Blood SIRT1 shows a coherent association with leptin and adiponectin in relation to the degree and distribution of adiposity: a study in obesity, normal weight and anorexia nervosa. Nutrients. 2020;12:3506.
  25. Nguyen MHT, Qian ZJ, Jung WK. Beneficial effect of abalone intestine gastro-intestinal digests on osteoblastic MG-63 cell differentiation. J Aquat Food Prod Technol. 2014;23:436-46. https://doi.org/10.1080/10498850.2012.721874
  26. Nguyen PH, Kim SA, Choi IW, Jung WK. Protective effects of in vitro gastrointestinal digests of abalone (Haliotis discus hannai) intestines against oxidative stress in RAW264.7 macrophage cells. Fish Aquat Sci. 2010;13:216-23.
  27. Obradovic M, Sudar-Milovanovic E, Soskic S, Essack M, Arya S, Stewart AJ, et al. Leptin and obesity: role and clinical implication. Front Endocrinol. 2021;12:585887.
  28. Park CJ, Kim SY. Abalone aquaculture in Korea. J Shellfish Res. 2013;32:17-9. https://doi.org/10.2983/035.032.0104
  29. Qian ZJ, Kim SA, Lee JS, Kim HJ, Choi IW, Jung WK. The antioxidant and anti-inflammatory effects of abalone intestine digest, Haliotis discus hannai in RAW 264.7 macrophages. Biotechnol Bioprocess Eng. 2012;17:475-84. https://doi.org/10.1007/s12257-011-0544-2
  30. Rahman MM, Rahaman MS, Islam MR, Rahman F, Mithi FM, Alqahtani T, et al. Role of phenolic compounds in human disease: current knowledge and future prospects. Molecules. 2021;27:233.
  31. Romulo A. Extraction of phenolic compounds using subcritical hot water extraction: a review. IOP Conf Ser Earth Environ Sci. 2020;426:012173.
  32. Roy B, Palaniyandi SS. Tissue-specific role and associated downstream signaling pathways of adiponectin. Cell Biosci. 2021;11:77.
  33. Ruiz-Ojeda FJ, Olza J, Gil A, Aguilera CM. Oxidative stress and inflammation in obesity and metabolic syndrome. In: Moral AM, Garcia CMA, editors. Obesity: oxidative stress and dietary antioxidants. Cambridge, MA: Academic Press; 2018. p. 1-15.
  34. Rumbaoa RGO, Cornago DF, Geronimo IM. Phenolic content and antioxidant capacity of Philippine sweet potato (Ipomoea batatas) varieties. Food Chem. 2009;113:1133-8. https://doi.org/10.1016/j.foodchem.2008.08.088
  35. Salminen A, Hyttinen JMT, Kaarniranta K. AMP-activated protein kinase inhibits NF-κB signaling and inflammation: impact on healthspan and lifespan. J Mol Med. 2011;89:667-76. https://doi.org/10.1007/s00109-011-0748-0
  36. Shin TS, Choi KS, Chun J, Kho KH, Son SA, Shim SY. Anti-inflammatory effects of abalone (Haliotis discus hannai) viscera via inhibition of ROS production in LPS stimulated RAW 264.7 cells. Microbiol Biotechnol Lett. 2022;50:22-30. https://doi.org/10.48022/mbl.2109.09005
  37. Singh A, Hardin BI, Singh D, Keyes D. Epidemiologic and etiologic considerations of obesity. In: Abai B, editor. StatPearls. Treasure Island, FL: StatPearls; 2023.
  38. Thakuri LS, Kim JE, Choi JY, Rhyu DY. Protective effect of Capsosiphon fulvescens on oxidative stress-stimulated neurodegenerative dysfunction of PC12 cells and zebrafish larva models. Fish Aquat Sci. 2023a;26:24-34. https://doi.org/10.47853/FAS.2023.e2
  39. Thakuri LS, Park CM, Park JW, Kim HA, Rhyu DY. Subcritical water extraction of Gracilaria chorda abbreviates lipid accumulation and obesity-induced inflammation. Algae. 2023b;38:81-92. https://doi.org/10.4490/algae.2023.38.12.26
  40. Thakuri LS, Park CM, Rhyu DY. Gracilaria chorda subcritical-water extracts as ameliorant of insulin resistance induced by high-glucose in zebrafish and dexamethasone in L6 myotubes. J Tradit Complement Med. 2023c;14:82-90. https://doi.org/10.1016/j.jtcme.2023.07.006
  41. Troell M, Robertson-Andersson D, Anderson RJ, Bolton JJ, Maneveldt G, Halling C, et al. Abalone farming in South Africa: an overview with perspectives on kelp resources, abalone feed, potential for on-farm seaweed production and socio-economic importance. Aquaculture. 2006;257:266-81. https://doi.org/10.1016/j.aquaculture.2006.02.066
  42. Wang L, Yao Y, Zhao Z, Li L, Gan H, Desouky H, et al. Effect of dietary protein, vitamin E, and vitamin C levels on the growth and gonad development of hybrid male abalone (Haliotis fulgens ♂ × H. discus hannai ♀) by the orthogonal array design. Aquac Int. 2023:1-23.
  43. Wang S, Sheng H, Bai Y, Weng Y, Fan X, Lou L, et al. Neohesperidin enhances PGC-1α-mediated mitochondrial biogenesis and alleviates hepatic steatosis in high fat diet fed mice. Nutr Diabetes. 2020;10:27.
  44. Wang Q, Sun J, Liu M, Zhou Y, Zhang L, Li Y. The new role of AMP-activated protein kinase in regulating fat metabolism and energy expenditure in adipose tissue. Biomolecules. 2021;11:1757.
  45. Wen X, Zhang B, Wu B, Xiao H, Li Z, Li R, et al. Signaling pathways in obesity: mechanisms and therapeutic interventions. Signal Transduct Target Ther. 2022;7:298.
  46. Yen GC, Cheng HL, Lin LY, Chen SC, Hsu CL. The potential role of phenolic compounds on modulating gut microbiota in obesity. J Food Drug Anal. 2020;28:195-205. https://doi.org/10.38212/2224-6614.1054
  47. Ylli D, Sidhu S, Parikh T, Burman KD. Endocrine changes in obesity [Internet].2022 [cited 2023 Sep 2]. https://www.ncbi.nlm.nih.gov/books/NBK279053/
  48. Yu W, Lu Y, Shen Y, Liu J, Gong S, Yu F, et al. Exploring the intestinal microbiota and metabolome profiles associated with feed efficiency in Pacific abalone (Haliotis discus hannai). Front Microbiol. 2022;13:852460.
  49. Zhang L, Qin Y, Liang D, Li L, Liang Y, Chen L, et al. Association of polymorphisms in LEPR with type 2 diabetes and related metabolic traits in a Chinese population. Lipids Health Dis. 2018;17:2.
  50. Zheng P, Hao G, Weng W, Ren H. Antioxidant activities of hydrolysates from abalone viscera using subcritical water-assisted enzymatic hydrolysis. Food Bioprocess Technol. 2019;12:910-8. https://doi.org/10.1007/s11947-019-02270-6