Hostname: page-component-5d59c44645-lfgmx Total loading time: 0 Render date: 2024-03-02T08:03:05.970Z Has data issue: false hasContentIssue false

Dietary palm oil enhances Sterol regulatory element-binding protein 2-mediated cholesterol biosynthesis through inducing endoplasmic reticulum stress in muscle of large yellow croaker (Larimichthys crocea)

Published online by Cambridge University Press:  13 September 2023

Zengqi Zhao
Affiliation:
Key Laboratory of Aquaculture Nutrition and Feed (Ministry of Agriculture and Rural Affairs), Ocean University of China, 5 Yushan Road, Qingdao, Shandong 266003, People’s Republic of China
Baolin Li
Affiliation:
Key Laboratory of Aquaculture Nutrition and Feed (Ministry of Agriculture and Rural Affairs), Ocean University of China, 5 Yushan Road, Qingdao, Shandong 266003, People’s Republic of China
Qiang Chen
Affiliation:
Key Laboratory of Aquaculture Nutrition and Feed (Ministry of Agriculture and Rural Affairs), Ocean University of China, 5 Yushan Road, Qingdao, Shandong 266003, People’s Republic of China
Xiaojun Xiang
Affiliation:
Key Laboratory of Aquaculture Nutrition and Feed (Ministry of Agriculture and Rural Affairs), Ocean University of China, 5 Yushan Road, Qingdao, Shandong 266003, People’s Republic of China
Xiang Xu
Affiliation:
Key Laboratory of Aquaculture Nutrition and Feed (Ministry of Agriculture and Rural Affairs), Ocean University of China, 5 Yushan Road, Qingdao, Shandong 266003, People’s Republic of China
Shangzhe Han
Affiliation:
Key Laboratory of Aquaculture Nutrition and Feed (Ministry of Agriculture and Rural Affairs), Ocean University of China, 5 Yushan Road, Qingdao, Shandong 266003, People’s Republic of China
Wencong Lai
Affiliation:
Key Laboratory of Aquaculture Nutrition and Feed (Ministry of Agriculture and Rural Affairs), Ocean University of China, 5 Yushan Road, Qingdao, Shandong 266003, People’s Republic of China
Yueru Li
Affiliation:
Key Laboratory of Aquaculture Nutrition and Feed (Ministry of Agriculture and Rural Affairs), Ocean University of China, 5 Yushan Road, Qingdao, Shandong 266003, People’s Republic of China
Wei Xu
Affiliation:
Key Laboratory of Aquaculture Nutrition and Feed (Ministry of Agriculture and Rural Affairs), Ocean University of China, 5 Yushan Road, Qingdao, Shandong 266003, People’s Republic of China
Kangsen Mai
Affiliation:
Key Laboratory of Aquaculture Nutrition and Feed (Ministry of Agriculture and Rural Affairs), Ocean University of China, 5 Yushan Road, Qingdao, Shandong 266003, People’s Republic of China Laboratory for Marine Fisheries Science and Food Production Processes, Qingdao National Laboratory for Marine Science and Technology, 1 Wenhai Road, Qingdao, Shandong 266237, People’s Republic of China
Qinghui Ai*
Affiliation:
Key Laboratory of Aquaculture Nutrition and Feed (Ministry of Agriculture and Rural Affairs), Ocean University of China, 5 Yushan Road, Qingdao, Shandong 266003, People’s Republic of China Laboratory for Marine Fisheries Science and Food Production Processes, Qingdao National Laboratory for Marine Science and Technology, 1 Wenhai Road, Qingdao, Shandong 266237, People’s Republic of China
*
*Corresponding author: Qinghui Ai, email qhai@ouc.edu.cn

Abstract

Sterol regulatory element-binding protein 2 (SREBP2) is considered to be a major regulator to control cholesterol homoeostasis in mammals. However, the role of SREBP2 in teleost remains poorly understand. Here, we explored the molecular characterisation of SREBP2 and identified SREBP2 as a key modulator for 3-hydroxy-3-methylglutaryl-coenzyme A reductase and 7-dehydrocholesterol reductase, which were rate-limiting enzymes of cholesterol biosynthesis. Moreover, dietary palm oil in vivo or palmitic acid (PA) treatment in vitro elevated cholesterol content through triggering SREBP2-mediated cholesterol biosynthesis in large yellow croaker. Furthermore, our results also found that PA-induced activation of SREBP2 was dependent on the stimulating of endoplasmic reticulum stress (ERS) in croaker myocytes and inhibition of ERS by 4-Phenylbutyric acid alleviated PA-induced SREBP2 activation and cholesterol biosynthesis. In summary, our findings reveal a novel insight for understanding the role of SREBP2 in the regulation of cholesterol metabolism in fish and may deepen the link between dietary fatty acid and cholesterol biosynthesis.

Type
Research Article
Copyright
© The Author(s), 2023. Published by Cambridge University Press on behalf of The Nutrition Society

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Luo, J, Yang, H & Song, B-L (2020) Mechanisms and regulation of cholesterol homeostasis. Nat Rev Mol Cell Biol 21, 225245.CrossRefGoogle ScholarPubMed
Soccio, RE & Breslow, JL (2004) Intracellular cholesterol transport. Arterioscler Thromb Vasc Biol 24, 11501160.CrossRefGoogle ScholarPubMed
Sezgin, E, Levental, I, Mayor, S, et al. (2017) The mystery of membrane organization: composition, regulation and roles of lipid rafts. Nat Rev Mol Cell Biol 18, 361374.CrossRefGoogle ScholarPubMed
Chen, L, Chen, XW, Huang, X, et al. (2019) Regulation of glucose and lipid metabolism in health and disease. Sci China Life Sci 62, 14201458.CrossRefGoogle ScholarPubMed
Porter, JA, Young, KE & Beachy, PA (1996) Cholesterol modification of hedgehog signaling proteins in animal development. Science 274, 255259.CrossRefGoogle ScholarPubMed
Xiao, X, Tang, J-J, Peng, C, et al. (2017) Cholesterol modification of smoothened is required for hedgehog signaling. Mol cell 66, 154162.e110.CrossRefGoogle ScholarPubMed
Subczynski, WK, Pasenkiewicz-Gierula, M, Widomska, J, et al. (2017) High cholesterol/low cholesterol: effects in biological membranes: a review. Cell Biochem Biophys 75, 369385.CrossRefGoogle ScholarPubMed
Cerqueira, NM, Oliveira, EF, Gesto, DS, et al. (2016) Cholesterol biosynthesis: a mechanistic overview. Biochemistry 55, 54835506.CrossRefGoogle ScholarPubMed
Lu, X-Y, Shi, X-J, Hu, A, et al. (2020) Feeding induces cholesterol biosynthesis via the mTORC1–USP20–HMGCR axis. Nature 588, 479484.CrossRefGoogle ScholarPubMed
Brown, MS, Radhakrishnan, A & Goldstein, JL (2018) Retrospective on cholesterol homeostasis: the central role of scap. Annu Rev Biochem 87, 783.CrossRefGoogle ScholarPubMed
Radhakrishnan, A, Goldstein, JL, McDonald, JG, et al. (2008) Switch-like control of SREBP-2 transport triggered by small changes in ER cholesterol: a delicate balance. Cell Metab 8, 512521.CrossRefGoogle ScholarPubMed
Fukumitsu, S, Villareal, MO, Onaga, S, et al. (2013) α-Linolenic acid suppresses cholesterol and triacylglycerol biosynthesis pathway by suppressing SREBP-2, SREBP-1a and-1c expression. Cytotechnology 65, 899907.CrossRefGoogle ScholarPubMed
Leaver, MJ, Villeneuve, LA, Obach, A, et al. (2008) Functional genomics reveals increases in cholesterol biosynthetic genes and highly unsaturated fatty acid biosynthesis after dietary substitution of fish oil with vegetable oils in Atlantic salmon (Salmo salar). BMC Genomics 9, 115.CrossRefGoogle ScholarPubMed
Cleveland, BM, Gao, G, Radler, LM, et al. (2021) Hepatic fatty acid and transcriptome profiles during the transition from vegetable-to fish oil-based diets in rainbow trout (Oncorhynchus mykiss). Lipids 56, 189200.CrossRefGoogle ScholarPubMed
Cao, X, Fang, W, Li, J, et al. (2023) Long noncoding RNA lincsc5d regulates hepatic cholesterol synthesis by modulating sterol C5 desaturase in large yellow croaker. Comp Biochem Physiol B: Biochem Mol Biol 263, 110800.CrossRefGoogle ScholarPubMed
Song, Y, Liu, J, Zhao, K, et al. (2021) Cholesterol-induced toxicity: an integrated view of the role of cholesterol in multiple diseases. Cell Metab 33, 19111925.CrossRefGoogle ScholarPubMed
Li, X, Ji, R, Cui, K, et al. (2019) High percentage of dietary palm oil suppressed growth and antioxidant capacity and induced the inflammation by activation of TLR-NF-κB signaling pathway in large yellow croaker (Larimichthys crocea). Fish Shellfish Immunol 87, 600608.CrossRefGoogle ScholarPubMed
Kwon, B, Lee, HK & Querfurth, HW (2014) Oleate prevents palmitate-induced mitochondrial dysfunction, insulin resistance and inflammatory signaling in neuronal cells. Biochim Biophys Acta 1843, 14021413.CrossRefGoogle ScholarPubMed
Calvo-Ochoa, E, Sanchez-Alegria, K, Gomez-Inclan, C, et al. (2017) Palmitic acid stimulates energy metabolism and inhibits insulin/PI3K/AKT signaling in differentiated human neuroblastoma cells: the role of mTOR activation and mitochondrial ROS production. Neurochem Int 110, 7583.CrossRefGoogle ScholarPubMed
Pascual, G, Dominguez, D, Elosua-Bayes, M, et al. (2021) Dietary palmitic acid promotes a prometastatic memory via Schwann cells. Nature 599, 485490.CrossRefGoogle ScholarPubMed
Lin, L, Ding, Y, Wang, Y, et al. (2017) Functional lipidomics: palmitic acid impairs hepatocellular carcinoma development by modulating membrane fluidity and glucose metabolism. Hepatology 66, 432448.CrossRefGoogle ScholarPubMed
Yuan, L, Mao, Y, Luo, W, et al. (2017) Palmitic acid dysregulates the Hippo–YAP pathway and inhibits angiogenesis by inducing mitochondrial damage and activating the cytosolic DNA sensor cGAS–STING–IRF3 signaling mechanism. J Biol Chem 292, 1500215015.CrossRefGoogle ScholarPubMed
Chen, L, Zhang, Q, Meng, Y, et al. (2023) Saturated fatty acids increase LPI to reduce FUNDC1 dimerization and stability and mitochondrial function. EMBO Rep 24, e54731.CrossRefGoogle ScholarPubMed
Fernández, A, Llacuna, L, Fernández-Checa, JC, et al. (2009) Mitochondrial cholesterol loading exacerbates amyloid β peptide-induced inflammation and neurotoxicity. J Neurosci 29, 63946405.CrossRefGoogle ScholarPubMed
Korbecki, J & Bajdak-Rusinek, K (2019) The effect of palmitic acid on inflammatory response in macrophages: an overview of molecular mechanisms. Inflammation Res 68, 915932.CrossRefGoogle ScholarPubMed
Westerterp, M, Gautier, EL, Ganda, A, et al. (2017) Cholesterol accumulation in dendritic cells links the inflammasome to acquired immunity. Cell Metab 25, 12941304.e1296.CrossRefGoogle ScholarPubMed
Cao, X, Fang, W, Li, X, et al. (2022) Increased LDL receptor by SREBP2 or SREBP2-induced lncRNA LDLR-AS promotes triglyceride accumulation in fish. iScience 25, 104670.CrossRefGoogle ScholarPubMed
Gu, Y & Yin, J (2020) Saturated fatty acids promote cholesterol biosynthesis: effects and mechanisms. Obes Med 18, 100201.CrossRefGoogle Scholar
Natali, F, Siculella, L, Salvati, S, et al. (2007) Oleic acid is a potent inhibitor of fatty acid and cholesterol synthesis in C6 glioma cells. J Lipid Res 48, 19661975.CrossRefGoogle ScholarPubMed
Priore, P, Gnoni, A, Natali, F, et al. (2017) Oleic acid and hydroxytyrosol inhibit cholesterol and fatty acid synthesis in C6 glioma cells. Oxid Med Cell Longevity 2017, 9076052.CrossRefGoogle ScholarPubMed
Horrobin, D & Huang, Y-S (1987) The role of linoleic acid and its metabolites in the lowering of plasma cholesterol and the prevention of cardiovascular disease. Int J Cardiol 17, 241255.CrossRefGoogle ScholarPubMed
Prabhu, AV, Sharpe, LJ & Brown, AJ (2014) The sterol-based transcriptional control of human 7-dehydrocholesterol reductase (DHCR7): evidence of a cooperative regulatory program in cholesterol synthesis. Biochim Biophys Acta (BBA)-Molecular Cell Biol Lipids 1841, 14311439.Google Scholar
Madison, BB (2016) Srebp2: a master regulator of sterol and fatty acid synthesis1. J Lipid Res 57, 333335.CrossRefGoogle Scholar
Radhakrishnan, A, Ikeda, Y, Kwon, HJ, et al. (2007) Sterol-regulated transport of SREBPs from endoplasmic reticulum to Golgi: oxysterols block transport by binding to Insig. Proc Natl Acad Sci 104, 65116518.CrossRefGoogle Scholar
Adams, CM, Reitz, J, De Brabander, JK, et al. (2004) Cholesterol and 25-hydroxycholesterol inhibit activation of SREBPs by different mechanisms, both involving SCAP and Insigs. J Biol Chem 279, 5277252780.CrossRefGoogle ScholarPubMed
Radhakrishnan, A, Sun, L-P, Kwon, HJ, et al. (2004) Direct binding of cholesterol to the purified membrane region of SCAP: mechanism for a sterol-sensing domain. Mol Cell 15, 259268.CrossRefGoogle Scholar
Oteng, AB, Loregger, A, van Weeghel, M, et al. (2019) Industrial trans fatty acids stimulate SREBP2-mediated cholesterogenesis and promote non-alcoholic fatty liver disease. Mol Nutr Food Res 63, 1900385.CrossRefGoogle ScholarPubMed
Yin, J, Wang, Y, Gu, L, et al. (2015) Palmitate induces endoplasmic reticulum stress and autophagy in mature adipocytes: implications for apoptosis and inflammation. Int J Mol Med 35, 932940.CrossRefGoogle ScholarPubMed
Zou, L, Li, X, Wu, N, et al. (2017) Palmitate induces myocardial lipotoxic injury via the endoplasmic reticulum stress-mediated apoptosis pathway. Mol Med Rep 16, 69346939.CrossRefGoogle ScholarPubMed
Ariyama, H, Kono, N, Matsuda, S, et al. (2010) Decrease in membrane phospholipid unsaturation induces unfolded protein response. J Biol Chem 285, 2202722035.CrossRefGoogle ScholarPubMed
Wei, Y, Wang, D, Gentile, CL, et al. (2009) Reduced endoplasmic reticulum luminal calcium links saturated fatty acid-mediated endoplasmic reticulum stress and cell death in liver cells. Mol Cell Biochem 331, 3140.CrossRefGoogle ScholarPubMed
Ge, X, He, Z, Cao, C, et al. (2022) Protein palmitoylation-mediated palmitic acid sensing causes blood-testis barrier damage via inducing ER stress. Redox Biol 54, 102380.CrossRefGoogle ScholarPubMed
Colgan, SM, Tang, D, Werstuck, GH, et al. (2007) Endoplasmic reticulum stress causes the activation of sterol regulatory element binding protein-2. Int J Biochem Cell Biol 39, 18431851.CrossRefGoogle ScholarPubMed
Werstuck, GH, Lentz, SR, Dayal, S, et al. (2001) Homocysteine-induced endoplasmic reticulum stress causes dysregulation of the cholesterol and triglyceride biosynthetic pathways. J Clin Investig 107, 12631273.CrossRefGoogle ScholarPubMed
Wei, M, Nurjanah, U, Herkilini, A, et al. (2022) Unspliced XBP1 contributes to cholesterol biosynthesis and tumorigenesis by stabilizing SREBP2 in hepatocellular carcinoma. Cell Mol Life Sci 79, 118.CrossRefGoogle ScholarPubMed
Cui, K, Li, X, Chen, Q, et al. (2020) Effect of replacement of dietary fish oil with four vegetable oils on prostaglandin E2 synthetic pathway and expression of inflammatory genes in marine fish Larimichthys crocea . Fish Shellfish Immunol 107, 529536.CrossRefGoogle ScholarPubMed
Du, J, Xiang, X, Li, Y, et al. (2018) Molecular cloning and characterization of farnesoid X receptor from large yellow croaker (Larimichthys crocea) and the effect of dietary CDCA on the expression of inflammatory genes in intestine and spleen. Comp Biochem Physiol B: Biochem Mol Biol 216, 1017.CrossRefGoogle ScholarPubMed