Abstract
Adipose tissue is an essential tissue for lipid deposition in fish and is associated with excess lipid accumulation in aquaculture. However, the knowledge of the distribution and characterization of adipose tissue in fish still needs further investigation. This study for the first time discovered perirenal adipose tissue (PAT) in large yellow croaker by MRI and CT technologies. Then, the morphological and cytological characteristics of PAT were observed, showing a typical characteristic of white adipose tissue. Meanwhile, the mRNA expression of marker genes of white adipose tissue was highly expressed in PAT compared with the liver and muscle in large yellow croaker. Moreover, based on the discovery of PAT, preadipocytes from PAT were isolated, and the differentiation system of preadipocytes was established. The lipid droplet and TG content of cell were gradually increased during adipocyte differentiation. In addition, mRNA expressions of lipoprotein lipase, adipose triglyceride lipase, and transcription factors related to adipogenesis (cebpα, srebp1, pparα, and pparγ) were quantified to explain the regulation mechanism during the differentiation process. In summary, the present study first discovered perirenal adipose tissue in fish, then explored the characterization of PAT, and revealed the regulation of adipocyte differentiation. These results could advance the understanding of adipose tissue in fish and provide a novel idea for the study of the mechanism of lipid accumulation.
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The datasets generated during or analyzed during the current study are available from the corresponding author on reasonable request.
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References
Albalat A, Saera-Vila A, Capilla E, Gutierrez J, Perez-Sanchez J, Navarro I (2007) Insulin regulation of lipoprotein lipase (LPL) activity and expression in gilthead sea bream (Sparus aurata). Comp Biochem Physiol B Biochem Mol Biol 148:151–159
Algire C, Medrikova D, Herzig S (2013) White and brown adipose stem cells: from signaling to clinical implications. Biochim Biophys Acta 1831:896–904
Bouraoui L, Gutierrez J, Navarro I (2008) Regulation of proliferation and differentiation of adipocyte precursor cells in rainbow trout (Oncorhynchus mykiss). J Endocrinol 198:459–469
Chatzifotis S, Panagiotidou M, Papaioannou N, Pavlidis M, Nengas I, Mylonas CC (2010) Effect of dietary lipid levels on growth, feed utilization, body composition and serum metabolites of meagre (Argyrosomus regius) juveniles. Aquaculture 307:65–70
Cheng YC, Chen HY (2015) Effects of different fatty acids on cell differentiation and lipid accumulation in preadipocytes of warm water fish cobia (Rachycentron canadum Linnaeus, 1766). Aquac Res 46:590–601
Choe SS, Huh JY, Hwang IJ, Kim JI, Kim JB (2016) Adipose tissue remodeling: its role in energy metabolism and metabolic disorders. Front Endocrinol 7:30
Collewet G, Bugeon J, Idier J, Quellec S, Quittet B, Cambert M, Haffray P (2013) Rapid quantification of muscle fat content and subcutaneous adipose tissue in fish using MRI. Food Chem 138:2008–2015
de Jong JM, Larsson O, Cannon B, Nedergaard J (2015) A stringent validation of mouse adipose tissue identity markers. Am J Physiol Endocrinol Metab 308:E1085-1105
de Mattos Carvalho A, Alves AL, Golim MA, Moroz A, Hussni CA, de Oliveira PG, Deffune E (2009) Isolation and immunophenotypic characterization of mesenchymal stem cells derived from equine species adipose tissue. Vet Immunol Immunopathol 132:303–306
Flynn EJ 3rd, Trent CM, Rawls JF (2009) Ontogeny and nutritional control of adipogenesis in zebrafish (Danio rerio). J Lipid Res 50:1641–1652
Gonzales AM, Orlando RA (2007) Role of adipocyte-derived lipoprotein lipase in adipocyte hypertrophy. Nutr Metab 4:22
Grigoras A, Balan RA, Caruntu ID, Giusca SE, Lozneanu L, Avadanei RE, Rusu A, Riscanu LA, Amalinei C (2021) Perirenal adipose tissue-current knowledge and future opportunities. J Clin Med 10:1291
Hammoud SH, AlZaim I, Al-Dhaheri Y, Eid AH, El-Yazbi AF (2021) Perirenal adipose tissue inflammation: novel insights linking metabolic dysfunction to renal diseases. Front Endocrinol 12:707126
Hotamisligil GS (2006) Inflammation and metabolic disorders. Nature 444:860–867
Huang TS, TodorÄEviÄ M, Ruyter B, Torstensen BE (2010) Altered expression of CCAAT/enhancer binding protein and FABP11 genes during adipogenesisin vitroin Atlantic salmon (Salmo salar). Aquac Nutr 16:72–80
Huang N, Mao EW, Hou NN, Liu YP, Han F, Sun XD (2020) Novel insight into perirenal adipose tissue: a neglected adipose depot linking cardiovascular and chronic kidney disease. World J Diabetes 11:115–125
Ibrahim MM (2010) Subcutaneous and visceral adipose tissue: structural and functional differences. Obes Rev 11:11–18
Imrie D, Sadler KC (2010) White adipose tissue development in zebrafish is regulated by both developmental time and fish size. Dev Dyn 239:3013–3023
Ji R, Xu X, Xiang X, Zhu S, Li Y, Mai K, Ai Q (2020) Regulation of adiponectin on lipid metabolism in large yellow croaker (Larimichthys crocea). Biochim Biophys Acta Mol Cell Biol Lipids 1865:158711
Kolstad K, Vegusdal A, Baeverfjord G, Einen O (2004) Quantification of fat deposits and fat distribution in Atlantic halibut (Hippoglossus hippoglossus L.) using computerised X-ray tomography (CT). Aquaculture 229:255–264
Lee MJ, Wu Y, Fried SK (2013) Adipose tissue heterogeneity: implication of depot differences in adipose tissue for obesity complications. Mol Aspects Med 34:1–11
Li Y (2012) Establishment and evaluation of a new model for studying lipogenesis in grass carp (Ctenopharyngodon idella) preadipocytes. In Vitro Cell Dev Biol Anim 48:37–42
Liu P, Li C, Huang J, Ji H (2014) Regulation of adipocytes lipolysis by n-3 HUFA in grass carp (Ctenopharyngodon idellus) in vitro and in vivo. Fish Physiol Biochem 40:1447–1460
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25:402–408
Mathiassen JR, Misimi E, Bondø M, Veliyulin E, Østvik SO (2011) Trends in application of imaging technologies to inspection of fish and fish products. Trends Food Sci Technol 22:257–275
Morigny P, Boucher J, Arner P, Langin D (2021) Lipid and glucose metabolism in white adipocytes: pathways, dysfunction and therapeutics. Nat Rev Endocrinol 17:276–295
Ntambi JM, Young-Cheul K (2000) Adipocyte differentiation and gene expression. J Nutr 130:3122S-3126S
Oku H, Tokuda M, Okumura T, Umino T (2006) Effects of insulin, triiodothyronine and fat soluble vitamins on adipocyte differentiation and LPL gene expression in the stromal-vascular cells of red sea bream, Pagrus major. Comp Biochem Physiol B Biochem Mol Biol 144:326–333
Ren W, Li J, Tan P, Cai Z, Mai K, Xu W, Zhang Y, Nian R, Macq B, Ai Q (2018) Lipid deposition patterns among different sizes of three commercial fish species. Aquac Res 49:1046–1052
Rosen ED, Sarraf P, Troy AE, Bradwin G, Moore K, Milstone DS, Spiegelman BM, Mortensen RM (1999) PPARγ is required for the differentiation of adipose tissue in vivo and in vitro. Mol Cell 4:611–617
Rutkowski JM, Stern JH, Scherer PE (2015) The cell biology of fat expansion. J Cell Biol 208:501–512
Salmeron C (2018) Adipogenesis in fish. J Exp Biol 221:jeb161588
Salmeron C, Acerete L, Gutierrez J, Navarro I, Capilla E (2013) Characterization and endocrine regulation of proliferation and differentiation of primary cultured preadipocytes from gilthead sea bream (Sparus aurata). Domest Anim Endocrinol 45:1–10
Schleinitz D, Krause K, Wohland T, Gebhardt C, Linder N, Stumvoll M, Bluher M, Bechmann I, Kovacs P, Gericke M et al (2020) Identification of distinct transcriptome signatures of human adipose tissue from fifteen depots. Eur J Hum Genet 28:1714–1725
Tan P, Dong X, Mai K, Xu W, Ai Q (2016) Vegetable oil induced inflammatory response by altering TLR-NF-kappaB signalling, macrophages infiltration and polarization in adipose tissue of large yellow croaker (Larimichthys crocea). Fish Shellfish Immunol 59:398–405
Tang Q-Q, Grønborg M, Huang H, Kim J-W, Otto TC, Pandey A, Lane MD (2005) Sequential phosphorylation of CCAAT enhancer-binding protein β by MAPK and glycogen synthase kinase 3β is required for adipogenesis. Proc Natl Acad Sci 102:9766–9771
Todorcevic M, Vegusdal A, Gjoen T, Sundvold H, Torstensen BE, Kjaer MA, Ruyter B (2008) Changes in fatty acids metabolism during differentiation of Atlantic salmon preadipocytes; effects of n-3 and n-9 fatty acids. Biochim Biophys Acta 1781:326–335
Todorčević M, Škugor S, Krasnov A, Ruyter B (2010) Gene expression profiles in Atlantic salmon adipose-derived stromo-vascular fraction during differentiation into adipocytes. BMC Genomics 11:1–17
Vegusdal A, Sundvold H, Gjøen T, Ruyter B (2003) An in vitro method for studying the proliferation and differentiation of Atlantic salmon preadipocytes. Lipids 38:289–296
Virtue S, Vidal-Puig A (2010) Adipose tissue expandability, lipotoxicity and the Metabolic Syndrome–an allostatic perspective. Biochim Biophys Acta 1801:338–349
Volkoff H, Hoskins LJ, Tuziak SM (2010) Influence of intrinsic signals and environmental cues on the endocrine control of feeding in fish: potential application in aquaculture. Gen Comp Endocrinol 167:352–359
Wang X, Huang M, Wang Y (2012) The effect of insulin, TNFalpha and DHA on the proliferation, differentiation and lipolysis of preadipocytes isolated from large yellow croaker (Pseudosciaena Crocea R.). PLoS One 7:e48069
Wang YW, Zhang JL, Jiao JG, Du XX, Limbu SM, Qiao F, Zhang ML, Li DL, Du ZY (2017) Physiological and metabolic differences between visceral and subcutaneous adipose tissues in Nile tilapia (Oreochromis niloticus). Am J Physiol Regul Integr Comp Physiol 313:R608–R619
Weil C, Lefèvre F, Bugeon J (2012) Characteristics and metabolism of different adipose tissues in fish. Rev Fish Biol Fisheries 23:157–173
Wu J-L, Zhang J-L, Du X-X, Shen Y-J, Lao X, Zhang M-L, Chen L-Q, Du Z-Y (2015) Evaluation of the distribution of adipose tissues in fish using magnetic resonance imaging (MRI). Aquaculture 448:112–122
Yan J, Liao K, Wang T, Mai K, Xu W, Ai Q (2015) Dietary lipid levels influence lipid deposition in the liver of large yellow croaker (Larimichthys crocea) by regulating lipoprotein receptors, fatty acid uptake and triacylglycerol synthesis and catabolism at the transcriptional level. PLoS ONE 10:e0129937
Funding
This work was supported by the Scientific and Technological Innovation of Blue Granary (Grant No. 2018YFD0900402), the Key Program of National Natural Science Foundation of China (Grant No. 31830103), the National Science Fund for Distinguished Young Scholars of China (Grant No. 31525024), the Ten-thousand Talents Program (Grant No. 2018–29), and the earmarked fund for CARS-47.
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Dan Xu: Conceptualization, Data curation, Formal analysis, Methodology, Visualization, Writing - review &editing. Ye Gong: Investigation, Validation, Writing - original draft. Xiaojun Xiang: Software, Methodology, Writing - review & editing. Yongtao Liu: Visualization, Software. Kangsen Mai: Data curation, Resources, Supervision. Qinghui Ai: Data curation, Resources, Writing - review & editing, Supervision, Project administration, Funding acquisition. All authors reviewed the manuscript.
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All experiments in this study were in accordance with the Management Rule of Laboratory Animals (Chinese Order No. 676 of the State Council, revised on 1 March 2017). The authors agree to collaborate and publish this article.
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Xu, D., Gong, Y., Xiang, X. et al. Discovery, characterization, and adipocyte differentiation regulation in perirenal adipose tissue of large yellow croaker (Larimichthys crocea). Fish Physiol Biochem 49, 627–639 (2023). https://doi.org/10.1007/s10695-023-01208-2
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DOI: https://doi.org/10.1007/s10695-023-01208-2