Proteomic Signatures of Human Visceral and Subcutaneous Adipocytes
Jazyk angličtina Země Spojené státy americké Médium print
Typ dokumentu časopisecké články, pozorovací studie, práce podpořená grantem
PubMed
34669916
PubMed Central
PMC8851937
DOI
10.1210/clinem/dgab756
PII: 6406610
Knihovny.cz E-zdroje
- Klíčová slova
- adipocytes, adipose tissue, metabolism, obesity, subcutaneous adipose tissue, visceral adipose tissue,
- MeSH
- bariatrická chirurgie MeSH
- dospělí MeSH
- genové regulační sítě MeSH
- lidé středního věku MeSH
- lidé MeSH
- morbidní obezita metabolismus patologie chirurgie MeSH
- nitrobřišní tuk cytologie metabolismus patologie MeSH
- omentum cytologie metabolismus patologie chirurgie MeSH
- podkožní břišní tuk cytologie metabolismus patologie MeSH
- proteomika MeSH
- tukové buňky metabolismus MeSH
- Check Tag
- dospělí MeSH
- lidé středního věku MeSH
- lidé MeSH
- ženské pohlaví MeSH
- Publikační typ
- časopisecké články MeSH
- pozorovací studie MeSH
- práce podpořená grantem MeSH
CONTEXT: Adipose tissue distribution is a key factor influencing metabolic health and risk in obesity-associated comorbidities. OBJECTIVE: Here we aim to compare the proteomic profiles of mature adipocytes from different depots. METHODS: Abdominal subcutaneous (SA) and omental visceral adipocytes (VA) were isolated from paired adipose tissue biopsies obtained during bariatric surgery on 19 severely obese women (body mass index > 30 kg/m2) and analyzed using state-of-the-art mass spectrometry. Differential expression analysis and weighted gene co-expression network analysis (WGCNA) were performed to investigate proteome signature properties and to examine a possible association of the protein expression with the clinical data. RESULTS: We identified 3686 protein groups and found 1140 differentially expressed proteins (adj. P value < 0.05), of which 576 proteins were upregulated in SA and 564 in VA samples. We provide a global protein profile of abdominal SA and omental VA, present the most differentially expressed pathways and processes distinguishing SA from VA, and correlate them with clinical and body composition data. We show that SA are significantly more active in processes linked to vesicular transport and secretion, and to increased lipid metabolism activity. Conversely, the expression of proteins involved in the mitochondrial energy metabolism and translational or biosynthetic activity is higher in VA. CONCLUSION: Our analysis represents a valuable resource of protein expression profiles in abdominal SA and omental VA, highlighting key differences in their role in obesity.
Central European Institute of Technology Masaryk University 62500 Brno Czech Republic
Department of Physiology Faculty of Medicine Masaryk University 70300 Brno Czech Republic
Department of Surgery Vitkovice Hospital 70300 Ostrava Czech Republic
Zobrazit více v PubMed
Sethi JK, Vidal-Puig AJ. Thematic review series: adipocyte biology. Adipose tissue function and plasticity orchestrate nutritional adaptation. J Lipid Res. 2007;48(6):1253-1262. PubMed PMC
Schoettl T, Fischer IP, Ussar S. Heterogeneity of adipose tissue in development and metabolic function. J Exp Biol. 2018;221(Suppl 1):jeb162958. PubMed
Tchkonia T, Thomou T, Zhu Y, et al. . Mechanisms and metabolic implications of regional differences among fat depots. Cell Metab. 2013;17(5):644-656. PubMed PMC
Kwok KH, Lam KS, Xu A. Heterogeneity of white adipose tissue: molecular basis and clinical implications. Exp Mol Med. 2016;48:e215. PubMed PMC
Lee MJ, Wu Y, Fried SK. Adipose tissue heterogeneity: implication of depot differences in adipose tissue for obesity complications. Mol Aspects Med. 2013;34(1):1-11. PubMed PMC
Tchernof A, Després JP. Pathophysiology of human visceral obesity: an update. Physiol Rev. 2013;93(1):359-404. PubMed
Brockman D, Chen X. Proteomics in the characterization of adipose dysfunction in obesity. Adipocyte. 2012;1(1):25-37. PubMed PMC
Gómez-Serrano M, Camafeita E, García-Santos E, et al. . Proteome-wide alterations on adipose tissue from obese patients as age-, diabetes- and gender-specific hallmarks. Sci Rep. 2016;6:1–19. PubMed PMC
Haard PMMV, Herbrink P, Schweitzer DH. Differentiation of paired human subcutaneous and visceral adipose tissues by holistic proteome profiling using LC-MS/MS: a pilot study. Int J Res Stud Biosci. 2016;4(7):32-42.
Murri M, Insenser M, Bernal-Lopez MR, Perez-Martinez P, Escobar-Morreale HF, Tinahones FJ. Proteomic analysis of visceral adipose tissue in pre-obese patients with type 2 diabetes. Mol Cell Endocrinol. 2013;376(1-2):99-106. PubMed
Vogel MAA, Wang P, Bouwman FG, et al. . A comparison between the abdominal and femoral adipose tissue proteome of overweight and obese women. Sci Rep. 2019;9(1):4202. PubMed PMC
Alfadda AA, Benabdelkamel H, Masood A, et al. . Proteomic analysis of mature adipocytes from obese patients in relation to aging. Exp Gerontol. 2013;48(11):1196-1203. PubMed
Benabdelkamel H, Masood A, Almidani GM, et al. . Mature adipocyte proteome reveals differentially altered protein abundances between lean, overweight and morbidly obese human subjects. Mol Cell Endocrinol. 2015;401:142-154. PubMed
Doulamis IP, Konstantopoulos P, Tzani A, et al. . Visceral white adipose tissue and serum proteomic alternations in metabolically healthy obese patients undergoing bariatric surgery. Cytokine. 2019;115:76-83. PubMed
Perez-Riverol Y, Csordas A, Bai J, et al. . The PRIDE database and related tools and resources in 2019: improving support for quantification data. Nucleic Acids Res. 2019;47(D1): D442-D450. PubMed PMC
Adamczyk P, Bužga M, Holéczy P, et al. . Bone mineral density and body composition after laparoscopic sleeve gastrectomy in men: a short-term longitudinal study. Int J Surg. 2015;23(Pt A):101-107. PubMed
Adamczyk P, Bužga M, Holéczy P, et al. . Body size, bone mineral density, and body composition in obese women after laparoscopic sleeve gastrectomy: a 1-year longitudinal study. Horm Metab Res. 2015;47(12):873-879. PubMed
Pluskiewicz W, Buzga M, Holeczy P, Smajstrla V, Adamczyk P. A comment on ‘Changes in bone mineral density in women following 1-year gastric bypass surgery’ published by Casagrande DS et al.Obes Surg. 2013;23(11):1885. PubMed
Bužga M, Holéczy P, Švagera Z, Švorc P, Zavadilová V. Effects of sleeve gastrectomy on parameters of lipid and glucose metabolism in obese women - 6 months after operation. Wideochirur Inne Tech Maloinwazyjne 2013;8(1):22-8. PubMed PMC
Bužga M, Holéczy P, Švagera Z, Zonča P. Laparoscopic gastric plication and its effect on saccharide and lipid metabolism: a 12-month prospective study. Wideochirur Inne Tech Maloinwazyjne 2015;10(3):398-405. PubMed PMC
Carswell KA, Lee MJ, Fried SK. Culture of isolated human adipocytes and isolated adipose tissue. Methods Mol Biol. 2012;806:203-214. PubMed PMC
Gallagher SR. One-dimensional SDS gel electrophoresis of proteins. Curr Protoc Mol Biol. 2012;97(1):10.2A.1-10.2A.44. PubMed
Wiśniewski JR, Rakus D. Multi-enzyme digestion FASP and the ‘Total Protein Approach’-based absolute quantification of the Escherichia coli proteome. J Proteomics. 2014;109:322-331. PubMed
Wiśniewski JR, Zougman A, Nagaraj N, Mann M. Universal sample preparation method for proteome analysis. Nat Methods. 2009;6(5):359-362. PubMed
Yeung YG, Nieves E, Angeletti RH, Stanley ER. Removal of detergents from protein digests for mass spectrometry analysis. Anal Biochem. 2008;382(2):135-137. PubMed PMC
Stejskal K, Potěšil D, Zdráhal Z. Suppression of peptide sample losses in autosampler vials. J Proteome Res. 2013;12(6):3057-3062. PubMed
Cox J, Mann M. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat Biotechnol. 2008;26(12):1367-1372. PubMed
R Development Core Team. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing; 2016.
Hruska P, Kucera J, Pekar M, et al. . Proteomic signatures of human visceral and subcutaneous adipocytes—supplementary files. Dataset posted on October 27, 2021. doi:10.6084/m9.figshare.14626341.v1. PubMed DOI PMC
Ritchie ME, Phipson B, Wu D, et al. . limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res. 2015;43(7):e47. PubMed PMC
Smyth GK, Michaud J, Scott HS. Use of within-array replicate spots for assessing differential expression in microarray experiments. Bioinformatics. 2005;21(9):2067-2075. PubMed
Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Series B (Methodol). 1995;57(1):289-300.
Ward JH Jr. Hierarchical grouping to optimize an objective function. J Am Stat Assoc 1963;58(301):236-244.
Langfelder P, Horvath S. WGCNA: an R package for weighted correlation network analysis. BMC Bioinformatics. 2008;9:559. PubMed PMC
Langfelder P, Horvath S. Fast R functions for robust correlations and hierarchical clustering. J Stat Softw. 2012;46(1):1-17. PubMed PMC
Horvath S, Dong J. Geometric interpretation of gene coexpression network analysis. PLoS Comput Biol. 2008;4(8):e1000117. PubMed PMC
Szklarczyk D, Gable AL, Lyon D, et al. . STRING v11: protein-protein association networks with increased coverage, supporting functional discovery in genome-wide experimental datasets. Nucleic Acids Res. 2019;47(D1):D607-D613. PubMed PMC
Bindea G, Mlecnik B, Hackl H, et al. . ClueGO: a Cytoscape plug-in to decipher functionally grouped gene ontology and pathway annotation networks. Bioinformatics. 2009;25(8):1091-1093. PubMed PMC
Jassal B, Matthews L, Viteri G, et al. . The reactome pathway knowledgebase. Nucleic Acids Res. 2020;48(D1):D498-D503. PubMed PMC
Almagro Armenteros JJ, Tsirigos KD, Sønderby CK, et al. . SignalP 5.0 improves signal peptide predictions using deep neural networks. Nat Biotechnol. 2019;37(4):420-423. PubMed
Kraunsøe R, Boushel R, Hansen CN, et al. . Mitochondrial respiration in subcutaneous and visceral adipose tissue from patients with morbid obesity. J Physiol. 2010;588(Pt 12):2023-2032. PubMed PMC
Pérez-Pérez R, Ortega-Delgado FJ, García-Santos E, et al. . Differential proteomics of omental and subcutaneous adipose tissue reflects their unalike biochemical and metabolic properties. J Proteome Res. 2009;8(4):1682-1693. PubMed
Fischer B, Schöttl T, Schempp C, et al. . Inverse relationship between body mass index and mitochondrial oxidative phosphorylation capacity in human subcutaneous adipocytes. Am J Physiol Endocrinol Metab. 2015;309(4):E380-E387. PubMed
Wessels B, Honecker J, Schöttl T, et al. . Adipose mitochondrial respiratory capacity in obesity is impaired independently of glycemic status of tissue donors. Obesity (Silver Spring). 2019;27(5):756-766. PubMed
Schöttl T, Pachl F, Giesbertz P, et al. . Proteomic and metabolite profiling reveals profound structural and metabolic reorganization of adipocyte mitochondria in obesity. Obesity (Silver Spring). 2020;28(3):590-600. PubMed
Keuper M, Jastroch M, Yi CX, et al. . Spare mitochondrial respiratory capacity permits human adipocytes to maintain ATP homeostasis under hypoglycemic conditions. FASEB J. 2014;28(2):761-770. PubMed
Gealekman O, Guseva N, Hartigan C, et al. . Depot-specific differences and insufficient subcutaneous adipose tissue angiogenesis in human obesity. Circulation. 2011;123(2):186-194. PubMed PMC
Dadson P, Landini L, Helmiö M, et al. . Effect of bariatric surgery on adipose tissue glucose metabolism in different depots in patients with or without type 2 diabetes. Diabetes Care. 2016;39(2):292-299. PubMed
Boden G, Merali S. Measurement of the increase in endoplasmic reticulum stress-related proteins and genes in adipose tissue of obese, insulin-resistant individuals. Methods Enzymol. 2011;489:67-82. PubMed PMC
Xie X, Yi Z, Bowen B, et al. . Characterization of the human adipocyte proteome and reproducibility of protein abundance by one-dimensional gel electrophoresis and HPLC-ESI-MS/MS. J Proteome Res. 2010;9(9):4521-4534. PubMed PMC
Kozlov G, Gehring K. Calnexin cycle—structural features of the ER chaperone system. FEBS J. 2020;287(20):4322-4340. PubMed PMC
Gurkan C, Lapp H, Alory C, Su AI, Hogenesch JB, Balch WE. Large-scale profiling of Rab GTPase trafficking networks: the membrome. Mol Biol Cell. 2005;16(8):3847-3864. PubMed PMC
Li C, Yu SS. Rab proteins as regulators of lipid droplet formation and lipolysis. Cell Biol Int. 2016;40(10):1026-1032. PubMed
Kaddai V, Le Marchand-Brustel Y, Cormont M. Rab proteins in endocytosis and Glut4 trafficking. Acta Physiol (Oxf). 2008;192(1):75-88. PubMed
Dominiczak MH, Caslake MJ. Apolipoproteins: metabolic role and clinical biochemistry applications. Ann Clin Biochem. 2011;48(Pt 6):498-515. PubMed
Huang ZH, Espiritu DJ, Uy A, Holterman AX, Vitello J, Mazzone T. Adipose tissue depot-specific differences in adipocyte apolipoprotein E expression. Metabolism. 2011;60(12):1692-1701. PubMed PMC
Clemente-Postigo M, Queipo-Ortuño MI, Fernandez-Garcia D, Gomez-Huelgas R, Tinahones FJ, Cardona F. Adipose tissue gene expression of factors related to lipid processing in obesity. PLoS One. 2011;6(9):e24783. PubMed PMC
Langeveld M, Aerts JM. Glycosphingolipids and insulin resistance. Prog Lipid Res. 2009;48(3-4):196-205. PubMed
Ruiz-Ojeda FJ, Méndez-Gutiérrez A, Aguilera CM, Plaza-Díaz J. Extracellular matrix remodeling of adipose tissue in obesity and metabolic diseases. Int J Mol Sci. 2019;20(19): 4888. PubMed PMC
Roca-Rivada A, Bravo SB, Pérez-Sotelo D, et al. . CILAIR-based secretome analysis of obese visceral and subcutaneous adipose tissues reveals distinctive ECM remodeling and inflammation mediators. Sci Rep. 2015;5:12214. PubMed PMC
Bertola A, Deveaux V, Bonnafous S, et al. . Elevated expression of osteopontin may be related to adipose tissue macrophage accumulation and liver steatosis in morbid obesity. Diabetes. 2009;58(1):125-133. PubMed PMC
Liu LF, Kodama K, Wei K, et al. . The receptor CD44 is associated with systemic insulin resistance and proinflammatory macrophages in human adipose tissue. Diabetologia. 2015;58(7):1579-1586. PubMed
Petrus P, Fernandez TL, Kwon MM, et al. . Specific loss of adipocyte CD248 improves metabolic health via reduced white adipose tissue hypoxia, fibrosis and inflammation. EBioMedicine. 2019;44:489-501. PubMed PMC
Insenser M, Montes-Nieto R, Vilarrasa N, et al. . A nontargeted proteomic approach to the study of visceral and subcutaneous adipose tissue in human obesity. Mol Cell Endocrinol. 2012;363(1-2):10-19. PubMed
Pessentheiner AR, Ducasa GM, Gordts PLSM. Proteoglycans in obesity-associated metabolic dysfunction and meta-inflammation. Front Immunol. 2020;11:1–18. PubMed PMC
Lim JM, Wollaston-Hayden EE, Teo CF, Hausman D, Wells L. Quantitative secretome and glycome of primary human adipocytes during insulin resistance. Clin Proteomics. 2014;11(1):20. PubMed PMC
Kochkodan J, Telem DA, Ghaferi AA. Physiologic and psychological gender differences in bariatric surgery. Surg Endosc. 2018;32(3):1382-1388. PubMed
Proteomic Signatures of Human Visceral and Subcutaneous Adipocytes