SILAC-MS based characterization of LPS and resveratrol induced changes in adipocyte proteomics - Resveratrol as ameliorating factor on LPS induced changes

PLoS ONE

Volumn 11, Issue 7, 2016, Pages

  Nøhr, Mark K ^a,b   Kroager, Toke P ^a   Sanggaard, Kristian W ^a   Knudsen, Anders D ^a   Stensballe, Allan ^c   Enghild, Jan J ^a   Ølholm, Jens ^a,b   Richelsen, Bjørn ^a,b   Pedersen, Steen B ^a,b  

^a AARHUS UNIVERSITY   (Denmark)

^b AARHUS UNIVERSITY HOSPITAL   (Denmark)

^c AALBORG UNIVERSITY   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

ADIPOCYTOKINE; ADIPONECTIN; ANGIOPOIETIN LIKE PROTEIN 3; APOLIPOPROTEIN C2; CHOLESTEROL; ESTERASE INHIBITOR; LIPOPOLYSACCHARIDE; LIVER TRIACYLGLYCEROL LIPASE; N ACETYLGALACTOSAMINYLTRANSFERASE; N ACETYLGALACTOSAMINYLTRANSFERASE 2; PROTEOME; RESVERATROL; TRIACYLGLYCEROL; UNCLASSIFIED DRUG; ANGIOPOIETIN; ANGPTL3 PROTEIN, HUMAN; INSULIN; POLYPEPTIDE N-ACETYLGALACTOSAMINYLTRANSFERASE; STILBENE DERIVATIVE;

3T3 CELL LINE; ADIPOCYTE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BIOINFORMATICS; CHOLESTEROL SYNTHESIS; CHRONIC INFLAMMATION; CONTROLLED STUDY; DOWN REGULATION; DRUG MECHANISM; DRUG SCREENING; INFLAMMATION; ISOTOPE LABELING; MASS SPECTROMETRY; MOUSE; NONHUMAN; OBESITY; PATHOPHYSIOLOGY; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN GLYCOSYLATION; PROTEOMICS; QUANTITATIVE ANALYSIS; RESPIRATORY CHAIN; STABLE ISOTOPE LABELING BY AMINO ACID IN CELL CULTURE; UPREGULATION; ADIPOSE TISSUE; BIOSYNTHESIS; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; GLYCOSYLATION; HUMAN; INSULIN RESISTANCE; INTESTINE FLORA; LIPID METABOLISM; LIPOGENESIS; METABOLISM; PATHOLOGY;

ADIPOCYTES; ADIPOSE TISSUE; ANGIOPOIETINS; GASTROINTESTINAL MICROBIOME; GENE EXPRESSION REGULATION; GLYCOSYLATION; HUMANS; INFLAMMATION; INSULIN; INSULIN RESISTANCE; LIPID METABOLISM; LIPOGENESIS; LIPOPOLYSACCHARIDES; N-ACETYLGALACTOSAMINYLTRANSFERASES; OBESITY; PROTEOME; PROTEOMICS; STILBENES;

EID: 84979642342     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0159747     Document Type: Article

References (56)

1. Gregor MF, Hotamisligil GS. Inflammatory mechanisms in obesity. Annual review of immunology. 2011; 29:415-45. doi: 10.1146/annurev-immunol-031210-101322 PMID: 21219177.
2. Cani PD, Amar J, Iglesias MA, Poggi M, Knauf C, Bastelica D, et al. Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes. 2007; 56(7):1761-72. doi: 10.2337/db06-1491 PMID: 17456850.
3. Amar J, Burcelin R, Ruidavets JB, Cani PD, Fauvel J, Alessi MC, et al. Energy intake is associated with endotoxemia in apparently healthy men. Am J Clin Nutr. 2008; 87(5):1219-23. PMID: 18469242.
4. Laugerette F, Vors C, Geloen A, Chauvin MA, Soulage C, Lambert-Porcheron S, et al. Emulsified lipids increase endotoxemia: possible role in early postprandial low-grade inflammation. J Nutr Biochem. 2011; 22(1):53-9. doi: 10.1016/j.jnutbio.2009.11.011 PMID: 20303729.
5. Wellhoener P, Vietheer A, Sayk F, Schaaf B, Lehnert H, Dodt C. Metabolic alterations in adipose tissue during the early phase of experimental endotoxemia in humans. Horm Metab Res. 2011; 43(11):754-9. doi: 10.1055/s-0031-1287854 PMID: 22009369.
6. Akira S, Uematsu S, Takeuchi O. Pathogen recognition and innate immunity. Cell. 2006; 124(4):783-801. doi: 10.1016/j.cell.2006.02.015 PMID: 16497588.
7. Shi H, Kokoeva MV, Inouye K, Tzameli I, Yin H, Flier JS. TLR4 links innate immunity and fatty acid-induced insulin resistance. J Clin Invest. 2006; 116(11):3015-25. doi: 10.1172/JCI28898 PMID: 17053832; PubMed Central PMCID: PMCPMC1616196.
8. Lu YC, Yeh WC, Ohashi PS. LPS/TLR4 signal transduction pathway. Cytokine. 2008; 42(2):145-51. doi: 10.1016/j.cyto.2008.01.006 PMID: 18304834.
9. Hotamisligil GS, Shargill NS, Spiegelman BM. Adipose expression of tumor necrosis factor-alpha: direct role in obesity-linked insulin resistance. Science. 1993; 259(5091):87-91. PMID: 7678183.
10. Vicennati V, Vottero A, Friedman C, Papanicolaou DA. Hormonal regulation of interleukin-6 production in human adipocytes. Int J Obes Relat Metab Disord. 2002; 26(7):905-11. doi: 10.1038/sj.ijo.0802035 PMID: 12080442.
11. Manna SK, Mukhopadhyay A, Aggarwal BB. Resveratrol suppresses TNF-induced activation of nuclear transcription factors NF-kappa B, activator protein-1, and apoptosis: potential role of reactive oxygen intermediates and lipid peroxidation. J Immunol. 2000; 164(12):6509-19. PMID: 10843709.
12. Heynekamp JJ, Weber WM, Hunsaker LA, Gonzales AM, Orlando RA, Deck LM, et al. Substituted trans-stilbenes, including analogues of the natural product resveratrol, inhibit the human tumor necrosis factor alpha-induced activation of transcription factor nuclear factor kappaB. J Med Chem. 2006; 49(24):7182-9. doi: 10.1021/jm060630x PMID: 17125270.
13. Dao TM, Waget A, Klopp P, Serino M, Vachoux C, Pechere L, et al. Resveratrol increases glucose induced GLP-1 secretion in mice: a mechanism which contributes to the glycemic control. PLoS One. 2011; 6(6):e20700. Epub 2011/06/16. doi: 10.1371/journal.pone.0020700 PMID: 21673955; PubMed Central PMCID: PMC3108962.
14. Baur JA, Pearson KJ, Price NL, Jamieson HA, Lerin C, Kalra A, et al. Resveratrol improves health and survival of mice on a high-calorie diet. Nature. 2006; 444(7117):337-42. Epub 2006/11/07. doi: 10.1038/nature05354 PMID: 17086191.
15. Lagouge M, Argmann C, Gerhart-Hines Z, Meziane H, Lerin C, Daussin F, et al. Resveratrol improves mitochondrial function and protects against metabolic disease by activating SIRT1 and PGC-1alpha. Cell. 2006; 127(6):1109-22. Epub 2006/11/23. doi: 10.1016/j.cell.2006.11.013 PMID: 17112576.
16. Baur JA, Ungvari Z, Minor RK, Le Couteur DG, de Cabo R. Are sirtuins viable targets for improving healthspan and lifespan? Nat Rev Drug Discov. 2012; 11(6):443-61. doi: 10.1038/nrd3738 PMID: 22653216.
17. Yeung F, Hoberg JE, Ramsey CS, Keller MD, Jones DR, Frye RA, et al. Modulation of NF-kappaB-dependent transcription and cell survival by the SIRT1 deacetylase. EMBO J. 2004; 23(12):2369-80. doi: 10.1038/sj.emboj.7600244 PMID: 15152190; PubMed Central PMCID: PMCPMC423286.
18. Apweiler R, Hermjakob H, Sharon N. On the frequency of protein glycosylation, as deduced from analysis of the SWISS-PROT database. Biochim Biophys Acta. 1999; 1473(1):4-8. PMID: 10580125.
19. Schjoldager KT, Clausen H. Site-specific protein O-glycosylation modulates proprotein processing - deciphering specific functions of the large polypeptide GalNAc-transferase gene family. Biochim Biophys Acta. 2012; 1820(12):2079-94. doi: 10.1016/j.bbagen.2012.09.014 PMID: 23022508.
20. Kato K, Jeanneau C, Tarp MA, Benet-Pages A, Lorenz-Depiereux B, Bennett EP, et al. Polypeptide GalNAc-transferase T3 and familial tumoral calcinosis. Secretion of fibroblast growth factor 23 requires O-glycosylation. J Biol Chem. 2006; 281(27):18370-7. doi: 10.1074/jbc.M602469200 PMID: 16638743.
21. Seidah NG. What lies ahead for the proprotein convertases? Ann N Y Acad Sci. 2011; 1220:149-61. doi: 10.1111/j.1749-6632.2010.05883.x PMID: 21388412.
22. Teslovich TM, Musunuru K, Smith AV, Edmondson AC, Stylianou IM, Koseki M, et al. Biological, clinical and population relevance of 95 loci for blood lipids. Nature. 2010; 466(7307):707-13. doi: 10.1038/nature09270 PMID: 20686565; PubMed Central PMCID: PMCPMC3039276.
23. Kathiresan S, Melander O, Guiducci C, Surti A, Burtt NP, Rieder MJ, et al. Six new loci associated with blood low-density lipoprotein cholesterol, high-density lipoprotein cholesterol or triglycerides in humans. Nat Genet. 2008; 40(2):189-97. doi: 10.1038/ng.75 PMID: 18193044; PubMed Central PMCID: PMCPMC2682493.
24. Willer CJ, Sanna S, Jackson AU, Scuteri A, Bonnycastle LL, Clarke R, et al. Newly identified loci that influence lipid concentrations and risk of coronary artery disease. Nat Genet. 2008; 40(2):161-9. doi: 10.1038/ng.76 PMID: 18193043.
25. Hotamisligil GS, Murray DL, Choy LN, Spiegelman BM. Tumor necrosis factor alpha inhibits signaling from the insulin receptor. Proc Natl Acad Sci U S A. 1994; 91(11):4854-8. PMID: 8197147; PubMed Central PMCID: PMCPMC43887.
26. Maier T, Guell M, Serrano L. Correlation of mRNA and protein in complex biological samples. FEBS Lett. 2009; 583(24):3966-73. doi: 10.1016/j.febslet.2009.10.036 PMID: 19850042.
27. Cullberg KB, Olholm J, Paulsen SK, Foldager CB, Lind M, Richelsen B, et al. Resveratrol has inhibitory effects on the hypoxia-induced inflammation and angiogenesis in human adipose tissue in vitro. Eur J Pharm Sci. 2013; 49(2):251-7. doi: 10.1016/j.ejps.2013.02.014 PMID: 23466666.
28. Gao X, Xu YX, Janakiraman N, Chapman RA, Gautam SC. Immunomodulatory activity of resveratrol: suppression of lymphocyte proliferation, development of cell-mediated cytotoxicity, and cytokine production. Biochem Pharmacol. 2001; 62(9):1299-308. PMID: 11705464.
29. Ølholm J, Paulsen SK, Cullberg KB, Richelsen B, Pedersen SB. Anti-inflammatory effect of resveratrol on adipokine expression and secretion in human adipose tissue explants. Int J Obes (Lond). 2010; 34(10):1546-53. doi: 10.1038/ijo.2010.98 PMID: 20531350.
30. Molina H, Yang Y, Ruch T, Kim JW, Mortensen P, Otto T, et al. Temporal profiling of the adipocyte proteome during differentiation using a five-plex SILAC based strategy. J Proteome Res. 2009; 8(1):48-58. doi: 10.1021/pr800650r PMID: 18947249; PubMed Central PMCID: PMCPMC2642533.
31. Stensballe A, Andersen S, Jensen ON. Characterization of phosphoproteins from electrophoretic gels by nanoscale Fe(III) affinity chromatography with off-line mass spectrometry analysis. Proteomics. 2001; 1(2):207-22. PMID: 11680868.
32. Nøhr MK, Dudele A, Poulsen MM, Ebbesen LH, Radko Y, Christensen LP, et al. LPS-Enhanced Glucose-Stimulated Insulin Secretion Is Normalized by Resveratrol. PLoS One. 2016; 11(1):e0146840. doi: 10.1371/journal.pone.0146840 PMID: 26751381.
33. Arvidsson S, Kwasniewski M, Riano-Pachon DM, Mueller-Roeber B. QuantPrime - a flexible tool for reliable high-throughput primer design for quantitative PCR. BMC Bioinformatics. 2008; 9:465. doi: 10.1186/1471-2105-9-465 PMID: 18976492; PubMed Central PMCID: PMC2612009.
34. 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):1367-72. doi: 10.1038/nbt.1511 PMID: 19029910.
35. Cox J, Neuhauser N, Michalski A, Scheltema RA, Olsen JV, Mann M. Andromeda: a peptide search engine integrated into the MaxQuant environment. J Proteome Res. 2011; 10(4):1794-805. doi: 10.1021/pr101065j PMID: 21254760.
36. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, et al. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet. 2000; 25(1):25-9. doi: 10.1038/75556 PMID: 10802651; PubMed Central PMCID: PMC3037419.
37. Ezzati P, Komher K, Severini G, Coombs KM. Comparative proteomic analyses demonstrate enhanced interferon and STAT-1 activation in reovirus T3D-infected HeLa cells. Front Cell Infect Microbiol. 2015; 5:30. doi: 10.3389/fcimb.2015.00030 PMID: 25905045; PubMed Central PMCID: PMCPMC4388007.
38. Mittal M, Siddiqui MR, Tran K, Reddy SP, Malik AB. Reactive oxygen species in inflammation and tissue injury. Antioxid Redox Signal. 2014; 20(7):1126-67. doi: 10.1089/ars.2012.5149 PMID: 23991888; PubMed Central PMCID: PMCPMC3929010.
39. Schjoldager KT, Vester-Christensen MB, Bennett EP, Levery SB, Schwientek T, Yin W, et al. O-glycosylation modulates proprotein convertase activation of angiopoietin-like protein 3: possible role of polypeptide GalNAc-transferase-2 in regulation of concentrations of plasma lipids. J Biol Chem. 2010; 285(47):36293-303. doi: 10.1074/jbc.M110.156950 PMID: 20837471; PubMed Central PMCID: PMCPMC2978557.
40. Schjoldager KT, Vakhrushev SY, Kong Y, Steentoft C, Nudelman AS, Pedersen NB, et al. Probing isoform-specific functions of polypeptide GalNAc-transferases using zinc finger nuclease glycoengineered SimpleCells. Proc Natl Acad Sci U S A. 2012; 109(25):9893-8. doi: 10.1073/pnas.1203563109 PMID: 22566642; PubMed Central PMCID: PMCPMC3382506.
41. Jin W, Wang X, Millar JS, Quertermous T, Rothblat GH, Glick JM, et al. Hepatic proprotein convertases modulate HDL metabolism. Cell Metab. 2007; 6(2):129-36. doi: 10.1016/j.cmet.2007.07.009 PMID: 17681148; PubMed Central PMCID: PMCPMC2565575.
42. Shimizugawa T, Ono M, Shimamura M, Yoshida K, Ando Y, Koishi R, et al. ANGPTL3 decreases very low density lipoprotein triglyceride clearance by inhibition of lipoprotein lipase. J Biol Chem. 2002; 277(37):33742-8. doi: 10.1074/jbc.M203215200 PMID: 12097324.
43. Holleboom AG, Karlsson H, Lin RS, Beres TM, Sierts JA, Herman DS, et al. Heterozygosity for a loss-of-function mutation in GALNT2 improves plasma triglyceride clearance in man. Cell Metab. 2011; 14(6):811-8. doi: 10.1016/j.cmet.2011.11.005 PMID: 22152306; PubMed Central PMCID: PMCPMC3523677.
44. Goth CK, Halim A, Khetarpal SA, Rader DJ, Clausen H, Schjoldager KT. A systematic study of modulation of ADAM-mediated ectodomain shedding by site-specific O-glycosylation. Proc Natl Acad Sci U S A. 2015. doi: 10.1073/pnas.1511175112 PMID: 26554003.
45. Mohorko E, Glockshuber R, Aebi M. Oligosaccharyltransferase: the central enzyme of N-linked protein glycosylation. J Inherit Metab Dis. 2011; 34(4):869-78. doi: 10.1007/s10545-011-9337-1 PMID: 21614585.
46. Ntambi JM, Miyazaki M, Stoehr JP, Lan H, Kendziorski CM, Yandell BS, et al. Loss of stearoyl-CoA desaturase-1 function protects mice against adiposity. Proc Natl Acad Sci U S A. 2002; 99(17):11482-6. doi: 10.1073/pnas.132384699 PMID: 12177411; PubMed Central PMCID: PMC123282.
47. Gutierrez-Juarez R, Pocai A, Mulas C, Ono H, Bhanot S, Monia BP, et al. Critical role of stearoyl-CoA desaturase-1 (SCD1) in the onset of diet-induced hepatic insulin resistance. J Clin Invest. 2006; 116(6):1686-95. doi: 10.1172/JCI26991 PMID: 16741579; PubMed Central PMCID: PMC1464900.
48. Carobbio S, Hagen RM, Lelliott CJ, Slawik M, Medina-Gomez G, Tan CY, et al. Adaptive changes of the Insig1/SREBP1/SCD1 set point help adipose tissue to cope with increased storage demands of obesity. Diabetes. 2013; 62(11):3697-708. doi: 10.2337/db12-1748 PMID: 23919961; PubMed Central PMCID: PMC3806615.
49. Kim JY, van de Wall E, Laplante M, Azzara A, Trujillo ME, Hofmann SM, et al. Obesity-associated improvements in metabolic profile through expansion of adipose tissue. J Clin Invest. 2007; 117(9):2621-37. doi: 10.1172/JCI31021 PMID: 17717599; PubMed Central PMCID: PMC1950456.
50. Wernstedt Asterholm I, Tao C, Morley TS, Wang QA, Delgado-Lopez F, Wang ZV, et al. Adipocyte inflammation is essential for healthy adipose tissue expansion and remodeling. Cell Metab. 2014; 20(1):103-18. doi: 10.1016/j.cmet.2014.05.005 PMID: 24930973; PubMed Central PMCID: PMCPMC4079756.
51. Horton JD, Shah NA, Warrington JA, Anderson NN, Park SW, Brown MS, et al. Combined analysis of oligonucleotide microarray data from transgenic and knockout mice identifies direct SREBP target genes. Proc Natl Acad Sci U S A. 2003; 100(21):12027-32. doi: 10.1073/pnas.1534923100 PMID: 14512514; PubMed Central PMCID: PMC218707.
52. Le Lay S, Lefrere I, Trautwein C, Dugail I, Krief S. Insulin and sterol-regulatory element-binding protein-1c (SREBP-1C) regulation of gene expression in 3T3-L1 adipocytes. Identification of CCAAT/enhancer-binding protein beta as an SREBP-1C target. J Biol Chem. 2002; 277(38):35625-34. doi: 10.1074/jbc.M203913200 PMID: 12048207.
53. Shimomura I, Shimano H, Korn BS, Bashmakov Y, Horton JD. Nuclear sterol regulatory element-binding proteins activate genes responsible for the entire program of unsaturated fatty acid biosynthesis in transgenic mouse liver. J Biol Chem. 1998; 273(52):35299-306. PMID: 9857071.
54. Misawa K, Horiba T, Arimura N, Hirano Y, Inoue J, Emoto N, et al. Sterol regulatory element-binding protein-2 interacts with hepatocyte nuclear factor-4 to enhance sterol isomerase gene expression in hepatocytes. J Biol Chem. 2003; 278(38):36176-82. doi: 10.1074/jbc.M302387200 PMID: 12855700.
55. Ornstrup MJ, Harslof T, Kjaer TN, Langdahl BL, Pedersen SB. Resveratrol increases bone mineral density and bone alkaline phosphatase in obese men: a randomized placebo-controlled trial. J Clin Endocrinol Metab. 2014; 99(12):4720-9. doi: 10.1210/jc.2014-2799 PMID: 25322274.
56. Pedersen SB, Olholm J, Paulsen SK, Bennetzen MF, Richelsen B. Low Sirt1 expression, which is upregulated by fasting, in human adipose tissue from obese women. Int J Obes (Lond). 2008; 32(8):1250-5. doi: 10.1038/ijo.2008.78 PMID: 18560370.