Adipose proteome analysis: focus on mediators of insulin resistance

As is well known, adipose tissue is an important site for lipid metabolism and insulin-responsive glucose uptake. The recent discovery of the endocrine function of adipose tissue and the association of obesity with chronic low-grade inflammation in adipose tissue has reinforced the concept of the central role of adipose tissue in mediating obesity-linked insulin resistance and metabolic dysregulation. The study of adipose cells has provided new insights into the mechanism underlying insulin resistance as well as the therapeutic strategies for diabetes. Numerous efforts have been made in identifying key molecular regulators of insulin action and metabolism, including the utilization of advanced proteomics technology. Various proteomic approaches have been applied to identify the adipose secretome, protein-expression profiling and post-translational modifications in adipose cells in the pathological state. In this review, we summarize the recent advances in the proteomics of adipose tissue, and discuss the identified proteins that potentially play important roles in insulin resistance and diabetes.

[1]  Chung-Hsuan Chen,et al.  Review of a current role of mass spectrometry for proteome research. , 2008, Analytica chimica acta.

[2]  J. Foekens,et al.  High-throughput proteomics of breast carcinoma cells: a focus on FTICR-MS , 2008, Expert review of proteomics.

[3]  M. Furuhashi,et al.  Fatty acid-binding proteins: role in metabolic diseases and potential as drug targets , 2008, Nature Reviews Drug Discovery.

[4]  D. Bernlohr,et al.  The role of lipocalin 2 in the regulation of inflammation in adipocytes and macrophages. , 2008, Molecular endocrinology.

[5]  Yuji Yamamoto,et al.  Beneficial effects of subcutaneous fat transplantation on metabolism. , 2008, Cell metabolism.

[6]  L. Orci,et al.  Adipogenic capacity and the susceptibility to type 2 diabetes and metabolic syndrome , 2008, Proceedings of the National Academy of Sciences.

[7]  T. Veenstra,et al.  Mass spectrometry: m/z 1983-2008. , 2008, BioTechniques.

[8]  M. Mann,et al.  Dissection of the insulin signaling pathway via quantitative phosphoproteomics , 2008, Proceedings of the National Academy of Sciences.

[9]  D. Lin,et al.  Defining the regulated secreted proteome of rodent adipocytes upon the induction of insulin resistance. , 2008, Journal of proteome research.

[10]  P. Scherer,et al.  Adiponectin, Cardiovascular Function, and Hypertension , 2008, Hypertension.

[11]  S. Hess,et al.  Applications of proteomics to the study of adipose tissue. , 2008, Methods in molecular biology.

[12]  John R. Yates,et al.  The biological impact of mass-spectrometry-based proteomics , 2007, Nature.

[13]  J. Shaw,et al.  Epidemiology of childhood type 2 diabetes and obesity , 2007, Pediatric diabetes.

[14]  C. Bult,et al.  A mouse model of conditional lipodystrophy , 2007, Proceedings of the National Academy of Sciences.

[15]  N. Houstis,et al.  The Adipokine Lipocalin 2 Is Regulated by Obesity and Promotes Insulin Resistance , 2007, Diabetes.

[16]  G. Shulman,et al.  Obesity-associated improvements in metabolic profile through expansion of adipose tissue. , 2007, The Journal of clinical investigation.

[17]  M. Mann,et al.  Is Proteomics the New Genomics? , 2007, Cell.

[18]  Y. Aso,et al.  Retinol binding protein-4 levels and clinical features of type 2 diabetes patients. , 2007, The Journal of clinical endocrinology and metabolism.

[19]  Matthias Mann,et al.  In-depth Analysis of the Adipocyte Proteome by Mass Spectrometry and Bioinformatics*S , 2007, Molecular & Cellular Proteomics.

[20]  Mark M. Melendez,et al.  Retinol-binding protein 4 is associated with insulin resistance and body fat distribution in nonobese subjects without type 2 diabetes. , 2007, The Journal of clinical endocrinology and metabolism.

[21]  Laura Herrero,et al.  Obesity, inflammation, and insulin resistance. , 2007, Gastroenterology.

[22]  David A. Bernlohr,et al.  Carbonylation of Adipose Proteins in Obesity and Insulin Resistance , 2007, Molecular & Cellular Proteomics.

[23]  K. Petersen,et al.  Disordered lipid metabolism and the pathogenesis of insulin resistance. , 2007, Physiological reviews.

[24]  B. Wolffenbuttel,et al.  Characterization of the Human Visceral Adipose Tissue Secretome*S , 2007, Molecular & Cellular Proteomics.

[25]  C. Magnan,et al.  Free fatty acids and insulin resistance , 2007, Current opinion in clinical nutrition and metabolic care.

[26]  J. DeLany,et al.  Secretome of Primary Cultures of Human Adipose-derived Stem Cells , 2007, Molecular & Cellular Proteomics.

[27]  M. Miyagi,et al.  Proteolytic 18O-labeling strategies for quantitative proteomics. , 2007, Mass spectrometry reviews.

[28]  E. Kraegen,et al.  Lipocalin-2 is an inflammatory marker closely associated with obesity, insulin resistance, and hyperglycemia in humans. , 2007, Clinical chemistry.

[29]  G. Hotamisligil,et al.  Inflammation and metabolic disorders , 2006, Nature.

[30]  David Carling,et al.  Tumor necrosis factor alpha-induced skeletal muscle insulin resistance involves suppression of AMP-kinase signaling. , 2006, Cell metabolism.

[31]  O. MacDougald,et al.  Adipocyte differentiation from the inside out , 2006, Nature Reviews Molecular Cell Biology.

[32]  J. Flier,et al.  TLR4 links innate immunity and fatty acid-induced insulin resistance. , 2006, The Journal of clinical investigation.

[33]  Herbert Tilg,et al.  Adipocytokines: mediators linking adipose tissue, inflammation and immunity , 2006, Nature Reviews Immunology.

[34]  Zihua Hu,et al.  Identification of Common Transcriptional Regulatory Elements in Interleukin-17 Target Genes* , 2006, Journal of Biological Chemistry.

[35]  J. Trimmer,et al.  Graded Regulation of the Kv2.1 Potassium Channel by Variable Phosphorylation , 2006, Science.

[36]  F. White,et al.  Temporal Dynamics of Tyrosine Phosphorylation in Insulin Signaling , 2006, Diabetes.

[37]  Ron Bose,et al.  Phosphoproteomic analysis of Her2/neu signaling and inhibition. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[38]  G. Shulman,et al.  Lipid metabolism and adipokine levels in fatty acid-binding protein null and transgenic mice. , 2006, American journal of physiology. Endocrinology and metabolism.

[39]  C. Kahn,et al.  Evidence for a role of developmental genes in the origin of obesity and body fat distribution. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[40]  R. Aebersold,et al.  Mass Spectrometry and Protein Analysis , 2006, Science.

[41]  K. Flegal,et al.  Prevalence of overweight and obesity in the United States, 1999-2004. , 2006, JAMA.

[42]  Daniel S Spellman,et al.  Quantitative phosphotyrosine proteomics of EphB2 signaling by stable isotope labeling with amino acids in cell culture (SILAC). , 2006, Journal of proteome research.

[43]  T. Mak,et al.  Lipocalin 2-deficient mice exhibit increased sensitivity to Escherichia coli infection but not to ischemia-reperfusion injury. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[44]  N. Ruderman,et al.  Mice Lacking Adiponectin Show Decreased Hepatic Insulin Sensitivity and Reduced Responsiveness to Peroxisome Proliferator-activated Receptor γ Agonists* , 2006, Journal of Biological Chemistry.

[45]  P. Arner.  Resistin: yet another adipokine tells us that men are not mice , 2005, Diabetologia.

[46]  D. Lauffenburger,et al.  Time-resolved Mass Spectrometry of Tyrosine Phosphorylation Sites in the Epidermal Growth Factor Receptor Signaling Network Reveals Dynamic Modules*S , 2005, Molecular & Cellular Proteomics.

[47]  Nimesh Mody,et al.  Serum retinol binding protein 4 contributes to insulin resistance in obesity and type 2 diabetes , 2005, Nature.

[48]  U. Smith,et al.  The effect of PPARγ ligands on the adipose tissue in insulin resistance , 2005 .

[49]  B. Kemp,et al.  Impaired activation of AMP-kinase and fatty acid oxidation by globular adiponectin in cultured human skeletal muscle of obese type 2 diabetics. , 2005, The Journal of clinical endocrinology and metabolism.

[50]  Sanjin Zvonic,et al.  Proteomic Analysis of Primary Cultures of Human Adipose-derived Stem Cells , 2005, Molecular & Cellular Proteomics.

[51]  P. Scherer,et al.  Adipose tissue, inflammation, and cardiovascular disease. , 2005, Circulation research.

[52]  K. Petersen,et al.  Mechanisms of insulin resistance in humans and possible links with inflammation. , 2005, Hypertension.

[53]  A. Makarov,et al.  The Orbitrap: a new mass spectrometer. , 2005, Journal of mass spectrometry : JMS.

[54]  I. Gromova,et al.  Identification of Extracellular and Intracellular Signaling Components of the Mammary Adipose Tissue and Its Interstitial Fluid in High Risk Breast Cancer Patients , 2005, Molecular & Cellular Proteomics.

[55]  L. Pannell,et al.  Quantitative proteomic analysis of the secretory proteins from rat adipose cells using a 2D liquid chromatography-MS/MS approach. , 2005, Journal of proteome research.

[56]  F. Giorgino,et al.  Regional differences of insulin action in adipose tissue: insights from in vivo and in vitro studies. , 2005, Acta physiologica Scandinavica.

[57]  Shizuo Akira,et al.  Lipocalin 2 mediates an innate immune response to bacterial infection by sequestrating iron , 2004, Nature.

[58]  K. Parker,et al.  Multiplexed Protein Quantitation in Saccharomyces cerevisiae Using Amine-reactive Isobaric Tagging Reagents*S , 2004, Molecular & Cellular Proteomics.

[59]  M. Quon,et al.  Inhibition of insulin sensitivity by free fatty acids requires activation of multiple serine kinases in 3T3-L1 adipocytes. , 2004, Molecular endocrinology.

[60]  Y. Awasthi,et al.  Antioxidant role of glutathione S-transferases: protection against oxidant toxicity and regulation of stress-mediated apoptosis. , 2004, Antioxidants & redox signaling.

[61]  A. Garg,et al.  Lipodystrophies: rare disorders causing metabolic syndrome. , 2004, Endocrinology and metabolism clinics of North America.

[62]  J. Yates.  Mass spectral analysis in proteomics. , 2004, Annual review of biophysics and biomolecular structure.

[63]  M. Lazar,et al.  The current biology of resistin , 2004, Journal of internal medicine.

[64]  Waltraud X. Schulze,et al.  A Novel Proteomic Screen for Peptide-Protein Interactions* , 2004, Journal of Biological Chemistry.

[65]  M. Lazar,et al.  Regulation of Fasted Blood Glucose by Resistin , 2004, Science.

[66]  E. Mariman,et al.  Profiling of the secreted proteins during 3T3-L1 adipocyte differentiation leads to the identification of novel adipokines , 2004, Cellular and Molecular Life Sciences CMLS.

[67]  M. Desai,et al.  Obesity is associated with macrophage accumulation in adipose tissue. , 2003, The Journal of clinical investigation.

[68]  L. Tartaglia,et al.  Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance. , 2003, The Journal of clinical investigation.

[69]  A. Marette,et al.  Molecular mechanisms of inflammation in obesity-linked insulin resistance , 2003, International Journal of Obesity.

[70]  A. Pandey,et al.  A proteomic approach for quantitation of phosphorylation using stable isotope labeling in cell culture. , 2003, Analytical chemistry.

[71]  M. Matsuda,et al.  Induction of adiponectin, a fat-derived antidiabetic and antiatherogenic factor, by nuclear receptors. , 2003, Diabetes.

[72]  D. Loskutoff,et al.  Monocyte chemoattractant protein 1 in obesity and insulin resistance , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[73]  C. Mantzoros,et al.  Human Immunodeficiency Virus/Highly Active Antiretroviral Therapy-Associated Metabolic Syndrome: Clinical Presentation, Pathophysiology, and Therapeutic Strategies , 2003 .

[74]  J. W. Rush,et al.  AMPK expression and phosphorylation are increased in rodent muscle after chronic leptin treatment. , 2003, American journal of physiology. Endocrinology and metabolism.

[75]  H. Lodish,et al.  Enhanced muscle fat oxidation and glucose transport by ACRP30 globular domain: Acetyl–CoA carboxylase inhibition and AMP-activated protein kinase activation , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[76]  S. Uchida,et al.  Adiponectin stimulates glucose utilization and fatty-acid oxidation by activating AMP-activated protein kinase , 2002, Nature Medicine.

[77]  B. Goldstein.  Insulin resistance as the core defect in type 2 diabetes mellitus. , 2002, The American journal of cardiology.

[78]  M. Matsuda,et al.  Diet-induced insulin resistance in mice lacking adiponectin/ACRP30 , 2002, Nature Medicine.

[79]  M. Mann,et al.  Stable Isotope Labeling by Amino Acids in Cell Culture, SILAC, as a Simple and Accurate Approach to Expression Proteomics* , 2002, Molecular & Cellular Proteomics.

[80]  K. Kristiansen,et al.  A Proteomic Approach for Identification of Secreted Proteins during the Differentiation of 3T3-L1 Preadipocytes to Adipocytes* , 2002, Molecular & Cellular Proteomics.

[81]  Young-Bum Kim,et al.  Leptin stimulates fatty-acid oxidation by activating AMP-activated protein kinase , 2002, Nature.

[82]  M. White,et al.  Phosphorylation of Ser307 in Insulin Receptor Substrate-1 Blocks Interactions with the Insulin Receptor and Inhibits Insulin Action* , 2002, The Journal of Biological Chemistry.

[83]  D. Figeys,et al.  18O labeling: a tool for proteomics. , 2001, Rapid communications in mass spectrometry : RCM.

[84]  Jeffrey B. Boord,et al.  Lack of macrophage fatty-acid–binding protein aP2 protects mice deficient in apolipoprotein E against atherosclerosis , 2001, Nature Medicine.

[85]  X. Yao,et al.  Proteolytic 18O labeling for comparative proteomics: model studies with two serotypes of adenovirus. , 2001, Analytical chemistry.

[86]  J. Yates,et al.  Large-scale analysis of the yeast proteome by multidimensional protein identification technology , 2001, Nature Biotechnology.

[87]  M. Lazar,et al.  The hormone resistin links obesity to diabetes , 2001, Nature.

[88]  E. Danforth.  Failure of adipocyte differentiation causes type II diabetes mellitus? , 2000, Nature Genetics.

[89]  K. Chada,et al.  In vivo modulation of Hmgic reduces obesity , 2000, Nature Genetics.

[90]  Roger Davis,et al.  The c-Jun NH2-terminal Kinase Promotes Insulin Resistance during Association with Insulin Receptor Substrate-1 and Phosphorylation of Ser307 * , 2000, The Journal of Biological Chemistry.

[91]  M. Olive,et al.  Life without white fat: a transgenic mouse. , 1998, Genes & development.

[92]  R. Hammer,et al.  Insulin resistance and diabetes mellitus in transgenic mice expressing nuclear SREBP-1c in adipose tissue: model for congenital generalized lipodystrophy. , 1998, Genes & development.

[93]  A. Greenberg,et al.  Journal of Clinical Endocrinology and Metabolism Printed in U.S.A. Copyright © 1998 by The Endocrine Society Omental and Subcutaneous Adipose Tissues of Obese Subjects Release Interleukin-6: Depot Difference and Regulation by Glucocorticoid* , 1997 .

[94]  D R Flower,et al.  The lipocalin protein family: structure and function. , 1996, The Biochemical journal.

[95]  O. Trygstad,et al.  Generalized lipodystrophy, congenital and acquired (lipoatrophy) , 1996, Acta paediatrica (Oslo, Norway : 1992). Supplement.

[96]  M. Kress,et al.  An apparent autocrine mechanism amplifies the dexamethasone- and retinoic acid-induced expression of mouse lipocalin-encoding gene 24p3. , 1996, Gene.

[97]  G. Reaven,et al.  Pathophysiology of insulin resistance in human disease. , 1995, Physiological reviews.

[98]  M. Maffei,et al.  Positional cloning of the mouse obese gene and its human homologue , 1995, Nature.

[99]  M. Maffei,et al.  Positional cloning of the mouse obese gene and its human homologue , 1994, Nature.

[100]  H. Sengeløv,et al.  Identification of neutrophil gelatinase-associated lipocalin as a novel matrix protein of specific granules in human neutrophils. , 1994, Blood.

[101]  M. Papa,et al.  Tumor necrosis factor-alpha suppresses insulin-induced tyrosine phosphorylation of insulin receptor and its substrates. , 1993, The Journal of biological chemistry.

[102]  B. Spiegelman,et al.  Adipose expression of tumor necrosis factor-alpha: direct role in obesity-linked insulin resistance. , 1993, Science.

[103]  J. Stephens,et al.  Transcriptional repression of the GLUT4 and C/EBP genes in 3T3-L1 adipocytes by tumor necrosis factor-alpha. , 1991, The Journal of biological chemistry.

[104]  B. Spiegelman,et al.  Molecular cloning of mRNA from 3T3 adipocytes. Regulation of mRNA content for glycerophosphate dehydrogenase and other differentiation-dependent proteins during adipocyte development. , 1983, The Journal of biological chemistry.

[105]  R. Sidhu.  Two-dimensional electrophoretic analyses of proteins synthesized during differentiation of 3T3-L1 preadipocytes. , 1979, The Journal of biological chemistry.