Proteomic analysis of visceral adipose tissue in pre-obese patients with type 2 diabetes

Molecular and Cellular Endocrinology

Volumn 376, Issue 1-2, 2013, Pages 99-106

  Murri, Mora ^a   Insenser, Maria ^a   Bernal Lopez, Maria Rosa ^b,d   Perez Martinez, Pablo ^c,d   Escobar Morreale, Hector F ^a   Tinahones, Francisco J ^b,d  

^a HOSPITAL RAMÓN Y CAJAL   (Spain)

^b HOSPITAL UNIVERSITARIO VIRGEN DE LA VICTORIA   (Spain)

^c HOSPITAL UNIVERSITARIO REINA SOFÍA   (Spain)

^d Instituto de Salud Carlos III   (Spain)

Author keywords

Overweight; Pre obesity; Proteomics; Type 2 diabetes; Visceral adipose tissue

Indexed keywords

ACTIN; ALDEHYDE DEHYDROGENASE ISOENZYME 2; ANTITHROMBIN III; APOLIPOPROTEIN A4; GLUTATHIONE TRANSFERASE M2; IMMUNOGLOBULIN KAPPA CHAIN; LIPOCORTIN 1; PEROXIREDOXIN 2; RETINALDEHYDE DEHYDROGENASE 1; RETINOID; UNCLASSIFIED DRUG; VINCULIN;

ACTB GENE; ADULT; ALDH1A1 GENE; ALDH2 GENE; AMINO ACID SEQUENCE; ANXA1 GENE; APOA4 GENE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOSKELETON; DISEASE COURSE; FEMALE; GENE; GLUCOSE TOLERANCE; GSTM2 GENE; HUMAN; HUMAN TISSUE; IGKC GENE; INFLAMMATION; INTRAABDOMINAL FAT; MALE; METABOLISM; NON INSULIN DEPENDENT DIABETES MELLITUS; OBESITY; OXIDATIVE STRESS; PRDX2 GENE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEOMICS; RETINOID METABOLISM; SERPINC1 GENE; VINC GENE;

OVERWEIGHT; PRE-OBESITY; PROTEOMICS; TYPE 2 DIABETES; VISCERAL ADIPOSE TISSUE;

ADULT; CYTOSKELETAL PROTEINS; DIABETES MELLITUS, TYPE 2; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; FEMALE; GENE EXPRESSION; GLUCOSE TOLERANCE TEST; HUMANS; INFLAMMATION; INTRA-ABDOMINAL FAT; MALE; MIDDLE AGED; MITOCHONDRIAL PROTEINS; OBESITY; OXIDATIVE STRESS; PROTEOMICS; RETINOIDS;

EID: 84879996748     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2013.06.010     Document Type: Article

References (51)

1. Alligier M., Meugnier E., Debard C., Lambert-Porcheron S., Chanseaume E., Sothier M., Loizon E., Hssain A.A., Brozek J., Scoazec J.Y., Morio B., Vidal H., Laville M. Subcutaneous adipose tissue remodeling during the initial phase of weight gain induced by overfeeding in humans. J. Clin. Endocrinol. Metab. 2012, 97:E183-E192.
2. Anderson L., Seilhamer J. A comparison of selected mRNA and protein abundances in human liver. Electrophoresis 1997, 18:533-537.
3. Astrup A., Finer N. Redefining type 2 diabetes: 'diabesity' or 'obesity dependent diabetes mellitus'?. Obes. Rev. 2000, 1:57-59.
4. Awartani F. Serum immunoglobulin levels in type 2 diabetes patients with chronic periodontitis. J. Contemp. Dent. Pract. 2010, 11:1-8.
5. Banga J.D. Coagulation and fibrinolysis in diabetes. Semin. Vasc. Med. 2002, 2:75-86.
6. Barbarroja N., Lopez-Pedrera R., Mayas M.D., Garcia-Fuentes E., Garrido-Sanchez L., Macias-Gonzalez M., El Bekay R., Vidal-Puig A., Tinahones F.J. The obese healthy paradox: is inflammation the answer?. Biochem. J. 2010, 430:141-149.
7. Cadoudal T., Leroyer S., Reis A.F., Tordjman J., Durant S., Fouque F., Collinet M., Quette J., Chauvet G., Beale E., Velho G., Antoine B., Benelli C., Forest C. Proposed involvement of adipocyte glyceroneogenesis and phosphoenolpyruvate carboxykinase in the metabolic syndrome. Biochimie 2005, 87:27-32.
8. Cadoudal T., Glorian M., Massias A., Fouque F., Forest C., Benelli C. Retinoids upregulate phosphoenolpyruvate carboxykinase and glyceroneogenesis in human and rodent adipocytes. J. Nutr. 2008, 138:1004-1009.
9. Ceriello A., Giugliano D., Quatraro A., Marchi E., Barbanti M., Lefebvre P. Evidence for a hyperglycaemia-dependent decrease of antithrombin III-thrombin complex formation in humans. Diabetologia 1990, 33:163-167.
10. Ceriello A., Taboga C., Giacomello R., Falleti E., De Stasio G., Motz E., Lizzio S., Gonano F., Bartoli E. Fibrinogen plasma levels as a marker of thrombin activation in diabetes. Diabetes 1994, 43:430-432.
11. Corton M., Villuendas G., Botella J.I., San Millan J.L., Escobar-Morreale H.F., Peral B. Improved resolution of the human adipose tissue proteome at alkaline and wide range pH by the addition of hydroxyethyl disulfide. Proteomics 2004, 4:438-441.
12. Chae H.Z., Kim I.H., Kim K., Rhee S.G. Cloning, sequencing, and mutation of thiol-specific antioxidant gene of Saccharomyces cerevisiae. J. Biol. Chem. 1993, 268:16815-16821.
13. Chen G., Gharib T.G., Huang C.C., Taylor J.M., Misek D.E., Kardia S.L., Giordano T.J., Iannettoni M.D., Orringer M.B., Hanash S.M., Beer D.G. Discordant protein and mRNA expression in lung adenocarcinomas. Mol. Cell. Proteomics 2002, 1:304-313.
14. Dandona P., Aljada A., Bandyopadhyay A. Inflammation: the link between insulin resistance, obesity and diabetes. Trends Immunol. 2004, 25:4-7.
15. Evans J.L., Goldfine I.D., Maddux B.A., Grodsky G.M. Oxidative stress and stress-activated signaling pathways: a unifying hypothesis of type 2 diabetes. Endocr. Rev. 2002, 23:599-622.
16. Fain J.N., Madan A.K., Hiler M.L., Cheema P., Bahouth S.W. Comparison of the release of adipokines by adipose tissue, adipose tissue matrix, and adipocytes from visceral and subcutaneous abdominal adipose tissues of obese humans. Endocrinology 2004, 145:2273-2282.
17. Flegal K.M., Graubard B.I., Williamson D.F., Gail M.H. Cause-specific excess deaths associated with underweight, overweight, and obesity. JAMA 2007, 298:2028-2037.
18. Goodpaster B.H., Krishnaswami S., Harris T.B., Katsiaras A., Kritchevsky S.B., Simonsick E.M., Nevitt M., Holvoet P., Newman A.B. Obesity, regional body fat distribution, and the metabolic syndrome in older men and women. Arch. Intern. Med. 2005, 165:777-783.
19. Hamulu F., Cetinkalp S., Ozgen A.G., Bayraktar F., Yilmaz C., Kabalak T., Tuzun M. The level of antithrombin III (AT III) in Turkish diabetics. Turk. J. Endocrinol. Metab. 1998, 4:209-212.
20. Haslam D.W., James W.P. Obesity. Lancet 2005, 366:1197-1209.
21. Hedley A.A., Ogden C.L., Johnson C.L., Carroll M.D., Curtin L.R., Flegal K.M. Prevalence of overweight and obesity among US children, adolescents, and adults, 1999-2002. JAMA 2004, 291:2847-2850.
22. Hossain P., Kawar B., El Nahas M. Obesity and diabetes in the developing world-a growing challenge. N. Engl. J. Med. 2007, 356:213-215.
23. Ibrahim M.M. Subcutaneous and visceral adipose tissue: structural and functional differences. Obes. Rev. 2010, 11:11-18.
24. Insenser M., Montes-Nieto R., Vilarrasa N., Lecube A., Simo R., Vendrell J., Escobar-Morreale H.F. A nontargeted proteomic approach to the study of visceral and subcutaneous adipose tissue in human obesity. Mol. Cell. Endocrinol. 2012, 363:10-19.
25. Janssen M.E., Kim E., Liu H., Fujimoto L.M., Bobkov A., Volkmann N., Hanein D. Three-dimensional structure of vinculin bound to actin filaments. Mol. Cell. 2006, 21:271-281.
26. Jowsey I.R., Smith S.A., Hayes J.D. Expression of the murine glutathione S-transferase alpha3 (GSTA3) subunit is markedly induced during adipocyte differentiation: activation of the GSTA3 gene promoter by the pro-adipogenic eicosanoid 15-deoxy-Delta12,14-prostaglandin J2. Biochem. Biophys. Res. Commun. 2003, 312:1226-1235.
27. Kanzaki M., Pessin J.E. Insulin-stimulated GLUT4 translocation in adipocytes is dependent upon cortical actin remodeling. J. Biol. Chem. 2001, 276:42436-42444.
28. Kershaw E.E., Flier J.S. Adipose tissue as an endocrine organ. J. Clin. Endocrinol. Metab. 2004, 89:2548-2556.
29. Kheterpal I., Ku G., Coleman L., Yu G., Ptitsyn A.A., Floyd Z.E., Gimble J.M. Proteome of human subcutaneous adipose tissue stromal vascular fraction cells versus mature adipocytes based on DIGE. J. Proteome. Res. 2011, 10:1519-1527.
30. Kiefer F.W., Orasanu G., Nallamshetty S., Brown J.D., Wang H., Luger P., Qi N.R., Burant C.F., Duester G., Plutzky J. Retinaldehyde dehydrogenase 1 coordinates hepatic gluconeogenesis and lipid metabolism. Endocrinology 2012, 153:3089-3099.
31. Kosicka A., Cunliffe A.D., Mackenzie R., Zariwala M.G., Perretti M., Flower R.J., Renshaw D. Attenuation of plasma annexin A1 in human obesity. FASEB J. 2013, 27:368-378.
32. Kuo Y.M., Shiue Y.L., Chen C.F., Tang P.C., Lee Y.P. Proteomic analysis of hypothalamic proteins of high and low egg production strains of chickens. Theriogenology 2005, 64:1490-1502.
33. Lagrost L., Gambert P., Meunier S., Morgado P., Desgres J., d'Athis P., Lallemant C. Correlation between apolipoprotein A-IV and triglyceride concentrations in human sera. J. Lipid Res. 1989, 30:701-710.
34. Lopez-Valencia V., Rangel P., Rodriguez S., Hernandez-Munoz R. Involvement of alcohol and aldehyde dehydrogenase activities on hepatic retinoid metabolism and its possible participation in the progression of rat liver regeneration. Biochem. Pharmacol. 2007, 73:586-596.
35. Mann M., Jensen O.N. Proteomic analysis of post-translational modifications. Nat. Biotechnol. 2003, 21:255-261.
36. Marongiu F., Conti M., Mameli G., Sorano G.G., Cossu E., Cirillo R., Balestrieri A. Is the imbalance between thrombin and plasmin activity in diabetes related to the behaviour of antiplasmin activity?. Thromb. Res. 1990, 58:91-99.
37. Matthews D.R., Hosker J.P., Rudenski A.S., Naylor B.A., Treacher D.F., Turner R.C. Homeostasis model assessment: insulin resistance and ß-cell function from fasting plasma insulin and glucose concentrations in man. Diabetologia 1985, 28:412-419.
38. McCarthy A.M., Spisak K.O., Brozinick J.T., Elmendorf J.S. Loss of cortical actin filaments in insulin-resistant skeletal muscle cells impairs GLUT4 vesicle trafficking and glucose transport. Am. J. Physiol. Cell. Physiol. 2006, 291:C860-C868.
39. Murata C., Taniyama M., Kuriyama S., Muramatsu T., Atsumi Y., Matsuoka K., Suzuki Y. Meta-analysis of three diabetes population studies: association of inactive ALDH2 genotype with maternal inheritance of diabetes. Diabetes. Res. Clin. Pract. 2004, 66(Suppl 1):S145-S147.
40. Neville M.J., Collins J.M., Gloyn A.L., McCarthy M.I., Karpe F. Comprehensive human adipose tissue mRNA and microRNA endogenous control selection for quantitative real-time-PCR normalization. Obesity (Silver Spring) 2011, 19:888-892.
41. Peinado J.R., Jimenez-Gomez Y., Pulido M.R., Ortega-Bellido M., Diaz-Lopez C., Padillo F.J., Lopez-Miranda J., Vazquez-Martinez R., Malagon M.M. The stromal-vascular fraction of adipose tissue contributes to major differences between subcutaneous and visceral fat depots. Proteomics 2010, 10:3356-3366.
42. Smith J.D., Borel A.L., Nazare J.A., Haffner S.M., Balkau B., Ross R., Massien C., Almeras N., Despres J.P. Visceral adipose tissue indicates the severity of cardiometabolic risk in patients with and without type 2 diabetes: results from the INSPIRE ME IAA study. J. Clin. Endocrinol. Metab. 2012, 97:1517-1525.
43. Sullivan P.W., Morrato E.H., Ghushchyan V., Wyatt H.R., Hill J.O. Obesity, inactivity, and the prevalence of diabetes and diabetes-related cardiovascular comorbidities in the U.S., 2000-2002. Diabetes Care 2005, 28:1599-1603.
44. Tinahones F.J., Coin Araguez L., Murri M., Oliva Olivera W., Mayas Torres M.D., Barbarroja N., Gomez Huelgas R., Malagon M.M., El Bekay R. Caspase Induction and BCL2 Inhibition in Human Adipose Tissue: a potential relationship with insulin signaling alteration. Diabetes Care 2013, 36:513-521.
45. Tsakiridis T., Vranic M., Klip A. Disassembly of the actin network inhibits insulin-dependent stimulation of glucose transport and prevents recruitment of glucose transporters to the plasma membrane. J. Biol. Chem. 1994, 269:29934-29942.
46. Verges B. Apolipoprotein A-IV in diabetes mellitus. Diabete Metab. 1995, 21:99-105.
47. Verges B., Guerci B., Durlach V., Galland-Jos C., Paul J.L., Lagrost L., Gambert P. Increased plasma apoA-IV level is a marker of abnormal postprandial lipemia: a study in normoponderal and obese subjects. J. Lipid Res. 2001, 42:2021-2029.
48. Wang F., Kohan A.B., Kindel T.L., Corbin K.L., Nunemaker C.S., Obici S., Woods S.C., Davidson W.S., Tso P. Apolipoprotein A-IV improves glucose homeostasis by enhancing insulin secretion. Proc. Natl. Acad. Sci. USA. 2012, 109:9641-9646.
49. Yohannes E., Chang J., Christ G.J., Davies K.P., Chance M.R. Proteomics analysis identifies molecular targets related to diabetes mellitus-associated bladder dysfunction. Mol. Cell. Proteomics 2008, 7:1270-1285.
50. Zhang Y., Babcock S.A., Hu N., Maris J.R., Wang H., Ren J. Mitochondrial aldehyde dehydrogenase (ALDH2) protects against streptozotocin-induced diabetic cardiomyopathy: role of GSK3beta and mitochondrial function. B.M.C. Med. 2012, 10:40.
51. Zhou X., Hurst R.D., Templeton D., Whiteside C.I. High glucose alters actin assembly in glomerular mesangial and epithelial cells. Lab. Invest. 1995, 73:372-383.