Adipose tissue inflammation and insulin resistance: All obese humans are not created equal

Biochemical Journal

Volumn 430, Issue 2, 2010, Pages

  Gauthier, Marie Soleil ^a,b   Ruderman, Neil B ^c  

^a CENTRE HOSPITALIER DE L UNIVERSITÉ DE MONTRÉAL   (Canada)

^b CLIN RESEARCH INSTITUTE OF MONTREAL   (Canada)

^c BOSTON UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Adipose tissue; AMP activated protein kinase (AMPK); Inflammation; Insulin resistance; Insulin sensitive obese (ISO); Metabolically healthy obese (MHO); Obesity

Indexed keywords

ADIPOSE TISSUE; BODY MASS; GLUCOSE METABOLISM; HUMAN; INSULIN RESISTANCE; METABOLIC SYNDROME X; NOTE; OBESITY; OXIDATIVE STRESS; PRIORITY JOURNAL; WHITE ADIPOSE TISSUE; IMMUNOLOGY; INTRAABDOMINAL FAT; METABOLISM;

HUMANS; INSULIN RESISTANCE; INTRA-ABDOMINAL FAT; OBESITY;

EID: 77956666561     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20101062     Document Type: Note

References (46)

1. Karelis, A. D. (2008) Metabolically healthy but obese individuals. Lancet 372, 1281-1283
2. Sims, E. A. H. (2001) Are there persons who are obese, but metabolically healthy? Metab., Clin. Exp. 50, 1499-1504
3. Andres, R. (1980) Effect of obesity on total mortality. Int. J. Obes. 4, 381-386
4. Sims, E. A. H. (1982) Characterization of the syndromes of obesity. In Diabetes Mellitus and Obesity (Brodoff, B. N. and Bleicher, S. J., eds), pp. 219-226, Williams & Wilkins, Baltimore
5. Wildman, R. P., Muntner, P., Reynolds, K., McGinn, A. P., Rajpathak, S., Wylie-Rosett, J. and Sowers, M. R. (2008) The obese without cardiometabolic risk factor clustering and the normal weight with cardiometabolic risk factor clustering: prevalence and correlates of 2 phenotypes among the US population (NHANES 1999-2004). Arch. Intern. Med. 168, 1617-1624
6. Klöting, N., Fasshauer, M., Dietrich, A., Kovacs, P., Schön, M. R., Kern, M., Stumvoll, M. and Bluher, M. (2010) Insulin sensitive obesity. Am. J. Physiol. Endocrinol. Metab., doi:10.1152/ajpendo.00586.2009
7. Karelis, A. D., Faraj, M., Bastard, J.-P., St-Pierre, D. H., Brochu, M., Prud'homme, D. and Rabasa-Lhoret, R. (2005) The metabolically healthy but obese individual presents a favorable inflammation profile. J. Clin. Endocrinol. Metab. 90, 4145-4150
8. Shin, M.-J., Hyun, Y. J., Kim, O. Y., Kim, J. Y., Jang, Y. and Lee, J. H. (2006) Weight loss effect on inflammation and LDL oxidation in metabolically healthy but obese (MHO) individuals: low inflammation and LDL oxidation in MHO women. Int. J. Obes. 30, 1529-1534
9. Lynch, L. A., O'Connell, J. M., Kwasnik, A. K., Cawood, T. J., O'Farrelly, C. and O'Shea, D. B. (2008) Are natural killer cells protecting the metabolically healthy obese patient? Obesity 17, 601-605
10. Stefan, N., Kantartzis, K., Machann, J., Schick, F., Thamer, C., Rittig, K., Balletshofer, B., Machicao, F., Fritsche, A. and Haring, H.-U. (2008) Identification and characterization of metabolically benign obesity in humans. Arch. Intern. Med. 168, 1609-1616
11. Messier, V., Karelis, A. D., Robillard, M. E., Bellefeuille, P., Brochu, M., Lavoie, J. M. and Rabasa-Lhoret, R. (2010) Metabolically healthy but obese individuals: relationship with hepatic enzymes. Metab., Clin. Exp. 59, 20-24
12. Tinahones, F. J., Garrido-Sanchez, L., Miranda, M., Garcia-Almeida, J. M., Macias-Gonzalez, M., Ceperuelo, V., Gluckmann, E., Rivas-Marin, J., Vendrell, J. and Garcia-Fuentes, E. (2010) Obesity and insulin resistance-related changes in the expression of lipogenic and lipolytic genes in morbidly obese subjects. Obes. Surg., doi:10.1007/s11695-010-0194-z
13. McLaughlin, T., Sherman, A., Tsao, P., Gonzalez, O., Yee, G., Lamendola, C., Reaven, G. M. and Cushman, S. W. (2007) Enhanced proportion of small adipose cells in insulin-resistant vs insulin-sensitive obese individuals implicates impaired adipogenesis. Diabetologia 50, 1707-1715
14. Aguilar-Salinas, C. A., Garcia, E. G., Robles, L., Riano, D., Ruiz-Gomez, D. G., Garcia-Ulloa, A. C., Melgarejo, M. A., Zamora, M., Guillen-Pineda, L. E., Mehta, R. et al. (2008) High adiponectin concentrations are associated with the metabolically healthy obese phenotype. J. Clin. Endocrinol. Metab. 93, 4075-4079
15. Unger, R. H. (2003) Weapons of lean body mass destruction: the role of ectopic lipids in the metabolic syndrome. Endocrinology 144, 5159-5165
16. Puri, V., Ranjit, S., Konda, S., Nicoloro, S. M. C., Straubhaar, J., Chawla, A., Chouinard, M., Lin, C., Burkart, A., Corvera, S. et al. (2008) Cidea is associated with lipid droplets and insulin sensitivity in humans. Proc. Natl. Acad. Sci. U.S.A. 105, 7833-7838
17. Greenberg, A., Egan, J., Wek, S., Garty, N., Blanchette-Mackie, E. and Londos, C. (1991) Perilipin, a major hormonally regulated adipocyte-specific phosphoprotein associated with the periphery of lipid storage droplets. J. Biol. Chem. 266, 11341-11346
18. Hotamisligil, G., Shargill, N. and Spiegelman, B. (1993) Adipose expression of tumor necrosis factor-α: direct role in obesity-linked insulin resistance. Science 259, 87-91
19. Feinstein, R., Kanety, H., Papa, M. Z., Lunenfeld, B. and Karasik, A. (1993) Tumor necrosis factor-α suppresses insulin-induced tyrosine phosphorylation of insulin receptor and its substrates. J. Biol. Chem. 268, 26055-26058
20. de Luca, C. and Olefsky, J. M. (2008) Inflammation and insulin resistance. FEBS Lett. 582, 97-105
21. Clement, K. and Langin, D. (2007) Regulation of inflammation-related genes in human adipose tissue. J. Intern. Med. 262, 422-430
22. Cinti, S., Mitchell, G., Barbatelli, G., Murano, I., Ceresi, E., Faloia, E., Wang, S., Fortier, M., Greenberg, A. S. and Obin, M. S. (2005) Adipocyte death defines macrophage localization and function in adipose tissue of obese mice and humans. J. Lipid Res. 46, 2347-2355 (Pubitemid 41532523)
23. Strissel, K. J., Stancheva, Z., Miyoshi, H., Perfield, II, J. W., DeFuria, J., Jick, Z., Greenberg, A. S. and Obin, M. S. (2007) Adipocyte death, adipose tissue remodeling and obesity complications. Diabetes 56, 2910-2918
24. Xu, H., Barnes, G. T., Yang, Q., Tan, G., Yang, D., Chou, C. J., Sole, J., Nichols, A., Ross, J. S., Tartaglia, L. A. and Chen, H. (2003) Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance. J. Clin. Invest. 112, 1821-1830
25. Weisberg, S. P., McCann, D., Desai, M., Rosenbaum, M., Leibel, R. L. and Ferrante, Jr, A. W. (2003) Obesity is associated with macrophage accumulation in adipose tissue. J. Clin. Invest. 112, 1796-1808
26. Abbasi, F., Chu, J. W., Lamendola, C., McLaughlin, T., Hayden, J., Reaven, G. M. and Reaven, P. D. (2004) Discrimination between obesity and insulin resistance in the relationship with adiponectin. Diabetes 53, 585-590
27. Weiss, R., Taksali, S. E., Dufour, S., Yeckel, C. W., Papademetris, X., Cline, G., Tamborlane, W. V., Dziura, J., Shulman, G. I. and Caprio, S. (2005) The 'obese insulin-sensitive' adolescent: importance of adiponectin and lipid partitioning. J. Clin. Endocrinol. Metab. 90, 3731-3737
28. Barbarroja, N., Lopez-Pedrera, R., Mayas, M. D., Garcia-Fuentes, E., Garrido-Sanchez, L., Macias-Gonzalez, M., El Bekay, R., Vidal-Puig, A. and Tinahones, F. J. (2010) The obese healthy paradox: is inflammation the answer? Biochem. J. 430, 141-150
29. McLaughlin, T., Deng, A., Gonzales, O., Aillaud, M., Yee, G., Lamendola, C., Abbasi, F., Connolly, A., Sherman, A., Cushman, S. et al. (2008) Insulin resistance is associated with a modest increase in inflammation in subcutaneous adipose tissue of moderately obese women. Diabetologia 51, 2303-2308
30. Apovian, C. M., Bigornia, S., Mott, M., Meyers, M. R., Ulloor, J., Gagua, M., McDonnell, M., Hess, D., Joseph, L. and Gokce, N. (2008) Adipose macrophage infiltration is associated with insulin resistance and vascular endothelial dysfunction in obese subjects. Arterioscler. Thromb. Vasc. Biol. 28, 1654-1659
31. Khan, T., Muise, E. S., Iyengar, P., Wang, Z. V., Chandalia, M., Abate, N., Zhang, B. B., Bonaldo, P., Chua, S. and Scherer, P. E. (2009) Metabolic dysregulation and adipose tissue fibrosis: role of collagen VI. Mol. Cell. Biol. 29, 1575-1591
32. Pasarica, M., Gowronska-Kozak, B., Burk, D., Remedios, I., Hymel, D., Gimble, J., Ravussin, E., Bray, G. A. and Smith, S. R. (2009) Adipose tissue collagen VI in obesity. J. Clin. Endocrinol. Metab. 94, 5155-5162
33. Halberg, N., Khan, T., Trujillo, M. E., Wernstedt-Asterholm, I., Attie, A. D., Sherwani, S., Wang, Z. V., Landskroner-Eiger, S., Dineen, S., Magalang, U. J. et al. (2009) HIF-1α induces fibrosis and insulin resistance in white adipose tissue. Mol. Cell. Biol. 29, 4467-4483
34. Hardie, D. and Carling, D. (1997) The AMP-activated protein kinase-fuel gauge of the mammalian cell? Eur. J. Biochem. 246, 259-273
35. Nagata, D., Mogi, M. and Walsh, K. (2003) AMP-activated protein kinase (AMPK) signaling in endothelial cells is essential for angiogenesis in response to hypoxic stress. J. Biol. Chem. 278, 31000-31006
36. Shimano, M., Ouchi, N., Shibata, R., Ohashi, K., Pimentel, D. R., Murohara, T. and Walsh, K. (2010) Adiponectin deficiency exacerbates cardiac dysfunction following pressure overload through disruption of an AMPK-dependent angiogenic response. J. Mol. Cell. Cardiol. 49, 210-220
37. Ohashi, K., Ouchi, N., Higuchi, A., Shaw, R. J. and Walsh, K. (2010) LKB1 deficiency in Tie2-Cre-expressing cells impairs ischemia-induced angiogenesis. J. Biol. Chem. 285, 22291-22298
38. Ruderman, N. B., Xu, X. J., Nelson, L., Cacicedo, J. M., Saha, A. K., Lan, F. and Ido, Y. (2010) AMPK and SIRT1: a long-standing partnership? Am. J. Physiol. Endocrinol. Metab. 298, E751-E760
39. Ruderman, N. and Prentki, M. (2004) AMP kinase and malonyl-CoA: targets for therapy of the metabolic syndrome. Nat. Rev. Drug Discovery 3, 340-351
40. Gaidhu, M. P., Anthony, N. M., Patel, P., Hawke, T. J. and Ceddia, R. B. (2010) Dysregulation of lipolysis and lipid metabolism in visceral and subcutaneous adipocytes by high-fat diet: role of ATGL, HSL, and AMPK. Am. J. Physiol. Cell Physiol. 298, C961-C971
41. Yang, Z., Kahn, B. B., Shi, H. and Xue, B. Z. (2010) Macrophage α1-AMP-activated protein kinase (α1AMPK) antagonizes fatty acid-induced inflammation through SIRT1. J. Biol. Chem. 285, 19051-19059
42. Cacicedo, J. M., Yagihashi, N., Keaney, Jr, J. F., Ruderman, N. B. and Ido, Y. (2004) AMPK inhibits fatty acid-induced increases in NF-κB transactivation in cultured human umbilical vein endothelial cells. Biochem. Biophys. Res. Commun. 324, 1204-1209
43. Katerelos, M., Mudge, S. J., Stapleton, D., Auwardt, R. B., Fraser, S. A., Chen, C.-G., Kemp, B. E. and Power, D. A. (2010) 5-Aminoimidazole-4- carboxamide ribonucleoside and AMP-activated protein kinase inhibit signalling through NF-κB. Immunol. Cell Biol., doi:10.1038/icb.2010.44
44. Gauthier, M.-S., O'Brien, E., Bigornia, S. J., Mott, M. M., Gokce, N., Apovian, C. M. and Ruderman, N. B. (2009) Decreased AMP-activated protein kinase activity is associated with markers of inflammation and infiltration of immune cells in visceral and subcutaneous adipose tissue, and with whole-body insulin resistance in obese patients. Obesity 17, S93
45. Gauthier, M.-S., Tao, R., Luo, Z. J., Schultz, V., Cacicedo, J., Perfield, J., Greenberg, A. and Ruderman, N. B. (2008) Inhibition of AMP-activated protein kinase activation during the stimulation of lipolysis augments energy depletion, oxidative stress, and inflammation in 3T3-L1 adipocytes. Obesity 16, S73
46. Gauthier, M.-S., Miyoshi, H., Souza, S. C., Cacicedo, J. M., Saha, A. K., Greenberg, A. S. and Ruderman, N. B. (2008) AMP-activated protein kinase is activated as a consequence of lipolysis in the adipocyte: potential mechanism and physiological relevance. J. Biol. Chem. 283, 16514-16524