Imbalance between neutrophil elastase and its inhibitor α1-antitrypsin in obesity alters insulin sensitivity, inflammation, and energy expenditure

Cell Metabolism

Volumn 17, Issue 4, 2013, Pages 534-548

  Mansuy Aubert, Virginie ^a   Zhou, Qiong L ^a   Xie, Xiangyang ^a   Gong, Zhenwei ^a   Huang, Jun Yuan ^a   Khan, Abdul R ^a,b   Aubert, Gregory ^a   Candelaria, Karla ^a   Thomas, Shantele ^a   Shin, Dong Ju ^a   Booth, Sarah ^c   Baig, Shahid M ^b   Bilal, Ahmed ^d   Hwang, Daehee ^e   Zhang, Hui ^e,f   Lovell Badge, Robin ^c   Smith, Steven R ^a,g   Awan, Fazli R ^b   Jiang, Zhen Y ^a  

^a BURNHAM INSTITUTE   (United States)

^b NATIONAL INSTITUTE FOR BIOTECHNOLOGY AND GENETIC ENGINEERING NIBGE   (Pakistan)

^c NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^d Allied Hospital Pakistan   (Pakistan)

^e INSTITUTE FOR SYSTEMS BIOLOGY   (United States)

^f JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^g FLORIDA HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADIPONECTIN; ALPHA 1 ANTITRYPSIN; LEUKOCYTE ELASTASE; PROTEIN KINASE; UNCOUPLING PROTEIN 1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; BROWN ADIPOSE TISSUE; CONTROLLED STUDY; DISEASE COURSE; ENERGY EXPENDITURE; ENZYME BLOOD LEVEL; FATTY ACID OXIDATION; FATTY LIVER; INFLAMMATION; INSULIN SENSITIVITY; LIPID DIET; MOUSE; NONHUMAN; OBESITY; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; TRANSGENIC MOUSE; WEIGHT GAIN;

ADIPONECTIN; ADIPOSE TISSUE, BROWN; ALPHA 1-ANTITRYPSIN; ANIMALS; DIET, HIGH-FAT; ENERGY METABOLISM; FATTY ACIDS; FATTY LIVER; HEP G2 CELLS; HUMANS; INFLAMMATION; INSULIN RESISTANCE; ION CHANNELS; LEPTIN; LEUKOCYTE ELASTASE; LIVER; METABOLOME; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, OBESE; MICE, TRANSGENIC; MITOCHONDRIAL PROTEINS; OBESITY; OXIDATION-REDUCTION; PHOSPHORYLATION; PIPERIDINES; PROTEIN KINASES; WEIGHT GAIN;

MUS; MUS MUSCULUS;

EID: 84875900576     PISSN: 15504131     EISSN: 19327420     Source Type: Journal    
DOI: 10.1016/j.cmet.2013.03.005     Document Type: Article

References (40)

1. M. Awazawa, K. Ueki, K. Inabe, T. Yamauchi, N. Kubota, K. Kaneko, M. Kobayashi, A. Iwane, T. Sasako, and Y. Okazaki Adiponectin enhances insulin sensitivity by increasing hepatic IRS-2 expression via a macrophage-derived IL-6-dependent pathway Cell Metab. 13 2011 401 412
2. A. Belaaouaj, R. McCarthy, M. Baumann, Z. Gao, T.J. Ley, S.N. Abraham, and S.D. Shapiro Mice lacking neutrophil elastase reveal impaired host defense against gram negative bacterial sepsis Nat. Med. 4 1998 615 618
3. V. Elgazar-Carmon, A. Rudich, N. Hadad, and R. Levy Neutrophils transiently infiltrate intra-abdominal fat early in the course of high-fat feeding J. Lipid Res. 49 2008 1894 1903
4. M. Feuerer, L. Herrero, D. Cipolletta, A. Naaz, J. Wong, A. Nayer, J. Lee, A.B. Goldfine, C. Benoist, S. Shoelson, and D. Mathis Lean, but not obese, fat is enriched for a unique population of regulatory T cells that affect metabolic parameters Nat. Med. 15 2009 930 939
5. G.S. Hotamisligil Inflammation and metabolic disorders Nature 444 2006 860 867
6. T. Kadowaki, T. Yamauchi, N. Kubota, K. Hara, K. Ueki, and K. Tobe Adiponectin and adiponectin receptors in insulin resistance, diabetes, and the metabolic syndrome J. Clin. Invest. 116 2006 1784 1792
7. B.B. Kahn, T. Alquier, D. Carling, and D.G. Hardie AMP-activated protein kinase: ancient energy gauge provides clues to modern understanding of metabolism Cell Metab. 1 2005 15 25
8. N. Kalsheker, S. Morley, and K. Morgan Gene regulation of the serine proteinase inhibitors alpha1-antitrypsin and alpha1-antichymotrypsin Biochem. Soc. Trans. 30 2002 93 98
9. N. Kamei, K. Tobe, R. Suzuki, M. Ohsugi, T. Watanabe, N. Kubota, N. Ohtsuka-Kowatari, K. Kumagai, K. Sakamoto, and M. Kobayashi Overexpression of monocyte chemoattractant protein-1 in adipose tissues causes macrophage recruitment and insulin resistance J. Biol. Chem. 281 2006 26602 26614
10. G.D. Kelsey, S. Povey, A.E. Bygrave, and R.H. Lovell-Badge Species- and tissue-specific expression of human alpha 1-antitrypsin in transgenic mice Genes Dev. 1 1987 161 171
11. B. Korkmaz, M.S. Horwitz, D.E. Jenne, and F. Gauthier Neutrophil elastase, proteinase 3, and cathepsin G as therapeutic targets in human diseases Pharmacol. Rev. 62 2010 726 759
12. R.S. Labow, D.J. Erfle, and J.P. Santerre Elastase-induced hydrolysis of synthetic solid substrates: poly(ester-urea-urethane) and poly(ether-urea- urethane) Biomaterials 17 1996 2381 2388
13. J. Liu, A. Divoux, J. Sun, J. Zhang, K. Clément, J.N. Glickman, G.K. Sukhova, P.J. Wolters, J. Du, and C.Z. Gorgun Genetic deficiency and pharmacological stabilization of mast cells reduce diet-induced obesity and diabetes in mice Nat. Med. 15 2009 940 945
14. C.N. Lumeng, and A.R. Saltiel Inflammatory links between obesity and metabolic disease J. Clin. Invest. 121 2011 2111 2117
15. C.N. Lumeng, J.L. Bodzin, and A.R. Saltiel Obesity induces a phenotypic switch in adipose tissue macrophage polarization J. Clin. Invest. 117 2007 175 184
16. S.J. Macdonald, M.D. Dowle, L.A. Harrison, P. Shah, M.R. Johnson, G.G. Inglis, G.D. Clarke, R.A. Smith, D. Humphreys, and C.R. Molloy The discovery of a potent, intracellular, orally bioavailable, long duration inhibitor of human neutrophil elastase - GW311616A a development candidate Bioorg. Med. Chem. Lett. 11 2001 895 898
17. M.G. Myers Jr., R.L. Leibel, R.J. Seeley, and M.W. Schwartz Obesity and leptin resistance: distinguishing cause from effect Trends Endocrinol. Metab. 21 2010 643 651
18. S. Nishimura, I. Manabe, M. Nagasaki, K. Eto, H. Yamashita, M. Ohsugi, M. Otsu, K. Hara, K. Ueki, and S. Sugiura CD8+ effector T cells contribute to macrophage recruitment and adipose tissue inflammation in obesity Nat. Med. 15 2009 914 920
19. K. Ohashi, J.L. Parker, N. Ouchi, A. Higuchi, J.A. Vita, N. Gokce, A.A. Pedersen, C. Kalthoff, S. Tullin, and A. Sams Adiponectin promotes macrophage polarization toward an anti-inflammatory phenotype J. Biol. Chem. 285 2010 6153 6160
20. O. Osborn, and J.M. Olefsky The cellular and signaling networks linking the immune system and metabolism in disease Nat. Med. 18 2012 363 374
21. N. Ouchi, J.L. Parker, J.J. Lugus, and K. Walsh Adipokines in inflammation and metabolic disease Nat. Rev. Immunol. 11 2011 85 97
22. U.B. Pajvani, X. Du, T.P. Combs, A.H. Berg, M.W. Rajala, T. Schulthess, J. Engel, M. Brownlee, and P.E. Scherer Structure-function studies of the adipocyte-secreted hormone Acrp30/adiponectin. Implications fpr metabolic regulation and bioactivity J. Biol. Chem. 278 2003 9073 9085
23. C.T. Pham Neutrophil serine proteases: specific regulators of inflammation Nat. Rev. Immunol. 6 2006 541 550
24. R.K. Semple, N.H. Halberg, K. Burling, M.A. Soos, T. Schraw, J. Luan, E.K. Cochran, D.B. Dunger, N.J. Wareham, and P.E. Scherer Paradoxical elevation of high-molecular weight adiponectin in acquired extreme insulin resistance due to insulin receptor antibodies Diabetes 56 2007 1712 1717
25. S. Shetty, C.M. Kusminski, and P.E. Scherer Adiponectin in health and disease: evaluation of adiponectin-targeted drug development strategies Trends Pharmacol. Sci. 30 2009 234 239
26. S. Shetty, M.A. Ramos-Roman, Y.R. Cho, J. Brown, J. Plutzky, E.S. Muise, J.D. Horton, P.E. Scherer, and E.J. Parks Enhanced fatty acid flux triggered by adiponectin overexpression Endocrinology 153 2012 113 122
27. S.E. Shoelson, J. Lee, and A.B. Goldfine Inflammation and insulin resistance J. Clin. Invest. 116 2006 1793 1801
28. K. Sun, C.M. Kusminski, and P.E. Scherer Adipose tissue remodeling and obesity J. Clin. Invest. 121 2011 2094 2101
29. S. Sun, Y. Ji, S. Kersten, and L. Qi Mechanisms of inflammatory responses in obese adipose tissue Annu. Rev. Nutr. 32 2012 261 286
30. S. Talukdar, Y. Oh, G. Bandyopadhyay, D. Li, J. Xu, J. McNelis, M. Lu, P. Li, Q. Yan, and Y. Zhu Neutrophils mediate insulin resistance in mice fed a high-fat diet through secreted elastase Nat. Med. 18 2012 1407 1412
31. Y. Tian, Y. Zhou, S. Elliott, R. Aebersold, and H. Zhang Solid-phase extraction of N-linked glycopeptides Nat. Protoc. 2 2007 334 339
32. A.T. Turer, and P.E. Scherer Adiponectin: mechanistic insights and clinical implications Diabetologia 55 2012 2319 2326
33. H. Waki, T. Yamauchi, J. Kamon, Y. Ito, S. Uchida, S. Kita, K. Hara, Y. Hada, F. Vasseur, and P. Froguel Impaired multimerization of human adiponectin mutants associated with diabetes. Molecular structure and multimer formation of adiponectin J. Biol. Chem. 278 2003 40352 40363
34. H. Waki, T. Yamauchi, J. Kamon, S. Kita, Y. Ito, Y. Hada, S. Uchida, A. Tsuchida, S. Takekawa, and T. Kadowaki Generation of globular fragment of adiponectin by leukocyte elastase secreted by monocytic cell line THP-1 Endocrinology 146 2005 790 796
35. S.P. Weisberg, D. McCann, M. Desai, M. Rosenbaum, R.L. Leibel, and A.W. Ferrante Jr. Obesity is associated with macrophage accumulation in adipose tissue J. Clin. Invest. 112 2003 1796 1808
36. D.A. Winer, S. Winer, L. Shen, P.P. Wadia, J. Yantha, G. Paltser, H. Tsui, P. Wu, M.G. Davidson, and M.N. Alonso B cells promote insulin resistance through modulation of T cells and production of pathogenic IgG antibodies Nat. Med. 17 2011 610 617
37. H. Xu, G.T. Barnes, Q. Yang, G. Tan, D. Yang, C.J. Chou, J. Sole, A. Nichols, J.S. Ross, L.A. Tartaglia, and H. Chen Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance J. Clin. Invest. 112 2003 1821 1830
38. T. Yamauchi, J. Kamon, Y. Minokoshi, Y. Ito, H. Waki, S. Uchida, S. Yamashita, M. Noda, S. Kita, and K. Ueki Adiponectin stimulates glucose utilization and fatty-acid oxidation by activating AMP-activated protein kinase Nat. Med. 8 2002 1288 1295
39. T. Yoshimura, L.N. Barker, and J.C. Powers Specificity and reactivity of human leukocyte elastase, porcine pancreatic elastase, human granulocyte cathepsin G, and bovine pancreatic chymotrypsin with arylsulfonyl fluorides. Discovery of a new series of potent and specific irreversible elastase inhibitors J. Biol. Chem. 257 1982 5077 5084
40. H. Zhang, X.J. Li, D.B. Martin, and R. Aebersold Identification and quantification of N-linked glycoproteins using hydrazide chemistry, stable isotope labeling and mass spectrometry Nat. Biotechnol. 21 2003 660 666