Macrophage metalloelastase (MMP12) regulates adipose tissue expansion, insulin sensitivity, and expression of inducible nitric oxide synthase

Endocrinology (United States)

Volumn 155, Issue 9, 2014, Pages 3409-3420

  Lee, Jung Ting ^a   Pamir, Nathalie ^a   Liu, Ning Chun ^a   Kirk, Elizabeth A ^b   Averill, Michelle M ^a   Becker, Lev ^a   Larson, Ilona ^d   Hagman, Derek K ^c   Foster Schubert, Karen E ^a   Van Yserloo, Brian ^a   Bornfeldt, Karin E ^a,b   LeBoeuf, Renee C ^a   Kratz, Mario ^a,b,c   Heinecke, Jay W ^a  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

^c Fred Hutchinson Cancer Research Center   (United States)

^d NONE

Author keywords

[No Author keywords available]

Indexed keywords

CD14 ANTIGEN; INDUCIBLE NITRIC OXIDE SYNTHASE; INSULIN; MACROPHAGE ELASTASE; NITRIC OXIDE;

ADIPOSE TISSUE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BODY COMPOSITION; BONE MARROW DERIVED MACROPHAGE; CONTROLLED STUDY; DENDRITIC CELL; FLOW CYTOMETRY; GLUCOSE HOMEOSTASIS; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IN VITRO STUDY; INSULIN RESISTANCE; INSULIN SENSITIVITY; MACROPHAGE; MOUSE; NONHUMAN; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; SUBCUTANEOUS FAT; WILD TYPE; ADULT; ANIMAL; C57BL MOUSE; ENZYMOLOGY; FEMALE; GENETICS; GROWTH, DEVELOPMENT AND AGING; MALE; METABOLISM; MIDDLE AGED; MOUSE MUTANT; OBESITY; YOUNG ADULT;

ADIPOSE TISSUE; ADULT; ANIMALS; FEMALE; HUMANS; INSULIN; INSULIN RESISTANCE; MACROPHAGES; MALE; MATRIX METALLOPROTEINASE 12; MICE; MICE, INBRED C57BL; MICE, OBESE; MIDDLE AGED; NITRIC OXIDE SYNTHASE TYPE II; OBESITY; YOUNG ADULT;

EID: 84907043854     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2014-1037     Document Type: Article

References (47)

1. Lumeng CN, Saltiel AR. Inflammatory links between obesity and metabolic disease. J Clin Invest. 2011;121:2111-2117.
2. Semenkovich C. Insulin resistance and atherosclerosis. J Clin Invest. 2006;116:1813-1822.
3. Scherer PE. Adipose tissue: from lipid storage compartment to endocrine organ. Diabetes. 2006;55:1537-1545.
4. Chawla A, Nguyen KD, Goh YP. Macrophage-mediated inflammation in metabolic disease. Nat Rev Immunol. 2011;11:738-749.
5. de Luca C, Olefsky JM. Inflammation and insulin resistance. FEBS Lett. 2008;582:97-105.
6. Nguyen MT, Favelyukis S, Nguyen AK, et al. A subpopulation of macrophages infiltrates hypertrophic adipose tissue and is activated by free fatty acids via Toll-like receptors 2 and 4 and JNK-dependent pathways. J Biol Chem. 2007;282:35279-35292.
7. Weisberg SP, McCann D, Desai M, Rosenbaum M, Leibel RL, Ferrante AW Jr. Obesityisassociated with macrophage accumulation in adipose tissue. J Clin Invest. 2003;112:1796-1808.
8. Xu H, Barnes GT, Yang Q, et al. Chronic inflammation in fat plays acrucialroleinthedevelopmentofobesity-relatedinsulin resistance. J Clin Invest. 2003;112:1821-1830.
9. Arkan MC, Hevener AL, Greten FR, et al. IKK-beta links inflammation to obesity-induced insulin resistance. Nat Med. 2005;11: 191-198.
10. Hevener AL, Olefsky JM, Reichart D, et al. Macrophage PPAR gamma is required for normal skeletal muscle and hepatic insulin sensitivity and full antidiabetic effects of thiazolidinediones. J Clin Invest. 2007;117:1658-1669.
11. Li P, Lu M, Nguyen M, et al. Functional heterogeneity of CD11c-positive adipose tissue macrophages in diet-induced obese mice. J Biol Chem. 2010;285:15333-15345.
12. Lumeng CN, Bodzin JL, Saltiel AR. Obesity induces a phenotypic switch in adipose tissue macrophage polarization. J Clin Invest. 2007;117:175-184.
13. Lumeng CN, Del Proposto JB, Westcott DJ, Saltiel AR. Phenotypic switchingofadipose tissuemacrophages withobesityisgeneratedby spatiotemporal differences in macrophage subtypes. Diabetes. 2008;57:3239-3246.
14. Odegaard JI, Ricardo-Gonzalez RR, Goforth MH, et al. Macro-phage-specific PPARgamma controls alternative activation and improves insulin resistance. Nature. 2007;447:1116-1120.
15. Chavey C, Mari B, Monthouel MN, et al. Matrix metalloproteinases are differentially expressed in adipose tissue during obesity and modulate adipocyte differentiation. J Biol Chem. 2003;278:11888-11896.
16. Maquoi E, Munaut C, Colige A, Collen D, Lijnen HR. Modulation of adipose tissue expression of murine matrix metalloproteinases and their tissue inhibitors with obesity. Diabetes. 2002;51:1093-1101.
17. Belaaouaj A, Shipley JM, Kobayashi DK, et al. Human macrophage metalloelastase. Genomic organization, chromosomal location, gene linkage, and tissue-specific expression. J Biol Chem. 1995;270: 14568-14575.
18. Werb Z, Gordon S. Elastase secretion by stimulated macrophages. Characterization and regulation. J Exp Med. 1975;142:361-377.
19. Rader DJ, Daugherty A. Translating molecular discoveries into new therapies for atherosclerosis. Nature. 2008;451:904-913.
20. Witztum JL, Steinberg D. Role of oxidized low density lipoprotein in atherogenesis. J Clin Invest. 1991;88:1785-1792.
21. Lijnen HR, Maquoi E, Hansen LB, Van Hoef B, Frederix L, Collen D. Matrix metalloproteinase inhibition impairs adipose tissue development in mice. Arterioscler Thromb Vasc Biol. 2002;22:374-379.
22. Bauters D, Van Hul M, Lijnen H. Macrophage elastase (MMP-12) in expanding murine adipose tissue. Biochim Biophys Acta. 2013; 1830:2954-2959.
23. Kratz M, Kuzma JN, Hagman DK, et al. n3 PUFAs do not affect adipose tissue inflammation in overweight to moderately obese men and women. J Nutr. 2013;143:1340-1347.
24. Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC. Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia. 1985;28:412-419.
25. Becker L, Liu N-C, Averill MM, et al. Unique proteomic signatures distinguish macrophages and dendritic cells. PLoS One. 2012;7: e33297.
26. Mystkowski P, Shankland E, Schreyer SA, et al. Validationofwhole-body magnetic resonance spectroscopy as a tool to assess murine body composition. Int J Obes Relat Metab Disord. 2000;24:719-724.
27. Pamir N, McMillen TS, Kaiyala KJ, Schwartz MW, LeBoeuf RC. Receptors for tumor necrosis factor-alpha play a protective role against obesity and alter adipose tissue macrophage status. Endocrinology. 2009;150:4124-4134.
28. Campbell KL, Makar KW, Kratz M, Foster-Schubert KE, McTiernan A, Ulrich CM. A pilot study of sampling subcutaneous adipose tissuetoexamine biomarkers of cancer risk. Cancer Prev Res (Phila). 2009;2:37-42.
29. Soukas A, Socci ND, Saatkamp BD, Novelli S, Friedman JM. Distinct transcriptional profiles of adipogenesis in vivo and in vitro. J Biol Chem. 2001;276:34167-34174.
30. Pamir N, McMillen TS, Li YI, Lai CM, Wong H, LeBoeuf RC. Overexpression of apolipoprotein A5 in mice is not protective against body weight gain and aberrant glucose homeostasis. Metabolism. 2009;58:560-567.
31. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods. 2001;25:402-408.
32. Becker L, Gharib SA, Irwin AD, et al. A macrophage sterol-respon-sive network linked to atherogenesis. Cell Metab. 2010;11:125-135.
33. Gordon S, Taylor PR. Monocyte and macrophage heterogeneity. Nat Rev Immunol. 2005;5:953-964.
34. Inaba K, Inaba M, Romani N, et al. Generation of large numbers of dendritic cells from mouse bone marrow cultures supplemented with granulocyte/macrophage colony-stimulating factor. J Exp Med. 1992;176:1693-1702.
35. Gordon S. Macrophage heterogeneity and tissue lipids. J Clin Invest. 2007;117:89-93.
36. Shaul ME, Bennett G, Strissel KJ, Greenberg AS, Obin MS. Dynamic, M2-like remodeling phenotypes of CD11c+ adipose tissue macrophages during high-fat diet-induced obesity in mice. Diabetes. 2010;59:1171-1181.
37. Cinti S, Mitchell G, Barbatelli G, et al. Adipocyte death defines macrophage localization and function in adipose tissue of obese mice and humans. J Lipid Res. 2005;46:2347-2355.
38. Combs TP, Pajvani UB, Berg AH, et al. A transgenic mouse with a deletion in the collagenous domain of adiponectin displays elevated circulating adiponectin and improved insulin sensitivity. Endocrinology. 2004;145:367-383.
39. Hume D. Differentiation and heterogeneity in the mononuclear phagocyte system. Mucosal Immunol. 2008;1:432-441.
40. Yang S, Kim J, Ryu JH, et al. Hypoxia-inducible factor-2alpha is a catabolic regulator of osteoarthritic cartilage destruction. Nat Med. 2010;16:687-693.
41. Eskin E. Increasing power in association studies by using linkage disequilibrium structure and molecular function as prior information. Genome Res. 2008;18:653-660.
42. Lu M, Li P, Pferdekamper J, et al. Inducible nitric oxide synthase deficiency in myeloid cells does not prevent diet-induced insulin resistance. Mol Endocrinol. 2010;24:1413-1422.
43. Ganesan S, Faris A, Comstock A, et al. Quercetin prevents progression of disease in elastase/LPS-exposed mice by negatively regulating MMP expression. Respir Res. 2010;11:131.
44. Rigotti A, Trigatti BL, Penman M, Rayburn H, Herz J, Krieger M. A targeted mutation in the murine gene encoding the high density lipoprotein (HDL) receptor scavenger receptor class B type I reveals its key role in HDL metabolism. Proc Natl Acad Sci USA. 1997; 94:12610-12615.
45. Wang N, Lan D, Chen W, Matsuura F, Tall AR. ATP-binding cassette transporters G1 and G4 mediate cellular cholesterol efflux to high-density lipoproteins. Proc Natl Acad Sci USA. 2004;101: 9774-9779.
46. Hotary KB, Allen ED, Brooks PC, Datta NS, Long MW, Weiss SJ. Membrane type I matrix metalloproteinase usurps tumor growth control imposed by the three-dimensional extracellular matrix. Cell. 2003;114:33-45.
47. Alexander CM, Selvarajan S, Mudgett J, Werb Z. Stromelysin-1 regulates adipogenesis during mammary gland involution. J Cell Biol. 2001;152:693-703.