TIMP3 overexpression in macrophages protects from insulin resistance, adipose inflammation, and nonalcoholic fatty liver disease in mice

Diabetes

Volumn 61, Issue 2, 2012, Pages 454-462

  Menghini, Rossella ^a   Casagrande, Viviana ^a   Menini, Stefano ^b   Marino, Arianna ^a   Marzano, Valeria ^a,c   Hribal, Marta L ^d   Gentileschi, Paolo ^a   Lauro, Davide ^a   Schillaci, Orazio ^a,e   Pugliese, Giuseppe ^b   Sbraccia, Paolo ^a   Urbani, Andrea ^a,c   Lauro, Renato ^a   Federici, Massimo ^a  

^a UNIVERSITY OF ROME TOR VERGATA   (Italy)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

^c IRCCS FONDAZIONE SANTA LUCIA   (Italy)

^d UNIVERSITY MAGNA GRAECIA OF CATANZARO   (Italy)

^e IRCCS NEUROMED   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; TISSUE INHIBITOR OF METALLOPROTEINASE 3;

ADIPOSE TISSUE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ENZYME ACTIVATION; GENE OVEREXPRESSION; GLUCOSE INTOLERANCE; INFLAMMATION; INSULIN RESISTANCE; MACROPHAGE; MOUSE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONALCOHOLIC FATTY LIVER; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; TRANSGENIC MOUSE;

ADIPOSE TISSUE; ADIPOSITY; ANIMALS; ANTIGENS, CD; ANTIGENS, DIFFERENTIATION, MYELOMONOCYTIC; DIET, HIGH-FAT; FATTY LIVER; FLUORODEOXYGLUCOSE F18; INFLAMMATION; INSULIN RESISTANCE; MACROPHAGES; MICE; OBESITY; RNA, MESSENGER; TISSUE INHIBITOR OF METALLOPROTEINASE-3;

EID: 84856551460     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db11-0613     Document Type: Article

References (45)

1. Caldwell SH, Oelsner DH, Iezzoni JC, Hespenheide EE, Battle EH, Driscoll CJ. Cryptogenic cirrhosis: clinical characterization and risk factors for underlying disease. Hepatology 1999;29:664-669 (Pubitemid 29109578)
2. Poonawala A, Nair SP, Thuluvath PJ. Prevalence of obesity and diabetes in patients with cryptogenic cirrhosis: a case-control study. Hepatology 2000;32:689-692
3. Hanley AJ, Williams K, Festa A, et al.; insulin resistance atherosclerosis study. Elevations in markers of liver injury and risk of type 2 diabetes: the insulin resistance atherosclerosis study. Diabetes 2004;53:2623-2632 (Pubitemid 39299271)
4. Tilg H, Hotamisligil GS. Nonalcoholic fatty liver disease: cytokine-adipokine interplay and regulation of insulin resistance. Gastroenterology 2006;131:934-945 (Pubitemid 44307061)
5. Pickup JC. Inflammation and activated innate immunity in the pathogenesis of type 2 diabetes. Diabetes Care 2004;27:813-823 (Pubitemid 38280558)
6. Schenk S, Saberi M, Olefsky JM. Insulin sensitivity: modulation by nutrients and inflammation. J Clin Invest 2008;118:2992-3002
7. Uysal KT, Wiesbrock SM, Marino MW, Hotamisligil GS. Protection from obesity-induced insulin resistance in mice lacking TNF-alpha function. Nature 1997;389:610-614 (Pubitemid 27446179)
8. Cai D, Yuan M, Frantz DF, et al. Local and systemic insulin resistance resulting from hepatic activation of IKK-beta and NF-kappaB. Nat Med 2005;11:183-190 (Pubitemid 40321354)
9. Winer S, Chan Y, Paltser G, et al. Normalization of obesity-associated insulin resistance through immunotherapy. Nat Med 2009;15:921-929
10. Federici M, Hribal ML, Menghini R, et al. Timp3 deficiency in insulin receptor-haploinsufficient mice promotes diabetes and vascular inflammation via increased TNF-alpha. J Clin Invest 2005;115:3494-3505 (Pubitemid 43121837)
11. Murphy G, Murthy A, Khokha R. Clipping, shedding and RIPping keep immunity on cue. Trends Immunol 2008;29:75-82
12. Davis GE, Senger DR. Extracellular matrix mediates a molecular balance between vascular morphogenesis and regression. Curr Opin Hematol 2008;15:197-203 (Pubitemid 351507571)
13. Menghini R, Menini S, Amoruso R, et al. Tissue inhibitor of metalloproteinase 3 deficiency causes hepatic steatosis and adipose tissue inflammation in mice. Gastroenterology 2009;136:663-672, e4
14. Fiorentino L, Vivanti A, Cavalera M, et al. Increased tumor necrosis factor alpha-converting enzyme activity induces insulin resistance and hepatosteatosis in mice. Hepatology 2010;51:103-110
15. Monroy A, Kamath S, Chavez AO, et al. Impaired regulation of the TNF-alpha converting enzyme/tissue inhibitor of metalloproteinase 3 proteolytic system in skeletal muscle of obese type 2 diabetic patients: a new mechanism of insulin resistance in humans. Diabetologia 2009;52:2169-2181
16. Cardellini M, Menghini R, Martelli E, et al. TIMP3 is reduced in atherosclerotic plaques from subjects with type 2 diabetes and increased by SirT1. Diabetes 2009;58:2396-2401
17. Ewens KG, George RA, Sharma K, Ziyadeh FN, Spielman RS. Assessment of 115 candidate genes for diabetic nephropathy by transmission/disequilibrium test. Diabetes 2005;54:3305-3318 (Pubitemid 43336530)
18. Barth JL, Yu Y, Song W, et al. Oxidised, glycated LDL selectively influences tissue inhibitor of metalloproteinase-3 gene expression and protein production in human retinal capillary pericytes. Diabetologia 2007;50:2200-2208 (Pubitemid 47373851)
19. Gelling RW, Yan W, Al-Noori S, et al. Deficiency of TNFalpha converting enzyme (TACE/ADAM17) causes a lean, hypermetabolic phenotype in mice. Endocrinology 2008;149:6053-6064
20. Serino M, Menghini R, Fiorentino L, et al. Mice heterozygous for tumor necrosis factor-alpha converting enzyme are protected from obesity-induced insulin resistance and diabetes. Diabetes 2007;56:2541-2546 (Pubitemid 47523261)
21. 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 (Pubitemid 36800160)
22. Lang R, Rutschman RL, Greaves DR, Murray PJ. Autocrine deactivation of macrophages in transgenic mice constitutively overexpressing IL-10 under control of the human CD68 promoter. J Immunol 2002;168:3402-3411 (Pubitemid 34250404)
23. Hogan B, Beddington R, Costantini F, Lacy E. Manipulating the Mouse Embryo. 2nd ed. Cold Spring Harbor, NY, Cold Spring Harbor Laboratory Press, 1994
24. Casagrande V, Menghini R, Menini S, et al. Overexpression of tissue inhibitor of metalloproteinase 3 in macrophages reduces atherosclerosis in low-density lipoprotein receptor knockout mice. Arterioscler Thromb Vasc Biol 2012;32:74-81
25. Menghini R, Marchetti V, Cardellini M, et al. Phosphorylation of GATA2 by Akt increases adipose tissue differentiation and reduces adipose tissue-related inflammation: a novel pathway linking obesity to atherosclerosis. Circulation 2005;111:1946-1953 (Pubitemid 40570214)
26. Smedsrød B, Pertoft H. Preparation of pure hepatocytes and reticuloendothelial cells in high yield from a single rat liver by means of Percoll centrifugation and selective adherence. J Leukoc Biol 1985;38:213-230 (Pubitemid 15243425)
27. Tilg H, Moschen AR. Evolution of inflammation in nonalcoholic fatty liver disease: the multiple parallel hits hypothesis. Hepatology 2010;52:1836-1846
28. Varlamov O, Somwar R, Cornea A, Kievit P, Grove KL, Roberts CT Jr. Single-cell analysis of insulin-regulated fatty acid uptake in adipocytes. Am J Physiol Endocrinol Metab 2010;299:E486-E496
29. Adachi M, Brenner DA. High molecular weight adiponectin inhibits proliferation of hepatic stellate cells via activation of adenosine monophosphate-activated protein kinase. Hepatology 2008;47:677-685 (Pubitemid 351280736)
30. Marra F, Bertolani C. Adipokines in liver diseases. Hepatology 2009;50:957-969
31. Saunders WB, Bohnsack BL, Faske JB, et al. Coregulation of vascular tube stabilization by endothelial cell TIMP-2 and pericyte TIMP-3. J Cell Biol 2006;175:179-191 (Pubitemid 44537209)
32. Rupnick MA, Panigrahy D, Zhang CY, et al. Adipose tissue mass can be regulated through the vasculature. Proc Natl Acad Sci USA 2002;99:10730-10735
33. Bernot D, Barruet E, Poggi M, Bonardo B, Alessi MC, Peiretti F. Downregulation of tissue inhibitor of metalloproteinase-3 (TIMP-3) expression is necessary for adipocyte differentiation. J Biol Chem 2010;285:6508-6514
34. Wang Y, Sul HS. Ectodomain shedding of preadipocyte factor 1 (Pref-1) by tumor necrosis factor alpha converting enzyme (TACE) and inhibition of adipocyte differentiation. Mol Cell Biol 2006;26:5421-5435 (Pubitemid 44036210)
35. Österreicher CH, Penz-Österreicher M, Grivennikov SI, et al. Fibroblast-specific protein 1 identifies an inflammatory subpopulation of macrophages in the liver. Proc Natl Acad Sci USA 2011;108:308-313
36. Murthy A, Defamie V, Smookler DS, et al. Ectodomain shedding of EGFR ligands and TNFR1 dictates hepatocyte apoptosis during fulminant hepatitis in mice. J Clin Invest 2010;120:2731-2744
37. Zou C, Ma J, Wang X, et al. Lack of Fas antagonism by Met in human fatty liver disease. Nat Med 2007;13:1078-1085 (Pubitemid 47517506)
38. Foveau B, Ancot F, Leroy C, et al. Down-regulation of the met receptor tyrosine kinase by presenilin-dependent regulated intramembrane proteolysis. Mol Biol Cell 2009;20:2495-2507
39. Gerin I, Louis GW, Zhang X, et al. Hyperphagia and obesity in female mice lacking tissue inhibitor of metalloproteinase-1. Endocrinology 2009;150:1697-1704
40. Jiang H, Zhu H, Chen X, et al. TIMP-1 transgenic mice recover from diabetes induced by multiple low-dose streptozotocin. Diabetes 2007;56:49-56
41. Boden G, SongW, Pashko L, Kresge K. In vivo effects of insulin and free fatty acids on matrix metalloproteinases in rat aorta. Diabetes 2008;57:476-483
42. Duval C, Thissen U, Keshtkar S, et al. Adipose tissue dysfunction signals progression of hepatic steatosis towards nonalcoholic steatohepatitis in C57BL/6 mice. Diabetes 2010;59:3181-3191
43. Jaworski DM, Sideleva O, Stradecki HM, et al. Sexually dimorphic diet-induced insulin resistance in obese tissue inhibitor of metalloproteinase-2 (TIMP-2)-deficient mice. Endocrinology 2011;152:1300-1313
44. Demeulemeester D, Scroyen I, Voros G, et al. Overexpression of tissue inhibitor of matrix metalloproteinases-1 (TIMP-1) in mice does not affect adipogenesis or adipose tissue development. Thromb Haemost 2006;95:1019-1024 (Pubitemid 43933760)
45. Kunz-Schughart LA, Weber A, Rehli M, et al. The "classical" macrophage marker CD68 is strongly expressed in primary human fibroblasts. Verh Dtsch Ges Pathol 2003;87:215-223 [in German]