Osteopontin deletion prevents the development of obesity and hepatic steatosis via impaired adipose tissue matrix remodeling and reduced inflammation and fibrosis in adipose tissue and liver in mice

PLoS ONE

Volumn 9, Issue 5, 2014, Pages

  Lancha, Andoni ^a,b   Rodríguez, Amaia ^a,b   Catalán, Victoria ^a,b   Becerril, Sara ^a,b   Sáinz, Neira ^a   Ramírez, Beatriz ^a,b   Burrell, María A ^b,c   Salvador, Javier ^a,b   Frühbeck, Gema ^a,b   Gómez Ambrosi, Javier ^a,b  

^a UNIVERSITY CLINIC OF NAVARRA   (Spain)

^b INSTITUTO DE SALUD CARLOS III   (Spain)

^c UNIVERSITY OF NAVARRA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

DIACYLGLYCEROL ACYLTRANSFERASE 2; GELATINASE A; GELATINASE B; OSTEOPONTIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; TRANSFORMING GROWTH FACTOR BETA1; COLLAGEN; THIOBARBITURIC ACID REACTIVE SUBSTANCE;

ADIPOCYTE; ADIPOSE TISSUE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY TEMPERATURE; BODY WEIGHT; BROWN ADIPOSE TISSUE; CIDEC GENE; COL1A1 GENE; COL6A1 GENE; COL6A3 GENE; CONTROLLED STUDY; DGAT2 GENE; EMR1 GENE; EPIDIDYMIS FAT; EXTRACELLULAR MATRIX; FASN GENE; FAT MASS; FATTY LIVER; FIBROSIS; GENE; GENE EXPRESSION; GENE INACTIVATION; INFLAMMATION; INSULIN SENSITIVITY; MALE; MOGAT1 GENE; MOUSE; NONHUMAN; OBESITY; OXIDATIVE STRESS; PPARG GENE; PROTEIN EXPRESSION; SREBF1 GENE; TGFB1 GENE; UPREGULATION; AFRICA; ANALYSIS OF VARIANCE; ANIMAL; DEFICIENCY; GENETICS; IMMUNOHISTOCHEMISTRY; INSULIN RESISTANCE; KNOCKOUT MOUSE; LIPID DIET; LIVER; METABOLISM; MICROARRAY ANALYSIS; PATHOLOGY; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION;

ADIPOSE TISSUE; AFRICA, WESTERN; ANALYSIS OF VARIANCE; ANIMALS; BODY TEMPERATURE; BODY WEIGHT; COLLAGEN; DIET, HIGH-FAT; EXTRACELLULAR MATRIX; FATTY LIVER; FIBROSIS; IMMUNOHISTOCHEMISTRY; INFLAMMATION; INSULIN RESISTANCE; LIVER; MICE; MICE, KNOCKOUT; MICROARRAY ANALYSIS; OBESITY; OSTEOPONTIN; OXIDATIVE STRESS; REAL-TIME POLYMERASE CHAIN REACTION; THIOBARBITURIC ACID REACTIVE SUBSTANCES;

EID: 84901630148     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0098398     Document Type: Article

References (59)

1. Berrington de Gonzalez A, Hartge P, Cerhan JR, Flint AJ, Hannan L, et al. (2010) Body-mass index and mortality among 1.46 million white adults. N Engl J Med 363: 2211-2219.
2. Scatena M, Liaw L, Giachelli CM (2007) Osteopontin. A multifunctional molecule regulating chronic inflammation and vascular disease. Arterioscler Thromb Vasc Biol 27: 2302-2309. (Pubitemid 350203943)
3. Denhardt DT, Noda M, O'Regan AW, Pavlin D, Berman JS (2001) Osteopontin as a means to cope with environmental insults: regulation of inflammation, tissue remodeling, and cell survival. J Clin Invest 107: 1055-1061. (Pubitemid 32422899)
4. Gerstenfeld LC (1999) Osteopontin in skeletal tissue homeostasis: An emerging picture of the autocrine/paracrine functions of the extracellular matrix. J Bone Miner Res 14: 850-855.
5. Sahai A, Malladi P, Melin-Aldana H, Green RM, Whitington PF (2004) Upregulation of osteopontin expression is involved in the development of nonalcoholic steatohepatitis in a dietary murine model. Am J Physiol Gastrointest Liver Physiol 287: G264-273. (Pubitemid 38802141)
6. Gómez-Ambrosi J, Catalán V, Ramírez B, Rodríguez A, Colina I, et al. (2007) Plasma osteopontin levels and expression in adipose tissue are increased in obesity. J Clin Endocrinol Metab 92: 3719-3727. (Pubitemid 47435361)
7. Gómez-Ambrosi J, Rodríguez A, Catalán V, Frühbeck G (2008) The bone-adipose axis in obesity and weight loss. Obes Surg 18: 1134-1143.
8. Nomiyama T, Perez-Tilve D, Ogawa D, Gizard F, Zhao Y, et al. (2007) Osteopontin mediates obesity-induced adipose tissue macrophage infiltration and insulin resistance in mice. J Clin Invest 117: 2877-2888. (Pubitemid 47529618)
9. Kiefer FW, Zeyda M, Todoric J, Huber J, Geyeregger R, et al. (2008) Osteopontin expression in human and murine obesity: extensive local upregulation in adipose tissue but minimal systemic alterations. Endocrinology 149: 1350-1357. (Pubitemid 351397930)
10. Bertola A, Deveaux V, Bonnafous S, Rousseau D, Anty R, et al. (2009) Elevated expression of osteopontin may be related to adipose tissue macrophage accumulation and liver steatosis in morbid obesity. Diabetes 58: 125-133.
11. Kiefer FW, Zeyda M, Gollinger K, Pfau B, Neuhofer A, et al. (2010) Neutralization of osteopontin inhibits obesity-induced inflammation and insulin resistance. Diabetes 59: 935-946.
12. Chapman J, Miles PD, Ofrecio JM, Neels JG, Yu JG, et al. (2010) Osteopontin is required for the early onset of high fat diet-induced insulin resistance in mice. PLoS ONE 5: e13959.
13. Lancha A, Frühbeck G, Gómez-Ambrosi J (2012) Peripheral signalling involved in energy homeostasis control. Nutr Res Rev 25: 223-248.
14. Aouadi M, Tencerova M, Vangala P, Yawe JC, Nicoloro SM, et al. (2013) Gene silencing in adipose tissue macrophages regulates whole-body metabolism in obese mice. Proc Natl Acad Sci U S A 110: 8278-8283.
15. Frühbeck G, Alonso R, Marzo F, Santidrián S (1995) A modified method for the indirect quantitative analysis of phytate in foodstuffs. Anal Biochem 225: 206-212.
16. Muruzábal FJ, Frühbeck G, Gómez-Ambrosi J, Archanco M, Burrell MA (2002) Immunocytochemical detection of leptin in non-mammalian vertebrate stomach. Gen Comp Endocrinol 128: 149-152. (Pubitemid 35257842)
17. Conti M, Morand PC, Levillain P, Lemonnier A (1991) Improved fluorometric determination of malonaldehyde. Clin Chem 37: 1273-1275. (Pubitemid 21925960)
18. Sáinz N, Rodríguez A, Catalán V, Becerril S, Ramírez B, et al. (2009) Leptin administration favors muscle mass accretion by decreasing FoxO3a and increasing PGC-1α in ob/ob mice. PLoS ONE 4: e6808.
19. Becerril S, Rodríguez A, Catalán V, Sáinz N, Ramírez B, et al. (2012) Transcriptional analysis of brown adipose tissue in leptin-deficient mice lacking inducible nitric oxide synthase: evidence of the role of Med1 in energy balance. Physiol Genomics 44: 678-688.
20. Catalán V, Gómez-Ambrosi J, Rotellar F, Silva C, Rodríguez A, et al. (2007) Validation of endogenous control genes in human adipose tissue: relevance to obesity and obesity-associated type 2 diabetes mellitus. Horm Metab Res 39: 495-500. (Pubitemid 47204192)
21. Catalán V, Gómez-Ambrosi J, Rodríguez A, Ramírez B, Silva C, et al. (2009) Increased adipose tissue expression of lipocalin-2 in obesity is related to inflammation and matrix metalloproteinase-2 and -9 activity in humans. J Mol Med 87: 803-813.
22. Miao B, Zondlo S, Gibbs S, Cromley D, Hosagrahara VP, et al. (2004) Raising HDL cholesterol without inducing hepatic steatosis and hypertriglyceridemia by a selective LXR modulator. J Lipid Res 45: 1410-1417. (Pubitemid 39006968)
23. Patsouris D, Li PP, Thapar D, Chapman J, Olefsky JM, et al. (2008) Ablation of CD11c-positive cells normalizes insulin sensitivity in obese insulin resistant animals. Cell Metab 8: 301-309.
24. Divoux A, Tordjman J, Lacasa D, Veyrie N, Hugol D, et al. (2010) Fibrosis in human adipose tissue: composition, distribution, and link with lipid metabolism and fat mass loss. Diabetes 59: 2817-2825.
25. Lo L, McLennan SV, Williams PF, Bonner J, Chowdhury S, et al. (2011) Diabetes is a progression factor for hepatic fibrosis in a high fat fed mouse obesity model of non-alcoholic steatohepatitis. J Hepatol 55: 435-444.
26. Frühbeck G (2005) Obesity: Aquaporin enters the picture. Nature 438: 436-437.
27. Kodama K, Horikoshi M, Toda K, Yamada S, Hara K, et al. (2012) Expression-based genome-wide association study links the receptor CD44 in adipose tissue with type 2 diabetes. Proc Natl Acad Sci U S A 109: 7049-7054.
28. Kang HS, Liao G, Degraff LM, Gerrish K, Bortner CD, et al. (2013) CD44 plays a critical role in regulating diet-induced adipose inflammation, hepatic steatosis, and insulin resistance. PLoS ONE 8: e58417.
29. Rittling SR (2011) Osteopontin in macrophage function. Expert Rev Mol Med 13: e15.
30. Kiefer FW, Neschen S, Pfau B, Legerer B, Neuhofer A, et al. (2011) Osteopontin deficiency protects against obesity-induced hepatic steatosis and attenuates glucose production in mice. Diabetologia 54: 2132-2142.
31. Rodríguez A, Gómez-Ambrosi J, Catalán V, Gil MJ, Becerril S, et al. (2009) Acylated and desacyl ghrelin stimulate lipid accumulation in human visceral adipocytes. Int J Obes 33: 541-552.
32. Sáinz N, Rodríguez A, Catalán V, Becerril S, Ramírez B, et al. (2012) Leptin reduces the expression and increases the phosphorylation of the negative regulators of GLUT4 Traffic TBC1D1 and TBC1D4 in muscle of ob/ob mice. PLoS ONE 7: e29389.
33. Sun K, Kusminski CM, Scherer PE (2011) Adipose tissue remodeling and obesity. J Clin Invest 121: 2094-2101.
34. Bouloumié A, Sengenes C, Portolan G, Galitzky J, Lafontan M (2001) Adipocyte produces matrix metalloproteinases 2 and 9: involvement in adipose differentiation. Diabetes 50: 2080-2086. (Pubitemid 33643675)
35. Bourboulia D, Stetler-Stevenson WG (2010) Matrix metalloproteinases (MMPs) and tissue inhibitors of metalloproteinases (TIMPs): Positive and negative regulators in tumor cell adhesion. Semin Cancer Biol 20: 161-168.
36. Hadler-Olsen E, Fadnes B, Sylte I, Uhlin-Hansen L, Winberg JO (2011) Regulation of matrix metalloproteinase activity in health and disease. FEBS J 278: 28-45.
37. Hopps E, Caimi G (2012) Matrix metalloproteinases in metabolic syndrome. Eur J Intern Med 23: 99-104.
38. Liu H, Chen A, Guo F, Yuan L (2010) A short-hairpin RNA targeting osteopontin downregulates MMP-2 and MMP-9 expressions in prostate cancer PC-3 cells. Cancer Lett 295: 27-37.
39. Bruemmer D, Collins AR, Noh G, Wang W, Territo M, et al. (2003) Angiotensin II-accelerated atherosclerosis and aneurysm formation is attenuated in osteopontin-deficient mice. J Clin Invest 112: 1318-1331. (Pubitemid 38057686)
40. Lai CF, Seshadri V, Huang K, Shao JS, Cai J, et al. (2006) An osteopontin-NADPH oxidase signaling cascade promotes pro-matrix metalloproteinase 9 activation in aortic mesenchymal cells. Circ Res 98: 1479-1489. (Pubitemid 44297070)
41. Furukawa S, Fujita T, Shimabukuro M, Iwaki M, Yamada Y, et al. (2004) Increased oxidative stress in obesity and its impact on metabolic syndrome. J Clin Invest 114: 1752-1761. (Pubitemid 40385531)
42. Georgiadou P, Iliodromitis EK, Varounis C, Mavroidis M, Kolokathis F, et al. (2008) Relationship between plasma osteopontin and oxidative stress in patients with coronary artery disease. Expert Opin Ther Targets 12: 917-920.
43. Irita J, Okura T, Jotoku M, Nagao T, Enomoto D, et al. (2011) Osteopontin deficiency protects against aldosterone-induced inflammation, oxidative stress, and interstitial fibrosis in the kidney. Am J Physiol Renal Physiol 301: F833-844.
44. Zeyda M, Gollinger K, Todoric J, Kiefer FW, Keck M, et al. (2011) Osteopontin is an activator of human adipose tissue macrophages and directly affects adipocyte function. Endocrinology 152: 2219-2227.
45. Lee YH, Petkova AP, Granneman JG (2013) Identification of an adipogenic niche for adipose tissue remodeling and restoration. Cell Metab 18: 355-367.
46. Matsui Y, Jia N, Okamoto H, Kon S, Onozuka H, et al. (2004) Role of osteopontin in cardiac fibrosis and remodeling in angiotensin II-induced cardiac hypertrophy. Hypertension 43: 1195-1201. (Pubitemid 38691740)
47. Syn WK, Agboola KM, Swiderska M, Michelotti GA, Liaskou E, et al. (2012) NKT-associated hedgehog and osteopontin drive fibrogenesis in non-alcoholic fatty liver disease. Gut 61: 1323-1329.
48. Halberg N, Khan T, Trujillo ME, Wernstedt-Asterholm I, Attie AD, et al. (2009) Hypoxia-inducible factor 1α induces fibrosis and insulin resistance in white adipose tissue. Mol Cell Biol 29: 4467-4483.
49. Khan T, Muise ES, Iyengar P, Wang ZV, Chandalia M, et al. (2009) Metabolic dysregulation and adipose tissue fibrosis: role of collagen VI. Mol Cell Biol 29: 1575-1591.
50. Zhang L, Peng X, Zhang Z, Feng Y, Jia X, et al. (2010) Subcellular proteome analysis unraveled annexin A2 related to immune liver fibrosis. J Cell Biochem 110: 219-228.
51. Sun K, Tordjman J, Clement K, Scherer PE (2013) Fibrosis and adipose tissue dysfunction. Cell Metab 18: 470-477.
52. Morales-Ibanez O, Domínguez M, Ki SH, Marcos M, Chaves JF, et al. (2013) Human and experimental evidence supporting a role for osteopontin in alcoholic hepatitis. Hepatology 58: 1742-1756.
53. Duval C, Thissen U, Keshtkar S, Accart B, Stienstra R, et al. (2010) Adipose tissue dysfunction signals progression of hepatic steatosis towards nonalcoholic steatohepatitis in C57BL/6 mice. Diabetes 59: 3181-3191.
54. Lima-Cabello E, Garcia-Mediavilla MV, Miquilena-Colina ME, Vargas-Castrillon J, Lozano-Rodriguez T, et al. (2011) Enhanced expression of pro-inflammatory mediators and liver X-receptor-regulated lipogenic genes in nonalcoholic fatty liver disease and hepatitis C. Clin Sci 120: 239-250.
55. Rodríguez A, Catalán V, Gómez-Ambrosi J, García-Navarro S, Rotellar F, et al. (2011) Insulin- and leptin-mediated control of aquaglyceroporins in human adipocytes and hepatocytes is mediated via the PI3K/Akt/mTOR signaling cascade. J Clin Endocrinol Metab 96: E586-597.
56. Borkham-Kamphorst E, Drews F, Weiskirchen R (2011) Induction of lipocalin-2 expression in acute and chronic experimental liver injury moderated by pro-inflammatory cytokines interleukin-1β through nuclear factor-κB activation. Liver Int 31: 656-665.
57. Law IK, Xu A, Lam KS, Berger T, Mak TW, et al. (2010) Lipocalin-2 deficiency attenuates insulin resistance associated with aging and obesity. Diabetes 59: 872-882.
58. Nau K, Fromme T, Meyer CW, von Praun C, Heldmaier G, et al. (2008) Brown adipose tissue specific lack of uncoupling protein 3 is associated with impaired cold tolerance and reduced transcript levels of metabolic genes. J Comp Physiol B 178: 269-277. (Pubitemid 351640697)
59. Frühbeck G, Becerril S, Sáinz N, Garrastachu P, García-Velloso MJ (2009) BAT: a new target for human obesity? Trends Pharmacol Sci 30: 387-396.