Osteopontin is required for the early onset of high fat diet-induced insulin resistance in mice

PLoS ONE

Volumn 5, Issue 11, 2010, Pages

  Chapman, Justin ^a   Miles, Philip D ^b   Ofrecio, Jachelle M ^b   Neels, Jaap G ^c   Yu, Joseph G ^b   Resnik, Jamie L ^d   Wilkes, Jason ^b   Talukdar, Saswata ^b   Thapar, Divya ^b   Johnson, Kristen ^b   Sears, Dorothy D ^b  

^a PFIZER INC   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^c INSERM   (France)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; FATTY ACID; GLITAZONE DERIVATIVE; OSTEOPONTIN; 2,4 THIAZOLIDINEDIONE; 2,4 THIAZOLIDINEDIONE DERIVATIVE; 2,4-THIAZOLIDINEDIONE; ANTIDIABETIC AGENT; INSULIN; PROTEIN KINASE B;

ADIPOCYTE; ADIPOGENESIS; ADIPOSE TISSUE; ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; BONE DEVELOPMENT; CHRONIC DISEASE; CLINICAL ARTICLE; CONTROLLED STUDY; FATTY ACID BLOOD LEVEL; FEMALE; GENE OVEREXPRESSION; HUMAN; HUMAN TISSUE; HYPERINSULINISM; HYPERLEPTINEMIA; HYPERTROPHY; IN VITRO STUDY; INFLAMMATION; INSULIN RESISTANCE; LIPID DIET; LIVER; MACROPHAGE; MALE; MOUSE; NONHUMAN; OBESITY; ONSET AGE; PATHOGENESIS; PROTEIN FUNCTION; RAT; SKELETAL MUSCLE; STROMA CELL; WILD TYPE; ANIMAL; BONE MARROW CELL; C57BL MOUSE; CELL DIFFERENTIATION; CYTOLOGY; DRUG EFFECT; FAT INTAKE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MIDDLE AGED; MOUSE MUTANT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; ZUCKER RAT;

MUS; RATTUS;

ADIPOSE TISSUE; ADULT; ANIMALS; BONE MARROW CELLS; CELL DIFFERENTIATION; CYTOKINES; DIETARY FATS; FEMALE; GENE EXPRESSION REGULATION; HUMANS; HYPOGLYCEMIC AGENTS; INSULIN; INSULIN RESISTANCE; MACROPHAGES; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MIDDLE AGED; OSTEOPONTIN; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RATS, ZUCKER; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; STROMAL CELLS; THIAZOLIDINEDIONES;

EID: 78649759561     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0013959     Document Type: Article

References (64)

1. de Luca C, Olefsky JM (2008) Inflammation and insulin resistance. FEBS Lett 582: 97-105.
2. Matsuzawa Y (2006) The metabolic syndrome and adipocytokines. FEBS Lett 580: 2917-2921.
3. Hotamisligil GS (2006) Inflammation and metabolic disorders. Nature 444: 860-867.
4. Olefsky JM (2000) Treatment of insulin resistance with peroxisome proliferator-activated receptor {gamma} agonists. J Clin Invest 106: 467-472.
5. Berger JP, Akiyama TE, Meinke PT (2005) PPARs: therapeutic targets for metabolic disease. Trends in Pharmacological Sciences 26: 244-251.
6. Evans RM, Barish GD, Wang YX (2004) PPARs and the complex journey to obesity. Nat Med 10: 355-361.
7. Park SY, Cho YR, Kim HJ, Higashimori T, Danton C, et al. (2005) Unraveling the temporal pattern of diet-induced insulin resistance in individual organs and cardiac dysfunction in C57BL/6 mice. Diabetes 54: 3530-3540.
8. Strissel KJ, Stancheva Z, Miyoshi H, Perfield JW, 2nd, DeFuria J, et al. (2007) Adipocyte death, adipose tissue remodeling, and obesity complications. Diabetes 56: 2910-2918.
9. Kim JK, Gimeno RE, Higashimori T, Kim HJ, Choi H, et al. (2004) Inactivation of fatty acid transport protein 1 prevents fat-induced insulin resistance in skeletal muscle. J Clin Invest 113: 756-763.
10. Kraegen EW, Clark PW, Jenkins AB, Daley EA, Chisholm DJ, et al. (1991) Development of muscle insulin resistance after liver insulin resistance in high-fat-fed rats. Diabetes 40: 1397-1403.
11. Nguyen MT, Favelyukis S, Nguyen AK, Reichart D, Scott PA, et al. (2007) 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 282: 35279-35292.
12. Sears DD, Miles PD, Chapman J, Ofrecio JM, Almazan F, et al. (2009) 12/15-lipoxygenase is required for the early onset of high fat diet-induced adipose tissue inflammation and insulin resistance in mice. PLoS One 4: e7250.
13. Hong EG, Ko HJ, Cho YR, Kim HJ, Ma Z, et al. (2009) Interleukin-10 prevents diet-induced insulin resistance by attenuating macrophage and cytokine response in skeletal muscle. Diabetes 58: 2525-2535.
14. Kiefer FW, Zeyda M, Gollinger K, Pfau B, Neuhofer A, et al. (2010) Neutralization of osteopontin inhibits obesity-induced inflammation and insulin resistance. Diabetes.
15. 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.
16. Wai PY, Kuo PC (2004) The role of Osteopontin in tumor metastasis. J Surg Res 121: 228-241.
17. 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.
18. Denhardt DT, Giachelli CM, Rittling SR (2001) Role of osteopontin in cellular signaling and toxicant injury. Annu Rev Pharmacol Toxicol 41: 723-749.
19. Ogawa D, Stone JF, Takata Y, Blaschke F, Chu VH, et al. (2005) Liver x receptor agonists inhibit cytokine-induced osteopontin expression in macro-phages through interference with activator protein-1 signaling pathways. Circ Res 96: e59-67.
20. Sears DD, Hsiao G, Hsiao A, Yu JG, Courtney CH, et al. (2009) Mechanisms of human insulin resistance and thiazolidinedione-mediated insulin sensitization. Proc Natl Acad Sci U S A 106: 18745-18750.
21. Oyama Y, Akuzawa N, Nagai R, Kurabayashi M (2002) PPARgamma ligand inhibits osteopontin gene expression through interference with binding of nuclear factors to A/T-rich sequence in THP-1 cells. Circ Res 90: 348-355.
22. Keen HL, Ryan MJ, Beyer A, Mathur S, Scheetz TE, et al. (2004) Gene expression profiling of potential PPARgamma target genes in mouse aorta. Physiol Genomics 18: 33-42.
23. Christensen B, Nielsen MS, Haselmann KF, Petersen TE, Sorensen ES (2005) Post-translationally modified residues of native human osteopontin are located in clusters: identification of 36 phosphorylation and five O-glycosylation sites and their biological implications. Biochem J 390: 285-292.
24. Chae S, Jun HO, Lee EG, Yang SJ, Lee DC, et al. (2009) Osteopontin splice variants differentially modulate the migratory activity of hepatocellular carcinoma cell lines. Int J Oncol 35: 1409-1416.
25. Shinohara ML, Kim HJ, Kim JH, Garcia VA, Cantor H (2008) Alternative translation of osteopontin generates intracellular and secreted isoforms that mediate distinct biological activities in dendritic cells. Proc Natl Acad Sci U S A 105: 7235-7239.
26. Weber GF, Zawaideh S, Hikita S, Kumar VA, Cantor H, et al. (2002) Phosphorylation-dependent interaction of osteopontin with its receptors regulates macrophage migration and activation. J Leukoc Biol 72: 752-761.
27. Kiefer FW, Zeyda M, Todoric J, Huber J, Geyeregger R, et al. (2008) Osteopontin expression in human and murine obesity: extensive local up-regulation in adipose tissue but minimal systemic alterations. Endocrinology 149: 1350-1357.
28. Patani N, Jouhra F, Jiang W, Mokbel K (2008) Osteopontin expression profiles predict pathological and clinical outcome in breast cancer. Anticancer Res 28: 4105-4110.
29. Hevener AL, Reichart D, Janez A, Olefsky J (2001) Thiazolidinedione treatment prevents free fatty acid-induced insulin resistance in male wistar rats. Diabetes 50: 2316-2322.
30. Hsiao G, Chapman J, Ofrecio JM, Wilkes J, Resnik JL, et al. (2010) Multi-tissue, selective PPARc modulation of insulin sensitivity and metabolic pathways in obese rats. Submitted.
31. Revers RR, Fink R, Griffin J, Olefsky JM, Kolterman OG (1984) Influence of hyperglycemia on insulin's in vivo effects in type II diabetes. J Clin Invest 73: 664-672.
32. Steele R (1959) Influences of glucose loading and of injected insulin on hepatic glucose output. Ann N Y Acad Sci 82: 420-430.
33. Rieusset J, Touri F, Michalik L, Escher P, Desvergne B, et al. (2002) A new selective peroxisome proliferator-activated receptor gamma antagonist with antiobesity and antidiabetic activity. Mol Endocrinol 16: 2628-2644.
34. Sciaudone M, Gazzerro E, Priest L, Delany AM, Canalis E (2003) Notch 1 impairs osteoblastic cell differentiation. Endocrinology 144: 5631-5639.
35. Sekiya I, Larson BL, Vuoristo JT, Cui JG, Prockop DJ (2004) Adipogenic differentiation of human adult stem cells from bone marrow stroma (MSCs). J Bone Miner Res 19: 256-264.
36. Xu H, Barnes GT, Yang Q, Tan G, Yang D, et al. (2003) Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance. J Clin Invest 112: 1821-1830.
37. 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.
38. Fruhbeck G (2006) Intracellular signalling pathways activated by leptin. Biochem J 393: 7-20.
39. Cinti S, Mitchell G, Barbatelli G, Murano I, Ceresi E, et al. (2005) Adipocyte death defines macrophage localization and function in adipose tissue of obese mice and humans. J Lipid Res 46: 2347-2355.
40. Shaul ME, Bennett G, Strissel KJ, Greenberg AS, Obin MS (2010) Dynamic, M2-like Remodeling Phenotypes of CD11c+ Adipose Tissue Macrophages During High Fat Diet-Induced Obesity in Mice. Diabetes, in press.
41. Olefsky JM, Glass CK (2010) Macrophages, inflammation, and insulin resistance. Annu Rev Physiol 72: 219-246.
42. Lumeng CN, Bodzin JL, Saltiel AR (2007) Obesity induces a phenotypic switch in adipose tissue macrophage polarization. J Clin Invest 117: 175-184.
43. Gimble JM, Zvonic S, Floyd ZE, Kassem M, Nuttall ME (2006) Playing with bone and fat. J Cell Biochem 98: 251-266.
44. Parhami F, Jackson SM, Tintut Y, Le V, Balucan JP, et al. (1999) Atherogenic diet and minimally oxidized low density lipoprotein inhibit osteogenic and promote adipogenic differentiation of marrow stromal cells. J Bone Miner Res 14: 2067-2078.
45. Ross SE, Erickson RL, Gerin I, DeRose PM, Bajnok L, et al. (2002) Microarray analyses during adipogenesis: understanding the effects of Wnt signaling on adipogenesis and the roles of liver X receptor alpha in adipocyte metabolism. Mol Cell Biol 22: 5989-5999.
46. Oyama Y, Kurabayashi M, Akuzawa N, Nagai R (2000) Troglitazone, a PPARgamma ligand, inhibits osteopontin gene expression in human mono-cytes/macrophage THP-1 cells. J Atheroscler Thromb 7: 77-82.
47. 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 Gastro-intest Liver Physiol 287: G264-273.
48. Lofgren P, Andersson I, Adolfsson B, Leijonhufvud BM, Hertel K, et al. (2005) Long-term prospective and controlled studies demonstrate adipose tissue hypercellularity and relative leptin deficiency in the postobese state. J Clin Endocrinol Metab 90: 6207-6213.
49. Frederich RC, Lollmann B, Hamann A, Napolitano-Rosen A, Kahn BB, et al. (1995) Expression of ob mRNA and its encoded protein in rodents. Impact of nutrition and obesity. J Clin Invest 96: 1658-1663.
50. Yamauchi T, Kamon J, Waki H, Murakami K, Motojima K, et al. (2001) The mechanisms by which both heterozygous peroxisome proliferator-activated receptor gamma (PPARgamma) deficiency and PPARgamma agonist improve insulin resistance. J Biol Chem 276: 41245-41254.
51. Sanchez-Margalet V, Martin-Romero C, Santos-Alvarez J, Goberna R, Najib S, et al. (2003) Role of leptin as an immunomodulator of blood mononuclear cells: mechanisms of action. Clin Exp Immunol 133: 11-19.
52. Hennige AM, Stefan N, Kapp K, Lehmann R, Weigert C, et al. (2006) Leptin down-regulates insulin action through phosphorylation of serine-318 in insulin receptor substrate 1. Faseb J 20: 1206-1208.
53. Sahai A, Malladi P, Pan X, Paul R, Melin-Aldana H, et al. (2004) Obese and diabetic db/db mice develop marked liver fibrosis in a model of nonalcoholic steatohepatitis: role of short-form leptin receptors and osteopontin. Am J Physiol Gastrointest Liver Physiol 287: G1035-1043.
54. Pausova Z (2006) From big fat cells to high blood pressure: a pathway to obesity-associated hypertension. Curr Opin Nephrol Hypertens 15: 173-178.
55. Rosen CJ, Bouxsein ML (2006) Mechanisms of disease: is osteoporosis the obesity of bone? Nat Clin Pract Rheumatol 2: 35-43.
56. Beresford JN, Bennett JH, Devlin C, Leboy PS, Owen ME (1992) Evidence for an inverse relationship between the differentiation of adipocytic and osteogenic cells in rat marrow stromal cell cultures. J Cell Sci 102 (Pt 2): 341-351.
57. Kveiborg M, Sabatakos G, Chiusaroli R, Wu M, Philbrick WM, et al. (2004) DeltaFosB induces osteosclerosis and decreases adipogenesis by two independent cell-autonomous mechanisms. Mol Cell Biol 24: 2820-2830.
58. Harmey D, Johnson KA, Zelken J, Camacho NP, Hoylaerts MF, et al. (2006) Elevated skeletal osteopontin levels contribute to the hypophosphatasia phenotype in Akp2(2/2) mice. J Bone Miner Res 21: 1377-1386.
59. Ishijima M, Ezura Y, Tsuji K, Rittling SR, Kurosawa H, et al. (2006) Osteopontin is associated with nuclear factor kappaB gene expression during tail-suspension-induced bone loss. Exp Cell Res 312: 3075-3083.
60. Yoshitake H, Rittling SR, Denhardt DT, Noda M (1999) Osteopontin-deficient mice are resistant to ovariectomy-induced bone resorption. Proc Natl Acad Sci U S A 96: 8156-8160.
61. Lee RH, Kim B, Choi I, Kim H, Choi HS, et al. (2004) Characterization and expression analysis of mesenchymal stem cells from human bone marrow and adipose tissue. Cell Physiol Biochem 14: 311-324.
62. Nakajima I, Yamaguchi T, Ozutsumi K, Aso H (1998) Adipose tissue extracellular matrix: newly organized by adipocytes during differentiation. Differentiation 63: 193-200.
63. Gregoire FM (2001) Adipocyte differentiation: from fibroblast to endocrine cell. Exp Biol Med (Maywood) 226: 997-1002.
64. Chun TH, Hotary KB, Sabeh F, Saltiel AR, Allen ED, et al. (2006) A pericellular collagenase directs the 3-dimensional development of white adipose tissue. Cell 125: 577-591.