Noncanonical wnt signaling promotes obesity-induced adipose tissue inflammation and metabolic dysfunction independent of adipose tissue expansion

Diabetes

Volumn 64, Issue 4, 2015, Pages 1235-1248

  Fuster, José J ^a   Zuriaga, María A ^a   Ngo, Doan Thi Minh ^a   Farb, Melissa G ^a   Aprahamian, Tamar ^a   Yamaguchi, Terry P ^b   Gokce, Noyan ^a   Walsh, Kenneth ^a  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD68 ANTIGEN; GLYCOPROTEIN P 15095; INSULIN; INTERLEUKIN 6; MONOCYTE CHEMOTACTIC PROTEIN 1; TUMOR NECROSIS FACTOR ALPHA; WNT PROTEIN; WNT10B PROTEIN; WNT11 PROTEIN; WNT5A PROTEIN; GLUCOSE;

ADIPOCYTE; ADIPOSE TISSUE; ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE MARROW CELL; CELL CULTURE; CELL SIZE; CLINICAL ARTICLE; CONTROLLED STUDY; FAT MASS; GENE EXPRESSION; GLUCOSE HOMEOSTASIS; GLUCOSE METABOLISM; HUMAN; HUMAN CELL; HUMAN TISSUE; INFLAMMATION; INSULIN RESISTANCE; INTRAABDOMINAL FAT; MACROPHAGE; METABOLIC DISORDER; NONHUMAN; OBESITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SUBCUTANEOUS FAT; TISSUE EXPANSION; UPREGULATION; ANIMAL; METABOLISM; MOUSE; PHOSPHORYLATION; PHYSIOLOGY; WNT SIGNALING PATHWAY;

ANIMALS; GLUCOSE; HUMANS; INFLAMMATION; INSULIN RESISTANCE; INTRA-ABDOMINAL FAT; MACROPHAGES; MICE; OBESITY; PHOSPHORYLATION; SUBCUTANEOUS FAT; WNT SIGNALING PATHWAY;

EID: 84961994260     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db14-1164     Document Type: Article

References (82)

1. Blüher M. The distinction of metabolically 'healthy' from 'unhealthy' obese individuals. Curr Opin Lipidol 2010;21: 38-43
2. Neeland IJ, Turer AT, Ayers CR, et al. Dysfunctional adiposity and the risk of prediabetes and type 2 diabetes in obese adults. JAMA 2012;308: 1150-1159
3. Boyko EJ, Fujimoto WY, Leonetti DL, Newell-Morris L. Visceral adiposity and risk of type 2 diabetes: A prospective study among Japanese Americans. Diabetes Care 2000;23: 465-471
4. Preis SR, Massaro JM, Robins SJ, et al. Abdominal subcutaneous and visceral adipose tissue and insulin resistance in the Framingham heart study. Obesity (Silver Spring) 2010;18: 2191-2198
5. McLaughlin T, Lamendola C, Liu A, Abbasi F. Preferential fat deposition in subcutaneous versus visceral depots is associated with insulin sensitivity. J Clin Endocrinol Metab 2011;96: E1756-E1760
6. Porter SA, Massaro JM, Hoffmann U, Vasan RS, O'Donnel CJ, Fox CS. Abdominal subcutaneous adipose tissue: A protective fat depot? Diabetes Care 2009;32: 1068-1075
7. Snijder MB, Visser M, Dekker JM, et al.; Health ABC Study. Low subcutaneous thigh fat is a risk factor for unfavourable glucose and lipid levels, independently of high abdominal fat. The Health ABC Study. Diabetologia 2005; 48: 301-308
8. Farb MG, Ganley-Leal L, Mott M, et al. Arteriolar function in visceral adipose tissue is impaired in human obesity. Arterioscler Thromb Vasc Biol 2012;32: 467-473
9. Klöting N, Fasshauer M, Dietrich A, et al. Insulin-sensitive obesity. Am J Physiol Endocrinol Metab 2010;299: E506-E515
10. Adams M, Montague CT, Prins JB, et al. Activators of peroxisome proliferatoractivated receptor gamma have depot-specific effects on human preadipocyte differentiation. J Clin Invest 1997;100: 3149-3153
11. Tchkonia T, Giorgadze N, Pirtskhalava T, et al. Fat depot origin affects adipogenesis in primary cultured and cloned human preadipocytes. Am J Physiol Regul Integr Comp Physiol 2002;282: R1286-R1296
12. Tchkonia T, Giorgadze N, Pirtskhalava T, et al. Fat depot-specific characteristics are retained in strains derived from single human preadipocytes. Diabetes 2006;55: 2571-2578
13. Gesta S, Blüher M, Yamamoto Y, et al. Evidence for a role of developmental genes in the origin of obesity and body fat distribution. Proc Natl Acad Sci U S A 2006;103: 6676-6681
14. Yamamoto Y, Gesta S, Lee KY, Tran TT, Saadatirad P, Kahn CR. Adipose depots possess unique developmental gene signatures. Obesity (Silver Spring) 2010;18: 872-878
15. Vohl M-C, Sladek R, Robitaille J, et al. A survey of genes differentially expressed in subcutaneous and visceral adipose tissue in men. Obes Res 2004; 12: 1217-1222
16. Gesta S, Tseng Y-H, Kahn CR. Developmental origin of fat: Tracking obesity to its source. Cell 2007;131: 242-256
17. Logan CY, Nusse R. The Wnt signaling pathway in development and disease. Annu Rev Cell Dev Biol 2004;20: 781-810
18. Christodoulides C, Lagathu C, Sethi JK, Vidal-Puig A. Adipogenesis and WNT signalling. Trends Endocrinol Metab 2009;20: 16-24
19. Bennett CN, Ross SE, Longo KA, et al. Regulation of Wnt signaling during adipogenesis. J Biol Chem 2002;277: 30998-31004
20. Ross SE, Hemati N, Longo KA, et al. Inhibition of adipogenesis by Wnt signaling. Science 2000;289: 950-953
21. Cawthorn WP, Bree AJ, Yao Y, et al. Wnt6, Wnt10a and Wnt10b inhibit adipogenesis and stimulate osteoblastogenesis through a b-catenin-dependent mechanism. Bone 2012;50: 477-489
22. Wright WS, Longo KA, Dolinsky VW, et al. Wnt10b inhibits obesity in ob/ob and agouti mice. Diabetes 2007;56: 295-303
23. Longo KA, Wright WS, Kang S, et al. Wnt10b inhibits development of white and brown adipose tissues. J Biol Chem 2004;279: 35503-35509
24. Halleskog C, Dijksterhuis JP, Kilander MBC, et al. Heterotrimeric G proteindependent WNT-5A signaling to ERK1/2 mediates distinct aspects of microglia proinflammatory transformation. J Neuroinflammation 2012;9: 111
25. Blumenthal A, Ehlers S, Lauber J, et al. The Wingless homolog WNT5A and its receptor Frizzled-5 regulate inflammatory responses of human mononuclear cells induced by microbial stimulation. Blood 2006;108: 965-973
26. Rauner M, Stein N, Winzer M, et al. WNT5A is induced by inflammatory mediators in bone marrow stromal cells and regulates cytokine and chemokine production. J Bone Miner Res 2012;27: 575-585
27. Pereira C, Schaer DJ, Bachli EB, Kurrer MO, Schoedon G. Wnt5A/CaMKII signaling contributes to the inflammatory response of macrophages and is a target for the antiinflammatory action of activated protein C and interleukin-10. Arterioscler Thromb Vasc Biol 2008;28: 504-510
28. Pukrop T, Klemm F, Hagemann T, et al. Wnt 5a signaling is critical for macrophage-induced invasion of breast cancer cell lines. Proc Natl Acad Sci U S A 2006;103: 5454-5459
29. Miyoshi H, Ajima R, Luo CT, Yamaguchi TP, Stappenbeck TS. Wnt5a potentiates TGF-b signaling to promote colonic crypt regeneration after tissue injury. Science 2012;338: 108-113
30. Yamaguchi TP, Bradley A, McMahon AP, Jones S. A Wnt5a pathway underlies outgrowth of multiple structures in the vertebrate embryo. Development 1999;126: 1211-1223
31. 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
32. Zhao C, Ma H, Bu X, Wang W, Zhang N. SFRP5 inhibits gastric epithelial cell migration induced by macrophage-derived Wnt5a. Carcinogenesis 2013;34: 146-152
33. Bilkovski R, Schulte DM, Oberhauser F, et al. Adipose tissue macrophages inhibit adipogenesis of mesenchymal precursor cells via wnt-5a in humans. Int J Obes (Lond) 2011;35: 1450-1454
34. Katoh M, Katoh M. Transcriptional mechanisms of WNT5A based on NFkappaB, Hedgehog, TGFbeta, and Notch signaling cascades. Int J Mol Med 2009; 23: 763-769
35. Ge XP, Gan YH, Zhang CG, et al. Requirement of the NF-kB pathway for induction of Wnt-5A by interleukin-1b in condylar chondrocytes of the temporomandibular joint: Functional crosstalk between the Wnt-5A and NF-kB signaling pathways. Osteoarthritis Cartilage 2011;19: 111-117
36. Glass CK, Olefsky JM. Inflammation and lipid signaling in the etiology of insulin resistance. Cell Metab 2012;15: 635-645
37. Maeda K, Kobayashi Y, Udagawa N, et al. Wnt5a-Ror2 signaling between osteoblast-lineage cells and osteoclast precursors enhances osteoclastogenesis. Nat Med 2012;18: 405-412
38. Nomachi A, Nishita M, Inaba D, Enomoto M, Hamasaki M, Minami Y. Receptor tyrosine kinase Ror2 mediates Wnt5a-induced polarized cell migration by activating c-Jun N-terminal kinase via actin-binding protein filamin A. J Biol Chem 2008;283: 27973-27981
39. Oishi I, Suzuki H, Onishi N, et al. The receptor tyrosine kinase Ror2 is involved in non-canonical Wnt5a/JNK signalling pathway. Genes Cells 2003;8: 645-654
40. Yamanaka H, Moriguchi T, Masuyama N, et al. JNK functions in the noncanonical Wnt pathway to regulate convergent extension movements in vertebrates. EMBO Rep 2002;3: 69-75
41. Schambony A, Wedlich D. Wnt-5A/Ror2 regulate expression of XPAPC through an alternative noncanonical signaling pathway. Dev Cell 2007;12: 779-792
42. Han MS, Jung DY, Morel C, et al. JNK expression by macrophages promotes obesity-induced insulin resistance and inflammation. Science 2013;339: 218-222
43. Hirosumi J, Tuncman G, Chang L, et al. A central role for JNK in obesity and insulin resistance. Nature 2002;420: 333-336
44. Sabio G, Das M, Mora A, et al. A stress signaling pathway in adipose tissue regulates hepatic insulin resistance. Science 2008;322: 1539-1543
45. Lumeng CN, Deyoung SM, Saltiel AR. Macrophages block insulin action in adipocytes by altering expression of signaling and glucose transport proteins. Am J Physiol Endocrinol Metab 2007;292: E166-E174
46. Suganami T, Nishida J, Ogawa Y. A paracrine loop between adipocytes and macrophages aggravates inflammatory changes: Role of free fatty acids and tumor necrosis factor alpha. Arterioscler Thromb Vasc Biol 2005;25: 2062-2068
47. Permana PA, Menge C, Reaven PD. Macrophage-secreted factors induce adipocyte inflammation and insulin resistance. Biochem Biophys Res Commun 2006;341: 507-514
48. Prats-Puig A, Soriano-Rodríguez P, Carreras-Badosa G, et al. Balanced duo of anti-inflammatory SFRP5 and proinflammatory WNT5A in children. Pediatr Res 2014;75: 793-797
49. Catalán V, Gómez-Ambrosi J, Rodríguez A, et al. Activation of noncanonical Wnt signaling through WNT5A in visceral adipose tissue of obese subjects is related to inflammation. J Clin Endocrinol Metab 2014;99: E1407-E1417
50. Masckauchán TNH, Agalliu D, Vorontchikhina M, et al. Wnt5a signaling induces proliferation and survival of endothelial cells in vitro and expression of MMP-1 and Tie-2. Mol Biol Cell 2006;17: 5163-5172
51. Bilkovski R, Schulte DM, Oberhauser F, et al. Role of WNT-5a in the determination of human mesenchymal stem cells into preadipocytes. J Biol Chem 2010;285: 6170-6178
52. Kim J, Kim J, Kim DW, et al. Wnt5a induces endothelial inflammation via beta-catenin-independent signaling. J Immunol 2010;185: 1274-1282
53. Oderup C, LaJevic M, Butcher EC. Canonical and noncanonical Wnt proteins program dendritic cell responses for tolerance. J Immunol 2013;190: 6126-6134
54. Valencia J, Hernández-López C, Martínez VG, et al. Wnt5a skews dendritic cell differentiation to an unconventional phenotype with tolerogenic features. J Immunol 2011;187: 4129-4139
55. Bergenfelz C, Medrek C, Ekström E, et al. Wnt5a induces a tolerogenic phenotype of macrophages in sepsis and breast cancer patients. J Immunol 2012;188: 5448-5458
56. Schaale K, Neumann J, Schneider D, Ehlers S, Reiling N. Wnt signaling in macrophages: Augmenting and inhibiting mycobacteria-induced inflammatory responses. Eur J Cell Biol 2011;90: 553-559
57. Malhotra S, Kincade PW. Canonical Wnt pathway signaling suppresses VCAM-1 expression by marrow stromal and hematopoietic cells. Exp Hematol 2009;37: 19-30
58. Manicassamy S, Reizis B, Ravindran R, et al. Activation of beta-catenin in dendritic cells regulates immunity versus tolerance in the intestine. Science 2010;329: 849-853
59. Neumann J, Schaale K, Farhat K, et al. Frizzled1 is a marker of inflammatory macrophages, and its ligand Wnt3a is involved in reprogramming Mycobacterium tuberculosis-infected macrophages. FASEB J 2010;24: 4599-4612
60. Ouchi N, Higuchi A, Ohashi K, et al. Sfrp5 is an anti-inflammatory adipokine that modulates metabolic dysfunction in obesity. Science 2010;329: 454-457
61. Li Y, Rankin SA, Sinner D, Kenny AP, Krieg PA, Zorn AM. Sfrp5 coordinates foregut specification and morphogenesis by antagonizing both canonical and noncanonical Wnt11 signaling. Genes Dev 2008;22: 3050-3063
62. Mori H, Prestwich TC, Reid MA, et al. Secreted frizzled-related protein 5 suppresses adipocyte mitochondrial metabolism through WNT inhibition. J Clin Invest 2012;122: 2405-2416
63. Wada N, Hashinaga T, Otabe S, et al. Selective modulation of Wnt ligands and their receptors in adipose tissue by chronic hyperadiponectinemia. PLoS ONE 2013;8: E67712
64. Nishizuka M, Koyanagi A, Osada S, Imagawa M. Wnt4 and Wnt5a promote adipocyte differentiation. FEBS Lett 2008;582: 3201-3205
65. van Tienen FHJ, Laeremans H, van der Kallen CJH, Smeets HJM. Wnt5b stimulates adipogenesis by activating PPARgamma, and inhibiting the betacatenin dependent Wnt signaling pathway together with Wnt5a. Biochem Biophys Res Commun 2009;387: 207-211
66. Laudes M. Role of WNT signalling in the determination of human mesenchymal stem cells into preadipocytes. J Mol Endocrinol 2011;46: R65-R72
67. Takada I, Mihara M, Suzawa M, et al. A histone lysine methyltransferase activated by non-canonical Wnt signalling suppresses PPAR-gamma transactivation. Nat Cell Biol 2007;9: 1273-1285
68. Ishitani T, Kishida S, Hyodo-Miura J, et al. The TAK1-NLK mitogen-activated protein kinase cascade functions in the Wnt-5a/Ca(2+) pathway to antagonize Wnt/beta-catenin signaling. Mol Cell Biol 2003;23: 131-139
69. Solinas G, Vilcu C, Neels JG, et al. JNK1 in hematopoietically derived cells contributes to diet-induced inflammation and insulin resistance without affecting obesity. Cell Metab 2007;6: 386-397
70. Wallenius V, Wallenius K, Ahrén B, et al. Interleukin-6-deficient mice develop mature-onset obesity. Nat Med 2002;8: 75-79
71. Di Gregorio GB, Hensley L, Lu T, Ranganathan G, Kern PA. Lipid and carbohydrate metabolism in mice with a targeted mutation in the IL-6 gene: Absence of development of age-related obesity. Am J Physiol Endocrinol Metab 2004;287: E182-E187
72. Park EJ, Lee JH, Yu G-Y, et al. Dietary and genetic obesity promote liver inflammation and tumorigenesis by enhancing IL-6 and TNF expression. Cell 2010;140: 197-208
73. Mauer J, Chaurasia B, Goldau J, et al. Signaling by IL-6 promotes alternative activation of macrophages to limit endotoxemia and obesity-associated resistance to insulin. Nat Immunol 2014;15: 423-430
74. Klover PJ, Zimmers TA, Koniaris LG, Mooney RA. Chronic exposure to interleukin-6 causes hepatic insulin resistance in mice. Diabetes 2003;52: 2784-2789
75. Klover PJ, Clementi AH, Mooney RA. Interleukin-6 depletion selectively improves hepatic insulin action in obesity. Endocrinology 2005;146: 3417-3427
76. Bastard JP, Maachi M, Van Nhieu JT, et al. Adipose tissue IL-6 content correlates with resistance to insulin activation of glucose uptake both in vivo and in vitro. J Clin Endocrinol Metab 2002;87: 2084-2089
77. Kern PA, Ranganathan S, Li C, Wood L, Ranganathan G. Adipose tissue tumor necrosis factor and interleukin-6 expression in human obesity and insulin resistance. Am J Physiol Endocrinol Metab 2001;280: E745-E751
78. Vozarova B, Weyer C, Hanson K, Tataranni PA, Bogardus C, Pratley RE. Circulating interleukin-6 in relation to adiposity, insulin action, and insulin secretion. Obes Res 2001;9: 414-417
79. Pradhan AD, Manson JE, Rifai N, Buring JE, Ridker PM. C-reactive protein, interleukin 6, and risk of developing type 2 diabetes mellitus. JAMA 2001;286: 327-334
80. Bashan N, Dorfman K, Tarnovscki T, et al. Mitogen-activated protein kinases, inhibitory-kappaB kinase, and insulin signaling in human omental versus subcutaneous adipose tissue in obesity. Endocrinology 2007;148: 2955-2962
81. Cartier A, Lemieux I, Alméras N, Tremblay A, Bergeron J, Després J-P. Visceral obesity and plasma glucose-insulin homeostasis: Contributions of interleukin-6 and tumor necrosis factor-alpha in men. J Clin Endocrinol Metab 2008;93: 1931-1938
82. Park HS, Park JY, Yu R. Relationship of obesity and visceral adiposity with serum concentrations of CRP, TNF-A and IL-6. Diabetes Res Clin Pract 2005;69: 29-35