Roles of chemokines and chemokine receptors in obesity-associated insulin resistance and nonalcoholic fatty liver disease

Biomolecules

Volumn 5, Issue 3, 2015, Pages 1563-1579

  Xu, Liang ^a   Kitade, Hironori ^a   Ni, Yinhua ^a   Ota, Tsuguhito ^a  

^a KANAZAWA UNIVERSITY   (Japan)

Author keywords

Adipose tissue macrophage; Chemokines; Inflammation; Insulin resistance; Kupffer cells; Macrophage polarization; Nonalcoholic fatty liver disease; Obesity

Indexed keywords

CHEMOKINE; CHEMOKINE RECEPTOR; CHEMOKINE RECEPTOR CCR2; CHEMOKINE RECEPTOR CCR5; G PROTEIN COUPLED RECEPTOR; INTERLEUKIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 4; MONOCYTE CHEMOTACTIC PROTEIN 1;

ADIPOSE TISSUE; CELL ACTIVITY; DISEASE ASSOCIATION; HOMEOSTASIS AND REGULATION; HUMAN; IMMUNE RESPONSE; INFLAMMATION; INSULIN RESISTANCE; INSULIN SENSITIVITY; MACROPHAGE ACTIVATION; NONALCOHOLIC FATTY LIVER; OBESITY; REVIEW; ANIMAL; COMPLICATION; DISEASE COURSE; IMMUNOLOGY; METABOLISM; PATHOLOGY;

ANIMALS; CHEMOKINES; DISEASE PROGRESSION; HUMANS; INSULIN RESISTANCE; NON-ALCOHOLIC FATTY LIVER DISEASE; OBESITY; RECEPTORS, CHEMOKINE;

EID: 85012065385     PISSN: None     EISSN: 2218273X     Source Type: Journal    
DOI: 10.3390/biom5031563     Document Type: Review

References (63)

1. Hotamisligil, G.S.; Erbay, E. Nutrient sensing and inflammation in metabolic diseases. Nat. Rev. Immunol. 2008, 8, 923-934.
2. Wajchenberg, B.L. Subcutaneous and visceral adipose tissue: Their relation to the metabolic syndrome. Endocr. Rev. 2000, 21, 697-738.
3. Mantovani, A.; Allavena, P.; Sica, A.; Balkwill, F. Cancer-related inflammation. Nature 2008, 454, 436-444.
4. Shoelson, S.E.; Lee, J.; Goldfine, A.B. Inflammation and insulin resistance. J. Clin. Invest. 2006, 115, 1793-1801.
5. Siiteri, P.K. Adipose tissue as a source of hormones. Am. J. Clin. Nutr. 1987, 45, 277-282.
6. Hotamisligil, G.S.; Shargill, N.S.; Spiegelman, B.M. Adipose expression of tumor necrosis factor-alpha: Direct role in obesity-linked insulin resistance. Science 1993, 259, 87-91.
7. Neels, J.G.; Olefsky, J.M. Inflamed fat: What starts the fire? J. Clin. Invest. 2006, 115, 33-35.
8. Xu, A.; Wang, Y.; Keshaw, H.; Xu, L.Y.; Lam, K.S.; Cooper, G.J. The fat-derived hormone adiponectin alleviates alcoholic and nonalcoholic fatty liver diseases in mice. J. Clin. Invest. 2003, 112,91-100.
9. Weisberg, S.P.; McCann, D.; Desai, M.; Rosenbaum, M.; Leibel, R.L.; Ferrante, A.W., Jr. Obesity is associated with macrophage accumulation in adipose tissue. J. Clin. Invest. 2003, 112, 1796-1808.
10. Obstfeld, A.E.; Sugaru, E.; Thearle, M.; Francisco, A.M.; Gayet, C.; Ginsberg, H.N.; Ables, E.V.; Ferrante, A.W., Jr. CC chemokine receptor 2 (CCR2) regulates the hepatic recruitment of myeloid cells that promote obesity-induced hepatic steatosis. Diabetes 2010, 59, 916-925.
11. Mantovani, A.; Sica, A.; Sozzani, S.; Allavena, P.; Vecchi, A.; Locati, M. The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol. 2004, 25, 677-686.
12. Lumeng, C.N.; Bodzin, J.L.; Saltiel, A.R. Obesity induces a phenotypic switch in adipose tissue macrophage polarization. J. Clin. Invest. 2007, 117, 175-184.
13. Proudfoot, A.E. Chemokine receptors: Multifaceted therapeutic targets. Nat. Rev. Immunol. 2002, 2, 106-115.
14. Mantovani, A.; Bonecchi, R.; Locati, M. Tuning inflammation and immunity by chemokine Sequestration: Decoys and more. Nat. Rev. Immunol. 2006, 6, 907-918.
15. Bachelerie, F.; Ben-Baruch, A.; Burkhardt, A.M.; Combadiere, C.; Farber, J.M.; Graham, G.J.; Horuk, R.; Sparre-Ulrich, A.H.; Locati, M.; Luster, A.D., et al. International Union of Basic and Clinical Pharmacology. [corrected]. LXXXIX. Update on the extended family of chemokine receptors and introducing a new nomenclature for atypical chemokine receptors. Pharmacol. Rev. 2014, 66, 1-79.
16. Weisberg, S.P.; Hunter, D.; Huber, R.; Lemieux, J.; Slaymaker, S.; Vaddi, K.; Charo, I.; Leibel, R.L.; Ferrante, A.W. CCR2 modulates inflammatory and metabolic effects of high-fat feeding. J. Clin. Invest. 2006, 116, 115-124.
17. Kanda, H.; Tateya, S.; Tamori, Y.; Kotani, K.; Hiasa, K.; Kitazawa, R.; Kitazawa, S.; Miyachi, H.; Maeda, S.; Egashira, K., et al. Mcp-1 contributes to macrophage infiltration into adipose tissue, insulin resistance, and hepatic steatosis in obesity. J. Clin. Invest. 2006, 116, 1494-1505.
18. Hotamisligil, G.S. Inflammation and metabolic disorders. Nature 2006, 444, 860-867.
19. Huang, W.; Metlakunta, A.; Dedousis, N.; Zhang, P.; Sipula, I.; Dube, J.J.; Scott, D.K.; O'Doherty, R.M. Depletion of liver Kupffer cells prevents the development of diet-induced hepatic steatosis and insulin resistance. Diabetes 2010, 59, 347-357.
20. Hong, E.G.; Ko, H.J.; Cho, Y.R.; Kim, H.J.; Ma, Z.; Yu, T.Y.; Friedline, R.H.; Kurt-Jones, E.; Finberg, R.; Fischer, M.A., et al. Interleukin-10 prevents diet-induced insulin resistance by attenuating macrophage and cytokine response in skeletal muscle. Diabetes 2009, 55, 2525-2535.
21. Odegaard, J.I.; Ricardo-Gonzalez, R.R.; Goforth, M.H.; Morel, C.R.; Subramanian, V.; Mukundan, L.; Eagle, A.R.; Vats, D.; Brombacher, F.; Ferrante, A.W., et al. Macrophage-specific PPARgamma controls alternative activation and improves insulin resistance. Nature 2007, 447, 1116-1120.
22. Lumeng, C.N.; DelProposto, J.B.; Westcott, D.J.; Saltiel, A.R. Phenotypic switching of adipose tissue macrophages with obesity is generated by spatiotemporal differences in macrophage subtypes. Diabetes 2008, 57, 3239-3246.
23. Nguyen, M.T.; Favelyukis, S.; Nguyen, A.K.; Reichart, D.; Scott, P.A.; Jenn, A.; Liu-Bryan, R.; Glass, C.K.; Neels, J.G.; Olefsky, J.M. 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.
24. Ouchi, N.; Parker, J.L.; Lugus, J.J.; Walsh, K. Adipokines in inflammation and metabolic disease. Nat. Rev. Immunol. 2011, 11, 85-97.
25. Ji, Y.; Sun, S.; Xu, A.; Bhargava, P.; Yang, L.; Lam, K.S., et al. Activation of natural killer T cells promotes M2 Macrophage polarization in adipose tissue and improves systemic glucose tolerance via interleukin-4(IL-4)/STAT6 protein signaling axis in obesity. J Biol Chem 2012, 287, 13561-13571.
26. Cintra, D.E.; Pauli, J.R.; Araujo, E.P.; Moraes, J.C.; de Souza, C.T.; Milanski, M.; Morari, J.; Gambero, A.; Saad, M.J.; Velloso, L.A. Interleukin-10 is a protective factor against diet-induced insulin resistance in liver. J. Hepatol. 2008, 48, 628-637.
27. Nishimura, S.; Manabe, I.; Nagasaki, M.; Eto, K.; Yamashita, H.; Ohsugi, M.; Otsu, M.; Hara, K.; Ueki, K.; Sugiura, S., et al. CD8+ effector T cells contribute to macrophage recruitment and adipose tissue inflammation in obesity. Nat. Med. 2009, 15, 914-920.
28. Winer, S.; Chan, Y.; Paltser, G.; Truong, D.; Tsui, H.; Bahrami, J.; Dorfman, R.; Wang, Y.; Zielenski, J.; Mastronardi, F., et al. Normalization of obesity-associated insulin resistance through immunotherapy. Nat. Med. 2009, 15, 921-929.
29. Feuerer, M.; Herrero, L.; Cipolletta, D.; Naaz, A.; Wong, J.; Nayer, A.; Lee, J.; Goldfine, A.B.; Benoist, C.; Shoelson, S., et al. Lean, but not obese, fat is enriched for a unique population of regulatory T cells that affect metabolic parameters. Nat. Med. 2009, 15, 930-939.
30. DeFuria, J.; Belkina, A.C.; Jagannathan-Bogdan, M.; Snyder-Cappione, J.; Carr, J.D.; Nersesova, Y.R.; Markham, D.; Strissel, K.J.; Watkins, A.A.; Zhu, M., et al. B cells promote inflammation in obesity and type 2 diabetes through regulation of T-cell function and an inflammatory cytokine profile. Proc. Natl. Acad. Sci. USA 2013, 110, 5133-5138.
31. Winer, D.A.; Winer, S.; Shen, L.; Wadia, P.P.; Yantha, J.; Paltser, G.; Tsui, H.; Wu, P.; Davidson, M.G.; Alonso, M.N., et al. B cells promote insulin resistance through modulation of T cells and production of pathogenic IgG antibodies. Nat. Med. 2011, 17, 610-617.
32. Wu, D.; Molofsky, A.B.; Liang, H.E.; Ricardo-Gonzalez, R.R.; Jouihan, H.A.; Bando, J.K.; Chawla, A.; Locksley, R.M. Eosinophils sustain adipose alternatively activated macrophages associated with glucose homeostasis. Science 2011, 332, 243-247.
33. Talukdar, S.; Oh, D.Y.; Bandyopadhyay, G.; Li, D.; Xu, J.; McNelis, J.; Lu, M.; Li, P.; Yan, Q.; Zhu, Y., et al. Neutrophils mediate insulin resistance in mice fed a high-fat diet through secreted elastase. Nat. Med. 2012, 18, 1407-1412.
34. Liu, J.; Divoux, A.; Sun, J.; Zhang, J.; Clement, K.; Glickman, J.N.; Sukhova, G.K.; Wolters, P.J.; Du, J.; Gorgun, C.Z., et al. Genetic deficiency and pharmacological stabilization of mast cells reduce diet-induced obesity and diabetes in mice. Nat. Med. 2009, 15, 940-945.
35. Tanaka, A.; Nomura, Y.; Matsuda, A.; Ohmori, K.; Matsuda, H. Mast cells function as an alternative modulator of adipogenesis through 15-deoxy-delta-12, 14-prostaglandin J2. Am. J. Physiol. Cell Physiol. 2011, 301, C1360-C1367.
36. Baggiolini, M. Chemokines and leukocyte traffic. Nature 1998, 392, 565-568.
37. Gerard, C.; Rollins, B.J. Chemokines and disease. Nat. Immunol. 2001, 2, 108-115.
38. Kamei, N.; Tobe, K.; Suzuki, R.; Ohsugi, M.; Watanabe, T.; Kubota, N.; Ohtsuka-Kowatari, N.; Kumagai, K.; Sakamoto, K.; Kobayashi, M., et al. Overexpression of monocyte chemoattractant protein-1 in adipose tissues causes macrophage recruitment and insulin resistance. J. Biol. Chem. 2006, 281, 26602-26614.
39. Tamura, Y.; Sugimoto, M.; Murayama, T.; Ueda, Y.; Kanamori, H.; Ono, K.; Ariyasu, H.; Akamizu, T.; Kita, T.; Yokode, M., et al. Inhibition of CCR2 ameliorates insulin resistance and hepatic steatosis in db/db mice. Arterioscler. Thromb. Vasc. Biol. 2008, 28, 2195-2201.
40. Inouye, K.E.; Shi, H.; Howard, J.K.; Daly, C.H.; Lord, G.M.; Rollins, B.J.; Flier, J.S. Absence of CC chemokine ligand 2 does not limit obesity-associated infiltration of macrophages into adipose tissue. Diabetes 2007, 56, 2242-2250.
41. Kirk, E.A.; Sagawa, Z.K.; McDonald, T.O.; O'Brien, K.D.; Heinecke, J.W. Monocyte chemoattractant protein deficiency fails to restrain macrophage infiltration into adipose tissue. Diabetes 2008, 57, 1254-1261.
42. Chavey, C.; Lazennec, G.; Lagarrigue, S.; Clape, C.; Iankova, I.; Teyssier, J.; Annicotte, J.S.; Schmidt, J.; Mataki, C.; Yamamoto, H., et al. CXC ligand 5 is an adipose-tissue derived factor that links obesity to insulin resistance. Cell. Metab. 2009, 9, 339-349.
43. Kim, D.; Kim, J.; Yoon, J.H.; Ghim, J.; Yea, K.; Song, P.; Park, S.; Lee, A.; Hong, C.P.; Jang, M.S., et al. CXCL12 secreted from adipose tissue recruits macrophages and induces insulin resistance in mice. Diabetologia 2014, 57, 1456-1465.
44. Kitade, H.; Sawamoto, K.; Nagashimada, M.; Inoue, H.; Yamamoto, Y.; Sai, Y.; Takamura, T.; Yamamoto, H.; Miyamoto, K.; Ginsberg, H.N., et al. CCR5 plays a critical role in obesity-induced adipose tissue inflammation and insulin resistance by regulating both macrophage recruitment and M1/M2 status. Diabetes 2012, 61, 1680-1690.
45. Angulo, P. Nonalcoholic fatty liver disease. N. Engl. J. Med. 2002, 346, 1221-1231.
46. Day, C.P.; James, O.F. Steatohepatitis: A tale of two "hits"? Gastroenterology 1998, 114, 842-845.
47. Tilg, H.; Moschen, A.R. Evolution of inflammation in nonalcoholic fatty liver disease: The multiple parallel hits hypothesis. Hepatology 2010, 52, 1836-1846.
48. Miura, K.; Yang, L.; van Rooijen, N.; Ohnishi, H.; Seki, E. Hepatic recruitment of macrophages promotes nonalcoholic steatohepatitis through CCR2. Am. J. Physiol. Gastrointest. Liver Physiol. 2012, 302, G1310-G1321.
49. Seki, E.; de Minicis, S.; Inokuchi, S.; Taura, K.; Miyai, K.; van Rooijen, N.; Schwabe, R.F.; Brenner, D.A. CCR2 promotes hepatic fibrosis in mice. Hepatology 2009, 50, 185-197.
50. Seki, E.; de Minicis, S.; Gwak, G.Y.; Kluwe, J.; Inokuchi, S.; Bursill, C.A.; Llovet, J.M.; Brenner, D.A.; Schwabe, R.F. CCR1 and CCR5 promote hepatic fibrosis in mice. J. Clin. Invest. 2009,119, 1858-1870.
51. Wu, H.; Ghosh, S.; Perrard, X.D.; Feng, L.; Garcia, G.E.; Perrard, J.L.; Sweeney, J.F.; Peterson, L.E.; Chan, L.; Smith, C.W., et al. T-cell accumulation and regulated on activation, normal T cell expressed and secreted upregulation in adipose tissue in obesity. Circulation 2007, 115, 1029-1038.
52. Braunersreuther, V.; Viviani, G.L.; Mach, F.; Montecucco, F. Role of cytokines and chemokines in non-alcoholic fatty liver disease. World J. Gastroenterol. 2012, 18, 727-735.
53. Bahcecioglu, I.H.; Yalniz, M.; Ataseven, H.; Ilhan, N.; Ozercan, I.H.; Seckin, D.; Sahin, K. Levels of serum hyaluronic acid, TNF-alpha and IL-8 in patients with nonalcoholic steatohepatitis. Hepatogastroenterology 2005, 52, 1549-1553.
54. Wasmuth, H.E.; Lammert, F.; Zaldivar, M.M.; Weiskirchen, R.; Hellerbrand, C.; Scholten, D.; Berres, M.L.; Zimmermann, H.; Streetz, K.L.; Tacke, F., et al. Antifibrotic effects of CXCL9 and its receptor CXCR3 in livers of mice and humans. Gastroenterology 2009, 137, 309-319.
55. Sica, A.; Invernizzi, P.; Mantovani, A. Macrophage plasticity and polarization in liver homeostasis and pathology. Hepatology 2014, 59, 2034-2042.
56. Wan, J.; Benkdane, M.; Teixeira-Clerc, F.; Bonnafous, S.; Louvet, A.; Lafdil, F.; Pecker, F.; Tran, A.; Gual, P.; Mallat, A., et al. M2 Kupffer cells promote M1 Kupffer cell apoptosis: A protective mechanism against alcoholic and nonalcoholic fatty liver disease. Hepatology 2014, 59, 130-142.
57. Louvet, A.; Teixeira-Clerc, F.; Chobert, M.N.; Deveaux, V.; Pavoine, C.; Zimmer, A.; Pecker, F.; Mallat, A.; Lotersztajn, S. Cannabinoid CB2 receptors protect against alcoholic liver disease by regulating Kupffer cell polarization in mice. Hepatology 2011, 54, 1217-1226.
58. Sugiura, M.; Nakamura, M.; Ikoma, Y.; Yano, M.; Ogawa, K.; Matsumoto, H.; Kato, M.; Ohshima, M.; Nagao, A. High serum carotenoids are inversely associated with serum gamma-glutamyltransferase in alcohol drinkers within normal liver function. J. Epidemiol. 2005, 15, 180-186.
59. Sugiura, M.; Nakamura, M.; Ikoma, Y.; Yano, M.; Ogawa, K.; Matsumoto, H.; Kato, M.; Ohshima, M.; Nagao, A. The homeostasis model assessment-insulin resistance index is inversely associated with serum carotenoids in non-diabetic subjects. J. Epidemiol. 2006, 15, 71-78.
60. Katsuura, S.; Imamura, T.; Bando, N.; Yamanishi, R. Beta-carotene and beta-cryptoxanthin but not lutein evoke redox and immune changes in RAW264 murine macrophages. Mol. Nutr. Food Res. 2009, 53, 1396-1405.
61. Takayanagi, K.; Morimoto, S.; Shirakura, Y.; Mukai, K.; Sugiyama, T.; Tokuji, Y.; Ohnishi, M. Mechanism of visceral fat reduction in Tsumura Suzuki obese, diabetes (TSOD) mice orally administered beta-cryptoxanthin from Satsuma mandarin oranges (Citrus unshiu Marc). J. Agric. Food Chem. 2011, 59, 12342-12351.
62. Kobori, M.; Ni, Y.; Takahashi, Y.; Watanabe, N.; Sugiura, M.; Ogawa, K.; Nagashimada, M.; Kaneko, S.; Naito, S.; Ota, T. Beta-cryptoxanthin alleviates diet-induced nonalcoholic steatohepatitis by suppressing inflammatory gene expression in mice. PLoS ONE 2014, 9, e98294.
63. Ni, Y.; Nagashimada, M.; Zhan, L.; Nagata, N.; Kobori, M.; Sugiura, M.; Ogawa, K.; Kaneko, S.; Ota, T. Prevention and reversal of lipotoxicity-induced hepatic insulin resistance and steatohepatitis in mice by an antioxidant carotenoid, beta-cryptoxanthin. Endocrinology 2015, 155, 987-999.