Lack of adiponectin leads to increased lymphocyte activation and increased disease severity in a mouse model of multiple sclerosis

European Journal of Immunology

Volumn 43, Issue 8, 2013, Pages 2089-2100

  Piccio, Laura ^a   Cantoni, Claudia ^a,b   Henderson, Jacob G ^c   Hawiger, Daniel ^c   Ramsbottom, Michael ^a   Mikesell, Robert ^a   Ryu, Jiyoon ^d   Hsieh, Chyi Song ^a   Cremasco, Viviana ^a   Haynes, Wesley ^a   Dong, Lily Q ^d   Chan, Lawrence ^e   Galimberti, Daniela ^b   Cross, Anne H ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b FONDAZIONE IRCCS CA GRANDA OSPEDALE MAGGIORE POLICLINICO   (Italy)

^c SAINT LOUIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d Mays Cancer Center at UT Health San Antonio   (United States)

^e BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Adiponectin; EAE; Immunomodulation; Multiple sclerosis

Indexed keywords

ADIPONECTIN; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 17; INTERLEUKIN 6; MYELIN; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA;

ALLERGIC ENCEPHALOMYELITIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN PRESENTING CELL; ARTICLE; AXONAL INJURY; CONTROLLED STUDY; DEMYELINATION; DISEASE SEVERITY; IMMUNIZATION; LYMPHOCYTE; LYMPHOCYTE ACTIVATION; MOUSE; MULTIPLE SCLEROSIS; NONHUMAN; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; SPINAL CORD; SPLEEN; T LYMPHOCYTE;

ADIPONECTIN; EAE; IMMUNOMODULATION; MULTIPLE SCLEROSIS;

ADIPONECTIN; ADOPTIVE TRANSFER; ANIMALS; AUTOIMMUNITY; CELL PROLIFERATION; CELLS, CULTURED; CENTRAL NERVOUS SYSTEM; DISEASE MODELS, ANIMAL; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; FORKHEAD TRANSCRIPTION FACTORS; INTERFERON-GAMMA; INTERLEUKIN-10; INTERLEUKIN-17; INTERLEUKIN-6; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MULTIPLE SCLEROSIS; MYELIN SHEATH; RISK FACTORS; SPLEEN; T-LYMPHOCYTES, REGULATORY; TH1 CELLS; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84881510394     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201242836     Document Type: Article

References (34)

1. Schwarz, S. and Leweling, H., Multiple sclerosis and nutrition. Mult. Scler. 2005. 11: 24-32.
2. Swank, R. L. and Dugan, B. B., Effect of low saturated fat diet in early and late cases of multiple sclerosis. Lancet 1990. 336: 37-39.
3. Gold, R., Linington, C. and Lassmann, H., Understanding pathogenesis and therapy of multiple sclerosis via animal models: 70 years of merits and culprits in experimental autoimmune encephalomyelitis research. Brain 2006. 129: 1953-1971.
4. Hedstrom, A. K., Olsson, T. and Alfredsson, L., High body mass index before age 20 is associated with increased risk for multiple sclerosis in both men and women. Mult. Scler. 2012. 18: 1334-1336.
5. Munger, K. L., Chitnis, T. and Ascherio, A., Body size and risk of MS in two cohorts of US women. Neurology 2009. 73: 1543-1550.
6. Shoelson, S. E., Herrero, L. and Naaz, A., Obesity, inflammation, and insulin resistance. Gastroenterology 2007. 132: 2169-2180.
7. Fantuzzi, G., Adipose tissue, adipokines, and inflammation. J. Allergy Clin. Immunol. 2005. 115: 911-919.
8. Piccio, L., Stark, J. L. and Cross, A. H., Chronic calorie restriction attenuates experimental autoimmune encephalomyelitis. J. Leukoc. Biol. 2008. 84: 940-948.
9. Fruebis, J., Tsao, T. S., Javorschi, S., Ebbets-Reed, D., Erickson, M. R., Yen, F. T., Bihain, B. E. et al., Proteolytic cleavage product of 30-kDa adipocyte complement-related protein increases fatty acid oxidation in muscle and causes weight loss in mice. Proc. Natl. Acad. Sci. USA 2001. 98: 2005-2010.
10. Kadowaki, T. and Yamauchi, T., Adiponectin and adiponectin receptors. Endocr. Rev. 2005. 26: 439-451.
11. Tilg, H. and Moschen, A. R., Adipocytokines: mediators linking adipose tissue, inflammation and immunity. Nat. Rev. Immunol. 2006. 6: 772-783.
12. Musabak, U., Demirkaya, S., Genc, G., Ilikci, R. S. and Odabasi, Z., Serum adiponectin, TNF-alpha, IL-12p70, and IL-13 levels in multiple sclerosis and the effects of different therapy regimens. Neuroimmunomodulation 2011. 18: 57-66.
13. Hietaharju, A., Kuusisto, H., Nieminen, R., Vuolteenaho, K., Elovaara, I. and Moilanen, E., Elevated cerebrospinal fluid adiponectin and adipsin levels in patients with multiple sclerosis: a Finnish co-twin study. Eur. J. Neurol. 2010. 17: 332-334.
14. O'Connor, R. A. and Anderton, S. M., Foxp3+ regulatory T cells in the control of experimental CNS autoimmune disease. J. Neuroimmunol. 2008. 193: 1-11.
15. Ma, K., Cabrero, A., Saha, P. K., Kojima, H., Li, L., Chang, B. H., Paul, A. et al., Increased beta oxidation but no insulin resistance or glucose intolerance in mice lacking adiponectin. J. Biol. Chem. 2002. 277: 34658-34661.
16. Nishida, M., Funahashi, T. and Shimomura, I., Pathophysiological significance of adiponectin. Med. Mol. Morphol. 2007. 40: 55-67.
17. Ouedraogo, R., Gong, Y., Berzins, B., Wu, X., Mahadev, K., Hough, K., Chan, L. et al., Adiponectin deficiency increases leukocyte-endothelium interactions via upregulation of endothelial cell adhesion molecules in vivo. J. Clin. Invest. 2007. 117: 1718-1726.
18. Brochu-Gaudreau, K., Rehfeldt, C., Blouin, R., Bordignon, V., Murphy, B. D. and Palin, M. F., Adiponectin action from head to toe. Endocrine 2010. 37: 11-32.
19. Wan, Y. Y. and Flavell, R. A., Identifying Foxp3-expressing suppressor T cells with a bicistronic reporter. Proc. Natl. Acad. Sci. USA 2005. 102: 5126-5131.
20. Wilk, S., Scheibenbogen, C., Bauer, S., Jenke, A., Rother, M., Guerreiro, M., Kudernatsch, R. et al., Adiponectin is a negative regulator of antigen-activated T cells. Eur. J. Immunol. 2011. 41: 2323-2332.
21. Fantuzzi, G., Adiponectin and inflammation: consensus and controversy. J. Allergy Clin. Immunol. 2008. 121: 326-330.
22. Tsang, J. Y., Li, D., Ho, D., Peng, J., Xu, A., Lamb, J., Chen, Y. et al., Novel immunomodulatory effects of adiponectin on dendritic cell functions. Int. Immunopharmacol. 2011. 11: 604-609.
23. Feuerer, M., Herrero, L., Cipolletta, D., Naaz, A., Wong, J., Nayer, A., Lee, J. 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.
24. Kraszula, L., Jasinska, A., Eusebio, M. O., Kuna, P., Glabinski, A. and Pietruczuk, M., Evaluation of the relationship between leptin, resistin, adiponectin and natural regulatory T cells in relapsing-remitting multiple sclerosis. Neurol. Neurochir. Pol. 2012. 46: 22-28.
25. Holland, W. L., Miller, R. A., Wang, Z. V., Sun, K., Barth, B. M., Bui, H. H., Davis, K. E. et al., Receptor-mediated activation of ceramidase activity initiates the pleiotropic actions of adiponectin. Nat. Med. 2011. 17: 55-63.
26. Mao, X., Kikani, C. K., Riojas, R. A., Langlais, P., Wang, L., Ramos, F. J., Fang, Q. et al., APPL1 binds to adiponectin receptors and mediates adiponectin signalling and function. Nat. Cell Biol. 2006. 8: 516-523.
27. Hug, C., Wang, J., Ahmad, N. S., Bogan, J. S., Tsao, T. S. and Lodish, H. F., T-cadherin is a receptor for hexameric and high-molecular-weight forms of Acrp30/adiponectin. Proc. Natl. Acad. Sci. USA 2004. 101: 10308-10313.
28. Takemura, Y., Ouchi, N., Shibata, R., Aprahamian, T., Kirber, M. T., Summer, R. S., Kihara, S. et al., Adiponectin modulates inflammatory reactions via calreticulin receptor-dependent clearance of early apoptotic bodies. J. Clin. Invest. 2007. 117: 375-386.
29. Okamoto, Y., Arita, Y., Nishida, M., Muraguchi, M., Ouchi, N., Takahashi, M., Igura, T. et al., An adipocyte-derived plasma protein, adiponectin, adheres to injured vascular walls. Horm. Metab. Res. 2000. 32: 47-50.
30. Yamauchi, T., Kamon, J., Waki, H., Imai, Y., Shimozawa, N., Hioki, K., Uchida, S. et al., Globular adiponectin protected ob/ob mice from diabetes and ApoE-deficient mice from atherosclerosis. J. Biol. Chem. 2003. 278: 2461-2468.
31. Qi, Y., Takahashi, N., Hileman, S. M., Patel, H. R., Berg, A. H., Pajvani, U. B., Scherer, P. E. et al., Adiponectin acts in the brain to decrease body weight. Nat. Med. 2004. 10: 524-529.
32. Gimenez, M. A., Sim, J., Archambault, A. S., Klein, R. S. and Russell, J. H., A tumor necrosis factor receptor 1-dependent conversation between central nervous system-specific T cells and the central nervous system is required for inflammatory infiltration of the spinal cord. Am. J. Pathol. 2006. 168: 1200-1209.
33. Wang, C., Xin, X., Xiang, R., Ramos, F. J., Liu, M., Lee, H. J., Chen, H. et al., Yin-Yang regulation of adiponectin signaling by APPL isoforms in muscle cells. J. Biol. Chem. 2009. 284: 31608-31615.
34. Fleming, K. K., Bovaird, J. A., Mosier, M. C., Emerson, M. R., LeVine, S. M. and Marquis, J. G., Statistical analysis of data from studies on experimental autoimmune encephalomyelitis. J. Neuroimmunol. 2005. 170: 71-84.