Adiponectin modulates inflammatory reactions via calreticulin receptor-dependent clearance of early apoptotic bodies

Journal of Clinical Investigation

Volumn 117, Issue 2, 2007, Pages 375-386

  Takemura, Yukihiro ^a   Ouchi, Noriyuki ^a   Shibata, Rei ^a   Aprahamian, Tamar ^a   Kirber, Michael T ^a   Summer, Ross S ^a   Kihara, Shinji ^b   Walsh, Kenneth ^a  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b OSAKA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ADIPONECTIN; CALRETICULIN; DEXAMETHASONE SODIUM PHOSPHATE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; AUTOIMMUNITY; CONTROLLED STUDY; DISEASE EXACERBATION; DRUG ACTIVITY; DRUG RECEPTOR BINDING; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; INFLAMMATION; KNOCKOUT MOUSE; MACROPHAGE; MOLECULAR DYNAMICS; MOUSE; MOUSE STRAIN; NONHUMAN; OPSONIZATION; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN DEFICIENCY; THYMOCYTE; TREATMENT RESPONSE; WILD TYPE;

ADIPONECTIN; ANIMALS; APOPTOSIS; BASE SEQUENCE; CALRETICULIN; CELL LINE; DNA PRIMERS; HUMANS; INFLAMMATION; JURKAT CELLS; MICE; MICE, INBRED C57BL; MICE, INBRED MRL LPR; MICE, KNOCKOUT; RECOMBINANT PROTEINS;

EID: 33846784058     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI29709     Document Type: Article

References (50)

1. Weisberg, S.P., et al. 2003. Obesity is associated with macrophage accumulation in adipose tissue. J. Clin. Invest. 112:1796-1808. doi:10.1172/JCI200319246.
2. Ruan, H., and Lodish, H.F. 2004. Regulation of insulin sensitivity by adipose tissue-derived hormones and inflammatory cytokines. Curr. Opin. Lipidol. 15:297-302.
3. Spiegelman, B.M., Choy, L., Hotamisligil, G.S., Graves, R.A., and Tontonoz, P. 1993. Regulation of adipocyte gene expression in differentiation and syndromes of obesity/diabetes. J. Biol. Chem. 268:6823-6826.
4. Maeda, K., et al. 1996. cDNA cloning and expression of a novel adipose specific collagen-like factor, apM1 (AdiPose Most abundant Gene transcript 1). Biochem. Biophys. Res. Commun. 221:286-289.
5. Hu, E., Liang, P., and Spiegelman, B.M. 1996. AdipoQ is a novel adipose-specific gene dysregulated in obesity. J. Biol. Chem. 271:10697-10703.
6. Spranger, J., et al. 2003. Adiponectin and protection against type 2 diabetes mellitus. Lancet. 361:226-228.
7. Yamauchi, T., et al. 2001. The fat-derived hormone adiponectin reverses insulin resistance associated with both lipoatrophy and obesity. Nat. Med. 7:941-946.
8. Maeda, N., et al. 2002. Diet-induced insulin resistance in mice lacking adiponectin/ACRP30. Nat. Med. 8:731-737.
9. Okamoto, Y., et al. 2002. Adiponectin reduces atherosclerosis in apolipoprotein E-deficient mice. Circulation. 106:2767-2770.
10. Shibata, R., et al. 2004. Adiponectin stimulates angiogenesis in response to tissue ischemia through stimulation of amp-activated protein kinase signaling. J. Biol. Chem. 279:28670-28674.
11. Shibata, R., et al. 2004. Adiponectin-mediated modulation of hypertrophic signals in the heart. Nat. Med. 10:1384-1389.
12. Yamauchi, T., et al. 2003. Cloning of adiponectin receptors that mediate antidiabetic metabolic effects. Nature. 423:762-769.
13. Hug, C., et al. 2004. T-cadherin is a receptor for hexameric and high-molecular-weight forms of Acrp30/adiponectin. Proc. Natl. Acad. Sci. U. S. A. 101:10308-10313.
14. Tataranni, P.A., and Ortega, E. 2005. A burning question: does an adipokine-induced activation of the immune system mediate the effect of overnutrition on type 2 diabetes? Diabetes. 54:917-927.
15. Ouchi, N., Kihara, S., Funahashi, T., Matsuzawa, Y., and Walsh, K. 2003. Obesity, adiponectin and vascular inflammatory disease. Curr. Opin. Lipidol. 14:561-566.
16. Ouchi, N., et al. 2003. Reciprocal association of C-reactive protein with adiponectin in blood stream and adipose tissue. Circulation. 107:671-674.
17. Krakoff, J., et al. 2003. Inflammatory markers, adiponectin, and risk of type 2 diabetes in the Pima Indian. Diabetes Care. 26:1745-1751.
18. Matsubara, M., Namioka, K., and Katayose, S. 2003. Decreased plasma adiponectin concentrations in women with low-grade C-reactive protein elevation. Eur. J. Endocrinol. 148:657-662.
19. Engeli, S., et al. 2003. Association between adiponectin and mediators of inflammation in obese women. Diabetes. 52:942-947.
20. Matsushita, K., et al. 2005. Inverse association between adiponectin and C-reactive protein in substantially healthy Japanese men. Atherosclerosis. 188:184-189.
21. Shibata, R., et al. 2005. Adiponectin protects against myocardial ischemia-reperfusion injury through AMPK- and COX-2-dependent mechanisms. Nat. Med. 11:1096-1103.
22. Xu, A., et al. 2003. The fat-derived hormone adiponectin alleviates alcoholic and nonalcoholic fatty liver diseases in mice. J. Clin. Invest. 112:91-100. doi:10.1172/JCI200317797.
23. Ujiie, H., et al. 2006. Identification of amino-terminal region of adiponectin as a physiologically functional domain. J. Cell. Biochem. 98:194-207.
24. Arita, Y., et al. 1999. Paradoxical decrease of an adipose-specific protein, adiponectin, in obesity. Biochem. Biophys. Res. Commun. 257:79-83.
25. Vandivier, R.W., et al. 2002. Role of surfactant proteins A, D, and C1q in the clearance of apoptotic cells in vivo and in vitro: calreticulin and CD91 as a common collectin receptor complex. J. Immunol. 169:3978-3986.
26. Savill, J., Dransfield, I., Gregory, C., and Haslett, C. 2002. A blast from the past: clearance of apoptotic cells regulates immune responses. Nat. Rev. Immunol. 2:965-975.
27. Berg, A.H., and Scherer, P.E. 2005. Adipose tissue, inflammation, and cardiovascular disease. Circ. Res. 96:939-949.
28. Scott, R.S., et al. 2001. Phagocytosis and clearance of apoptotic cells is mediated by MER. Nature. 411:207-211.
29. Aprahamian, T., et al. 2004. Impaired clearance of apoptotic cells promotes synergy between atherogenesis and autoimmune disease. J. Exp. Med. 199:1121-1131.
30. Licht, R., Dieker, J.W., Jacobs, C.W., Tax, W.J., and Berden, J.H. 2004. Decreased phagocytosis of apoptotic cells in diseased SLE mice. J. Autoimmun. 22:139-145.
31. Kelley, V.E., and Roths, J.B. 1985. Interaction of mutant lpr gene with background strain influences renal disease. Clin. Immunol. Immunopathol. 37:220-229.
32. Cohen, P.L., and Eisenberg, R.A. 1991. Lpr and gld: single gene models of systemic autoimmunity and lymphoproliferative disease. Annu. Rev. Immunol. 9:243-269.
33. Morse, H.C., III, et al. 1985. Abnormalities induced by the mutant gene, lpr. Patterns of disease and expression of murine leukemia viruses in SJL/J mice homozygous and heterozygous for lpr. J. Exp. Med. 161:602-616.
34. Botto, M., et al. 1998. Homozygous C1q deficiency causes glomerulonephritis associated with multiple apoptotic bodies. Nat. Genet. 19:56-59.
35. Ogden, C.A., et al. 2001. C1q and mannose binding lectin engagement of cell surface calreticulin and CD91 initiates macropinocytosis and uptake of apoptotic cells. J. Exp. Med. 194:781-795.
36. Gardai, S.J., et al. 2005. Cell-surface calreticulin initiates clearance of viable or apoptotic cells through trans-activation of LRP on the phagocyte. Cell. 123:321-334.
37. Yokota, T., et al. 2000. Adiponectin, a new member of the family of soluble defense collagens, negatively regulates the growth of myelomonocytic progenitors and the functions of macrophages. Blood. 96:1723-1732.
38. Kumada, M., et al. 2004. Adiponectin specifically increased tissue inhibitor of metalloproteinase-1 through interleukin-10 expression in human macrophages. Circulation. 109:2046-2049.
39. Stern, M., Savill, J., and Haslett, C. 1996. Human monocyte-derived macrophage phagocytosis of senescent eosinophils undergoing apoptosis. Mediation by alpha v beta 3/CD36/thrombospondin recognition mechanism and lack of phlogistic response. Am. J. Pathol. 149:911-921.
40. Voll, R.E., et al. 1997. Immunosuppressive effects of apoptotic cells. Nature. 390:350-351.
41. Newman, S.L., Henson, J.E., and Henson, P.M. 1982. Phagocytosis of senescent neutrophils by human monocyte-derived macrophages and rabbit inflammatory macrophages. J. Exp. Med. 156:430-442.
42. Byrne, A., and Reen, D.J. 2002. Lipopolysaccharide induces rapid production of IL-10 by monocytes in the presence of apoptotic neutrophils. J. Immunol. 168:1968-1977.
43. Saijo, S., et al. 2005. Inhibition by adiponectin of IL-8 production by human macrophages upon coculturing with late apoptotic cells. Biochem. Biophys. Res. Commun. 334:1180-1183.
44. Peake, P.W., Shen, Y., Campbell, L.V., and Charlesworth, J.A. 2006. Human adiponectin binds to bacterial lipopolysaccharide. Biochem. Biophys. Res. Commun. 341:108-115.
45. Wright, J.R. 2005. Immunoregulatory functions of surfactant proteins. Nat. Rev. Immunol. 5:58-68.
46. Potter, P.K., Cortes-Hernandez, J., Quartier, P., Botto, M., and Walport, M.J. 2003. Lupus-prone mice have an abnormal response to thioglycolate and an impaired clearance of apoptotic cells. J. Immunol. 170:3223-3232.
47. Kollias, G. 2005. TNF pathophysiology in murine models of chronic inflammation and autoimmunity. Semin. Arthritis Rheum. 34:3-6.
48. Taylor, P.R., et al. 2000. A hierarchical role for classical pathway complement proteins in the clearance of apoptotic cells in vivo. J. Exp. Med. 192:359-366.
49. Meyer, T.W., and Rennke, H.G. 1988. Increased single-nephron protein excretion after renal ablation in nephrotic rats. Am. J. Physiol. 255:F1243-F1248.
50. Vereb, G., et al. 2000. Cholesterol-dependent clustering of IL-2Ralpha and its colocalization with HLA and CD48 on T lymphoma cells suggest their functional association with lipid rafts. Proc. Natl. Acad. Sci. U. S. A. 97:6013-6018.