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Mediators of Inflammation
Volume 2016, Article ID 5701959, 9 pages
http://dx.doi.org/10.1155/2016/5701959
Research Article

Adiponectin Inhibits LPS-Induced HMGB1 Release through an AMP Kinase and Heme Oxygenase-1-Dependent Pathway in RAW 264 Macrophage Cells

1Department of Biomedical Sciences, Graduate School of Veterinary Medicine, Hokkaido University, Kita 18, Nishi 9, Kita-ku, Sapporo 060-0818, Japan
2Department of Biochemistry, Faculty of Veterinary Medicine, Alexandria University, Edfina, Behera 22785, Egypt

Received 9 February 2016; Accepted 10 May 2016

Academic Editor: Denis Girard

Copyright © 2016 Mohamed Elfeky et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. G. S. Martin, D. M. Mannino, S. Eaton, and M. Moss, “The epidemiology of sepsis in the United States from 1979 through 2000,” The New England Journal of Medicine, vol. 348, no. 16, pp. 1546–1554, 2003. View at Publisher · View at Google Scholar · View at Scopus
  2. N. C. Riedemann, R.-F. Guo, and P. A. Ward, “The enigma of sepsis,” The Journal of Clinical Investigation, vol. 112, no. 4, pp. 460–467, 2003. View at Publisher · View at Google Scholar · View at Scopus
  3. A. Oberholzer, C. Oberholzer, and L. L. Moldawer, “Sepsis syndromes: understanding the role of innate and acquired immunity,” Shock, vol. 16, no. 2, pp. 83–96, 2001. View at Publisher · View at Google Scholar · View at Scopus
  4. H. Wang, O. Bloom, M. Zhang et al., “HMG-1 as a late mediator of endotoxin lethality in mice,” Science, vol. 285, no. 5425, pp. 248–251, 1999. View at Publisher · View at Google Scholar · View at Scopus
  5. M. Guha and N. Mackman, “LPS induction of gene expression in human monocytes,” Cellular Signalling, vol. 13, no. 2, pp. 85–94, 2001. View at Publisher · View at Google Scholar · View at Scopus
  6. B. Beutler and E. T. Rietschel, “Innate immune sensing and its roots: the story of endotoxin,” Nature Reviews Immunology, vol. 3, no. 2, pp. 169–176, 2003. View at Publisher · View at Google Scholar · View at Scopus
  7. E. Abraham, A. Anzueto, G. Gutierrez et al., “Double-blind randomised controlled trial of monoclonal antibody to human tumour necrosis factor in treatment of septic shock. NORASEPT II Study Group,” The Lancet, vol. 351, no. 9107, pp. 929–933, 1998. View at Publisher · View at Google Scholar · View at Scopus
  8. A. Leelahavanichkul, H. Yasuda, K. Doi et al., “Methyl-2-acetamidoacrylate, an ethyl pyruvate analog, decreases sepsis-induced acute kidney injury in mice,” American Journal of Physiology—Renal Physiology, vol. 295, no. 6, pp. F1825–F1835, 2008. View at Publisher · View at Google Scholar · View at Scopus
  9. U. Andersson, H. Wang, K. Palmblad et al., “High mobility group 1 protein (HMG-1) stimulates proinflammatory cytokine synthesis in human monocytes,” Journal of Experimental Medicine, vol. 192, no. 4, pp. 565–570, 2000. View at Publisher · View at Google Scholar · View at Scopus
  10. J. S. Park, D. Svetkauskaite, Q. He et al., “Involvement of toll-like receptors 2 and 4 in cellular activation by high mobility group box 1 protein,” The Journal of Biological Chemistry, vol. 279, no. 9, pp. 7370–7377, 2004. View at Publisher · View at Google Scholar · View at Scopus
  11. M. T. Lotze and K. J. Tracey, “High-mobility group box 1 protein (HMGB1): nuclear weapon in the immune arsenal,” Nature Reviews Immunology, vol. 5, no. 4, pp. 331–342, 2005. View at Publisher · View at Google Scholar · View at Scopus
  12. A. Rouhiainen, S. Tumova, L. Valmu, N. Kalkkinen, and H. Rauvala, “Pivotal Advance: analysis of proinflammatory activity of highly purified eukaryotic recombinant HMGB1 (amphoterin),” Journal of Leukocyte Biology, vol. 81, no. 1, pp. 49–58, 2007. View at Publisher · View at Google Scholar · View at Scopus
  13. H. Wang, H. Yang, and K. J. Tracey, “Extracellular role of HMGB1 in inflammation and sepsis,” Journal of Internal Medicine, vol. 255, no. 3, pp. 320–331, 2004. View at Publisher · View at Google Scholar · View at Scopus
  14. H. Yang, M. Ochani, J. Li et al., “Reversing established sepsis with antagonists of endogenous high-mobility group box 1,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 1, pp. 296–301, 2004. View at Publisher · View at Google Scholar · View at Scopus
  15. Y. Arita, S. Kihara, N. Ouchi et al., “Paradoxical decrease of an adipose-specific protein, adiponectin, in obesity,” Biochemical and Biophysical Research Communications, vol. 257, no. 1, pp. 79–83, 1999. View at Publisher · View at Google Scholar · View at Scopus
  16. H. Tilg and A. M. Wolf, “Adiponectin: a key fat-derived molecule regulating inflammation,” Expert Opinion on Therapeutic Targets, vol. 9, no. 2, pp. 245–251, 2005. View at Publisher · View at Google Scholar · View at Scopus
  17. N. Ouchi and K. Walsh, “A novel role for adiponectin in the regulation of inflammation,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 28, no. 7, pp. 1219–1221, 2008. View at Publisher · View at Google Scholar · View at Scopus
  18. N. Ouchi, J. L. Parker, J. J. Lugus, and K. Walsh, “Adipokines in inflammation and metabolic disease,” Nature Reviews Immunology, vol. 11, no. 2, pp. 85–97, 2011. View at Publisher · View at Google Scholar · View at Scopus
  19. T. Yokota, K. Oritani, I. Takahashi et al., “Adiponectin, a new member of the family of soluble defense collagens, negatively regulates the growth of myelomonocytic progenitors and the functions of macrophages,” Blood, vol. 96, no. 5, pp. 1723–1732, 2000. View at Google Scholar · View at Scopus
  20. K. Ohashi, J. L. Parker, N. Ouchi et al., “Adiponectin promotes macrophage polarization toward an anti-inflammatory phenotype,” Journal of Biological Chemistry, vol. 285, no. 9, pp. 6153–6160, 2010. View at Publisher · View at Google Scholar · View at Scopus
  21. P. Mandal, B. T. Pratt, M. Barnes, M. R. McMullen, and L. E. Nagy, “Molecular mechanism for adiponectin-dependent m2 macrophage polarization: link between the metabolic and innate immune activity of full-length adiponectin,” The Journal of Biological Chemistry, vol. 286, no. 15, pp. 13460–13469, 2011. View at Publisher · View at Google Scholar · View at Scopus
  22. M. C. Wulster-Radcliffe, K. M. Ajuwon, J. Wang, J. A. Christian, and M. E. Spurlock, “Adiponectin differentially regulates cytokines in porcine macrophages,” Biochemical and Biophysical Research Communications, vol. 316, no. 3, pp. 924–929, 2004. View at Publisher · View at Google Scholar · View at Scopus
  23. A. M. Wolf, D. Wolf, H. Rumpold, B. Enrich, and H. Tilg, “Adiponectin induces the anti-inflammatory cytokines IL-10 and IL-1RA in human leukocytes,” Biochemical and Biophysical Research Communications, vol. 323, no. 2, pp. 630–635, 2004. View at Publisher · View at Google Scholar · View at Scopus
  24. A. Xu, Y. Wang, H. Keshaw, L. Y. Xu, K. S. L. Lam, and G. J. S. Cooper, “The fat-derived hormone adiponectin alleviates alcoholic and nonalcoholic fatty liver diseases in mice,” Journal of Clinical Investigation, vol. 112, no. 1, pp. 91–100, 2003. View at Publisher · View at Google Scholar · View at Scopus
  25. T. Masaki, S. Chiba, H. Tatsukawa et al., “Adiponectin protects LPS-induced liver injury through modulation of TNF-α in KK-Ay obese mice,” Hepatology, vol. 40, no. 1, pp. 177–184, 2004. View at Publisher · View at Google Scholar · View at Scopus
  26. J. M. Konter, J. L. Parker, E. Baez et al., “Adiponectin attenuates lipopolysaccharide-induced acute lung injury through suppression of endothelial cell activation,” Journal of Immunology, vol. 188, no. 2, pp. 854–863, 2012. View at Publisher · View at Google Scholar · View at Scopus
  27. Y. Watanabe, R. Shibata, N. Ouchi et al., “Adiponectin ameliorates endotoxin-induced acute cardiac injury,” BioMed Research International, vol. 2014, Article ID 382035, 6 pages, 2014. View at Publisher · View at Google Scholar · View at Scopus
  28. Y. Uji, H. Yamamoto, H. Tsuchihashi et al., “Adiponectin deficiency is associated with severe polymicrobial sepsis, high inflammatory cytokine levels, and high mortality,” Surgery, vol. 145, no. 5, pp. 550–557, 2009. View at Publisher · View at Google Scholar · View at Scopus
  29. W. Jiang and D. S. Pisetsky, “The role of IFN-alpha; and nitric oxide in the release of HMGB1 by RAW 264.7 cells stimulated with polyinosinic-polycytidylic acid or lipopolysaccharide,” Journal of Immunology, vol. 177, no. 5, pp. 3337–3343, 2006. View at Publisher · View at Google Scholar · View at Scopus
  30. K. Tsoyi, H. J. Jang, I. T. Nizamutdinova et al., “Metformin inhibits HMGB1 release in LPS-treated RAW 264.7 cells and increases survival rate of endotoxaemic mice,” British Journal of Pharmacology, vol. 162, no. 7, pp. 1498–1508, 2011. View at Publisher · View at Google Scholar · View at Scopus
  31. C. K. Zetterström, W. Jiang, H. Wähämaa et al., “Pivotal Advance: inhibition of HMGB1 nuclear translocation as a mechanism for the anti-rheumatic effects of gold sodium thiomalate,” Journal of Leukocyte Biology, vol. 83, no. 1, pp. 31–38, 2008. View at Publisher · View at Google Scholar · View at Scopus
  32. A. Chorny and M. Delgado, “Neuropeptides rescue mice from lethal sepsis by down-regulating secretion of the late-acting inflammatory mediator high mobility group box 1,” American Journal of Pathology, vol. 172, no. 5, pp. 1297–1307, 2008. View at Publisher · View at Google Scholar
  33. T. Kadowaki and T. Yamauchi, “Adiponectin and adiponectin receptors,” Endocrine Reviews, vol. 26, no. 3, pp. 439–451, 2005. View at Publisher · View at Google Scholar · View at Scopus
  34. T. Yamauchi, J. Kamon, Y. Ito et al., “Cloning of adiponectin receptors that mediate antidiabetic metabolic effects,” Nature, vol. 423, pp. 762–769, 2003. View at Publisher · View at Google Scholar
  35. T. Kadowaki, T. Yamauchi, N. Kubota, K. Hara, K. Ueki, and K. Tobe, “Adiponectin and adiponectin receptors in insulin resistance, diabetes, and the metabolic syndrome,” Journal of Clinical Investigation, vol. 116, no. 7, pp. 1784–1792, 2006. View at Publisher · View at Google Scholar · View at Scopus
  36. G. Ashabi, L. Khalaj, F. Khodagholi, M. Goudarzvand, and A. Sarkaki, “Pre-treatment with metformin activates Nrf2 antioxidant pathways and inhibits inflammatory responses through induction of AMPK after transient global cerebral ischemia,” Metabolic Brain Disease, vol. 30, no. 3, pp. 747–754, 2015. View at Publisher · View at Google Scholar · View at Scopus
  37. J. Lee and S. Kim, “Upregulation of heme oxygenase-1 expression by dehydrodiconiferyl alcohol (DHCA) through the AMPK-Nrf2 dependent pathway,” Toxicology and Applied Pharmacology, vol. 281, no. 1, pp. 87–100, 2014. View at Publisher · View at Google Scholar · View at Scopus
  38. K. Tsoyi, T. Y. Lee, Y. S. Lee et al., “Heme-oxygenase-1 induction and carbon monoxide-releasing molecule inhibit lipopolysaccharide (LPS)-induced high-mobility group box 1 release in vitro and improve survival of mice in LPS- and cecal ligation and puncture-induced sepsis model in vivo,” Molecular Pharmacology, vol. 76, no. 1, pp. 173–182, 2009. View at Publisher · View at Google Scholar · View at Scopus
  39. H.-G. Chen, K.-L. Xie, H.-Z. Han et al., “Heme oxygenase-1 mediates the anti-inflammatory effect of molecular hydrogen in LPS-stimulated RAW 264.7 macrophages,” International Journal of Surgery, vol. 11, no. 10, pp. 1060–1066, 2013. View at Publisher · View at Google Scholar · View at Scopus
  40. C. N. Lumeng, “Innate immune activation in obesity,” Molecular Aspects of Medicine, vol. 34, no. 1, pp. 12–29, 2013. View at Publisher · View at Google Scholar · View at Scopus
  41. D. M. Rocha, A. P. Caldas, L. L. Oliveira, J. Bressan, and H. H. Hermsdorff, “Saturated fatty acids trigger TLR4-mediated inflammatory response,” Atherosclerosis, vol. 244, pp. 211–215, 2016. View at Publisher · View at Google Scholar
  42. P. Mandal, S. Roychowdhury, P.-H. Park, B. T. Pratt, T. Roger, and L. E. Nagy, “Adiponectin and heme oxygenase-1 suppress TLR4/MyD88-independent signaling in rat Kupffer cells and in mice after chronic ethanol exposure,” The Journal of Immunology, vol. 185, no. 8, pp. 4928–4937, 2010. View at Publisher · View at Google Scholar · View at Scopus
  43. M. J. Yoon, G. Y. Lee, J.-J. Chung et al., “Adiponectin increases fatty acid oxidation in skeletal muscle cells by sequential activation of AMP-activated protein kinase, p38 mitogen-activated protein kinase, and peroxisome proliferator-activated receptor α,” Diabetes, vol. 55, no. 9, pp. 2562–2570, 2006. View at Publisher · View at Google Scholar
  44. E. J. Folco, V. Z. Rocha, M. López-Ilasaca, and P. Libby, “Adiponectin inhibits pro-inflammatory signaling in human macrophages independent of interleukin-10,” The Journal of Biological Chemistry, vol. 284, no. 38, pp. 25569–25575, 2009. View at Publisher · View at Google Scholar · View at Scopus
  45. M. E. Grossmann, K. J. Nkhata, N. K. Mizuno, A. Ray, and M. P. Cleary, “Effects of adiponectin on breast cancer cell growth and signaling,” British Journal of Cancer, vol. 98, no. 2, pp. 370–379, 2008. View at Publisher · View at Google Scholar · View at Scopus
  46. N. T. Pun, A. Subedi, M. J. Kim, and P.-H. Park, “Globular adiponectin causes tolerance to LPS-induced TNF-α expression via autophagy induction in RAW 264.7 macrophages: involvement of SIRT1/FoxO3A axis,” PLoS ONE, vol. 10, no. 5, Article ID e0124636, 2015. View at Publisher · View at Google Scholar · View at Scopus
  47. Y. M. Kim, H. J. Kim, and K. C. Chang, “Glycyrrhizin reduces HMGB1 secretion in lipopolysaccharide-activated RAW 264.7 cells and endotoxemic mice by p38/Nrf2-dependent induction of HO-1,” International Immunopharmacology, vol. 26, no. 1, pp. 112–118, 2015. View at Publisher · View at Google Scholar · View at Scopus
  48. J. Wang, X. Hu, J. Xie, W. Xu, and H. Jiang, “Beta-1-adrenergic receptors mediate Nrf2-HO-1-HMGB1 axis regulation to attenuate hypoxia/reoxygenation-induced cardiomyocytes injury in vitro,” Cellular Physiology and Biochemistry, vol. 35, no. 2, pp. 767–777, 2015. View at Publisher · View at Google Scholar
  49. T. D. Walko III, V. Di Caro, J. Piganelli, T. R. Billiar, R. S. Clark, and R. K. Aneja, “Poly(ADP-ribose) polymerase 1-sirtuin 1 functional interplay regulates LPS-mediated high mobility group box 1 secretion,” Molecular Medicine, vol. 20, pp. 612–624, 2014. View at Publisher · View at Google Scholar
  50. M. Kumada, S. Kihara, N. Ouchi et al., “Adiponectin specifically increased tissue inhibitor of metalloproteinase-1 through interleukin-10 expression in human macrophages,” Circulation, vol. 109, no. 17, pp. 2046–2049, 2004. View at Publisher · View at Google Scholar · View at Scopus
  51. P.-H. Park, M. R. McMullen, H. Huang, V. Thakur, and L. E. Nagy, “Short-term treatment of RAW264.7 macrophages with adiponectin increases tumor necrosis factor-α (TNF-α) expression via ERK1/2 activation and Egr-1 expression: role of TNF-α in adiponectin-stimulated interleukin-10 production,” The Journal of Biological Chemistry, vol. 282, no. 30, pp. 21695–21703, 2007. View at Publisher · View at Google Scholar · View at Scopus
  52. P. Mandal, P.-H. Park, M. R. McMullen, B. T. Pratt, and L. E. Nagy, “The anti-inflammatory effects of adiponectin are mediated via a heme oxygenase-1-dependent pathway in rat kupffer cells,” Hepatology, vol. 51, no. 4, pp. 1420–1429, 2010. View at Publisher · View at Google Scholar · View at Scopus
  53. J. F. Ndisang, “Role of the heme oxygenase-adiponectin-atrial natriuretic peptide axis in renal function,” Current Pharmaceutical Design, vol. 21, no. 30, pp. 4380–4391, 2015. View at Publisher · View at Google Scholar · View at Scopus
  54. A. Paine, B. Eiz-Vesper, R. Blasczyk, and S. Immenschuh, “Signaling to heme oxygenase-1 and its anti-inflammatory therapeutic potential,” Biochemical Pharmacology, vol. 80, no. 12, pp. 1895–1903, 2010. View at Publisher · View at Google Scholar · View at Scopus