Table of Contents Author Guidelines Submit a Manuscript
Journal of Diabetes Research
Volume 2016, Article ID 2543268, 11 pages
http://dx.doi.org/10.1155/2016/2543268
Review Article

The Role of HMGB1 in the Pathogenesis of Type 2 Diabetes

1Department of Immunology, Medical School, Yangtze University, Jingzhou 434023, China
2Department of Medicine, University of Maryland School of Medicine, Baltimore, MD 21201, USA
3Department of Medicine, Hospital of Yangtze University, Jingzhou 434000, China

Received 15 July 2016; Revised 8 November 2016; Accepted 29 November 2016

Academic Editor: Konstantinos Kantartzis

Copyright © 2016 Yanan Wang 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. IDF, IDF Diabetes Atlas, International Diabetes Federation, 6th edition, 2013.
  2. A. E. Butler, J. Janson, S. Bonner-Weir, R. Ritzel, R. A. Rizza, and P. C. Butler, “β-cell deficit and increased β-cell apoptosis in humans with type 2 diabetes,” Diabetes, vol. 52, no. 1, pp. 102–110, 2003. View at Publisher · View at Google Scholar · View at Scopus
  3. F. M. Ashcroft and P. Rorsman, “Diabetes mellitus and the β cell: the last ten years,” Cell, vol. 148, no. 6, pp. 1160–1171, 2012. View at Publisher · View at Google Scholar · View at Scopus
  4. J. McNelis and J. Olefsky, “Macrophages, immunity, and metabolic disease,” Immunity, vol. 41, no. 1, pp. 36–48, 2014. View at Publisher · View at Google Scholar · View at Scopus
  5. J. R. Klune, R. Dhupar, J. Cardinal, T. R. Billiar, and A. Tsung, “HMGB1: endogenous danger signaling,” Molecular Medicine, vol. 14, no. 7-8, pp. 476–484, 2008. View at Publisher · View at Google Scholar · View at Scopus
  6. L. L. Mantell, W. R. Parrish, and L. Ulloa, “HMGB-1 as a therapeutic target for infectious and inflammatory disorders,” Shock, vol. 25, no. 1, pp. 4–11, 2006. View at Publisher · View at Google Scholar · View at Scopus
  7. B.-C. Lee and J. Lee, “Cellular and molecular players in adipose tissue inflammation in the development of obesity-induced insulin resistance,” Biochimica et Biophysica Acta, vol. 1842, no. 3, pp. 446–462, 2014. View at Publisher · View at Google Scholar · View at Scopus
  8. M. Massaro, E. Scoditti, M. Pellegrino et al., “Therapeutic potential of the dual peroxisome proliferator activated receptor (PPAR)α/γ agonist aleglitazar in attenuating TNF-α-mediated inflammation and insulin resistance in human adipocytes,” Pharmacological Research, vol. 107, pp. 125–136, 2016. View at Publisher · View at Google Scholar
  9. P. Dandona, H. Ghanim, A. Bandyopadhyay et al., “Insulin suppresses endotoxin-induced oxidative, nitrosative, and inflammatory stress in humans,” Diabetes Care, vol. 33, no. 11, pp. 2416–2423, 2010. View at Publisher · View at Google Scholar · View at Scopus
  10. J. M. Stephens and P. H. Pekala, “Transcriptional repression of the C/EBP-α and GLUT4 genes in 3T3-L1 adipocytes by tumor necrosis factor-α: regulation is coordinate and independent of protein synthesis,” Journal of Biological Chemistry, vol. 267, no. 19, pp. 13580–13584, 1992. View at Google Scholar · View at Scopus
  11. J. M. Stephens, J. Lee, and P. F. Pilch, “Tumor necrosis factor-α-induced insulin resistance in 3T3-L1 adipocytes is accompanied by a loss of insulin receptor substrate-1 and GLUT4 expression without a loss of insulin receptor-mediated signal transduction,” Journal of Biological Chemistry, vol. 272, no. 2, pp. 971–976, 1997. View at Publisher · View at Google Scholar · View at Scopus
  12. G. S. Hotamisligil, N. S. Shargill, and B. M. Spiegelman, “Adipose expression of tumor necrosis factor-α: direct role in obesity-linked insulin resistance,” Science, vol. 259, no. 5091, pp. 87–91, 1993. View at Publisher · View at Google Scholar · View at Scopus
  13. M. Li, L. Song, X. Gao, W. Chang, and X. Qin, “Toll-like receptor 4 on islet β cells senses expression changes in high-mobility group box 1 and contributes to the initiation of type 1 diabetes,” Experimental & Molecular Medicine, vol. 44, no. 4, pp. 260–267, 2012. View at Publisher · View at Google Scholar · View at Scopus
  14. D. Tang, R. Kang, H. J. Zeh III, and M. T. Lotze, “High-mobility group box 1 and cancer,” Biochimica et Biophysica Acta, vol. 1799, no. 1-2, pp. 131–140, 2010. View at Publisher · View at Google Scholar · View at Scopus
  15. G. H. Goodwin and E. W. Johns, “Isolation and characterisation of two calf thymus chromatin non histone proteins with high contents of acidic and basic amino acids,” European Journal of Biochemistry, vol. 40, no. 1, pp. 215–219, 1973. View at Publisher · View at Google Scholar · View at Scopus
  16. Y. Liu, R. Prasad, and S. H. Wilson, “HMGB1: roles in base excision repair and related function,” Biochimica et Biophysica Acta, vol. 1799, no. 1-2, pp. 119–130, 2010. View at Publisher · View at Google Scholar · View at Scopus
  17. J. O. Thomas and K. Stott, “H1 and HMGB1: modulators of chromatin structure,” Biochemical Society Transactions, vol. 40, no. 2, pp. 341–346, 2012. View at Publisher · View at Google Scholar · View at Scopus
  18. R. Kang, R. Chen, Q. Zhang et al., “HMGB1 in health and disease,” Molecular Aspects of Medicine, vol. 40, pp. 1–116, 2014. View at Publisher · View at Google Scholar
  19. J. Li, R. Kokkola, S. Tabibzadeh et al., “Structural basis for the proinflammatory cytokine activity of high mobility group box 1,” Molecular Medicine, vol. 9, no. 1-2, pp. 37–45, 2003. View at Google Scholar · View at Scopus
  20. D. Messmer, H. Yang, G. Telusma et al., “High mobility group box protein 1: an endogenous signal for dendritic cell maturation and Th1 polarization,” Journal of Immunology, vol. 173, no. 1, pp. 307–313, 2004. View at Publisher · View at Google Scholar · View at Scopus
  21. 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
  22. Q. Gong, J.-F. Xu, H. Yin, S.-F. Liu, L.-H. Duan, and Z.-L. Bian, “Protective effect of antagonist of high-mobility group box 1 on lipopolysaccharide-induced acute lung injury in mice,” Scandinavian Journal of Immunology, vol. 69, no. 1, pp. 29–35, 2009. View at Publisher · View at Google Scholar · View at Scopus
  23. H. Yang, D. J. Antoine, U. Andersson, and K. J. Tracey, “The many faces of HMGB1: molecular structure-functional activity in inflammation, apoptosis, and chemotaxis,” Journal of Leukocyte Biology, vol. 93, no. 6, pp. 865–873, 2013. View at Publisher · View at Google Scholar · View at Scopus
  24. Y. Tang, X. Zhao, D. Antoine et al., “Regulation of posttranslational modifications of HMGB1 during immune responses,” Antioxidants & Redox Signaling, vol. 24, no. 12, pp. 620–634, 2016. View at Publisher · View at Google Scholar
  25. I. Ito, J. Fukazawa, and M. Yoshida, “Post-translational methylation of high mobility group box 1 (HMGB1) causes its cytoplasmic localization in neutrophils,” Journal of Biological Chemistry, vol. 282, no. 22, pp. 16336–16344, 2007. View at Publisher · View at Google Scholar · View at Scopus
  26. 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
  27. M. Štros, “HMGB proteins: interactions with DNA and chromatin,” Biochimica et Biophysica Acta, vol. 1799, no. 1-2, pp. 101–113, 2010. View at Publisher · View at Google Scholar · View at Scopus
  28. H. J. Min, E. A. Ko, J. Wu et al., “Chaperone-like activity of high-mobility group box 1 protein and its role in reducing the formation of polyglutamine aggregates,” Journal of Immunology, vol. 190, no. 4, pp. 1797–1806, 2013. View at Publisher · View at Google Scholar · View at Scopus
  29. M. E. Bianchi, M. Beltrame, and G. Paonessa, “Specific recognition of cruciform DNA by nuclear protein HMGl,” Science, vol. 243, no. 4894, pp. 1056–1059, 1989. View at Publisher · View at Google Scholar · View at Scopus
  30. K. Giese, J. Cox, and R. Grosschedl, “The HMG domain of lymphoid enhancer factor 1 bends DNA and facilitates assembly of functional nucleoprotein structures,” Cell, vol. 69, no. 1, pp. 185–195, 1992. View at Publisher · View at Google Scholar · View at Scopus
  31. K. Javaherian, L. F. Liu, and J. C. Wang, “Nonhistone proteins HMG1 and HMG2 change the DNA helical structure,” Science, vol. 199, no. 4335, pp. 1345–1346, 1978. View at Publisher · View at Google Scholar · View at Scopus
  32. 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
  33. C. W. Bell, W. Jiang, C. F. Reich III, and D. S. Pisetsky, “The extracellular release of HMGB1 during apoptotic cell death,” American Journal of Physiology—Cell Physiology, vol. 291, no. 6, pp. C1318–C1325, 2006. View at Publisher · View at Google Scholar · View at Scopus
  34. 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
  35. P. Rovere-Querini, A. Capobianco, P. Scaffidi et al., “HMGB1 is an endogenous immune adjuvant released by necrotic cells,” EMBO Reports, vol. 5, no. 8, pp. 825–830, 2004. View at Publisher · View at Google Scholar · View at Scopus
  36. J. Fucikova, I. Moserova, I. Truxova et al., “High hydrostatic pressure induces immunogenic cell death in human tumor cells,” International Journal of Cancer, vol. 135, no. 5, pp. 1165–1177, 2014. View at Publisher · View at Google Scholar · View at Scopus
  37. A. Tsung, R. Sahai, H. Tanaka et al., “The nuclear factor HMGB1 mediates hepatic injury after murine liver ischemia-reperfusion,” Journal of Experimental Medicine, vol. 201, no. 7, pp. 1135–1143, 2005. View at Publisher · View at Google Scholar · View at Scopus
  38. U. Andersson and K. J. Tracey, “HMGB1 is a therapeutic target for sterile inflammation and infection,” Annual Review of Immunology, vol. 29, pp. 139–162, 2011. View at Publisher · View at Google Scholar · View at Scopus
  39. Q. Gong, H. Zhang, J.-H. Li et al., “High-mobility group box 1 exacerbates concanavalin A-induced hepatic injury in mice,” Journal of Molecular Medicine, vol. 88, no. 12, pp. 1289–1298, 2010. View at Publisher · View at Google Scholar · View at Scopus
  40. U. Andersson and H. Erlandsson-Harris, “HMGB1 is a potent trigger of arthritis,” Journal of Internal Medicine, vol. 255, no. 3, pp. 344–350, 2004. View at Publisher · View at Google Scholar · View at Scopus
  41. N. Taniguchi, K.-I. Kawahara, K. Yone et al., “High mobility group box chromosomal protein 1 plays a role in the pathogenesis of rheumatoid arthritis as a novel cytokine,” Arthritis and Rheumatism, vol. 48, no. 4, pp. 971–981, 2003. View at Publisher · View at Google Scholar · View at Scopus
  42. J. A. Nogueira-Machado, C. M. D. O. Volpe, C. A. Veloso, and M. M. Chaves, “HMGB1, TLR and RAGE: a functional tripod that leads to diabetic inflammation,” Expert Opinion on Therapeutic Targets, vol. 15, no. 8, pp. 1023–1035, 2011. View at Publisher · View at Google Scholar · View at Scopus
  43. J. R. Van Beijnum, W. A. Buurman, and A. W. Griffioen, “Convergence and amplification of toll-like receptor (TLR) and receptor for advanced glycation end products (RAGE) signaling pathways via high mobility group B1 (HMGB1),” Angiogenesis, vol. 11, no. 1, pp. 91–99, 2008. View at Publisher · View at Google Scholar · View at Scopus
  44. V. V. Orlova, E. Y. Choi, C. Xie et al., “A novel pathway of HMGB1-mediated inflammatory cell recruitment that requires Mac-1-integrin,” The EMBO Journal, vol. 26, no. 4, pp. 1129–1139, 2007. View at Publisher · View at Google Scholar · View at Scopus
  45. M. Schiraldi, A. Raucci, L. M. Muñoz et al., “HMGB1 promotes recruitment of inflammatory cells to damaged tissues by forming a complex with CXCL12 and signaling via CXCR4,” Journal of Experimental Medicine, vol. 209, no. 3, pp. 551–563, 2012. View at Publisher · View at Google Scholar · View at Scopus
  46. R. R. Kew, M. Penzo, D. M. Habiel, and K. B. Marcu, “The IKKα-dependent NF-κB p52/RelB noncanonical pathway is essential to sustain a CXCL12 autocrine loop in cells migrating in response to HMGB1,” Journal of Immunology, vol. 188, no. 5, pp. 2380–2386, 2012. View at Publisher · View at Google Scholar · View at Scopus
  47. J. Wu, J. Li, R. Salcedo, N. F. Mivechi, G. Trinchieri, and A. Horuzsko, “The proinflammatory myeloid cell receptor TREM-1 controls Kupffer cell activation and development of hepatocellular carcinoma,” Cancer Research, vol. 72, no. 16, pp. 3977–3986, 2012. View at Publisher · View at Google Scholar · View at Scopus
  48. S. D. Yan, X. Chen, J. Fu et al., “RAGE and amyloid-β peptide neurotoxicity in Alzheimer's disease,” Nature, vol. 382, no. 6593, pp. 685–691, 1996. View at Publisher · View at Google Scholar · View at Scopus
  49. H. J. Huttunen and H. Rauvala, “Amphoterin as an extracellular regulator of cell motility: from discovery to disease,” Journal of Internal Medicine, vol. 255, no. 3, pp. 351–366, 2004. View at Publisher · View at Google Scholar · View at Scopus
  50. M. A. Hofmann, S. Drury, C. Fu et al., “RAGE mediates a novel proinflammatory axis: a central cell surface receptor for S100/calgranulin polypeptides,” Cell, vol. 97, no. 7, pp. 889–901, 1999. View at Publisher · View at Google Scholar · View at Scopus
  51. O. Hori, J. Brett, T. Slattery et al., “The receptor for advanced glycation end products (RAGE) is a cellular binding site for amphoterin: mediation of neurite outgrowth and co-expression of rage and amphoterin in the developing nervous system,” Journal of Biological Chemistry, vol. 270, no. 43, pp. 25752–25761, 1995. View at Publisher · View at Google Scholar · View at Scopus
  52. A. Taguchi, D. C. Blood, G. Del Toro et al., “Blockade of RAGE-amphoterin signalling suppresses tumour growth and metastases,” Nature, vol. 405, no. 6784, pp. 354–360, 2000. View at Publisher · View at Google Scholar · View at Scopus
  53. H. Yang, H. Wang, C. J. Czura, and K. J. Tracey, “The cytokine activity of HMGB1,” Journal of Leukocyte Biology, vol. 78, no. 1, pp. 1–8, 2005. View at Publisher · View at Google Scholar · View at Scopus
  54. J. Heijmans, N. V. J. A. Büller, E. Hoff et al., “Rage signalling promotes intestinal tumourigenesis,” Oncogene, vol. 32, no. 9, pp. 1202–1206, 2013. View at Publisher · View at Google Scholar · View at Scopus
  55. R. Kang, D. Tang, N. E. Schapiro et al., “The receptor for advanced glycation end products (RAGE) sustains autophagy and limits apoptosis, promoting pancreatic tumor cell survival,” Cell Death and Differentiation, vol. 17, no. 4, pp. 666–676, 2010. View at Publisher · View at Google Scholar · View at Scopus
  56. D. Tang, R. Kang, K. M. Livesey, H. J. Zeh, and M. T. Lotze, “High mobility group box 1 (HMGB1) activates an autophagic response to oxidative stress,” Antioxidants and Redox Signaling, vol. 15, no. 8, pp. 2185–2195, 2011. View at Publisher · View at Google Scholar · View at Scopus
  57. H. J. Huttunen, C. Fages, and H. Rauvala, “Receptor for advanced glycation end products (RAGE)-mediated neurite outgrowth and activation of NF-κB require the cytoplasmic domain of the receptor but different downstream signaling pathways,” The Journal of Biological Chemistry, vol. 274, no. 28, pp. 19919–19924, 1999. View at Publisher · View at Google Scholar · View at Scopus
  58. R. Palumbo, B. G. Galvez, T. Pusterla et al., “Cells migrating to sites of tissue damage in response to the danger signal HMGB1 require NF-κB activation,” The Journal of Cell Biology, vol. 179, no. 1, pp. 33–40, 2007. View at Publisher · View at Google Scholar · View at Scopus
  59. C. J. Treutiger, G. E. Mullins, A.-S. M. Johansson et al., “High mobility group 1 B-box mediates activation of human endothelium,” Journal of Internal Medicine, vol. 254, no. 4, pp. 375–385, 2003. View at Publisher · View at Google Scholar · View at Scopus
  60. I. E. Dumitriu, P. Baruah, M. E. Bianchi, A. A. Manfredi, and P. Rovere-Querini, “Requirement of HMGB1 and RAGE for the maturation of human plasmacytoid dendritic cells,” European Journal of Immunology, vol. 35, no. 7, pp. 2184–2190, 2005. View at Publisher · View at Google Scholar · View at Scopus
  61. D. Yang, Q. Chen, H. Yang, K. J. Tracey, M. Bustin, and J. J. Oppenheim, “High mobility group box-1 protein induces the migration and activation of human dendritic cells and acts as an alarmin,” Journal of Leukocyte Biology, vol. 81, no. 1, pp. 59–66, 2007. View at Publisher · View at Google Scholar · View at Scopus
  62. V. Urbonaviciute, B. G. Fürnrohr, S. Meister et al., “Induction of inflammatory and immune responses by HMGB1-nucleosome complexes: implications for the pathogenesis of SLE,” Journal of Experimental Medicine, vol. 205, no. 13, pp. 3007–3018, 2008. View at Publisher · View at Google Scholar · View at Scopus
  63. J. S. Park, J. Arcaroli, H.-K. Yum et al., “Activation of gene expression in human neutrophils by high mobility group box 1 protein,” American Journal of Physiology—Cell Physiology, vol. 284, no. 4, pp. C870–C879, 2003. View at Publisher · View at Google Scholar · View at Scopus
  64. K. Li, J. Yang, and X. Han, “Ketamine attenuates sepsis-induced acute lung injury via regulation of HMGB1-RAGE pathways,” International Immunopharmacology, vol. 34, pp. 114–128, 2016. View at Publisher · View at Google Scholar
  65. L. Zhu, Z. Zhang, L. Zhang et al., “HMGB1-RAGE signaling pathway in severe preeclampsia,” Placenta, vol. 36, no. 10, pp. 1148–1152, 2015. View at Publisher · View at Google Scholar · View at Scopus
  66. M. B. Manigrasso, J. Juranek, R. Ramasamy, and A. M. Schmidt, “Unlocking the biology of RAGE in diabetic microvascular complications,” Trends in Endocrinology and Metabolism, vol. 25, no. 1, pp. 15–22, 2014. View at Publisher · View at Google Scholar · View at Scopus
  67. G. P. Sims, D. C. Rowe, S. T. Rietdijk, R. Herbst, and A. J. Coyle, “HMGB1 and RAGE in inflammation and cancer,” Annual Review of Immunology, vol. 28, pp. 367–388, 2010. View at Publisher · View at Google Scholar · View at Scopus
  68. J. Zhang, J.-S. Zhu, Z. Zhou, W.-X. Chen, and N.-W. Chen, “Inhibitory effects of ethyl pyruvate administration on human gastric cancer growth via regulation of the HMGB1-RAGE and Akt pathways in vitro and in vivo,” Oncology Reports, vol. 27, no. 5, pp. 1511–1519, 2012. View at Publisher · View at Google Scholar · View at Scopus
  69. M. A. Ullah, Z. Loh, W. J. Gan et al., “Receptor for advanced glycation end products and its ligand high-mobility group box-1 mediate allergic airway sensitization and airway inflammation,” Journal of Allergy and Clinical Immunology, vol. 134, no. 2, pp. 440–450.e3, 2014. View at Publisher · View at Google Scholar · View at Scopus
  70. S. Akira, M. Yamamoto, and K. Takeda, “Role of adapters in Toll-like receptor signalling,” Biochemical Society Transactions, vol. 31, no. 3, pp. 637–642, 2003. View at Publisher · View at Google Scholar · View at Scopus
  71. S. Akira and K. Takeda, “Toll-like receptor signalling,” Nature Reviews Immunology, vol. 4, no. 7, pp. 499–511, 2004. View at Publisher · View at Google Scholar · View at Scopus
  72. M. Yu, H. Wang, A. Ding et al., “HMGB1 signals through toll-like receptor (TLR) 4 and TLR2,” Shock, vol. 26, no. 2, pp. 174–179, 2006. View at Publisher · View at Google Scholar · View at Scopus
  73. S. Ivanov, A.-M. Dragoi, X. Wang et al., “A novel role for HMGB1 in TLR9-mediated inflammatory responses to CpG-DNA,” Blood, vol. 110, no. 6, pp. 1970–1981, 2007. View at Publisher · View at Google Scholar · View at Scopus
  74. 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
  75. H. Yang, H. S. Hreggvidsdottir, K. Palmblad et al., “A critical cysteine is required for HMGB1 binding to toll-like receptor 4 and activation of macrophage cytokine release,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 26, pp. 11942–11947, 2010. View at Publisher · View at Google Scholar · View at Scopus
  76. H. Yang, P. Lundbäck, L. Ottosson et al., “Redox modification of cysteine residues regulates the cytokine activity of high mobility group box-1 (HMGB1),” Molecular Medicine, vol. 18, no. 2, pp. 250–259, 2012. View at Publisher · View at Google Scholar · View at Scopus
  77. J. H. Youn, M. S. Kwak, J. Wu et al., “Identification of lipopolysaccharide-binding peptide regions within HMGB1 and their effects on subclinical endotoxemia in a mouse model,” European Journal of Immunology, vol. 41, no. 9, pp. 2753–2762, 2011. View at Publisher · View at Google Scholar · View at Scopus
  78. J. H. Youn, Y. J. Oh, E. S. Kim, J. E. Choi, and J.-S. Shin, “High mobility group box 1 protein binding to lipopolysaccharide facilitates transfer of lipopolysaccharide to CD14 and enhances lipopolysaccharide-mediated TNF-α production in human monocytes,” The Journal of Immunology, vol. 180, no. 7, pp. 5067–5074, 2008. View at Publisher · View at Google Scholar · View at Scopus
  79. S. Kim, S. Young Kim, J. P. Pribis et al., “Signaling of high mobility group box 1 (HMGB1) through toll-like receptor 4 in macrophages requires CD14,” Molecular Medicine, vol. 19, no. 1, pp. 88–98, 2013. View at Publisher · View at Google Scholar · View at Scopus
  80. H. Yang, H. Wang, Z. Ju et al., “MD-2 is required for disulfide HMGB1-dependent TLR4 signaling,” Journal of Experimental Medicine, vol. 212, no. 1, pp. 5–14, 2015. View at Publisher · View at Google Scholar · View at Scopus
  81. E. Latz, A. Schoenemeyer, A. Visintin et al., “TLR9 signals after translocating from the ER to CpG DNA in the lysosome,” Nature Immunology, vol. 5, no. 2, pp. 190–198, 2004. View at Publisher · View at Google Scholar · View at Scopus
  82. K. Takeda and S. Akira, “Toll-like receptors in innate immunity,” International Immunology, vol. 17, no. 1, pp. 1–14, 2005. View at Publisher · View at Google Scholar · View at Scopus
  83. J. Tian, A. M. Avalos, S.-Y. Mao et al., “Toll-like receptor 9-dependent activation by DNA-containing immune complexes is mediated by HMGB1 and RAGE,” Nature Immunology, vol. 8, no. 5, pp. 487–496, 2007. View at Publisher · View at Google Scholar · View at Scopus
  84. S. I. Pachydaki, S. R. Tari, S. E. Lee et al., “Upregulation of RAGE and its ligands in proliferative retinal disease,” Experimental Eye Research, vol. 82, no. 5, pp. 807–815, 2006. View at Publisher · View at Google Scholar · View at Scopus
  85. Y. Yu, L. Yang, J. Lv et al., “The role of high mobility group box 1 (HMGB-1) in the diabetic retinopathy inflammation and apoptosis,” International Journal of Clinical and Experimental Pathology, vol. 8, no. 6, pp. 6807–6813, 2015. View at Google Scholar · View at Scopus
  86. M. R. Dasu, S. Devaraj, S. Park, and I. Jialal, “Increased Toll-Like Receptor (TLR) activation and TLR ligands in recently diagnosed type 2 diabetic subjects,” Diabetes Care, vol. 33, no. 4, pp. 861–868, 2010. View at Publisher · View at Google Scholar · View at Scopus
  87. J. Škrha, M. Kalousová, J. Švarcová et al., “Relationship of soluble RAGE and RAGE ligands HMGB1 and EN-RAGE to endothelial dysfunction in type 1 and type 2 diabetes mellitus,” Experimental and Clinical Endocrinology and Diabetes, vol. 120, no. 5, pp. 277–281, 2012. View at Publisher · View at Google Scholar · View at Scopus
  88. S. Hagiwara, H. Iwasaka, A. Hasegawa, H. Koga, and T. Noguchi, “Effects of hyperglycemia and insulin therapy on high mobility group box 1 in endotoxin-induced acute lung injury in a rat model,” Critical Care Medicine, vol. 36, no. 8, pp. 2407–2413, 2008. View at Publisher · View at Google Scholar · View at Scopus
  89. 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
  90. T. Zhang, X. Hu, Y. Cai, B. Yi, and Z. Wen, “Metformin protects against hyperglycemia-induced cardiomyocytes injury by inhibiting the expressions of receptor for advanced glycation end products and high mobility group box 1 protein,” Molecular Biology Reports, vol. 41, no. 3, pp. 1335–1340, 2014. View at Publisher · View at Google Scholar · View at Scopus
  91. K. J. Strissel, Z. Stancheva, H. Miyoshi et al., “Adipocyte death, adipose tissue remodeling, and obesity complications,” Diabetes, vol. 56, no. 12, pp. 2910–2918, 2007. View at Publisher · View at Google Scholar · View at Scopus
  92. M. A. McArdle, O. M. Finucane, R. M. Connaughton, A. M. McMorrow, and H. M. Roche, “Mechanisms of obesity-induced inflammation and insulin resistance: insights into the emerging role of nutritional strategies,” Frontiers in Endocrinology, vol. 4, article 52, 2013. View at Publisher · View at Google Scholar · View at Scopus
  93. S. Galic, J. S. Oakhill, and G. R. Steinberg, “Adipose tissue as an endocrine organ,” Molecular and Cellular Endocrinology, vol. 316, no. 2, pp. 129–139, 2010. View at Publisher · View at Google Scholar · View at Scopus
  94. P. Bhargava and C.-H. Lee, “Role and function of macrophages in the metabolic syndrome,” Biochemical Journal, vol. 442, no. 2, pp. 253–262, 2012. View at Publisher · View at Google Scholar · View at Scopus
  95. C. N. Lumeng, J. B. Delproposto, D. J. Westcott, and A. R. Saltiel, “Phenotypic switching of adipose tissue macrophages with obesity is generated by spatiotemporal differences in macrophage subtypes,” Diabetes, vol. 57, no. 12, pp. 3239–3246, 2008. View at Publisher · View at Google Scholar · View at Scopus
  96. X. Prieur, C. Y. L. Mok, V. R. Velagapudi et al., “Differential lipid partitioning between adipocytes and tissue macrophages modulates macrophage lipotoxicity and M2/M1 polarization in obese mice,” Diabetes, vol. 60, no. 3, pp. 797–809, 2011. View at Publisher · View at Google Scholar · View at Scopus
  97. C. N. Lumeng, S. M. DeYoung, J. L. Bodzin, and A. R. Saltiel, “Increased inflammatory properties of adipose tissue macrophages recruited during diet-induced obesity,” Diabetes, vol. 56, no. 1, pp. 16–23, 2007. View at Publisher · View at Google Scholar · View at Scopus
  98. J. M. Olefsky and C. K. Glass, “Macrophages, inflammation, and insulin resistance,” Annual Review of Physiology, vol. 72, pp. 219–246, 2010. View at Publisher · View at Google Scholar · View at Scopus
  99. E. Maury, L. Noël, R. Detry, and S. M. Brichard, “In Vitro hyperresponsiveness to tumor necrosis factor-α contributes to adipokine dysregulation in omental adipocytes of obese subjects,” Journal of Clinical Endocrinology and Metabolism, vol. 94, no. 4, pp. 1393–1400, 2009. View at Publisher · View at Google Scholar · View at Scopus
  100. B. Vandanmagsar, Y.-H. Youm, A. Ravussin et al., “The NLRP3 inflammasome instigates obesity-induced inflammation and insulin resistance,” Nature Medicine, vol. 17, no. 2, pp. 179–188, 2011. View at Publisher · View at Google Scholar · View at Scopus
  101. R. K. Murumalla, M. K. Gunasekaran, J. K. Padhan et al., “Fatty acids do not pay the toll: effect of SFA and PUFA on human adipose tissue and mature adipocytes inflammation,” Lipids in Health and Disease, vol. 11, article 175, 2012. View at Publisher · View at Google Scholar · View at Scopus
  102. T. Arrigo, V. Chirico, V. Salpietro et al., “High-mobility group protein B1: a new biomarker of metabolic syndrome in obese children,” European Journal of Endocrinology, vol. 168, no. 4, pp. 631–638, 2013. View at Publisher · View at Google Scholar · View at Scopus
  103. V. N. Montes, S. Subramanian, L. Goodspeed et al., “Anti-HMGB1 antibody reduces weight gain in mice fed a high-fat diet,” Nutrition and Diabetes, vol. 5, article no. e161, 2015. View at Publisher · View at Google Scholar · View at Scopus
  104. P. Kanellakis, A. Agrotis, T. S. Kyaw et al., “High-mobility group box protein 1 neutralization reduces development of diet-induced atherosclerosis in apolipoprotein E-deficient mice,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 31, no. 2, pp. 313–319, 2011. View at Publisher · View at Google Scholar · View at Scopus
  105. F. Song, C. H. Del Pozo, R. Rosario et al., “RAGE regulates the metabolic and inflammatory response to high-fat feeding in mice,” Diabetes, vol. 63, no. 6, pp. 1948–1965, 2014. View at Publisher · View at Google Scholar · View at Scopus
  106. S. E. Kahn, R. L. Hull, and K. M. Utzschneider, “Mechanisms linking obesity to insulin resistance and type 2 diabetes,” Nature, vol. 444, no. 7121, pp. 840–846, 2006. View at Publisher · View at Google Scholar · View at Scopus
  107. S. B. Biddinger and C. R. Kahn, “From mice to men: insights into the insulin resistance syndromes,” Annual Review of Physiology, vol. 68, pp. 123–158, 2006. View at Publisher · View at Google Scholar · View at Scopus
  108. H. Xu, G. T. Barnes, Q. Yang et al., “Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance,” The Journal of Clinical Investigation, vol. 112, no. 12, pp. 1821–1830, 2003. View at Publisher · View at Google Scholar · View at Scopus
  109. S. E. Shoelson, L. Herrero, and A. Naaz, “Obesity, inflammation, and insulin resistance,” Gastroenterology, vol. 132, no. 6, pp. 2169–2180, 2007. View at Publisher · View at Google Scholar · View at Scopus
  110. S. Schenk, M. Saberi, and J. M. Olefsky, “Insulin sensitivity: modulation by nutrients and inflammation,” Journal of Clinical Investigation, vol. 118, no. 9, pp. 2992–3002, 2008. View at Publisher · View at Google Scholar · View at Scopus
  111. G. S. Hotamisligil, “Endoplasmic reticulum stress and the inflammatory basis of metabolic disease,” Cell, vol. 140, no. 6, pp. 900–917, 2010. View at Publisher · View at Google Scholar · View at Scopus
  112. J. Hirosumi, G. Tuncman, L. Chang et al., “A central role for JNK in obesity and insulin resistance,” Nature, vol. 420, no. 6913, pp. 333–336, 2002. View at Publisher · View at Google Scholar · View at Scopus
  113. A. Jaeschke, M. P. Czech, and R. J. Davis, “An essential role of the JIP1 scaffold protein for JNK activation in adipose tissue,” Genes and Development, vol. 18, no. 16, pp. 1976–1980, 2004. View at Publisher · View at Google Scholar · View at Scopus
  114. A. Oeckinghaus, M. S. Hayden, and S. Ghosh, “Crosstalk in NF-κB signaling pathways,” Nature Immunology, vol. 12, no. 8, pp. 695–708, 2011. View at Publisher · View at Google Scholar · View at Scopus
  115. G. Ghosh, V. Y.-F. Wang, D.-B. Huang, and A. Fusco, “NF-κB regulation: lessons from structures,” Immunological Reviews, vol. 246, no. 1, pp. 36–58, 2012. View at Publisher · View at Google Scholar · View at Scopus
  116. M. Yuan, N. Konstantopoulos, J. Lee et al., “Reversal of obesity- and diet-induced insulin resistance with salicylates or targeted disruption of Ikkβ,” Science, vol. 293, no. 5535, pp. 1673–1677, 2001. View at Publisher · View at Google Scholar · View at Scopus
  117. T. Zeng, J. Zhou, L. He et al., “Blocking nuclear factor-kappa B protects against diet-induced hepatic steatosis and insulin resistance in mice,” PLoS ONE, vol. 11, no. 3, Article ID e0149677, 2016. View at Publisher · View at Google Scholar
  118. H. Wang, H. Qu, and H. Deng, “Plasma HMGB-1 levels in subjects with obesity and type 2 diabetes: a cross-sectional study in China,” PLOS ONE, vol. 10, no. 8, Article ID e0136564, 2015. View at Publisher · View at Google Scholar · View at Scopus
  119. I. Jialal, U. Rajamani, B. Adams-Huet, and H. Kaur, “Circulating pathogen associated molecular pattern—binding proteins and High Mobility Group Box protein 1 in nascent metabolic syndrome: Implications for cellular Toll-like receptor activity,” Atherosclerosis, vol. 236, no. 1, pp. 182–187, 2014. View at Publisher · View at Google Scholar · View at Scopus
  120. R. Guzmán-Ruiz, F. Ortega, A. Rodríguez et al., “Alarmin high-mobility group B1 (HMGB1) is regulated in human adipocytes in insulin resistance and influences insulin secretion in β-cells,” International Journal of Obesity, vol. 38, no. 12, pp. 1545–1554, 2014. View at Publisher · View at Google Scholar · View at Scopus
  121. X.-L. Chen, X.-D. Zhang, Y.-Y. Li, X.-M. Chen, D.-R. Tang, and R.-J. Ran, “Involvement of HMGB1 mediated signalling pathway in diabetic retinopathy: evidence from type 2 diabetic rats and ARPE-19 cells under diabetic condition,” British Journal of Ophthalmology, vol. 97, no. 12, pp. 1598–1603, 2013. View at Publisher · View at Google Scholar · View at Scopus
  122. Y. Chen, F. Qiao, Y. Zhao, Y. Wang, and G. Liu, “HMGB1 is activated in type 2 diabetes mellitus patients and in mesangial cells in response to high glucose,” International Journal of Clinical and Experimental Pathology, vol. 8, no. 6, pp. 6683–6691, 2015. View at Google Scholar · View at Scopus
  123. M. Böni-Schnetzler, S. Boller, S. Debray et al., “Free fatty acids induce a proinflammatory response in islets via the abundantly expressed interleukin-1 receptor I,” Endocrinology, vol. 150, no. 12, pp. 5218–5229, 2009. View at Publisher · View at Google Scholar · View at Scopus
  124. K. Eguchi, I. Manabe, Y. Oishi-Tanaka et al., “Saturated fatty acid and TLR signaling link β cell dysfunction and islet inflammation,” Cell Metabolism, vol. 15, no. 4, pp. 518–533, 2012. View at Publisher · View at Google Scholar · View at Scopus
  125. J. A. Ehses, G. Lacraz, M.-H. Giroix et al., “IL-1 antagonism reduces hyperglycemia and tissue inflammation in the type 2 diabetic GK rat,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 33, pp. 13998–14003, 2009. View at Publisher · View at Google Scholar · View at Scopus
  126. C. Westwell-Roper, D. Nackiewicz, M. Dan, and J. A. Ehses, “Toll-like receptors and NLRP3 as central regulators of pancreatic islet inflammation in type 2 diabetes,” Immunology and Cell Biology, vol. 92, no. 4, pp. 314–323, 2014. View at Publisher · View at Google Scholar · View at Scopus
  127. S. A. Steer, A. L. Scarim, K. T. Chambers, and J. A. Corbett, “Interleukin-1 stimulates β-cell necrosis and release of the immunological adjuvant HMGB1,” PLoS Medicine, vol. 3, no. 2, article no. e17, 2006. View at Publisher · View at Google Scholar · View at Scopus
  128. G. A. Paredes-Juarez, N. M. Sahasrabudhe, R. S. Tjoelker et al., “DAMP production by human islets under low oxygen and nutrients in the presence or absence of an immunoisolating-capsule and necrostatin-1,” Scientific Reports, vol. 5, Article ID 14623, 2015. View at Publisher · View at Google Scholar · View at Scopus
  129. T. Itoh, T. Nitta, H. Nishinakamura et al., “HMGB1-mediated early loss of transplanted islets is prevented by anti-IL-6R antibody in mice,” Pancreas, vol. 44, no. 1, pp. 166–171, 2015. View at Publisher · View at Google Scholar · View at Scopus
  130. E. H. Jo, Y. H. Hwang, and D. Y. Lee, “Encapsulation of pancreatic islet with HMGB1 fragment for attenuating inflammation,” Biomaterials Research, vol. 19, article 21, 2015. View at Publisher · View at Google Scholar
  131. D. Kuraya, M. Watanabe, Y. Koshizuka et al., “Efficacy of DHMEQ, a NF-κB inhibitor, in islet transplantation: I. HMGB1 suppression by DHMEQ prevents early islet graft damage,” Transplantation, vol. 96, no. 5, pp. 445–453, 2013. View at Publisher · View at Google Scholar · View at Scopus
  132. T. Mera, T. Itoh, S. Kita et al., “Pretreatment of donor islets with the Na+/Ca2+ exchanger inhibitor improves the efficiency of islet transplantation,” American Journal of Transplantation, vol. 13, no. 8, pp. 2154–2160, 2013. View at Publisher · View at Google Scholar · View at Scopus
  133. T. Itoh, S. Iwahashi, M. A. Kanak et al., “Elevation of high-mobility group box 1 after clinical autologous islet transplantation and its inverse correlation with outcomes,” Cell Transplantation, vol. 23, no. 2, pp. 153–165, 2014. View at Publisher · View at Google Scholar · View at Scopus
  134. Q. Gao, L. L. Ma, X. Gao, W. Yan, P. Williams, and D. P. Yin, “TLR4 mediates early graft failure after intraportal islet transplantation,” American Journal of Transplantation, vol. 10, no. 7, pp. 1588–1596, 2010. View at Publisher · View at Google Scholar · View at Scopus
  135. C. Talchai, S. Xuan, H. V. Lin, L. Sussel, and D. Accili, “Pancreatic β cell dedifferentiation as a mechanism of diabetic β cell failure,” Cell, vol. 150, no. 6, pp. 1223–1234, 2012. View at Publisher · View at Google Scholar · View at Scopus
  136. S. J. Richardson, A. Willcox, A. J. Bone, A. K. Foulis, and N. G. Morgan, “Islet-associated macrophages in type 2 diabetes,” Diabetologia, vol. 52, no. 8, pp. 1686–1688, 2009. View at Publisher · View at Google Scholar · View at Scopus
  137. J. Han, J. Zhong, W. Wei et al., “Extracellular high-mobility group box 1 acts as an innate immune mediator to enhance autoimmune progression and diabetes onset in NOD mice,” Diabetes, vol. 57, no. 8, pp. 2118–2127, 2008. View at Publisher · View at Google Scholar · View at Scopus
  138. B.-W. Lee, H. Y. Chae, S. J. Kwon, S. Y. Park, J. Ihm, and S.-H. Ihm, “RAGE ligands induce apoptotic cell death of pancreatic β-cells via oxidative stress,” International Journal of Molecular Medicine, vol. 26, no. 6, pp. 813–818, 2010. View at Publisher · View at Google Scholar · View at Scopus
  139. X.-R. Ni, Z.-J. Sun, G.-H. Hu, and R.-H. Wang, “High concentration of insulin promotes apoptosis of primary cultured rat ovarian granulosa cells via its increase in extracellular HMGB1,” Reproductive Sciences, vol. 22, no. 3, pp. 271–277, 2015. View at Publisher · View at Google Scholar · View at Scopus