High-mobility group box 1 (HMGB1) protein at the crossroads between innate and adaptive immunity

Immunological Reviews

Volumn 220, Issue 1, 2007, Pages 35-46

  Bianchi, Marco E ^a   Manfredi, Angelo A ^a  

^a VITA SALUTE SAN RAFFAELE UNIVERSITY   (Italy)

Author keywords

Alarmins; Autoimmunity; Cell death; Cross presentation; Dendritic cells

Indexed keywords

HIGH MOBILITY GROUP B1 PROTEIN; TOLL LIKE RECEPTOR;

ADAPTIVE IMMUNITY; APOPTOSIS; AUTOIMMUNITY; CELL DEATH; CELL DIVISION; CELL MATURATION; CELL MIGRATION; CELL PROLIFERATION; DENDRITIC CELL; GLYCATION; HUMAN; IMMUNE RESPONSE; INFLAMMATION; INFLAMMATORY CELL; INNATE IMMUNITY; LEUKOCYTE; LYMPH NODE; MICROENVIRONMENT; NONHUMAN; PRIORITY JOURNAL; REVIEW; SEPSIS; STEM CELL; SYSTEMIC LUPUS ERYTHEMATOSUS; TISSUE REGENERATION; TISSUE REPAIR;

ANIMALS; AUTOIMMUNITY; DENDRITIC CELLS; HMGB1 PROTEIN; HUMANS; IMMUNITY, NATURAL; LUPUS ERYTHEMATOSUS, SYSTEMIC; SEPSIS; T-LYMPHOCYTES; TOLL-LIKE RECEPTORS;

EID: 35748967851     PISSN: 01052896     EISSN: 1600065X     Source Type: Journal    
DOI: 10.1111/j.1600-065X.2007.00574.x     Document Type: Review

References (84)

1. Bianchi ME, Manfredi A. Chromatin and cell death. Biochim Biophys Acta 2004 1677 : 181 186.
2. Mahoney JA, Rosen A. Apoptosis and autoimmunity. Curr Opin Immunol 2005 17 : 583 588.
3. Cook HT, Botto M. Mechanisms of disease: the complement system and the pathogenesis of systemic lupus erythematosus. Nat Clin Pract Rheumatol 2006 2 : 330 337.
4. Gaipl US, et al. Clearance deficiency and systemic lupus erythematosus (SLE). J Autoimmun 2007 28 : 114 121.
5. Bianchi ME. DAMPs, PAMPs and alarmins: all we need to know about danger. J Leukoc Biol 2007 81 : 1 5.
6. Agresti A, Bianchi ME. HMGB proteins and gene expression. Curr Opin Genet Develop 2003 13 : 170 178.
7. Scaffidi P, Misteli T, Bianchi ME. Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature 2002 418 : 191 195.
8. Wang H, et al. HMG-1 as a late mediator of endotoxin lethality in mice. Science 1999 285 : 248 251.
9. Goodwin GH, Sanders C, Johns EW. A new group of chromatin-associated proteins with a high content of acidic and basic amino acids. Eur J Biochem 1973 38 : 14 19.
10. Thomas JO, Travers AA. HMG1 and 2, and related 'architectural' DNA-binding proteins. Trends Biochem Sci 2001 26 : 167 174.
11. Knapp S, Muller S, Digilio G, Bonaldi T, Bianchi ME, Musco G. The long acidic tail of high mobility group box 1 (HMGB1) protein forms an extended and flexible structure that interacts with specific residues within and between the HMG boxes. Biochemistry 2004 43 : 11992 11997.
12. Wang Q, Zeng M, Wang W, Tang J. The HMGB1 acidic tail regulates HMGB1 DNA binding specificity by a unique mechanism. Biochem Biophys Res Commun 2007 360 : 14 19.
13. Sessa L, Bianchi ME. The evolution of high mobility group box (HMGB) chromatin proteins in multicellular animals. Gene 2006 387 : 133 140.
14. Calogero S, et al. The lack of chromosomal protein Hmg1 does not disrupt cell growth, but causes lethal hypoglycaemia in newborn mice. Nat Genet 1999 22 : 276 80.
15. Ronfani L, et al. Reduced fertility and spermatogenesis defects in mice lacking chromosomal protein Hmgb2. Development 2001 128 : 1265 1273.
16. Nemeth MJ, Cline AP, Anderson SM, Garrett-Beal LJ, Bodine DM. Hmgb3 deficiency deregulates proliferation and differentiation of common lymphoid and myeloid progenitors. Blood 2005 105 : 627 634.
17. Müller S, Ronfani L, Bianchi ME. Regulated expression and subcellular localization of HMGB1, a chromatin protein with a cytokine function. J Intern Med 2004 255 : 332 343.
18. Müller S, et al. The double life of HMGB1 chromatin protein: architectural factor and extracellular signal. EMBO J 2001 20 : 4337 4340.
19. Bianchi ME, Agresti A. HMG proteins: dynamic players in gene regulation and differentiation. Curr Opin Genet Dev 2005 15 : 496 506.
20. Yang H, et al. Reversing established sepsis with antagonists of endogenous high-mobility group box 1. Proc Natl Acad Sci USA 2004 101 : 296 301.
21. Calandra T, et al. Protection from septic shock by neutralization of macrophage migration inhibitory factor. Nat Med 2000 6 : 164 170.
22. Andersson U, et al. High mobility group 1 protein (HMG-1) stimulates proinflammatory cytokine synthesis in human monocytes. J Exp Med 2000 192 : 565 570.
23. Rouhiainen A, Tumova S, Valmu L, Kalkkinen N, Rauvala H. Analysis of proinflammatory activity of highly purified eukaryotic recombinant HMGB1 (amphoterin). J Leukoc Biol 2007 81 : 49 58.
24. Tian J, et al. Toll-like receptor 9-dependent activation by DNA-containing immune complexes is mediated by HMGB1 and RAGE. Nat Immunol 2007 8 : 487 496.
25. Ivanov S, et al. A novel role for HMGB1 in TLR9-mediated inflammatory responses to CpG-DNA. Blood 2007 110 : 1970 1981.
26. Yang R, et al. Anti-HMGB1 neutralizing antibody ameliorates gut barrier dysfunction and improves survival after hemorrhagic shock. Mol Med 2006 12 : 105 114.
27. Fiuza C, et al. Inflammatory promoting activity of HMGB1 on human microvascular endothelial cells. Blood 2002 27 : 2652 2660.
28. Abraham E, Arcaroli J, Carmody A, Wang H, Tracey KJ. HMG-1 as a mediator of acute lung inflammation. J Immunol 2000 165 : 2950 2954.
29. Bonaldi T, et al. Monocytic cells hyperacetylate chromatin protein HMGB1 to redirect it towards secretion. EMBO J 2003 22 : 5551 5560.
30. Gardella S, et al. The nuclear protein HMGB1 is secreted by monocytes via a non-classical, vesicle-mediated secretory pathway. EMBO Rep 2002 3 : 995 1001.
31. Youn JH, Shin JS. Nucleocytoplasmic shuttling of HMGB1 is regulated by phosphorylation that redirects it toward secretion. J Immunol 2006 177 : 7889 7897.
32. Ito I, Fukazawa J, Yoshida M. Post-translational methylation of HMGB1 causes its cytoplasmic localization in neutrophils. J Biol Chem 2007 282 : 16336 16344.
33. Ito N, et al. Cytolytic cells induce HMGB1 release from melanoma cell lines. J Leukoc Biol 2007 81 : 75 83.
34. Steer SA, Scarim AL, Chambers KT, Corbett JA. Interleukin-1 stimulates beta-cell necrosis and release of the immunological adjuvant HMGB1. PLoS Med 2005 3 : e17.
35. Ogawa EN, et al. Contribution of high-mobility group box-1 to the development of ventilator-induced lung injury. Am J Respir Crit Care Med 2006 174 : 400 407.
36. Moser B, et al. Blockade of RAGE suppresses alloimmune reactions in vitro and delays allograft rejection in murine heart transplantation. Am J Transplant 2007 7 : 293 302.
37. Tsung A, et al. The nuclear factor HMGB1 mediates hepatic injury after murine liver ischemia-reperfusion. J Exp Med 2005 201 : 1135 1143.
38. Tsung A, et al. Increasing numbers of hepatic dendritic cells promote HMGB1-mediated ischemia-reperfusion injury. J Leukoc Biol 2007 81 : 119 128.
39. Sitia G, Iannacone M, Muller S, Bianchi ME, Guidotti LG. Treatment with HMGB1 inhibitors diminishes CTL-induced liver disease in HBV transgenic mice. J Leukoc Biol 2007 81 : 100 107.
40. Hori O, et al. The receptor for advanced glycation end products (RAGE) is a cellular binding site for amphoterin. J Biol Chem 1995 270 : 25752 25761.
41. Bierhaus A, et al. Understanding RAGE, the receptor for advanced glycation end products. J Mol Med 2005 83 : 876 886.
42. Shirasawa M, et al. Receptor for advanced glycation end-products is a marker of type I lung alveolar cells. Genes Cells 2004 9 : 165 174.
43. Palumbo R, et al. Extracellular HMGB1, a signal of tissue damage, induces mesoangioblast migration and proliferation. J Cell Biol 2004 164 : 441 449.
44. Orlova VV, et al. A novel pathway of HMGB1-mediated inflammatory cell recruitment that requires Mac-1-integrin. EMBO J 2007 26 : 1129 1139.
45. Degryse B, et al. The high mobility group (HMG) boxes of the nuclear protein HMG1 induce chemotaxis and cytoskeleton reorganization in rat smooth muscle cells. J Cell Biol 2001 152 : 1197 1206.
46. Yang D, Chen Q, Yang H, Tracey KJ, Bustin M, Oppenheim JJ. High mobility group box-1 protein induces the migration and activation of human dendritic cells and acts as an alarmin. J Leukoc Biol 2007 81 : 59 66.
47. Liliensiek B, et al. Receptor for advanced glycation end products (RAGE) regulates sepsis but not the adaptive immune response. J Clin Invest 2004 113 : 1641 1650.
48. Galvez BG, et al. Complete repair of dystrophic skeletal muscle by mesoangioblasts with enhanced migration ability. J Cell Biol 2006 174 : 231 243.
49. Limana F, et al. Exogenous high-mobility group box 1 protein induces myocardial regeneration after infarction via enhanced cardiac C-kit+cell proliferation and differentiation. Circ Res 2005 97 : e73 e83.
50. Mitola S, et al. Cutting edge: extracellular high mobility group box-1 protein is a proangiogenic cytokine. J Immunol 2006 176 : 12 15.
51. Schlueter C, et al. Angiogenetic signaling through hypoxia: HMGB1: an angiogenetic switch molecule. Am J Pathol 2005 166 : 1259 1263.
52. Chavakis E, et al. High-mobility group box 1 activates integrin-dependent homing of endothelial progenitor cells. Circ Res 2007 100 : 204 212.
53. Kalinina N, et al. Increased expression of the DNA-binding cytokine HMGB1 in human atherosclerotic lesions. Role of activated macrophages and cytokines. Arterioscler Thromb Vasc Biol 2004 24 : 2320 2325.
54. Porto A, et al. Smooth muscle cells in human atherosclerotic plaques secrete and proliferate in response to high mobility group box 1 protein. FASEB J 2006 20 : E1955 E1963.
55. Inoue K, et al. HMGB1 expression by activated vascular smooth muscle cells in advanced human atherosclerosis plaques. Cardiovasc Pathol 2007 16 : 136 143.
56. Andersson U, Erlandsson-Harris H. HMGB1 is a potent trigger of arthritis. J Intern Med 2004 255 : 344 350.
57. Foell D, Wittkowski H, Roth J. Mechanisms of disease: a 'DAMP' view of inflammatory arthritis. Nat Clin Pract Rheumatol 2007 3 : 382 390.
58. Park JS, et al. Involvement of TLR2 and TLR4 in cellular activation by high mobility group box 1 protein (HMGB1). J Biol Chem 2004 279 : 7370 7377.
59. Tsung A, et al. Hepatic ischemia/reperfusion injury involves functional TLR4 signaling in nonparenchymal cells. J Immunol 2005 175 : 7661 7668.
60. Kokkola R, et al. RAGE is the major receptor for the proinflammatory activity of HMGB1 in rodent macrophages. Scand J Immunol 2005 61 : 1 9.
61. Popovic K, et al. Increased expression of the novel proinflammatory cytokine high mobility group box chromosomal protein 1 in skin lesions of patients with lupus erythematosus. Arthritis Rheum 2005 5 : 3639 3645.
62. Rovere-Querini P, et al. HMGB1 is an endogenous immune adjuvant released by necrotic cells. EMBO Rep 2004 5 : 825 830.
63. Ronchetti A, et al. Immunogenicity of apoptotic cells in vivo: role of antigen load, antigen-presenting cells, and cytokines. J Immunol 1999 163 : 130 136.
64. Messmer D, et al. High mobility group box protein 1: an endogenous signal for dendritic cell maturation and Th1 polarization. J Immunol 2004 173 : 307 313.
65. Randolph GJ, Angeli V, Swartz MA. Dendritic-cell trafficking to lymph nodes through lymphatic vessels. Nat Rev Immunol 2005 5 : 617 628.
66. Dumitriu IE, et al. Release of high mobility group box 1 by dendritic cells controls T cell activation via the receptor for advanced glycation end products. J Immunol 2005 174 : 7506 7515.
67. Dumitriu IE, Bianchi ME, Bacci M, Manfredi AA, Rovere-Querini P. The secretion of HMGB1 is required for the migration of maturing dendritic cells. J Leukoc Biol 2007 81 : 84 91.
68. Lucas M, et al. Requirements for apoptotic cell contact in regulation of macrophage responses. J Immunol 2006 177 : 4047 4054.
69. Hristov M, Erl W, Linder S, Weber PC. Apoptotic bodies from endothelial cells enhance the number and initiate the differentiation of human endothelial progenitor cells in vitro. Blood 2004 104 : 2761 2766.
70. Golpon HA, et al. Life after corpse engulfment: phagocytosis of apoptotic cells leads to VEGF secretion and cell growth. FASEB J 2004 18 : 1716 1718.
71. Blander JM. Coupling Toll-like receptor signaling with phagocytosis: potentiation of antigen presentation. Trends Immunol 2007 28 : 19 25.
72. Mathis D, Vence L, Benoist C. Beta-cell death during progression to diabetes. Nature 2001 414 : 792 798.
73. Pearl-Yafe M, Iskovich S, Kaminitz A, Stein J, Yaniv I, Askenasy N. Does physiological beta cell turnover initiate autoimmune diabetes in the regional lymph nodes? Autoimmun Rev 2006 5 : 338 343.
74. Bondanza A, et al. Requirement of dying cells and environmental adjuvants for the induction of autoimmunity. Arthritis Rheum 2004 50 : 1549 1560.
75. Sobajima J, et al. Prevalence and characterization of perinuclear anti-neutrophil cytoplasmic antibodies (P-ANCA) directed against HMG1 and HMG2 in ulcerative colitis (UC). Clin Exp Immunol 1998 111 : 402 407.
76. Desai-Mehta A, Mao C, Rajagopalan S, Robinson T, Datta SK. Structure and specificity of T cell receptors expressed by potentially pathogenic anti-DNA autoantibody-inducing T cells in human lupus. J Clin Invest 1995 95 : 531 541.
77. Qin S, et al. Role of HMGB1 in apoptosis-mediated sepsis lethality. J Exp Med 2006 203 : 1637 1642.
78. Pascual V, Farkas L, Banchereau J. Systemic lupus erythematosus: all roads lead to type I interferons. Curr Opin Immunol 2006 18 : 676 682.
79. Rumore PM, Steinman CR. Endogenous circulating DNA in systemic lupus erythematosus: occurrence as multimeric complexes bound to histone. J Clin Invest 1990 86 : 69 74.
80. Botezatu I, et al. Genetic analysis of DNA excreted in urine: a new approach for detecting specific genomic DNA sequences from cells dying in an organism. Clin Chem 2000 46 : 1078 1084.
81. Su YH, et al. Human urine contains small, 150 to 250 nucleotide-sized, soluble DNA derived from the circulation and may be useful in the detection of colorectal cancer. J Mol Diagn 2004 6 : 101 107.
82. Bell CW, Jiang W, Reich CF, Pisetsky DS. The extracellular release of HMGB1 during apoptotic cell death. Am J Physiol Cell Physiol 2006 291 : C1318 C1325.
83. Leadbetter EA, Rifkin IR, Hohlbaum AM, Beaudette BC, Shlomchik MJ, Marshak-Rothstein A. Chromatin-IgG complexes activate B cells by dual engagement of IgM and Toll-like receptors. Nature 2002 416 : 603 607.
84. Apetoh L, et al. Toll-like receptor 4-dependent contribution of the immune systems to anticancer chemotherapy and radiotherapy. Nat Med 2007 13 : 1050 1059.