High-mobility group protein box-1 and its relevance to cerebral ischemia

Journal of Cerebral Blood Flow and Metabolism

Volumn 30, Issue 2, 2010, Pages 243-254

  Yang, Qing Wu ^a   Wang, Jing Zhou ^a   Li, Jing Cheng ^a   Zhou, Yu ^a   Zhong, Qi ^a   Lu, Feng Lin ^b   Xiang, Jing ^a  

^a THIRD MILITARY MEDICAL UNIVERSITY   (China)

^b CHONGQING UNIVERSITY   (China)

Author keywords

Cerebral ischemia; HMGB1; Inflammation; RAGE; TLR

Indexed keywords

ADVANCED GLYCATION END PRODUCT; DNA BINDING PROTEIN; HIGH MOBILITY GROUP B1 PROTEIN; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 9;

BRAIN ISCHEMIA; CELL NUCLEUS; EXTRACELLULAR MATRIX; HOMEOSTASIS; HUMAN; INFECTION; INFLAMMATION; INFLAMMATORY DISEASE; NEUROPROTECTION; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; BRAIN; BRAIN ISCHEMIA; HMGB1 PROTEIN; HUMANS;

EID: 76349101890     PISSN: 0271678X     EISSN: None     Source Type: Journal    
DOI: 10.1038/jcbfm.2009.202     Document Type: Review

References (78)

1. Agnello D, Wang H, Yang H, Tracey KJ, Ghezzi P (2002) HMGB-1, a DNA-binding protein with cytokine activity, induces brain TNF and IL-6 production, and mediates anorexia and taste aversion. Cytokine 18:231-236
2. Bianchi ME (2004) Significant (re)location: how to use chromatin and/or abundant proteins as messages of life and death. Trends Cell Biol 14:287-293
3. Bianchi ME, Manfredi AA (2007) High-mobility group box 1 (HMGB1) protein at the crossroads between innate and adaptive immunity. Immunol Rev 220:35-46
4. Bierhaus A, Humpert PM, Morcos M, Wendt T, Chavakis T, Arnold B, Stern DM, Nawroth PP (2005) Understanding RAGE, the receptor for advanced glycation end products. J Mol Med 83:876-886
5. Bonaldi T, Talamo F, Scaffidi P, Ferrera D, Porto A, Bachi A, Rubartelli A, Agresti A, Bianchi ME (2003) Monocytic cells hyperacetylate chromatin protein HMGB1 to redirect it towards secretion. EMBO J 22:5551-5560
6. Bonanno G, Raiteri L, Milanese M, Zappettini S, Melloni E, Pedrazzi M, Passalacqua M, Tacchetti C, Usai C, Sparatore B (2007) The high-mobility group box 1 cytokine induces transporter-mediated release of gluta-mate from glial subcellular particles (gliosomes) prepared from in situ-matured astrocytes. Int Rev Neurobiol 82:73-93
7. Bustin M (2001) Revised nomenclature for high mobility group (HMG) chromosomal proteins. Trends Biochem Sci 26:152-153
8. Bustin M, Neihart NK (1979) Antibodies against chromosomal HMG proteins stain the cytoplasm of mammalian cells. Cell 16:181-189
9. Calogero S, Grassi F, Aguzzi A, Voigtlander T, Ferrier P, Ferrari S, Bianchi ME (1999) The lack of chromosomal protein Hmg1 does not disrupt cell growth but causes lethal hypoglycaemia in newborn mice. Nat Genet 22:276-280
10. Cao CX, Yang QW, Lv FL, Cui J, Fu HB, Wang JZ (2007) Reduced cerebral ischemia-reperfusion injury in Tolllike receptor 4 deficient mice. Biochem Biophys Res Commun 353:509-514
11. Cardin AD, Weintraub HJ (1989) Molecular modeling of protein- glycosaminoglycan interactions. Arteriosclerosis 9:21-32
12. Chou DK, Zhang J, Smith FI, McCaffery P, Jungalwala FB (2004) Developmental expression of receptor for advanced glycation end products (RAGE), amphoterin and sulfoglucuronyl (HNK-1) carbohydrate in mouse cerebellum and their role in neurite outgrowth and cell migration. J Neurochem 90:1389-1401
13. Cokol M, Nair R, Rost B (2000) Finding nuclear localization signals. EMBO Rep 1:411-415
14. Dumitriu IE, Baruah P, Manfredi AA, Bianchi ME, Rovere-Querini P (2005) HMGB1: guiding immunity from within. Trends Immunol 26:381-387
15. Ellwood KB, Yen YM, Johnson RC, Carey M (2000) Mechanism for specificity by HMG-1 in enhanceosome assembly. Mol Cell Biol 20:4359-4370
16. Faraco G, Fossati S, Bianchi ME, Patrone M, Pedrazzi M, Sparatore B, Moroni F, Chiarugi A (2007) High mobility group box 1 protein is released by neural cells upon different stresses and worsens ischemic neurodegenera-tion in vitro and in vivo. J Neurochem 103:590-603
17. Fiuza C, Bustin M, Talwar S, Tropea M, Gerstenberger E, Shelhamer JH, Suffredini AF (2003) Inflammation-promoting activity of HMGB1 on human microvascular endothelial cells. Blood 101:2652-2660
18. Gardella S, Andrei C, Ferrera D, Lotti LV, Torrisi MR, Bianchi ME, Rubartelli A (2002) The nuclear protein HMGB1 is secreted by monocytes via a non-classical, vesicle-mediated secretory pathway. EMBO Rep 3: 995-1001
19. Goldstein RS, Gallowitsch-Puerta M, Yang L, Rosas-Ballina M, Huston JM, Czura CJ, Lee DC, Ward MF, Bruchfeld AN, Wang H, Lesser ML, Church AL, Litroff AH, Sama AE, Tracey KJ (2006) Elevated high-mobility group box 1 levels in patients with cerebral and myocardial ischemia. Shock 25:571-574
20. Goodwin GH, Sanders C, Johns EW (1973) A new group of chromatin-associated proteins with a high content of acidic and basic amino acids. Eur J Biochem 38: 14-19
21. Guazzi S, Strangio A, Franzi AT, Bianchi ME (2003) HMGB1, an architectural chromatin protein and extracellular signalling factor, has a spatially and temporally restricted expression pattern in mouse brain. Gene Expr Patterns 3:29-33
22. Harris HE, Raucci A (2006) Alarmin(g) news about danger: workshop on innate danger signals and HMGB1. EMBO Rep 7:774-778
23. Hassid BG, Nair MN, Ducruet AF, Otten ML, Komotar RJ, Pinsky DJ, Schmidt AM, Yan SF, Connolly ES (2009) Neuronal RAGE expression modulates severity of injury following transient focal cerebral ischemia. J Clin Neurosci 16:302-306
24. Hock R, Furusawa T, Ueda T, Bustin M (2007) HMG chromosomal proteins in development and disease. Trends Cell Biol 17:72-79
25. Hoppe G, Talcott KE, Bhattacharya SK, Crabb JW, Sears JE (2006) Molecular basis for the redox control of nuclear transport of the structural chromatin protein Hmgb1. Exp Cell Res 312:3526-3538
26. Hori O, Brett J, Slattery T, Cao R, Zhang J, Chen JX, Nagashima M, Lundh ER, Vijay S, Nitecki D et al (1995) 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. J Biol Chem 270:25752-25761
27. Huttunen HJ, Fages C, Kuja-Panula J, Ridley AJ, Rauvala H (2002) Receptor for advanced glycation end products-binding COOH-terminal motif of amphoterin inhibits invasive migration and metastasis. Cancer Res 62: 4805-4811
28. Huttunen HJ, Fages C, Rauvala H (1999) Receptor for advanced glycation end products (RAGE)-mediated neurite outgrowth and activation of NF-kappaB require the cytoplasmic domain of the receptor but different downstream signaling pathways. J Biol Chem 274: 19919-19924
29. Huttunen HJ, Rauvala H (2004) Amphoterin as an extracellular regulator of cell motility: from discovery to disease. J Intern Med 255:351-366
30. Ivanov S, Dragoi AM, Wang X, Dallacosta C, Louten J, Musco G, Sitia G, Yap GS, Wan Y, Biron CA, Bianchi ME, Wang H, Chu WM (2007) A novel role for HMGB1 in TLR9-mediated inflammatory responses to CpG-DNA. Blood 110:1970-1981
31. Kallijarvi J, Haltia M, Baumann MH (2001) Amphoterin includes a sequence motif which is homologous to the Alzheimer's beta-amyloid peptide (Abeta), forms amyloid fibrils in vitro, and binds avidly to Abeta. Biochemistry 40:10032-10037
32. Kim JB, Lim CM, Yu YM, Lee JK (2008) Induction and subcellular localization of high-mobility group box-1 (HMGB1) in the postischemic rat brain. J Neurosci Res 86:1125-1131
33. Kim JB, Sig Choi J, Yu YM, Nam K, Piao CS, Kim SW, Lee MH, Han PL, Park JS, Lee JK (2006) HMGB1, a novel cytokine-like mediator linking acute neuronal death and delayed neuroinflammation in the postischemic brain. J Neurosci 26:6413-6421
34. Knapp S, Wieland CW, van 't Veer C, Takeuchi O, Akira S, Florquin S, van der Poll T (2004) Toll-like receptor 2 plays a role in the early inflammatory response to murine pneumococcal pneumonia but does not contribute to antibacterial defense. J Immunol 172:3132-3138
35. Kokkola R, Li J, Sundberg E, Aveberger AC, Palmblad K, Yang H, Tracey KJ, Andersson U, Harris HE (2003) Successful treatment of collagen-induced arthritis in mice and rats by targeting extracellular high mobility group box chromosomal protein 1 activity. Arthritis Rheum 48:2052-2058
36. Kruger B, Krick S, Dhillon N, Lerner SM, Ames S, Bromberg JS, Lin M, Walsh L, Vella J, Fischereder M, Kramer BK, Colvin RB, Heeger PS, Murphy BT, Schroppel B (2009) Donor Toll-like receptor 4 contributes to ischemia and reperfusion injury following human kidney transplantation. Proc Natl Acad Sci USA 106:3390-3395
37. Landsman D, Bustin M (1993) A signature for the HMG-1 box DNA-binding proteins. Bioessays 15:539-546
38. Liliensiek B, Weigand MA, Bierhaus A, Nicklas W, Kasper M, Hofer S, Plachky J, Grone HJ, Kurschus FC, Schmidt AM, Yan SD, Martin E, Schleicher E, Stern DM, Hammerling GG, Nawroth PP, Arnold B (2004) Receptor for advanced glycation end products (RAGE) regulates sepsis but not the adaptive immune response. J Clin Invest 113:1641-1650 (Pubitemid 39071688)
39. Liu K, Mori S, Takahashi HK, Tomono Y, Wake H, Kanke T, Sato Y, Hiraga N, Adachi N, Yoshino T, Nishibori M (2007) Anti-high mobility group box 1 monoclonal antibody ameliorates brain infarction induced by transient ischemia in rats. FASEB J 21:3904-3916
40. Lotze MT, Tracey KJ (2005) High-mobility group box 1 protein (HMGB1): nuclear weapon in the immune arsenal. Nat Rev Immunol 5:331-342
41. Lutterloh EC, Opal SM, Pittman DD, Keith JC Jr, Tan XY, Clancy BM, Palmer H, Milarski K, Sun Y, Palardy JE, Parejo NA, Kessimian N (2007) Inhibition of the RAGE products increases survival in experimental models of severe sepsis and systemic infection. Crit Care 11:R122
42. Martin M, Katz J, Vogel SN, Michalek SM (2001) Differential induction of endotoxin tolerance by lipopolysac-charides derived from Porphyromonas gingivalis and Escherichia coli. J Immunol 167:5278-5285
43. Means TK, Jones BW, Schromm AB, Shurtleff BA, Smith JA, Keane J, Golenbock DT, Vogel SN, Fenton MJ (2001) Differential effects of a Toll-like receptor antagonist on Mycobacterium tuberculosis-induced macrophage responses. J Immunol 166:4074-4082
44. Merenmies J, Pihlaskari R, Laitinen J, Wartiovaara J, Rauvala H (1991) 30-kDa heparin-binding protein of brain (amphoterin) involved in neurite outgrowth. Amino acid sequence and localization in the filopodia of the advancing plasma membrane. J Biol Chem 266:16722-16729
45. Mori S, Liu K, Takahashi HK, Nishibori M (2009) [Therapeutic effect of anti-nucleokine monoclonal antibody on ischemic brain infarction]. Yakugaku Zasshi 129:25-31
46. Muhammad S, Barakat W, Stoyanov S, Murikinati S, Yang H, Tracey KJ, Bendszus M, Rossetti G, Nawroth PP, Bierhaus A, Schwaninger M (2008) The HMGB1 receptor RAGE mediates ischemic brain damage. J Neurosci 28:12023-12031
47. O'Connor KA, Hansen MK, Rachal Pugh C, Deak MM, Biedenkapp JC, Milligan ED, Johnson JD, Wang H, Maier SF, Tracey KJ, Watkins LR (2003) Further characterization of high mobility group box 1 (HMGB1) as a proinflammatory cytokine: central nervous system effects. Cytokine 24:254-265
48. Park JS, Gamboni-Robertson F, He Q, Svetkauskaite D, Kim JY, Strassheim D, Sohn JW, Yamada S, Maruyama I, Banerjee A, Ishizaka A, Abraham E (2006) High mobility group box 1 protein interacts with multiple Toll-like receptors. Am J Physiol Cell Physiol 290:C917-24
49. Park JS, Svetkauskaite D, He Q, Kim JY, Strassheim D, Ishizaka A, Abraham E (2004) Involvement of toll-like receptors 2 and 4 in cellular activation by high mobility group box 1 protein. J Biol Chem 279:7370-7377
50. Parrish W, Ulloa L (2007) High-mobility group box-1 isoforms as potential therapeutic targets in sepsis. Methods Mol Biol 361:145-162
51. Passalacqua M, Patrone M, Picotti GB, Del Rio M, Sparatore B, Melloni E, Pontremoli S (1998) Stimulated astrocytes release high-mobility group 1 protein, an inducer of LAN-5 neuroblastoma cell differentiation. Neuroscience 82:1021-1028
52. Pedrazzi M, Raiteri L, Bonanno G, Patrone M, Ledda S, Passalacqua M, Milanese M, Melloni E, Raiteri M, Pontremoli S, Sparatore B (2006) Stimulation of excitatory amino acid release from adult mouse brain glia subcellular particles by high mobility group box 1 protein. J Neurochem 99:827-838
53. Qiu J, Nishimura M, Wang Y, Sims JR, Qiu S, Savitz SI, Salomone S, Moskowitz MA (2008) Early release of HMGB-1 from neurons after the onset of brain ischemia. J Cereb Blood Flow Metab 28:927-938
54. Rauvala H, Pihlaskari R (1987) Isolation and some characteristics of an adhesive factor of brain that enhances neurite outgrowth in central neurons. J Biol Chem 262:16625-16635
55. Rauvala H, Rouhiainen A (2007) RAGE as a receptor of HMGB1 (Amphoterin): roles in health and disease. Curr Mol Med 7:725-734
56. Rouhiainen A, Kuja-Panula J, Wilkman E, Pakkanen J, Stenfors J, Tuominen RK, Lepantalo M, Carpen O, Parkkinen J, Rauvala H (2004) Regulation of monocyte migration by amphoterin (HMGB1). Blood 104:1174-1182
57. Scaffidi P, Misteli T, Bianchi ME (2002) Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature 418:191-195
58. Schmidt AM, Hasu M, Popov D, Zhang JH, Chen J, Yan SD, Brett J, Cao R, Kuwabara K, Costache G et al (1994) Receptor for advanced glycation end products (AGEs) has a central role in vessel wall interactions and gene activation in response to circulating AGE proteins. Proc Natl Acad Sci USA 91:8807-8811
59. Sha Y, Zmijewski J, Xu Z, Abraham E (2008) HMGB1 develops enhanced proinflammatory activity by binding to cytokines. J Immunol 180:2531-2537
60. Sitia G, Iannacone M, Muller S, Bianchi ME, Guidotti LG (2007) Treatment with HMGB1 inhibitors diminishes CTL-induced liver disease in HBV transgenic mice. J Leukoc Biol 81:100-107
61. Sparatore B, Patrone M, Passalacqua M, Pedrazzi M, Gaggero D, Pontremoli S, Melloni E (2001) Extracellular processing of amphoterin generates a peptide active on erythroleukaemia cell differentiation. Biochem J 357:569-574
62. Takata K, Kitamura Y, Kakimura J, Shibagaki K, Tsuchiya D, Taniguchi T, Smith MA, Perry G, Shimohama S (2003) Role of high mobility group protein-1 (HMG1) in amyloid-beta homeostasis. Biochem Biophys Res Com-mun 301:699-703
63. Takata K, Kitamura Y, Tsuchiya D, Kawasaki T, Taniguchi T, Shimohama S (2004) High mobility group box protein-1 inhibits microglial Abeta clearance and enhances Abeta neurotoxicity. J Neurosci Res 78:880-891
64. Tian J, Avalos AM, Mao SY, Chen B, Senthil K, Wu H, Parroche P, Drabic S, Golenbock D, Sirois C, Hua J, An LL, Audoly L, La Rosa G, Bierhaus A, Naworth P, Marshak-Rothstein A, Crow MK, Fitzgerald KA, Latz E, Kiener PA, Coyle AJ (2007) Toll-like receptor 9-depen-dent activation by DNA-containing immune complexes is mediated by HMGB1 and RAGE. Nat Immunol 8:487-496
65. Ulloa L (2005) The vagus nerve and the nicotinic anti-inflammatory pathway. Nat Rev Drug Discov 4:673-684
66. Ulloa L, Messmer D (2006) High-mobility group box 1 (HMGB1) protein: friend and foe. Cytokine Growth Factor Rev 17:189-201
67. Ulloa L, Tracey KJ (2005) The 'cytokine profile': a code for sepsis. Trends Mol Med 11:56-63
68. van Zoelen MA, Yang H, Florquin S, Meijers JC, Akira S, Arnold B, Nawroth PP, Bierhaus A, Tracey KJ, Poll T (2009) Role of toll-like receptors 2 and 4, and the receptor for advanced glycation end products in high-mobility group box 1-induced inflammation in vivo. Shock 31:280-284
69. Verrijdt G, Haelens A, Schoenmakers E, Rombauts W, Claessens F (2002) Comparative analysis of the influence of the high-mobility group box 1 protein on DNA binding and transcriptional activation by the androgen, glucocorticoid, progesterone and mineralocorticoid receptors. Biochem J 361:97-103
70. Wang H, Bloom O, Zhang M, Vishnubhakat JM, Ombrellino M, Che J, Frazier A, Yang H, Ivanova S, Borovikova L, Manogue KR, Faist E, Abraham E, Andersson J, Andersson U, Molina PE, Abumrad NN, Sama A, Tracey KJ (1999a) HMG-1 as a late mediator of endotoxin lethality in mice. Science 285:248-251
71. Wang H, Vishnubhakat JM, Bloom O, Zhang M, Ombrellino M, Sama A, Tracey KJ (1999b) Proinflammatory cytokines (tumor necrosis factor and interleukin 1) stimulate release of high mobility group protein-1 by pituicytes. Surgery 126:389-392
72. Yamada S, Maruyama I (2007) HMGB1, a novel inflammatory cytokine. Clin Chim Acta 375:36-42
73. Yan SD, Schmidt AM, Anderson GM, Zhang J, Brett J, Zou YS, Pinsky D, Stern D (1994) Enhanced cellular oxidant stress by the interaction of advanced glycation end products with their receptors/binding proteins. J Biol Chem 269:9889-9897
74. Yang H, Ochani M, Li J, Qiang X, Tanovic M, Harris HE, Susarla SM, Ulloa L, Wang H, DiRaimo R, Czura CJ, Wang H, Roth J, Warren HS, Fink MP, Fenton MJ, Andersson U, Tracey KJ (2004) Reversing established sepsis with antagonists of endogenous high-mobility group box 1. Proc Natl Acad Sci USA 101: 296-301
75. Yang H, Wang H, Czura CJ, Tracey KJ (2005) The cytokine activity of HMGB1. J Leukoc Biol 78:1-8
76. Yang QW, Li JC, Lu FL, Wen AQ, Xiang J, Zhang LL, Huang ZY, Wang JZ (2008) Upregulated expression of toll-like receptor 4 in monocytes correlates with severity of acute cerebral infarction. J Cereb Blood Flow Metab 28:1588-1596
77. Youn JH, Oh YJ, Kim ES, Choi JE, Shin JS (2008) High mobility group box 1 protein binding to lipopolysac-charide facilitates transfer of lipopolysaccharide to CD14 and enhances lipopolysaccharide-mediated TNF-alpha production in human monocytes. J Immunol 180:5067-5074
78. Yu M, Wang H, Ding A, Golenbock DT, Latz E, Czura CJ, Fenton MJ, Tracey KJ, Yang H (2006) HMGB1 signals through toll-like receptor (TLR) 4 and TLR2. Shock 26:174-179