A dual-role of Gu-4 in suppressing HMGB1 secretion and blocking HMGB1 pro-inflammatory activity during inflammation

PLoS ONE

Volumn 9, Issue 3, 2014, Pages

  Zhou, HuiTing ^a   Ji, XueMei ^a   Wu, Yun ^a   Xuan, Ju ^a   Qi, ZhiLin ^a   Shen, Lei ^a   Lan, Lei ^a,c   Li, Qing ^b   Yin, ZhiMin ^a,c   Li, ZhongJun ^b   Zhao, ZhiHu I ^a,c  

^a NANJING NORMAL UNIVERSITY   (China)

^b PEKING UNIVERSITY HEALTH SCIENCE CENTER   (China)

^c Collaborative Innovation Center of Biomedicine for Public Hygiene Emergency and Critical Care Jiangsu Life Sciences and Technology Innovation Park ^*  (China)

Author keywords

[No Author keywords available]

Indexed keywords

CD11B ANTIGEN; GU 4; HIGH MOBILITY GROUP B1 PROTEIN; I KAPPA B KINASE ALPHA; I KAPPA B KINASE BETA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; MITOGEN ACTIVATED PROTEIN KINASE; N [2 (1,3 DILACTOSYL)PROPANYL] 2 AMINO PENTANDIAMIDE; OLIGOSACCHARIDE; RECOMBINANT HIGH MOBILITY GROUP B1 PROTEIN; RECOMBINANT PROTEIN; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; GLUTAMINE; GU-4 COMPOUND; I KAPPA B KINASE; LACTOSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CELL ADHESION; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOPLASM; DOSE RESPONSE; DRUG EFFICACY; DRUG MECHANISM; ENZYME PHOSPHORYLATION; EXPERIMENTAL MODEL; FLOW CYTOMETRY; GENE SILENCING; HISTOPATHOLOGY; HUMAN; HUMAN CELL; INFLAMMATION; LUNG INJURY; MACROPHAGE; MALE; MOUSE; NONHUMAN; PROTEIN BLOOD LEVEL; PROTEIN SECRETION; PROTEIN SYNTHESIS INHIBITION; PROTEIN TRANSPORT; RAT; RAT MODEL; SEPSIS; SIGNAL TRANSDUCTION; SURVIVAL RATE; UMBILICAL VEIN ENDOTHELIAL CELL; WESTERN BLOTTING; ANALOGS AND DERIVATIVES; ANIMAL; BLOOD; CELL CULTURE; CELL LINE; DRUG EFFECTS; GENETICS; METABOLISM; MORTALITY; PHOSPHORYLATION; RNA INTERFERENCE; SECRETION (PROCESS); TUMOR CELL LINE;

ANIMALS; ANTIGENS, CD11B; BLOTTING, WESTERN; CELL ADHESION; CELL LINE; CELL LINE, TUMOR; CELLS, CULTURED; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GLUTAMINE; HMGB1 PROTEIN; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; I-KAPPA B KINASE; INFLAMMATION; LACTOSE; LIPOPOLYSACCHARIDES; MACROPHAGES; PHOSPHORYLATION; PROTEIN TRANSPORT; RATS; RECOMBINANT PROTEINS; RNA INTERFERENCE; SEPSIS; SURVIVAL RATE;

EID: 84897432815     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0089634     Document Type: Article

References (46)

1. Bustin M (1999) Regulation of DNA-dependent activities by the functional motifs of the high-mobility-group chromosomal proteins. Molecular and cellular biology 19: 5237-5246.
2. Yamada S, Maruyama I (2007) HMGB1, a novel inflammatory cytokine. Clinica Chimica Acta 375: 36-42. (Pubitemid 44584241)
3. Andersson U, Tracey KJ (2011) HMGB1 is a therapeutic target for sterile inflammation and infection. Annual review of immunology 29: 139-162.
4. Diener KR, Al-Dasooqi N, Lousberg EL, Hayball JD (2013) The multifunctional alarmin HMGB1 with roles in the pathophysiology of sepsis and cancer. Immunology and cell biology 91: 443-450.
5. Gardella S, Andrei C, Ferrera D, Lotti LV, Torrisi MR, et al. (2002) The nuclear protein HMGB1 is secreted by monocytes via a non-classical, vesicle-mediated secretory pathway. EMBO reports 3: 995-1001. (Pubitemid 35256475)
6. Scaffidi P, Misteli T, Bianchi ME (2002) Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature 418: 191-195. (Pubitemid 34773774)
7. Wang H, Bloom O, Zhang M, Vishnubhakat JM, Ombrellino M, et al. (1999) HMG-1 as a late mediator of endotoxin lethality in mice. Science 285: 248-251. (Pubitemid 29329996)
8. Youn JH, Shin J-S (2006) Nucleocytoplasmic shuttling of HMGB1 is regulated by phosphorylation that redirects it toward secretion. The Journal of Immunology 177: 7889-7897.
9. Fiuza C, Bustin M, Talwar S, Tropea M, Gerstenberger E, et al. (2003) Inflammation-promoting activity of HMGB1 on human microvascular endothelial cells. Blood 101: 2652-2660. (Pubitemid 36857626)
10. Li J, Wang H, Mason JM, Levine J, Yu M, et al. (2004) Recombinant HMGB1 with cytokine-stimulating activity. Journal of immunological methods 289: 211-223. (Pubitemid 38900918)
11. Park JS, Arcaroli J, Yum H-K, Yang H, Wang H, et al. (2003) Activation of gene expression in human neutrophils by high mobility group box 1 protein. American Journal of Physiology-Cell Physiology 284: C870-C879. (Pubitemid 36336943)
12. Yang D, Chen Q, Yang H, Tracey KJ, Bustin M, et al. (2007) High mobility group box-1 protein induces the migration and activation of human dendritic cells and acts as an alarmin. Journal of leukocyte biology 81: 59-66. (Pubitemid 46021253)
13. Dumitriu IE, Baruah P, Valentinis B, Voll RE, Herrmann M, et al. (2005) Release of high mobility group box 1 by dendritic cells controls T cell activation via the receptor for advanced glycation end products. The Journal of Immunology 174: 7506-7515. (Pubitemid 40806253)
14. Park JS, Svetkauskaite D, He Q, Kim J-Y, Strassheim D, et al. (2004) Involvement of toll-like receptors 2 and 4 in cellular activation by high mobility group box 1 protein. Journal of Biological Chemistry 279: 7370-7377. (Pubitemid 38294612)
15. Yu M, Wang H, Ding A, Golenbock DT, Latz E, et al. (2006) HMGB1 signals through toll-like receptor (TLR) 4 and TLR2. Shock 26: 174-179. (Pubitemid 44162504)
16. Venereau E, Casalgrandi M, Schiraldi M, Antoine DJ, Cattaneo A, et al. (2012) Mutually exclusive redox forms of HMGB1 promote cell recruitment or proinflammatory cytokine release. The Journal of experimental medicine 209: 1519-1528.
17. Yang H, Hreggvidsdottir HS, Palmblad K, Wang H, Ochani M, et al. (2010) 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 107: 11942-11947.
18. Yang H, Lundbäck P, Ottosson L, Erlandsson-Harris H, Venereau E, et al. (2012) Redox modification of cysteine residues regulates the cytokine activity of high mobility group box-1 (HMGB1). Molecular Medicine 18: 250.
19. LaRosa SP, Opal SM (2011) Strategies to treat sepsis: old and new. Clinical Investigation 1: 195-210.
20. Abraham E, Anzueto A, Gutierrez G, Tessler S, Pedro GS, et al. (1998) Double-blind randomised controlled trial of monoclonal antibody to human tumour necrosis factor in treatment of septic shock. The Lancet 351: 929-933. (Pubitemid 28138465)
21. Abraham E, Wunderink R, Silverman H, Perl TM, Nasraway S, et al. (1995) Efficacy and safety of monoclonal antibody to human tumor necrosis factor α in patients with sepsis syndrome. JAMA: the journal of the American Medical Association 273: 934-941.
22. Fisher Jr CJ, Dhainaut J-FA, Opal SM, Pribble JP, Balk RA, et al. (1994) Recombinant human interleukin 1 receptor antagonist in the treatment of patients with sepsis syndrome. JAMA: the journal of the American Medical Association 271: 1836-1843.
23. Pruitt JH, Copeland III EM, Moldawer LL (1995) Interleukin-1 and interleukin-1 antagonism in sepsis, systemic inflammatory response syndrome, and septic shock. Shock 3: 235-251.
24. Yan T, Li Q, Zhou H, Zhao Y, Yu S, et al. (2012) Gu-4 suppresses affinity and avidity modulation of CD11b and improves the outcome of mice with endotoxemia and sepsis. PloS one 7: e30110.
25. Zhao Z, Li Q, Hu J, Li Z, Liu J, et al. (2009) Lactosyl derivatives function in a rat model of severe burn shock by acting as antagonists against CD11b of integrin on leukocytes. Glycoconjugate journal 26: 173-188.
26. Orlova VV, Choi EY, Xie C, Chavakis E, Bierhaus A, et al. (2007) A novel pathway of HMGB1-mediated inflammatory cell recruitment that requires Mac-1-integrin. EMBO J 26: 1129-1139.
27. Li Q, Su B, Li H, Meng X-B, Cai M-S, et al. (2003) Synthesis and potential antimetastatic activity of monovalent and divalent β-d-galactopyranosyl-(1→4)-2-acetamido-2-deoxy-d-glucopyranosides. Carbohydrate research 338: 207-217. (Pubitemid 36120697)
28. Li H, Li Q, Cai M-S, Li Z-J (2000) Synthesis of galactosyl and lactosyl derivatives as potential anti-metastasis compounds. Carbohydrate research 328: 611-615.
29. Soriano FG, Lorigados CB, Pacher P, Szabó C (2011) Effects of a potent peroxynitrite decomposition catalyst in murine models of endotoxemia and sepsis. Shock (Augusta, Ga) 35: 560.
30. Hagiwara S, Iwasaka H, Hidaka S, Hishiyama S, Noguchi T (2008) Danaparoid sodium inhibits systemic inflammation and prevents endotoxin-induced acute lung injury in rats. Crit Care 12: R43.
31. Liu Z, Fan Y, Wang Y, Han C, Pan Y, et al. (2008) Dipyrithione inhibits lipopolysaccharide-induced iNOS and COX-2 up-regulation in macrophages and protects against endotoxic shock in mice. FEBS letters 582: 1643-1650.
32. Hubbard WJ, Choudhry M, Schwacha MG, Kerby JD, Rue III LW, et al. (2005) Cecal ligation and puncture. Shock 24: 52-57.
33. Ulloa L, Ochani M, Yang H, Tanovic M, Halperin D, et al. (2002) Ethyl pyruvate prevents lethality in mice with established lethal sepsis and systemic inflammation. Proceedings of the National Academy of Sciences 99: 12351.
34. Davé SH, Tilstra JS, Matsuoka K, Li F, DeMarco RA, et al. (2009) Ethyl pyruvate decreases HMGB1 release and ameliorates murine colitis. Journal of leukocyte biology 86: 633-643.
35. Yang H, Tracey KJ (2010) Targeting HMGB1 in inflammation. Biochimica et Biophysica Acta (BBA)-Gene Regulatory Mechanisms 1799: 149-156.
36. Fan J, Zhou H, Wang S, Wang H, Zhang Y, et al. (2012) Therapeutic effects of lactosyl derivative Gu-4 in a collagen-induced arthritis rat model. Glycoconjugate journal 29: 305-313.
37. Bianchi ME (2007) DAMPs, PAMPs and alarmins: all we need to know about danger. Journal of leukocyte biology 81: 1-5.
38. Bonaldi T, Talamo F, Scaffidi P, Ferrera D, Porto A, et al. (2003) Monocytic cells hyperacetylate chromatin protein HMGB1 to redirect it towards secretion. Science Signalling 22: 5551.
39. Harris HE, Raucci A (2006) Alarmin (g) news about danger. EMBO reports 7: 774-778.
40. Gao H-M, Zhou H, Zhang F, Wilson BC, Kam W, et al. (2011) HMGB1 acts on microglia Mac1 to mediate chronic neuroinflammation that drives progressive neurodegeneration. The Journal of Neuroscience 31: 1081-1092.
41. Kazama H, Ricci J-E, Herndon JM, Hoppe G, Green DR, et al. (2008) Induction of immunological tolerance by apoptotic cells requires caspase-dependent oxidation of high-mobility group box-1 protein. Immunity 29: 21-32. (Pubitemid 351952462)
42. Yang H, Ochani M, Li J, Qiang X, Tanovic M, et al. (2004) Reversing established sepsis with antagonists of endogenous high-mobility group box 1. Proceedings of the National Academy of Sciences 101: 296-301. (Pubitemid 38084244)
43. Li J, Kokkola R, Tabibzadeh S, Yang R, Ochani M, et al. (2003) Structural basis for the proinflammatory cytokine activity of high mobility group box 1. Molecular Medicine 9: 37.
44. Wang H, Liao H, Ochani M, Justiniani M, Lin X, et al. (2004) Cholinergic agonists inhibit HMGB1 release and improve survival in experimental sepsis. Nature medicine 10: 1216-1221. (Pubitemid 39540438)
45. Li W, Zhu S, Li J, Assa A, Jundoria A, et al. (2011) EGCG stimulates autophagy and reduces cytoplasmic HMGB1 levels in endotoxin-stimulated macrophages. Biochemical pharmacology 81: 1152-1163.
46. Li W, Li J, Ashok M, Wu R, Chen D, et al. (2007) A cardiovascular drug rescues mice from lethal sepsis by selectively attenuating a late-acting proinflammatory mediator, high mobility group box 1. The Journal of Immunology 178: 3856-3864. (Pubitemid 46417655)