Heparin inhibits the inflammatory response induced by LPS and HMGB1 by blocking the binding of HMGB1 to the surface of macrophages

Cytokine

Volumn 72, Issue 1, 2015, Pages 36-42

  Li, Li ^a   Ling, Yan ^a   Huang, Min ^a   Yin, Tao ^a   Gou, Shan Miao ^a   Zhan, Nai Yang ^a   Xiong, Jiong Xin ^a   Wu, He Shui ^a   Yang, Zhi Yong ^a   Wang, Chun You ^a  

^a HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

Author keywords

Heparin; High mobility group box 1 protein; Lipopolysaccharide; Mitogen activated protein kinase; Tumour necrosis factor

Indexed keywords

HEPARIN; HIGH MOBILITY GROUP B1 PROTEIN; LIPOPOLYSACCHARIDE; MITOGEN ACTIVATED PROTEIN KINASE P38; TUMOR NECROSIS FACTOR ALPHA; MITOGEN ACTIVATED PROTEIN KINASE 3;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CELL SURFACE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DRUG EFFICACY; ENZYME ACTIVATION; ENZYME REPRESSION; LETHALITY; MACROPHAGE; MALE; MOUSE; MOUSE MODEL; NONHUMAN; PROTEIN BINDING; PROTEIN INDUCTION; PROTEIN PHOSPHORYLATION; SEPSIS; TREATMENT OUTCOME; ANIMAL; C57BL MOUSE; CELL LINE; DISEASE MODEL; DRUG EFFECTS; IMMUNOLOGY; INFLAMMATION; METABOLISM; PHOSPHORYLATION; SIGNAL TRANSDUCTION;

MURINAE; MUS;

ANIMALS; CELL LINE; DISEASE MODELS, ANIMAL; ENZYME ACTIVATION; HEPARIN; HMGB1 PROTEIN; INFLAMMATION; LIPOPOLYSACCHARIDES; MACROPHAGES; MAP KINASE SIGNALING SYSTEM; MICE; MICE, INBRED C57BL; MITOGEN-ACTIVATED PROTEIN KINASE 3; PHOSPHORYLATION; SEPSIS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84920286131     PISSN: 10434666     EISSN: 10960023     Source Type: Journal    
DOI: 10.1016/j.cyto.2014.12.010     Document Type: Article

References (48)

1. Wang H., Bloom O., Zhang M., Vishnubhakat J.M., Ombrellino M., Che J., et al. HMG-1 as a late mediator of endotoxin lethality in mice. Science 1999, 285:248-251.
2. Klune J.R., Dhupar R., Cardinal J., Billiar T.R., Tsung A. HMGB1: endogenous danger signaling. Mol Med 2008, 14:476-484.
3. Rauvala H., Rouhiainen A. Physiological and pathophysiological outcomes of the interactions of HMGB1 with cell surface receptors. Biochim Biophys Acta (BBA)-Gene Regul Mech 2010, 1799:164-170.
4. Sims G., Rowe D., Rietdijk S., Herbst R., Coyle A. HMGBl and RAGE in inflammation and cancer. Annu Rev Immunol 2010, 281367-281388.
5. Andersson U., Wang H., Palmblad K., Aveberger A.C., Bloom O., Erlandsson-Harris H., et al. High mobility group 1 protein (HMG-1) stimulates proinflammatory cytokine synthesis in human monocytes. J Exp Med 2000, 192:565-570.
6. Park J.S., Arcaroli J., Yum H.-K., Yang H., Wang H., Yang K.-Y., et al. Activation of gene expression in human neutrophils by high mobility group box 1 protein. Am J Physiol-Cell Physiol 2003, 284:C870-C879.
7. Kalinina N., Agrotis A., Antropova Y., DiVitto G., Kanellakis P., Kostolias G., 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.
8. Yang H., Wang H., Czura C.J., Tracey K.J. The cytokine activity of HMGB1. J Leukoc Biol 2005, 78:1-8.
9. Park J.S., Svetkauskaite D., He Q., Kim J.Y., Strassheim D., Ishizaka A., et al. Involvement of toll-like receptors 2 and 4 in cellular activation by high mobility group box 1 protein. J Biol Chem 2004, 279:7370-7377.
10. van Zoelen M.A., Yang H., Florquin S., Meijers J.C., Akira S., Arnold B., et al. 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 2009, 31:280-284.
11. Rouhiainen A., Tumova S., Valmu L., Kalkkinen N., Rauvala H. Pivotal advance: analysis of proinflammatory activity of highly purified eukaryotic recombinant HMGB1 (amphoterin). J Leukoc Biol 2007, 81:49-58.
12. Sha Y., Zmijewski J., Xu Z., Abraham E. HMGB1 develops enhanced proinflammatory activity by binding to cytokines. J Immunol 2008, 180:2531-2537.
13. Youn J.H., Oh Y.J., Kim E.S., Choi J.E., Shin J.-S. 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. J Immunol 2008, 180:5067-5074.
14. Hreggvidsdottir H.S., Östberg T., Wähämaa H., Schierbeck H., Aveberger A.-C., Klevenvall L., et al. The alarmin HMGB1 acts in synergy with endogenous and exogenous danger signals to promote inflammation. J Leukoc Biol 2009, 86:655-662.
15. Bianchi M.E. HMGB1 loves company. J Leukoc Biol 2009, 86:573-576.
16. Carr J. The anti-inflammatory action of heparin: heparin as an antagonist to histamine, bradykinin and prostaglandin E1. Thromb Res 1979, 16:507-516.
17. Niers T., Klerk C., DiNisio M., Van Noorden C., Büller H., Reitsma P., et al. Mechanisms of heparin induced anti-cancer activity in experimental cancer models. Crit Rev Oncol/Hematol 2007, 61:195-207.
18. Wang M., He J., Mei B., Ma X., Huo Z. Therapeutic effects and anti-inflammatory mechanisms of heparin on acute lung injury in rabbits. Acad Emerg Med 2008, 15:656-663.
19. Han J., Ding R., Zhao D., Zhang Z., Ma X. Unfractionated heparin attenuates lung vascular leak in a mouse model of sepsis: role of RhoA/Rho kinase pathway. Thromb Res 2013, 132:e42-e47.
20. Wildhagen K.C., de Frutos P.G., Reutelingsperger C.P., Schrijver R., Aresté C., Ortega-Gómez A., et al. Non-anticoagulant heparin prevents histone-mediated cytotoxicity in vitro and improves survival in sepsis. Blood 2014, 123:1098-1101.
21. Cornet A.D., Smit E.G., Beishuizen A., Groeneveld A.J. The role of heparin and allied compounds in the treatment of sepsis. Thromb Haemostasis-Stuttgart 2007, 98:579-586.
22. Ling Y., Yang Z.Y., Yin T., Li L., Yuan W.W., Wu H.S., et al. Heparin changes the conformation of high-mobility group protein 1 and decreases its affinity toward receptor for advanced glycation endproducts in vitro. Int Immunopharmacol 2011, 11:187-193.
23. Ding R., Zhao D., Guo R., Zhang Z., Ma X. Treatment with unfractionated heparin attenuates coagulation and inflammation in endotoxemic mice. Thromb Res 2011, 128:e160-e165.
24. Harris H.E., Andersson U., Pisetsky D.S. HMGB1: a multifunctional alarmin driving autoimmune and inflammatory disease. Nat Rev Rheumatol 2012, 8:195-202.
25. Johansson L., Snäll J., Sendi P., Linnér A., Thulin P., Linder A., et al. HMGB1 in severe soft tissue infections caused by Streptococcus pyogenes. Front Cell Infect Microbiol 2014, 4:4.
26. Lu B., Antoine D.J., Kwan K., Lundbäck P., Wähämaa H., Schierbeck H., et al. JAK/STAT1 signaling promotes HMGB1 hyperacetylation and nuclear translocation. Proc Natl Acad Sci 2014, 111:3068-3073.
27. Schiraldi M., Raucci A., Muñoz L.M., Livoti E., Celona B., Venereau E., et al. HMGB1 promotes recruitment of inflammatory cells to damaged tissues by forming a complex with CXCL12 and signaling via CXCR4. J Exp Med 2012, 209:551-563.
28. Ito Y., Bhawal U.K., Sasahira T., Toyama T., Sato T., Matsuda D., et al. Involvement of HMGB1 and RAGE in IL-1β-induced gingival inflammation. Arch Oral Biol 2012, 57:73-80.
29. Tian J., Avalos A.M., Mao S.Y., Chen B., Senthil K., Wu H., 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.
30. Palumbo R., Sampaolesi M., De Marchis F., Tonlorenzi R., Colombetti S., Mondino A., et al. Extracellular HMGB1, a signal of tissue damage, induces mesoangioblast migration and proliferation. J Cell Biol 2004, 164:441-449.
31. Yang H., Ochani M., Li J., Qiang X., Tanovic M., Harris H.E., et al. Reversing established sepsis with antagonists of endogenous high-mobility group box 1. Proc Natl Acad Sci USA 2004, 101:296-301.
32. Kokkola R., Li J., Sundberg E., Aveberger A.C., Palmblad K., Yang H., et al. Successful treatment of collagen-induced arthritis in mice and rats by targeting extracellular high mobility group box chromosomal protein 1 activity. Arthritis Rheum 2003, 48:2052-2058.
33. Yan S.F., Ramasamy R., Schmidt A.M. The RAGE axis a fundamental mechanism signaling danger to the vulnerable vasculature. Circ Res 2010, 106:842-853.
34. Liu S., Feng G., Wang G.-L., Liu G.-J. P38MAPK inhibition attenuates LPS-induced acute lung injury involvement of NF-κB pathway. Eur J Pharmacol 2008, 584:159-165.
35. Gao M., Chen L., Yu H., Sun Q., Kou J., Yu B. Diosgenin down-regulates NF-κB p65/p50 and p38MAPK pathways and attenuates acute lung injury induced by lipopolysaccharide in mice. Int Immunopharmacol 2013, 15:240-245.
36. Brewster J.L., de Valoir T., Dwyer N.D., Winter E., Gustin M.C. An osmosensing signal transduction pathway in yeast. Science 1993, 259:1760-1763.
37. Bannerman D.D., Goldblum S.E. Direct effects of endotoxin on the endothelium: barrier function and injury. Lab Invest 1999, 79:1181-1199.
38. Qin Y.H., Dai S.M., Tang G.S., Zhang J., Ren D., Wang Z.W., et al. HMGB1 enhances the proinflammatory activity of lipopolysaccharide by promoting the phosphorylation of MAPK p38 through receptor for advanced glycation end products. J Immunol 2009, 183:6244-6250.
39. Marianneau P., Steffan A.M., Royer C., Drouet M.T., Jaeck D., Kirn A., et al. Infection of primary cultures of human Kupffer cells by dengue virus: no viral progeny synthesis, but cytokine production is evident. J Virol 1999, 73:5201-5206.
40. Ndengele M.M., Bellone C.J., Lechner A.J., Matuschak G.M. Brief hypoxia differentially regulates LPS-induced IL-1β and TNF-α gene transcription in RAW 264.7 cells. Am J Physiol-Lung Cell and Mol Physiol 2000, 278:L1289-L1296.
41. Boilly B., Vercoutter-Edouart A., Hondermarck H., Nurcombe V., Le Bourhis X. FGF signals for cell proliferation and migration through different pathways. Cytokine Growth Factor Rev 2000, 11:295-302.
42. Hibi M., Lin A., Smeal T., Minden A., Karin M. Identification of an oncoprotein-and UV-responsive protein kinase that binds and potentiates the c-Jun activation domain. Genes Dev 1993, 7:2135-2148.
43. Davis R.J. Signal transduction by the JNK group of MAP kinases. Cell 2000, 103:239-252.
44. Yoon Y.M., Oh C.D., Kim D.Y., Lee Y.S., Park J.W., Huh T.L., et al. Epidermal growth factor negatively regulates chondrogenesis of mesenchymal cells by modulating the protein kinase C-α, Erk-1, and p38 MAPK signaling pathways. J Biol Chem 2000, 275:12353-12359.
45. Rendon-Mitchell B., Ochani M., Li J., Han J., Wang H., Yang H., et al. IFN-γ induces high mobility group box 1 protein release partly through a TNF-dependent mechanism. J Immunol 2003, 170:3890-3897.
46. Ma C.-Y., Jiao Y.-L., Zhang J., Yang Q.-R., Zhang Z.-F., Shen Y.-J., et al. Elevated plasma level of HMGB1 is associated with disease activity and combined alterations with IFN-alpha and TNF-alpha in systemic lupus erythematosus. Rheumatol Int 2012, 32:395-402.
47. Li W., Sama A.E., Wang H. Role of HMGB1 in cardiovascular diseases. Curr Opin Pharmacol 2006, 6:130-135.
48. Ito T., Kawahara K., Nakamura T., Yamada S., Abeyama K., Hashiguchi T., et al. High-mobility group box 1 protein promotes development of microvascular thrombosis in rats. J Thromb Haemost 2007, 5:109-116.