Anti-septic effects of glyceollins in HMGB1-induced inflammatory responses in vitro and in vivo

Food and Chemical Toxicology

Volumn 63, Issue , 2014, Pages 1-8

  Lee, Wonhwa ^a,b   Ku, Sae Kwang ^c   Lee, You Mie ^a   Bae, Jong Sup ^a  

^a Kyungpook National University   (South Korea)

^b Kyungpook National University School of Medicine   (South Korea)

^c Daegu Haany University   (South Korea)

Author keywords

Glyceollins; HMGB1; Inflammation; Sepsis

Indexed keywords

BACTERIUM LIPOPOLYSACCHARIDE; CELL ADHESION MOLECULE; GLYCEOLLIN DERIVATIVE; HIGH MOBILITY GROUP B1 PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 6; MITOGEN ACTIVATED PROTEIN KINASE 1; PLANT MEDICINAL PRODUCT; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIINFLAMMATORY ACTIVITY; ANTIMICROBIAL ACTIVITY; ARTICLE; CELL MEMBRANE PERMEABILITY; DRUG STRUCTURE; ENZYME ACTIVATION; ENZYME INHIBITION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATORY DISEASE; LEUKOCYTE ADHERENCE; LEUKOCYTE MIGRATION; MALE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN SYNTHESIS INHIBITION; STRUCTURE ANALYSIS; UMBILICAL VEIN ENDOTHELIAL CELL; VASCULITIS;

ASPERGILLUS SOJAE; MUS;

GLYCEOLLINS; HMGB1; INFLAMMATION; SEPSIS;

ANIMALS; CELLS, CULTURED; HMGB1 PROTEIN; HUMANS; INFLAMMATION; MICE; PTEROCARPANS; SEPSIS;

EID: 84887550545     PISSN: 02786915     EISSN: 18736351     Source Type: Journal    
DOI: 10.1016/j.fct.2013.10.034     Document Type: Article

References (61)

1. Aggarwal B.B., Ichikawa H., Garodia P., Weerasinghe P., Sethi G., Bhatt I.D., Pandey M.K., Shishodia S., Nair M.G. From traditional Ayurvedic medicine to modern medicine: identification of therapeutic targets for suppression of inflammation and cancer. Expert Opin. Ther. Targets 2006, 10:87-118.
2. Akeson A.L., Woods C.W. A fluorometric assay for the quantitation of cell adherence to endothelial cells. J. Immunol. Methods 1993, 163:181-185.
3. Andersson U., Tracey K.J. HMGB1 is a therapeutic target for sterile inflammation and infection. Annu. Rev. Immunol. 2011, 29:139-162.
4. Andersson U., Wang H., Palmblad K., Aveberger A.C., Bloom O., Erlandsson-Harris H., Janson A., Kokkola R., Zhang M., Yang H., Tracey K.J. High mobility group 1 protein (HMG-1) stimulates proinflammatory cytokine synthesis in human monocytes. J. Exp. Med. 2000, 192:565-570.
5. Andreu Ballester J.C., Ballester F., Gonzalez Sanchez A., Almela Quilis A., Colomer Rubio E., Penarroja Otero C. Epidemiology of sepsis in the Valencian Community (Spain), 1995-2004. Infect. Control Hosp. Epidemiol. 2008, 29:630-634.
6. Angus D.C., Wax R.S. Epidemiology of sepsis: an update. Crit. Care Med. 2001, 29:S109-116.
7. Bae J.S. Role of high mobility group box 1 in inflammatory disease: Focus on sepsis. Arch. Pharm. Res. 2012, 35:1511-1523.
8. Bae, J.W., Bae, J.S., 2011. Barrier protective effects of lycopene in human endothelial cells. Inflammat. Res.: Official J. European Histamine Res. Soc.. et al. 60, 751-758.
9. Bae J.S., Rezaie A.R. Activated protein C inhibits high mobility group box 1 signaling in endothelial cells. Blood 2011, 118:3952-3959.
10. Bianchi M.E., Manfredi A. Chromatin and cell death. Biochim. Biophys. Acta 2004, 1677:181-186.
11. Blackwell T.S., Christman J.W. Sepsis and cytokines: current status. Br. J. Anaesth. 1996, 77:110-117.
12. Boue S.M., Carter C.H., Ehrlich K.C., Cleveland T.E. Induction of the soybean phytoalexins coumestrol and glyceollin by Aspergillus. J. Agric. Food Chem. 2000, 48:2167-2172.
13. Branen L., Hovgaard L., Nitulescu M., Bengtsson E., Nilsson J., Jovinge S. Inhibition of tumor necrosis factor-alpha reduces atherosclerosis in apolipoprotein E knockout mice. Arterioscler. Thromb. Vasc. Biol. 2004, 24:2137-2142.
14. Buras J.A., Holzmann B., Sitkovsky M. Animal models of sepsis: setting the stage. Nat. Rev. Drug Discovery 2005, 4:854-865.
15. Calixto J.B., Campos M.M., Otuki M.F., Santos A.R. Anti-inflammatory compounds of plant origin. Part II. modulation of pro-inflammatory cytokines, chemokines and adhesion molecules. Planta Med. 2004, 70:93-103.
16. Che W., Lerner-Marmarosh N., Huang Q., Osawa M., Ohta S., Yoshizumi M., Glassman M., Lee J.D., Yan C., Berk B.C., Abe J. Insulin-like growth factor-1 enhances inflammatory responses in endothelial cells: role of Gab1 and MEKK3 in TNF-alpha-induced c-Jun and NF-kappaB activation and adhesion molecule expression. Circ. Res. 2002, 90:1222-1230.
17. Chen G., Li J., Ochani M., Rendon-Mitchell B., Qiang X., Susarla S., Ulloa L., Yang H., Fan S., Goyert S.M., Wang P., Tracey K.J., Sama A.E., Wang H. Bacterial endotoxin stimulates macrophages to release HMGB1 partly through CD14- and TNF-dependent mechanisms. J. Leukoc. Biol. 2004, 76:994-1001.
18. Chen G., Ward M.F., Sama A.E., Wang H. Extracellular HMGB1 as a proinflammatory cytokine. J. Interferon Cytokine Res.: Official J. Int. Soc. Interferon Cytokine Res. 2004, 24:329-333.
19. Choi J.H., Nguyen M.P., Jung S.Y., Kwon S.M., Jee J.G., Bae J.S., Lee S., Lee M.Y., Lee Y.M. Inhibitory effect of glyceollins on vasculogenesis through suppression of endothelial progenitor cell function. Mol. Nutr. Food Res. 2013.
20. Cohen J. The immunopathogenesis of sepsis. Nature 2002, 420:885-891.
21. Degryse B., Bonaldi T., Scaffidi P., Muller S., Resnati M., Sanvito F., Arrigoni G., Bianchi M.E. 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.
22. Dellinger R.P., Levy M.M., Carlet J.M., Bion J., Parker M.M., Jaeschke R., Reinhart K., Angus D.C., Brun-Buisson C., Beale R., Calandra T., Dhainaut J.F., Gerlach H., Harvey M., Marini J.J., Marshall J., Ranieri M., Ramsay G., Sevransky J., Thompson B.T., Townsend S., Vender J.S., Zimmerman J.L., Vincent J.L. Surviving Sepsis Campaign: international guidelines for management of severe sepsis and septic shock: 2008. Crit. Care Med. 2008, 36:296-327.
23. Dumitriu I.E., Baruah P., Bianchi M.E., Manfredi A.A., Rovere-Querini P. Requirement of HMGB1 and RAGE for the maturation of human plasmacytoid dendritic cells. Eur. J. Immunol. 2005, 35:2184-2190.
24. El Gazzar, M., 2007. HMGB1 modulates inflammatory responses in LPS-activated macrophages. Inflammat. Res.: Official J. European Histamine Res. Soc.. et al. 56, 162-167.
25. Fiuza C., Bustin M., Talwar S., Tropea M., Gerstenberger E., Shelhamer J.H., Suffredini A.F. Inflammation-promoting activity of HMGB1 on human microvascular endothelial cells. Blood 2003, 101:2652-2660.
26. Hori O., Brett J., Slattery T., Cao R., Zhang J., Chen J.X., Nagashima M., Lundh E.R., Vijay S., Nitecki D., Morser J., Stern D., Schmidt A.M. 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. 1995, 270:25752-25761.
27. Karlsson S., Pettila V., Tenhunen J., Laru-Sompa R., Hynninen M., Ruokonen E. HMGB1 as a predictor of organ dysfunction and outcome in patients with severe sepsis. Intensive Care Med. 2008, 34:1046-1053.
28. Kim I., Moon S.O., Kim S.H., Kim H.J., Koh Y.S., Koh G.Y. Vascular endothelial growth factor expression of intercellular adhesion molecule 1 (ICAM-1), vascular cell adhesion molecule 1 (VCAM-1), and E-selectin through nuclear factor-kappa B activation in endothelial cells. J. Biol. Chem. 2001, 276:7614-7620.
29. Kim, H.J., Sung, M.K., Kim, J.S., 2011. Anti-inflammatory effects of glyceollins derived from soybean by elicitation with Aspergillus sojae. Inflammat. Res.: Official J. European Histamine Res. Soc.. et al. 60, 909-917.
30. Kim T.H., Ku S.K., Lee I.C., Bae J.S. Anti-inflammatory functions of purpurogallin in LPS-activated human endothelial cells. BMB Rep. 2012, 45:200-205.
31. Lee J.D., Huh J.E., Jeon G., Yang H.R., Woo H.S., Choi D.Y., Park D.S. Flavonol-rich RVHxR from Rhus verniciflua Stokes and its major compound fisetin inhibits inflammation-related cytokines and angiogenic factor in rheumatoid arthritic fibroblast-like synovial cells and in vivo models. Int. Immunopharmacol. 2009, 9:268-276.
32. Lee W., Kim T.H., Ku S.K., Min K.J., Lee H.S., Kwon T.K., Bae J.S. Barrier protective effects of withaferin A in HMGB1-induced inflammatory responses in both cellular and animal models. Toxicol. Appl. Pharmacol. 2012, 262:91-98.
33. Lin W.N., Luo S.F., Wu C.B., Lin C.C., Yang C.M. Lipopolysaccharide induces VCAM-1 expression and neutrophil adhesion to human tracheal smooth muscle cells: involvement of Src/EGFR/PI3-K/Akt pathway. Toxicol. Appl. Pharmacol. 2008, 228:256-268.
34. Lockyer J.M., Colladay J.S., Alperin-Lea W.L., Hammond T., Buda A.J. Inhibition of nuclear factor-kappaB-mediated adhesion molecule expression in human endothelial cells. Circ. Res. 1998, 82:314-320.
35. Lotze M.T., Tracey K.J. High-mobility group box 1 protein (HMGB1): nuclear weapon in the immune arsenal. Nat. Rev. Immunol. 2005, 5:331-342.
36. Marui N., Offermann M.K., Swerlick R., Kunsch C., Rosen C.A., Ahmad M., Alexander R.W., Medford R.M. Vascular cell adhesion molecule-1 (VCAM-1) gene transcription and expression are regulated through an antioxidant-sensitive mechanism in human vascular endothelial cells. J. Clin. Investig. 1993, 92:1866-1874.
37. Mullins G.E., Sunden-Cullberg J., Johansson A.S., Rouhiainen A., Erlandsson-Harris H., Yang H., Tracey K.J., Rauvala H., Palmblad J., Andersson J., Treutiger C.J. Activation of human umbilical vein endothelial cells leads to relocation and release of high-mobility group box chromosomal protein 1. Scand. J. Immunol. 2004, 60:566-573.
38. Ng T.B., Ye X.J., Wong J.H., Fang E.F., Chan Y.S., Pan W., Ye X.Y., Sze S.C., Zhang K.Y., Liu F., Wang H.X. Glyceollin, a soybean phytoalexin with medicinal properties. Appl. Microbiol. Biotechnol. 2011, 90:59-68.
39. Palumbo R., Galvez B.G., Pusterla T., De Marchis F., Cossu G., Marcu K.B., Bianchi M.E. Cells migrating to sites of tissue damage in response to the danger signal HMGB1 require NF-kappaB activation. J. Cell Biol. 2007, 179:33-40.
40. Park J.S., Arcaroli J., Yum H.K., Yang H., Wang H., Yang K.Y., Choe K.H., Strassheim D., Pitts T.M., Tracey K.J., Abraham E. Activation of gene expression in human neutrophils by high mobility group box 1 protein. Am. J. Physiol. Cell Physiol. 2003, 284:C870-879.
41. Park J.S., Svetkauskaite D., He Q., Kim J.Y., Strassheim D., Ishizaka A., Abraham E. 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.
42. Park J.S., Gamboni-Robertson F., He Q., Svetkauskaite D., Kim J.Y., Strassheim D., Sohn J.W., Yamada S., Maruyama I., Banerjee A., Ishizaka A., Abraham E. High mobility group box 1 protein interacts with multiple Toll-like receptors. Am. J. Physiol. Cell Physiol. 2006, 290:C917-924.
43. Pinsky M.R., Vincent J.L., Deviere J., Alegre M., Kahn R.J., Dupont E. Serum cytokine levels in human septic shock. Relation to multiple-system organ failure and mortality. Chest 1993, 103:565-575.
44. Qin Y.H., Dai S.M., Tang G.S., Zhang J., Ren D., Wang Z.W., Shen Q. 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.
45. Qureshi S.H., Manithody C., Bae J.S., Yang L., Rezaie A.R. Autolysis loop restricts the specificity of activated protein C: analysis by FRET and functional assays. Biophys. Chem. 2008, 134:239-245.
46. Ranieri V.M., Thompson B.T., Barie P.S., Dhainaut J.F., Douglas I.S., Finfer S., Gardlund B., Marshall J.C., Rhodes A., Artigas A., Payen D., Tenhunen J., Al-Khalidi H.R., Thompson V., Janes J., Macias W.L., Vangerow B., Williams M.D. Drotrecogin alfa (activated) in adults with septic shock. N Engl. J. Med. 2012, 366:2055-2064.
47. Rose B.A., Force T., Wang Y. Mitogen-activated protein kinase signaling in the heart: angels versus demons in a heart-breaking tale. Physiol. Rev. 2010, 90:1507-1546.
48. Ruiz-Torres M.P., Perez-Rivero G., Rodriguez-Puyol M., Rodriguez-Puyol D., Diez-Marques M.L. The leukocyte-endothelial cell interactions are modulated by extracellular matrix proteins. Cell Physiol. Biochem. 2006, 17:221-232.
49. Sama A.E., D'Amore J., Ward M.F., Chen G., Wang H. Bench to bedside: HMGB1-a novel proinflammatory cytokine and potential therapeutic target for septic patients in the emergency department. Acad. Emerg. Med.: Official J. Soc. Acad. Emerg. Med. 2004, 11:867-873.
50. Sluiter W., Pietersma A., Lamers J.M., Koster J.F. Leukocyte adhesion molecules on the vascular endothelium: their role in the pathogenesis of cardiovascular disease and the mechanisms underlying their expression. J. Cardiovasc. Pharmacol. 1993, 22(Suppl. 4):S37-44.
51. Spiecker M., Darius H., Liao J.K. A functional role of I kappa B-epsilon in endothelial cell activation. J. Immunol. 2000, 164:3316-3322.
52. Sun C., Liang C., Ren Y., Zhen Y., He Z., Wang H., Tan H., Pan X., Wu Z. Advanced glycation end products depress function of endothelial progenitor cells via p38 and ERK 1/2 mitogen-activated protein kinase pathways. Basic Res. Cardiol. 2009, 104:42-49.
53. Takeda R., Suzuki E., Satonaka H., Oba S., Nishimatsu H., Omata M., Fujita T., Nagai R., Hirata Y. Blockade of endogenous cytokines mitigates neointimal formation in obese Zucker rats. Circulation 2005, 111:1398-1406.
54. Treutiger C.J., Mullins G.E., Johansson A.S., Rouhiainen A., Rauvala H.M., Erlandsson-Harris H., Andersson U., Yang H., Tracey K.J., Andersson J., Palmblad J.E. High mobility group 1 B-box mediates activation of human endothelium. J. Int. Med. 2003, 254:375-385.
55. Wang X., Feuerstein G.Z., Gu J.L., Lysko P.G., Yue T.L. Interleukin-1 beta induces expression of adhesion molecules in human vascular smooth muscle cells and enhances adhesion of leukocytes to smooth muscle cells. Atherosclerosis 1995, 115:89-98.
56. Wang H., Liao H., Ochani M., Justiniani M., Lin X., Yang L., Al-Abed Y., Metz C., Miller E.J., Tracey K.J., Ulloa L. Cholinergic agonists inhibit HMGB1 release and improve survival in experimental sepsis. Nat. Med. 2004, 10:1216-1221.
57. Wolfson R.K., Chiang E.T., Garcia J.G. HMGB1 induces human lung endothelial cell cytoskeletal rearrangement and barrier disruption. Microvasc. Res. 2011, 81:189-197.
58. Yang H., Tracey K.J. Targeting HMGB1 in inflammation. Biochim. Biophys. Acta 2010, 1799:149-156.
59. Yang H., Wang H., Czura C.J., Tracey K.J. The cytokine activity of HMGB1. J. Leukoc. Biol. 2005, 78:1-8.
60. Yang R., Harada T., Mollen K.P., Prince J.M., Levy R.M., Englert J.A., Gallowitsch-Puerta M., Yang L., Yang H., Tracey K.J., Harbrecht B.G., Billiar T.R., Fink M.P. Anti-HMGB1 neutralizing antibody ameliorates gut barrier dysfunction and improves survival after hemorrhagic shock. Mol. Med. 2006, 12:105-114.
61. Yoon E.K., Kim H.K., Cui S., Kim Y.H., Lee S.H. Soybean glyceollins mitigate inducible nitric oxide synthase and cyclooxygenase-2 expression levels via suppression of the NF-kappaB signaling pathway in RAW 264.7 cells. Int. J. Mol. Med. 2012, 29:711-717.