Withaferin A is an inhibitor of endothelial protein C receptor shedding in vitro and in vivo

Food and Chemical Toxicology

Volumn 68, Issue , 2014, Pages 23-29

  Ku, Sae Kwang ^a   Han, Min Su ^b   Bae, Jong Sup ^c  

^a Daegu Haany University   (South Korea)

^b Daegu Fatima Hospital   (South Korea)

^c Kyungpook National University   (South Korea)

Author keywords

CLP; EPCR shedding; PMA; Withaferin A

Indexed keywords

ENDOTHELIAL PROTEIN C RECEPTOR; INTERLEUKIN 1BETA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; PHORBOL 13 ACETATE 12 MYRISTATE; STRESS ACTIVATED PROTEIN KINASE; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR ALPHA CONVERTING ENZYME; WITHAFERIN A; ACTIVATED PROTEIN C RECEPTOR; ADAM PROTEIN; ANTIINFLAMMATORY AGENT; BLOOD CLOTTING FACTOR; CELL SURFACE RECEPTOR; PHORBOLOL MYRISTATE ACETATE; TUMOR NECROSIS FACTOR-ALPHA CONVERTASE; WITHANOLIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ANTISEPSIS; AREA UNDER THE CURVE; ARTICLE; CONTROLLED STUDY; DRUG EFFECT; DRUG HALF LIFE; ENZYME ACTIVITY; EXPERIMENTAL LIGATION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MALE; MAXIMUM PLASMA CONCENTRATION; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN SHEDDING; SEPTICEMIA; SIGNAL TRANSDUCTION; UMBILICAL VEIN ENDOTHELIAL CELL; ANALOGS AND DERIVATIVES; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; DRUG EFFECTS; METABOLISM; PHOSPHORYLATION;

ADAM PROTEINS; ANIMALS; ANTI-INFLAMMATORY AGENTS; BLOOD COAGULATION FACTORS; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; INTERLEUKIN-1BETA; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MALE; MICE; MICE, INBRED C57BL; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; RECEPTORS, CELL SURFACE; SIGNAL TRANSDUCTION; TETRADECANOYLPHORBOL ACETATE; TUMOR NECROSIS FACTOR-ALPHA; WITHANOLIDES;

EID: 84897077244     PISSN: 02786915     EISSN: 18736351     Source Type: Journal    
DOI: 10.1016/j.fct.2014.03.009     Document Type: Article

References (44)

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. Bae J.S., Rezaie A.R. Activated protein C inhibits high mobility group box 1 signaling in endothelial cells. Blood 2011, 118:3952-3959.
3. Bae J.S., Yang L., Rezaie A.R. Receptors of the protein C activation and activated protein C signaling pathways are colocalized in lipid rafts of endothelial cells. Proc. Natl. Acad. Sci. USA 2007, 104:2867-2872.
4. Black R.A., Rauch C.T., Kozlosky C.J., Peschon J.J., Slack J.L., Wolfson M.F., Castner B.J., Stocking K.L., Reddy P., Srinivasan S., Nelson N., Boiani N., Schooley K.A., Gerhart M., Davis R., Fitzner J.N., Johnson R.S., Paxton R.J., March C.J., Cerretti D.P. A metalloproteinase disintegrin that releases tumour-necrosis factor-alpha from cells. Nature 1997, 385:729-733.
5. Blobel C.P. ADAMs: key components in EGFR signalling and development. Nat. Rev. Mol. Cell Biol. 2005, 6:32-43.
6. Borgel D., Bornstain C., Reitsma P.H., Lerolle N., Gandrille S., Dali-Ali F., Esmon C.T., Fagon J.Y., Aiach M., Diehl J.L. A comparative study of the protein C pathway in septic and nonseptic patients with organ failure. Am. J. Respir. Crit. Care Med. 2007, 176:878-885.
7. Buras J.A., Holzmann B., Sitkovsky M. Animal models of sepsis: setting the stage. Nat. Rev. Drug Discov. 2005, 4:854-865.
8. Buxbaum J.D., Liu K.N., Luo Y., Slack J.L., Stocking K.L., Peschon J.J., Johnson R.S., Castner B.J., Cerretti D.P., Black R.A. Evidence that tumor necrosis factor alpha converting enzyme is involved in regulated alpha-secretase cleavage of the Alzheimer amyloid protein precursor. J. Biol. Chem. 1998, 273:27765-27767.
9. Esmon C.T. The interactions between inflammation and coagulation. Br. J. Haematol. 2005, 131:417-430.
10. Essawi T., Srour M. Screening of some Palestinian medicinal plants for antibacterial activity. J. Ethnopharmacol. 2000, 70:343-349.
11. Fingleton B. MMPs as therapeutic targets-still a viable option?. Semin. Cell Dev. Biol. 2008, 19:61-68.
12. Fukudome K., Esmon C.T. Identification, cloning, and regulation of a novel endothelial cell protein C/activated protein C receptor. J. Biol. Chem. 1994, 269:26486-26491.
13. Fulcher C.A., Gardiner J.E., Griffin J.H., Zimmerman T.S. Proteolytic inactivation of human factor VIII procoagulant protein by activated human protein C and its analogy with factor V. Blood 1984, 63:486-489.
14. Han H., Du B., Pan X., Liu J., Zhao Q., Lian X., Qian M., Liu M. CADPE inhibits PMA-stimulated gastric carcinoma cell invasion and matrix metalloproteinase-9 expression by FAK/MEK/ERK-mediated AP-1 activation. Mol. Cancer Res. 2010, 8:1477-1488.
15. Hayashi T., Nakamura H., Okada A., Takebayashi S., Wakita T., Yuasa H., Okumura K., Suzuki K. Organization and chromosomal localization of the human endothelial protein C receptor gene. Gene 1999, 238:367-373.
16. Huovila A.P., Turner A.J., Pelto-Huikko M., Karkkainen I., Ortiz R.M. Shedding light on ADAM metalloproteinases. Trends Biochem. Sci. 2005, 30:413-422.
17. Kaileh M., Vanden Berghe W., Heyerick A., Horion J., Piette J., Libert C., De Keukeleire D., Essawi T., Haegeman G. Withaferin A strongly elicits IkappaB kinase beta hyperphosphorylation concomitant with potent inhibition of its kinase activity. J. Biol. Chem. 2007, 282:4253-4264.
18. Kim D.C., Lee W., Bae J.S. Vascular anti-inflammatory effects of curcumin on HMGB1-mediated responses in vitro. Inflamm. Res. 2011, 60:1161-1168.
19. Kremer J.P., Jarrar D., Steckholzer U., Ertel W. Interleukin-1, -6 and tumor necrosis factor-alpha release is down-regulated in whole blood from septic patients. Acta Haematol. 1996, 95:268-273.
20. Kurosawa S., Stearns-Kurosawa D.J., Hidari N., Esmon C.T. Identification of functional endothelial protein C receptor in human plasma. J. Clin. Invest. 1997, 100:411-418.
21. Kurosawa S., Stearns-Kurosawa D.J., Carson C.W., D'Angelo A., Della Valle P., Esmon C.T. Plasma levels of endothelial cell protein C receptor are elevated in patients with sepsis and systemic lupus erythematosus: lack of correlation with thrombomodulin suggests involvement of different pathological processes. Blood 1998, 91:725-727.
22. Lee D.C., Sunnarborg S.W., Hinkle C.L., Myers T.J., Stevenson M.Y., Russell W.E., Castner B.J., Gerhart M.J., Paxton R.J., Black R.A., Chang A., Jackson L.F. TACE/ADAM17 processing of EGFR ligands indicates a role as a physiological convertase. Ann. NY. Acad. Sci. 2003, 995:22-38.
23. 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.
24. Lee W., Ku S.K., Bae J.S. Emodin-6-O-beta-D-glucoside down-regulates endothelial protein C receptor shedding. Arch. Pharm. Res. 2013, 36:1160-1165.
25. Leng Y., Steiler T.L., Zierath J.R. Effects of insulin, contraction, and phorbol esters on mitogen-activated protein kinase signaling in skeletal muscle from lean and ob/ob mice. Diabetes 2004, 53:1436-1444.
26. Liaw P.C., Neuenschwander P.F., Smirnov M.D., Esmon C.T. Mechanisms by which soluble endothelial cell protein C receptor modulates protein C and activated protein C function. J. Biol. Chem. 2000, 275:5447-5452.
27. Menschikowski M., Hagelgans A., Eisenhofer G., Siegert G. Regulation of endothelial protein C receptor shedding by cytokines is mediated through differential activation of MAP kinase signaling pathways. Exp. Cell Res. 2009, 315:2673-2682.
28. Michie H.R., Manogue K.R., Spriggs D.R., Revhaug A., O'Dwyer S., Dinarello C.A., Cerami A., Wolff S.M., Wilmore D.W. Detection of circulating tumor necrosis factor after endotoxin administration. N. Engl. J. Med. 1988, 318:1481-1486.
29. Miller M.A., Meyer A.S., Beste M.T., Lasisi Z., Reddy S., Jeng K.W., Chen C.H., Han J., Isaacson K., Griffith L.G., Lauffenburger D.A. ADAM-10 and -17 regulate endometriotic cell migration via concerted ligand and receptor shedding feedback on kinase signaling. Proc. Natl. Acad. Sci. USA 2013, 110:E2074-E2083.
30. Mosnier L.O., Zlokovic B.V., Griffin J.H. The cytoprotective protein C pathway. Blood 2007, 109:3161-3172.
31. Moss M.L., Lambert M.H. Shedding of membrane proteins by ADAM family proteases. Essays Biochem. 2002, 38:141-153.
32. Murphy G. The ADAMs: signalling scissors in the tumour microenvironment. Nat. Rev. Cancer 2008, 8:929-941.
33. Qu D., Wang Y., Song Y., Esmon N.L., Esmon C.T. The Ser219 Gly dimorphism of the endothelial protein C receptor contributes to the higher soluble protein levels observed in individuals with the A3 haplotype. J. Thromb. Haemost. 2006, 4:229-235.
34. Qu D., Wang Y., Esmon N.L., Esmon C.T. Regulated endothelial protein C receptor shedding is mediated by tumor necrosis factor-alpha converting enzyme/ADAM17. J. Thromb. Haemost. 2007, 5:395-402.
35. Scaldaferri F., Sans M., Vetrano S., Graziani C., De Cristofaro R., Gerlitz B., Repici A., Arena V., Malesci A., Panes J., Grinnell B.W., Danese S. Crucial role of the protein C pathway in governing microvascular inflammation in inflammatory bowel disease. J. Clin. Invest. 2007, 117:1951-1960.
36. Sesin C.A., Yin X., Esmon C.T., Buyon J.P., Clancy R.M. Shedding of endothelial protein C receptor contributes to vasculopathy and renal injury in lupus: in vivo and in vitro evidence. Kidney Int. 2005, 68:110-120.
37. Simmonds R.E., Lane D.A. Structural and functional implications of the intron/exon organization of the human endothelial cell protein C/activated protein C receptor (EPCR) gene: comparison with the structure of CD1/major histocompatibility complex alpha1 and alpha2 domains. Blood 1999, 94:632-641.
38. Thalhamer T., McGrath M.A., Harnett M.M. MAPKs and their relevance to arthritis and inflammation. Rheumatology (Oxford) 2008, 47:409-414.
39. Villoutreix B.O., Blom A.M., Dahlback B. Structural prediction and analysis of endothelial cell protein C/activated protein C receptor. Protein Eng. 1999, 12:833-840.
40. 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.
41. Ware L.B., Camerer E., Welty-Wolf K., Schultz M.J., Matthay M.A. Bench to bedside: targeting coagulation and fibrinolysis in acute lung injury. Am. J. Physiol. Lung Cell Mol. Physiol. 2006, 291:L307-L311.
42. Xu J., Qu D., Esmon N.L., Esmon C.T. Metalloproteolytic release of endothelial cell protein C receptor. J. Biol. Chem. 2000, 275:6038-6044.
43. Yang H., Ochani M., Li J., Qiang X., Tanovic M., Harris H.E., Susarla S.M., Ulloa L., Wang H., DiRaimo R., Czura C.J., Roth J., Warren H.S., Fink M.P., Fenton M.J., Andersson U., Tracey K.J. Reversing established sepsis with antagonists of endogenous high-mobility group box 1. Proc. Natl. Acad. Sci. USA 2004, 101:296-301.
44. Zhang Y., Jiang J., Black R.A., Baumann G., Frank S.J. Tumor necrosis factor-alpha converting enzyme (TACE) is a growth hormone binding protein (GHBP) sheddase: the metalloprotease TACE/ADAM-17 is critical for (PMA-induced) GH receptor proteolysis and GHBP generation. Endocrinology 2000, 141:4342-4348.