Inhibition of microsomal prostaglandin E2synthase-1 as a molecular basis for the anti-inflammatory actions of boswellic acids from frankincense

British Journal of Pharmacology

Volumn 162, Issue 1, 2011, Pages 147-162

  Siemoneit, U ^a   Koeberle, A ^a   Rossi, Antonietta ^b   Dehm, F ^a   Verhoff, M ^a   Reckel, S ^c   Maier, T J ^c   Jauch, J ^d   Northoff, H ^e   Bernhard, F ^c   Doetsch, V ^c   Sautebin, L ^b   Werz, O ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^c GOETHE UNIVERSITY   (Germany)

^d SAARLAND UNIVERSITY   (Germany)

^e UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

Author keywords

arachidonic acid; boswellic acid; inflammation; prostaglandin

Indexed keywords

6 OXOPROSTAGLANDIN F1 ALPHA; BETA BOSWELLIC ACID; BOSWELLIC ACID; CARRAGEENAN; FRANKINCENSE; INDOMETACIN; LIPOPOLYSACCHARIDE; PLANT RESIN; PROSTAGLANDIN E2; PROSTAGLANDIN E2 SYNTHASE 1; PROSTAGLANDIN H2; PROSTAGLANDIN SYNTHASE; THROMBOXANE B2; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BINDING AFFINITY; CELL FREE SYSTEM; CONTROLLED STUDY; DRUG EFFICACY; DRUG STRUCTURE; ENZYME INHIBITION; HUMAN; HUMAN CELL; IC 50; IMMOBILIZATION; IN VITRO STUDY; IN VIVO STUDY; INHIBITION KINETICS; MALE; MOUSE; NONHUMAN; PAW EDEMA; PLEURISY; PRIORITY JOURNAL; PROSTAGLANDIN SYNTHESIS INHIBITION; SURFACE PLASMON RESONANCE;

EID: 78650114566     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/j.1476-5381.2010.01020.x     Document Type: Article

References (46)

1. Alexander SPH, Mathie A, Peters JA, (2009). Guide to receptors and channels (GRAC), 4th edn. Br J Pharmacol 158 (Suppl. 1): S1-S254.
2. Ammon HP, (2006). Boswellic acids in chronic inflammatory diseases. Planta Med 72: 1100-1116.
3. Asano K, Lilly CM, Drazen JM, (1996). Prostaglandin G/H synthase-2 is the constitutive and dominant isoform in cultured human lung epithelial cells. Am J Physiol 271: L126-L131. (Pubitemid 27369268)
4. Buchele B, Simmet T, (2003). Analysis of 12 different pentacyclic triterpenic acids from frankincense in human plasma by high-performance liquid chromatography and photodiode array detection. J Chromatogr B Analyt Technol Biomed Life Sci 795: 355-362.
5. Cheng Y, Wang M, Yu Y, Lawson J, Funk CD, Fitzgerald GA, (2006). Cyclooxygenases, microsomal prostaglandin E synthase-1, and cardiovascular function. J Clin Invest 116: 1391-1399.
6. Claveau D, Sirinyan M, Guay J, Gordon R, Chan CC, Bureau Y, et al. (2003). Microsomal prostaglandin E synthase-1 is a major terminal synthase that is selectively up-regulated during cyclooxygenase-2-dependent prostaglandin E2 production in the rat adjuvant-induced arthritis model. J Immunol 170: 4738-4744.
7. Funk CD, (2001). Prostaglandins and leukotrienes: advances in eicosanoid biology. Science 294: 1871-1875.
8. Gemmell DK, Cottney J, Lewis AJ, (1979). Comparative effects of drugs on four paw oedema models in the rat. Agents Actions 9: 107-116.
9. Giannetti AM, Koch BD, Browner MF, (2008). Surface plasmon resonance based assay for the detection and characterization of promiscuous inhibitors. J Med Chem 51: 574-580.
10. Guay J, Bateman K, Gordon R, Mancini J, Riendeau D, (2004). Carrageenan-induced paw edema in rat elicits a predominant prostaglandin E2 (PGE2) response in the central nervous system associated with the induction of microsomal PGE2 synthase-1. J Biol Chem 279: 24866-24872.
11. Harada Y, Tanaka K, Uchida Y, Ueno A, Oh-Ishi S, Yamashita K, et al. (1982). Changes in the levels of prostaglandins and thromboxane and their roles in the accumulation of exudate in rat carrageenin-induced pleurisy-a profile analysis using gas chromatography-mass spectrometry. Prostaglandins 23: 881-895.
12. Jakobsson PJ, Thoren S, Morgenstern R, Samuelsson B, (1999). Identification of human prostaglandin E synthase: a microsomal, glutathione-dependent, inducible enzyme, constituting a potential novel drug target. Proc Natl Acad Sci USA 96: 7220-7225.
13. Jauch J, Bergmann J, (2003). An efficient method for the large-scale preparation of 3-O-acetyl-11-oxo-beta-boswellic acid and other boswellic acids. Eur J Org Chem 24: 4752-4756.
14. Karlsson R, Falt A, (1997). Experimental design for kinetic analysis of protein-protein interactions with surface plasmon resonance biosensors. J Immunol Methods 200: 121-133.
15. Kawamura M, Hatanaka K, Saito M, Ogino M, Ono T, Ogino K, et al. (2000). Are the anti-inflammatory effects of dexamethasone responsible for inhibition of the induction of enzymes involved in prostanoid formation in rat carrageenin-induced pleurisy? Eur J Pharmacol 400: 127-135.
16. Koeberle A, Werz O, (2009). Inhibitors of the microsomal prostaglandin E(2) synthase-1 as alternative to non steroidal anti-inflammatory drugs (NSAIDs)-a critical review. Curr Med Chem 16: 4274-4296.
17. Koeberle A, Siemoneit U, Buehring U, Northoff H, Laufer S, Albrecht W, et al. (2008). Licofelone suppresses prostaglandin E2 formation by interference with the inducible microsomal prostaglandin E2 synthase-1. J Pharmacol Exp Ther 326: 975-982.
18. Koeberle A, Pollastro F, Northoff H, Werz O, (2009). Myrtucommulone, a natural acylphloroglucinol, inhibits microsomal prostaglandin E(2) synthase-1. Br J Pharmacol 156: 952-961.
19. Kruger P, Daneshfar R, Eckert GP, Klein J, Volmer DA, Bahr U, et al. (2008). Metabolism of boswellic acids in vitro and in vivo. Drug Metab Dispos 36: 1135-1142.
20. Kruger P, Kanzer J, Hummel J, Fricker G, Schubert-Zsilavecz M, Abdel-Tawab M, (2009). Permeation of Boswellia extract in the Caco-2 model and possible interactions of its constituents KBA and AKBA with OATP1B3 and MRP2. Eur J Pharm Sci 36: 275-284.
21. Kunnumakkara AB, Nair AS, Sung B, Pandey MK, Aggarwal BB, (2009). Boswellic acid blocks signal transducers and activators of transcription 3 signaling, proliferation, and survival of multiple myeloma via the protein tyrosine phosphatase SHP-1. Mol Cancer Res 7: 118-128.
22. Li X, Afif H, Cheng S, Martel-Pelletier J, Pelletier JP, Ranger P, et al. (2005). Expression and regulation of microsomal prostaglandin E synthase-1 in human osteoarthritic cartilage and chondrocytes. J Rheumatol 32: 887-895.
23. Murakami M, Nakatani Y, Tanioka T, Kudo I, (2002). Prostaglandin E synthase. Prostaglandins Other Lipid Mediat 68-69: 383-399.
24. Poeckel D, Werz O, (2006). Boswellic acids: biological actions and molecular targets. Curr Med Chem 13: 3359-3369.
25. Poeckel D, Tausch L, George S, Jauch J, Werz O, (2006a). 3-O-Acetyl-11-keto-boswellic acid decreases basal intracellular Ca2+ levels and inhibits agonist-induced Ca2+ mobilization and mitogen-activated protein kinase activation in human monocytic cells. J Pharmacol Exp Ther 316: 224-232.
26. Poeckel D, Tausch L, Kather N, Jauch J, Werz O, (2006b). Boswellic acids stimulate arachidonic acid release and 12-lipoxygenase activity in human platelets independent of Ca2+ and differentially interact with platelet-type 12-lipoxygenase. Mol Pharmacol 70: 1071-1078.
27. Roden LD, Myszka DG, (1996). Global analysis of a macromolecular interaction measured on BIAcore. Biochem Biophys Res Commun 225: 1073-1077.
28. Safayhi H, Mack T, Sabieraj J, Anazodo MI, Subramanian LR, Ammon HP, (1992). Boswellic acids: novel, specific, nonredox inhibitors of 5-lipoxygenase. J Pharmacol Exp Ther 261: 1143-1146.
29. Safayhi H, Rall B, Sailer ER, Ammon HP, (1997). Inhibition by boswellic acids of human leukocyte elastase. J Pharmacol Exp Ther 281: 460-463.
30. Samuelsson B, Morgenstern R, Jakobsson PJ, (2007). Membrane prostaglandin E synthase-1: a novel therapeutic target. Pharmacol Rev 59: 207-224.
31. Schwarz D, Klammt C, Koglin A, Lohr F, Schneider B, Dotsch V, et al. (2007). Preparative scale cell-free expression systems: new tools for the large scale preparation of integral membrane proteins for functional and structural studies. Methods 41: 355-369.
32. Sengupta K, Alluri KV, Satish AR, Mishra S, Golakoti T, Sarma KV, et al. (2008). A double blind, randomized, placebo controlled study of the efficacy and safety of 5-Loxin for treatment of osteoarthritis of the knee. Arthritis Res Ther 10: R85.
33. Siemoneit U, Hofmann B, Kather N, Lamkemeyer T, Madlung J, Franke L, et al. (2008). Identification and functional analysis of cyclooxygenase-1 as a molecular target of boswellic acids. Biochem Pharmacol 75: 503-513.
34. Siemoneit U, Pergola C, Jazzar B, Northoff H, Skarke C, Jauch J, et al. (2009). On the interference of boswellic acids with 5-lipoxygenase: mechanistic studies in vitro and pharmacological relevance. Eur J Pharmacol 606: 246-254.
35. Singh S, Khajuria A, Taneja SC, Khajuria RK, Singh J, Qazi GN, (2007). Boswellic acids and glucosamine show synergistic effect in preclinical anti-inflammatory study in rats. Bioorg Med Chem Lett 17: 3706-3711.
36. Singh S, Khajuria A, Taneja SC, Khajuria RK, Singh J, Johri RK, et al. (2008). The gastric ulcer protective effect of boswellic acids, a leukotriene inhibitor from Boswellia serrata, in rats. Phytomedicine 15: 408-415.
37. Smith WL, (1989). The eicosanoids and their biochemical mechanisms of action. Biochem J 259: 315-324.
38. Sterk V, Buchele B, Simmet T, (2004). Effect of food intake on the bioavailability of boswellic acids from a herbal preparation in healthy volunteers. Planta Med 70: 1155-1160.
39. Syrovets T, Buchele B, Krauss C, Laumonnier Y, Simmet T, (2005). Acetyl-boswellic acids inhibit lipopolysaccharide-mediated TNF-alpha induction in monocytes by direct interaction with IkappaB kinases. J Immunol 174: 498-506.
40. Tausch L, Henkel A, Siemoneit U, Poeckel D, Kather N, Franke L, et al. (2009). Identification of human cathepsin G as a functional target of boswellic acids from the anti-inflammatory remedy frankincense. J Immunol 183: 3433-3442.
41. Thoren S, Jakobsson PJ, (2000). Coordinate up- and down-regulation of glutathione-dependent prostaglandin E synthase and cyclooxygenase-2 in A549 cells. Inhibition by NS-398 and leukotriene C4. Eur J Biochem 267: 6428-6434.
42. Trebino CE, Stock JL, Gibbons CP, Naiman BM, Wachtmann TS, Umland JP, et al. (2003). Impaired inflammatory and pain responses in mice lacking an inducible prostaglandin E synthase. Proc Natl Acad Sci USA 100: 9044-9049.
43. Wang M, Zukas AM, Hui Y, Ricciotti E, Pure E, FitzGerald GA, (2006). Deletion of microsomal prostaglandin E synthase-1 augments prostacyclin and retards atherogenesis. Proc Natl Acad Sci USA 103: 14507-14512.
44. Werz O, Steinhilber D, (2006). Therapeutic options for 5-lipoxygenase inhibitors. Pharmacol Ther 112: 701-718.
45. Westman M, Korotkova M, Af Klint E, Stark A, Audoly LP, Klareskog L, et al. (2004). Expression of microsomal prostaglandin E synthase 1 in rheumatoid arthritis synovium. Arthritis Rheum 50: 1774-1780.
46. Xu D, Rowland SE, Clark P, Giroux A, Cote B, Guiral S, et al. (2008). MF63 [2-(6-chloro-1H-phenanthro[9,10-d]imidazol-2-yl)-isophthalonitrile], a selective microsomal prostaglandin E synthase-1 inhibitor, relieves pyresis and pain in preclinical models of inflammation. J Pharmacol Exp Ther 326: 754-763.