A pseudopterane diterpene isolated from the octocoral Pseudopterogorgia acerosa inhibits the inflammatory response mediated by TLR-ligands and TNF-alpha in macrophages

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  González, Yisett ^a,b   Doens, Deborah ^a,b   Santamaría, Ricardo ^a   Ramos, Marla ^a   Restrepo, Carlos M ^a,b   Barros De Arruda, Luciana ^c   Lleonart, Ricardo ^a   Gutiérrez, Marcelino ^a   Fernández, Patricia L ^a  

^a INSTITUTO DE INVESTIGACIONES CIENTÍFICAS Y SERVICIOS DE ALTA TECNOLOGÍA   (Panama)

^b ACHARYA NAGARJUNA UNIVERSITY   (India)

^c FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIINFLAMMATORY AGENT; B7 ANTIGEN; CD86 ANTIGEN; CELL PROTEIN; CYCLOOXYGENASE 2; DITERPENE; I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERFERON GAMMA INDUCED PROTEIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 6; LIGAND; MONOCYTE CHEMOTACTIC PROTEIN 1; NITRIC OXIDE; PSEUDOPTERANE; PSEUDOPTEROGORGIA ACEROSA EXTRACT; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 3; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CONTROLLED STUDY; CORAL; DRUG ISOLATION; FEMALE; MACROPHAGE ACTIVATION; MALE; MOUSE; NONHUMAN; PERITONEUM MACROPHAGE; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN SECRETION; PROTEIN SYNTHESIS INHIBITION; PSEUDOPTEROGORGIA ACEROSA; TRANSCRIPTION INITIATION;

ANIMALS; ANTHOZOA; ANTI-INFLAMMATORY AGENTS; ANTIGENS, CD80; ANTIGENS, CD86; CELLS, CULTURED; DITERPENES; ENZYME ACTIVATION; FEMALE; INFLAMMATION MEDIATORS; INTERLEUKIN-6; LIGANDS; LIPOPOLYSACCHARIDES; MACROPHAGE ACTIVATION; MACROPHAGES; MACROPHAGES, PERITONEAL; MALE; MICE; MITOGEN-ACTIVATED PROTEIN KINASES; NF-KAPPA B; TOLL-LIKE RECEPTORS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84892662082     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0084107     Document Type: Article

References (43)

1. Martinez FO, Helming L, Gordon S (2009) Alternative activation of macrophages: an immunologic functional perspective. Annu Rev Immunol 27: 451-483. doi:10.1146/annurev.immunol.021908.132532. PubMed: 19105661.
2. Kleinert H, Pautz A, Linker K, Schwarz PM (2004) Regulation of the expression of inducible nitric oxide synthase. Eur J Pharmacol 500: 255-266. doi:10.1016/j.ejphar.2004.07.030. PubMed: 15464038.
3. Doyle SL, O'Neill LA (2006) Toll-like receptors: from the discovery of NFkappaB to new insights into transcriptional regulations in innate immunity. Biochem Pharmacol 72: 1102-1113. doi:10.1016/j.bcp.2006.07.010. PubMed: 16930560.
4. de las Heras B, Hortelano S (2009) Molecular basis of the anti-inflammatory effects of terpenoids. Inflamm Allergy Drug Targets 8: 28-39. PubMed: 19275691.
5. Pahl HL (1999) Activators and target genes of Rel/NF-kappaB transcription factors. Oncogene 18: 6853-6866. doi:10.1038/sj.onc.1203239. PubMed: 10602461.
6. Karin M, Ben-Neriah Y (2000) Phosphorylation meets ubiquitination: The control of NF-κB activity. Annu Rev Immunol 18: 621-663. doi: 10.1146/annurev.immunol.18.1.621. PubMed: 10837071.
7. Karin M, Yamamoto Y, Wang QM (2004) The IKK NF-κB system: a treasure trove for drug development. Nat Rev Drug Discov 3: 17-26. doi:10.1038/nrd1279. PubMed: 14708018.
8. Newman DJ, Cragg GM (2007) Natural products as sources of new drugs over the last 25 years. J Nat Prod 70: 461-477. doi:10.1021/np068054v. PubMed: 17309302.
9. Medina RA, Goeger DE, Hills P, Mooberry SL, Huang N et al. (2008) Coibamide A, a Potent Antiproliferative Cyclic Depsipeptide from the Panamanian Marine Cyanobacterium Leptolyngbya sp. J Am Chem Soc 130: 6324-6325. doi:10.1021/ja801383f. PubMed: 18444611.
10. Hughes CC, MacMillan JB, Gaudêncio SP, Jensen PR, Fenical W (2009) The Ammosamides: Structures of Cell Cycle Modulators from a Marine-Derived Streptomyces Species. Angew Chem - Int Ed 48: 725-727. doi:10.1002/anie. 200804890.
11. Kondratyuk TP, Park E-J, Yu R, van Breemen RB, Asolkar RN et al. (2012) Novel Marine Phenazines as Potential Cancer Chemopreventive and Anti-Inflammatory Agents. Mar Drugs 10: 451-464. doi:10.3390/md10020451. PubMed: 22412812.
12. Blunt JW, Copp BR, Keyzers RA, Munro MHG, Prinsep MR (2013) Marine natural products. Nat Prod Rep 30: 237-323. doi:10.1039/c2np20112g. PubMed: 23263727.
13. Singh M, Pal M, Sharma RP (1999) Biological activity of the labdane diterpenes. Planta Med 65: 2-8. doi:10.1055/s-1999-13952. PubMed: 10083836.
14. Berrue F, Kerr RG (2009) Diterpenes from gorgian corals. Nat Prod Rep 26: 681-710. doi:10.1039/b821918b. PubMed: 19387501.
15. Wei W-C, Lin S-Y, Chen Y-J, Wen C-C, Huang C-Y et al. (2011) Topical application of marine briarane-type diterpenes effectively inhibits 12-O-ttetradecanoylphorbol-13-acetate-induced inflammation and dermatitis in murine skin. J Biomed Sci 18: 94-107. doi: 10.1186/1423-0127-18-94. PubMed: 22189182.
16. Oda T, Wewengkang DS, Kapojos MM, Mangindaan REP, Lee J-S, et al. (2011) Lobohedleeolide induces interleukin-8 production in LPS-stimulated human monocytic cell line THP-1. Int J App Res Nat Prod 4: 16-21
17. Quang TH, Ha TT, Minh CV, Kiem PV, Huong HT et al. (2011) Cytotoxic and anti-inflammatory cembranoids from the Vietnamese soft coral Lobophytum laevigatum. Bioorg Med Chem 19: 2625-2632. doi: 10.1016/j.bmc.2011.03.009. PubMed: 21458279.
18. Roethle PA, Trauner D (2008) The chemistry of marine furanocembranoids, pseudopteranes, gersolanes and related natural products. Nat Prod Rep 25: 298-317. doi:10.1039/b705660p. PubMed: 18389139.
19. Fenical W (1987) Marine soft corals of the genus Pseudopterogorgia: a resource for novel anti-inflammatory diterpenoids. J Nat Prod 50: 1001-1008. doi:10.1021/np50054a001. PubMed: 2895165.
20. Bandurraga MM, Fenical W, Donovan SF, Clardy J (1982) Pseudopterolide, an Irregular Diterpenoid with Unusual Cytotoxic Properties from the Caribbean Sea Whip Pseudopterogorgia acerosa (Palias) (Gorgonacea). J Am Chem Soc 104: 6463-6465. doi:10.1021/ja00387a059.
21. Tinto WF, John L, Reynolds WF, McLean S (1991) Novel pseudopteranoids of Pseudopterogorgia acerosa. Tetrahedron 47: 8679-8686. doi:10.1016/S0040-4020(01) 96190-3.
22. Kawai T, Akira S (2010) The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat Immunol 11: 373-384. doi:10.1038/ni.1863. PubMed: 20404851.
23. Girón N, Través PG, Rodríguez B, López-Fontal R, Boscá L et al. (2008) Suppression of inflammatory responses by labdane-type diterpenoids. Toxicol Appl Pharmacol 228: 179-189. doi:10.1016/j.taap.2007.12.006. PubMed: 18190942.
24. Van Gool SW, Vandenberghe P, De Boer M, Ceuppens JL (1996) CD80, CD86 and CD40 provide accessory signals in a multiple-step Tcell activation model. Immunol Rev 153: 47-83. doi:10.1111/j.1600-065X.1996.tb00920.x. PubMed: 9010719.
25. Hayden MS, Ghosh S (2012) NF-κB, the first quarter-century: remarkable progress and outstanding questions. Genes Dev 26: 203-234. doi:10.1101/gad.183434.111. PubMed: 22302935.
26. Figueiredo RT, Fernandez PL, Mourao-Sa DS, Porto BN, Dutra FF et al. (2007) Characterization of Heme as Activator of Toll-like Receptor 4. J Biol Chem 282: 20221-20229. doi:10.1074/jbc.M610737200. PubMed: 17502383.
27. Mateo CR, Prieto M, Micol V, Shapiro S, Villalaín J (2000) A fluorescence study of the interaction and location of (+)-totarol, a diterpenoid bioactive molecule, in model membranes. Biochim Biophys Acta 1509: 167-175. doi:10.1016/S0005-2736(00)00291-1. PubMed: 11118528.
28. Micol V, Mateo CR, Shapiro S, Aranda FJ, Villalaín J (2001) Effects of (+)-totarol, a diterpenoid antibacterial agent, on phospholipid model membranes. Biochim Biophys Acta 1511: 281-290. doi:10.1016/S0005-2736(01)00284- X. PubMed: 11286971.
29. Urzúa A, Rezende MC, Mascayano C, Vásquez L (2008) A Structure-Activity Study of Antibacterial Diterpenoids. Molecules 13: 882-891. doi: 10.3390/molecules13040822. PubMed: 18463590.
30. Lee J-H, Koo TH, Hwang BY, Lee JJ (2002) Kaurane Diterpene, Kamebakaurin, Inhibits NF-κB by directly targeting the DNA-binding activity of p50 and blocks the expression of antiapoptotic NF-κB target genes. J Biol Chem 277: 18411-18420. doi:10.1074/jbc.M201368200. PubMed: 11877450.
31. Amigó M, Payá M, Braza-Boïls A, De Rosa S, Terencio MC (2008) Avarol inhibits TNF-alpha generation and NF-kappaB activation in human cells and in animal models. Life Sci 82: 256-264. doi:10.1016/j.lfs.2007.11.017. PubMed: 18177902.
32. Folmer F, Jaspars M, Dicato M, Diederich M (2008) Marine natural products as targeted modulators of the transcription factor NFkappaB. Biochem Pharmacol 75: 603-617. doi:10.1016/j.bcp.2007.07.044. PubMed: 17919455.
33. Gupta SC, Kannappan R, Kim JH, Rahman GM, Francis SK et al. (2011) Bharangin, a diterpenoid quinonemethide, abolishes constitutive and inducible NF-κB activation by modifying p65 on cysteine 38 residue and inhibiting IκBα kinase activation, leading to suppression of NF-κB-regulated gene expression and sensitization of tumor cells to chemotherapeutic agents. Mol Pharmacol 80: 769-781. doi:10.1124/mol.111.073122. PubMed: 21795584.
34. Yang H, Di Chen, Cui QC, Yuan X, Dou QP (2006) Celastrol, a triterpene extracted from the chinese "Thunder of God Vine," is a potent proteasome inhibitor and suppresses human prostate cancer growth in nude mice. Cancer Res 66: 4758-4765. doi: 10.1158/0008-5472.CAN-05-4529. PubMed: 16651429.
35. Lu L, Kanwar J, Schmitt S, Cui QC, Zhang C et al. (2011) Inhibition of tumor cellular proteasome activity by triptolide extracted from the chinese medicinal plant 'Thunder God Vine'. Anticancer Res 31: 1-10. PubMed: 21273574.
36. Keshet Y, Seger R (2010) The MAP kinase signaling cascades: a system of hundreds of components regulates a diverse array of physiological functions. Methods Mol Biol 661: 3-38. doi: 10.1007/978-1-60761-795-2-1. PubMed: 20811974.
37. Chung JY, Park YC, Ye H, Wu H (2002) All TRAFs are not created equal: common and distinct molecular mechanisms of TRAF-mediated signal transduction. J Cell Sci 115: 679-688. PubMed: 11865024.
38. Oeckinghaus A, Hayden MS, Ghosh S (2011) Crosstalk in NF-κB signaling pathways. Nat Immunol 12: 695-708. doi:10.1038/nrm3207. PubMed: 21772278.
39. Lucas R, Casapullo A, Ciasullo L, Gomez-Paloma L, Payá M (2003) Cycloamphilectenes, a new type of potent marine diterpenes: inhibition of nitric oxide production in murine macrophages. Life Sci 72: 2543-2552. doi:10.1016/S0024-3205(03)00167-X. PubMed: 12650863.
40. Premkumar V, Dey M, Dorn R, Raskin I (2010) MyD88-dependent and independent pathways of Toll-Like Receptors are engaged in biological activity of Triptolide in ligand-stimulated macrophages. BMC Chem Biol 13: 3-16. PubMed: 20385024.
41. Crow MK (2006) Modification of accessory molecule signaling. Springer Semin Immunopathol 27: 409-424. doi:10.1007/s00281-006-0018-3. PubMed: 16738953.
42. Liu J, Wu Q-L, Feng Y-H, Wang Y-F, Li X-Y et al. (2005) Triptolide suppresses CD80 and CD86 expressions and IL-12 production in THP-1 cells. Acta Pharmacol Sin 26: 223-227. doi:10.1111/j.1745-7254.2005.00035.x. PubMed: 15663903.
43. Wang W, Wang J, Dong S-F, Liu C-H, Italiani P, et al. (2010) Immunomodulatory activity of andrographolide on macrophage activation and specific antibody response. Acta Pharmacol Sin 31: 191-201