Hop bitter acids efficiently block inflammation independent of GRα, PPARα, or PPARγ

Molecular Nutrition and Food Research

Volumn 53, Issue 9, 2009, Pages 1143-1155

  van Cleemput, Marjan ^a   Heyerick, Arne ^a   Libert, Claude ^a   Swerts, Katrien ^b   Philippé, Jan ^b   de Keukeleire, Denis ^a   Haegeman, Guy ^a   de Bosscher, Karolien ^a  

^a GHENT UNIVERSITY   (Belgium)

^b GHENT UNIVERSITY HOSPITAL   (Belgium)

Author keywords

Hop bitter acids; Humulus lupulus L.; Inflammation; NR B; Nuclear receptors

Indexed keywords

ANTIINFLAMMATORY AGENT; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; GLUCOCORTICOID RECEPTOR; GLUCOCORTICOID RECEPTOR ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 6; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; TRANSCRIPTION FACTOR AP 1;

ANIMAL; ARTICLE; BIOSYNTHESIS; C57BL MOUSE; CHEMISTRY; DRUG ANTAGONISM; DRUG EFFECT; FEMALE; GENETIC TRANSCRIPTION; HUMAN; HUMULUS; MOUSE; PHYSIOLOGY; TUMOR CELL LINE;

ANIMALS; ANTI-INFLAMMATORY AGENTS; CELL LINE, TUMOR; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; FEMALE; HUMANS; HUMULUS; INTERLEUKIN-6; MICE; MICE, INBRED C57BL; NF-KAPPA B; PPAR ALPHA; PPAR GAMMA; RECEPTORS, GLUCOCORTICOID; TRANSCRIPTION FACTOR AP-1; TRANSCRIPTION, GENETIC;

HUMULUS; HUMULUS LUPULUS;

EID: 70349635075     PISSN: 16134125     EISSN: 16134133     Source Type: Journal    
DOI: 10.1002/mnfr.200800493     Document Type: Article

References (56)

1. Udenigwe, C. C., Ramprasath, V. R., Aluko, R. E., Jones, P. J.H., Potential of resveratrol in anticancer and anti-inflamma-tory therapy, Nutr. Rev. 2008, 66, 445-454.
2. Joe, B., Vijaykumar, M., Lokesh, B. R., Biological propertiesof curcumin-cellular and molecular mechanisms of action, Crit. Rev. Food Sci. Nutr. 2004, 44, 97-111.
3. Surh, Y. J., Chun, K. S., Cha, H. H., Han, S. S., et al., Molecular mechanisms underlying chemopreventive activities ofanti-inflammatory phytochemicals: Down-regulation ofCOX-2 and iNOS through suppression of NF-kappa B activation, Mutat. Res. 2001, 480, 243-268.
4. Calixto, J. B., Otuki, M. F., Santos, A. R. S., Anti-inflammatory compounds of plant origin. Part I. Action on arachidonicacid pathway, nitric oxide and nuclear factor kappa B (NF-kappa B), Planta Med. 2003, 69, 973-983.
5. Calixto, J. B., Campos, M. M., Otuki, M. F., Santos, A. R. S., Anti-inflammatory compounds of plant origin. Part II. Modu-lation of pro-inflammatory cytokines, chemokines and adhe-sion molecules, Planta Med. 2004, 70, 93-103.
6. Bremner, P., Heinrich, M., Natural products as targeted modulators of the nuclear factor-kappa B pathway, J. Pharm. Pharmacol. 2002, 54, 453-472.
7. Barnes, P. J., Larin, M., Mechanisms of disease - Nuclear factor-kappa b - A pivotal transcription factor in chronicinflammatory diseases, N. Eng. J. Med. 1997, 336, 1066-1071.
8. Kumar, A., Takada, Y., Boriek, A. M., Aggarwal, B. B., Nuclear factor-kappa B: Its role in health and disease, J. Mol. Med. 2004, 82, 434-448.
9. Van den Berghe, W., Vermeulen, L., Delerive, P., De Bosscher, K. et al., A paradigm for gene regulation: Inflammation, NF-kappa B and PPAR, Adv. Exp. Med. Biol. 2003, 544, 181-196.
10. Hayden, M. S., Ghosh, S., Signaling to NF-kappa B, Genes. Dev. 2004, 18, 2195-2224.
11. Beck, I. M., Berghe, W. V., Vermeulen, L., Bougarne, N., et al., Altered subcellular distribution of MSK1 induced by glucocorticoids contributes to NF-kappa B inhibition, EMBO J.2008, 27, 1682-1693.
12. Pascual, G., Glass, C. K., Nuclear receptors versus inflammation: Mechanisms of transrepression, Trends Endocrinol. Metab. 2006, 17, 321-327.
13. Gossye, V., Haegeman, G., De Bosscher, K., Therapeuticimplications of the nuclear factor-kappaB/nuclear receptorcross-talk, Front. Biosci. 2008, 13, 4122-4143.
14. Staels, B., Koenig, W., Habib, A., Merval, R., et al., Activation of human aortic smooth-muscle cells is inhibited byPPAR alpha but not by PPAR gamma activators, Nature 1998, 393, 790-793.
15. Delerive, P., De Bosscher, K., Besnard, S., Van den Berghe, W., et al., Peroxisome proliferator-activated receptor alphanegatively regulates the vascular inflammatory gene responseby negative cross-talk with transcription factors NF-kappa Band AP-1, J. Biol. Chem. 1999, 274, 32048-32054.
16. Smoak, K. A., Cidlowski, J. A., Mechanisms of glucocorticoid receptor signaling during inflammation, Mech. Ageing Dev. 2004, 125, 697-706.
17. Forman, B. M., Chen, J., Evans, R. M., The peroxisome proliferator-activated receptors: Ligands and activators, Ann. NYAcad. Sci. 1996, 804, 266-275.
18. Haffner, S. M., Greenberg, A. S., Weston, W. M., Chen, H., et al., Effect of rosiglitazone treatment on nontraditionalmarkers of cardiovascular disease in patients with type 2 diabetes mellitus, Circulation 2002, 106, 679-684.
19. Madej, A., Okopien, B., Kowalski, J., Zielinski, M., et al., Effects of fenofibrate on plasma cytokine concentrations inpatients with atherosclerosis and hyperlipoproteinemia IIb. Int. J. Clin. Pharmacol. Ther. 1998, 36, 345-349.
20. De Bosscher, K., Van den Berghe, W., Haegeman, G., Crosstalk between nuclear receptors and nuclear factor kappa B, Oncogene 2006, 25, 6868-6886.
21. Simpson, W. J., Smith, A. R. W., Factors affecting antibacterial activity of hop compounds and their derivatives, J. Appl. Bacteriol. 1992, 72, 327-334.
22. Zanoli, P., Rivasi, M., Zavatti, M., Brusiani, F., Baraldi, M., New insight in the neuropharmacological activity of Humuluslupulus L., J. Ethnopharmacol. 2005, 102, 102-106.
23. Chadwick, L. R., Pauli, G. F., Farnsworth, N. R., The pharmacognosy of Humulus lupulus L. (hops) with an emphasis onestrogenic properties, Phytomedicine 2006, 13, 119-131.
24. Gerh user, C., Beer constituents as potential cancer chemopreventive agents, Eur. J. Cancer 2005, 41, 1941-1954.
25. Milligan, S. R., Kalita, J. C., Heyerick, A., Rong, H., et al., Identification of a potent phytoestrogen in hops (Humuluslupulus L.) and beer. J. Clin. Endocrinol. Metab. 1999, 84, 2249-2252.
26. De Keukeleire, D., Milligan, S. R., De Cooman, L., Heyerick, A., The oestrogenic activity of hops (Humulus lupulus L.)revisited, Pharm. Pharmacol. Lett. 1997, 7, 83-86.
27. De Keukeleire, D., Fundamentals of beer and hop chemistry, Quim. Nova. 2000, 23, 108-112.
28. Chinetti-Gbaguidi, G., Fruchart, J. C., Staels, B., Role of the PPAR family of nuclear receptors in the regulation of metabolic and cardiovascular homeostasis: New approaches totherapy, Curr. Opin. Pharmacol. 2005, 5, 177-183.
29. Imhof, A., Woodward, M., Doering, A., Helbecque, N., et al., Overall alcohol intake, beer, wine, and systemic markers ofinflammation in western Europe: Results from three MONICA samples (Augsburg, Glasgow, Lille), Eur. Heart J. 2004, 25, 2092-2100.
30. Winkler, C., Wirleitner, B., Schroecksnadel, K., Schennach, H., Fuchs, D., Beer down-regulates activated peripheral bloodmononuclear cells in vitro, Int. Immunopharmacol. 2006, 6, 390-395.
31. Shimamura, M., Hazato, T., Ashino, H., Yamamoto, Y., et al., Inhibition of angiogenesis by humulone, a bitter acid frombeer hop, Biochem. Biophys. Res. Commun. 2001, 289, 220-224.
32. Yasukawa, K., Takeuchi, M., Takido, M. H., A bitter in theHop, inhibits tumor promotion by 12-O-tetradecanoylphorbol-13-acetate in 2-stage carcinogenesis in mouse skin, Oncology 1995, 52, 156-158.
33. Lee, J. C., Kundu, J. K., Hwang, D. M., Na, H. K., Surh, Y. J., Humulone inhibits phorbol ester-induced COX-2 expressionin mouse skin by blocking activation of NF-{kappa}B andAP-1: I{kappa}B kinase and c-Jun-N-terminal kinase asrespective potential upstream targets, Carcinogenesis 2007, 28, 1491-1498.
34. Yamamoto, K., Wang, J. N., Yamamoto, S., Tobe, H., Suppression of cyclooxygenase-2 gene transcription by humulon, Adv. Exp. Med. Biol. 2002, 507, 73-77.
35. Smith, T. J., Insights into the role of fibroblasts in humanautoimmune diseases, Clin. Exp. Immunol. 2005, 141, 388-397.
36. De Bosscher, K., Schmitz, M. L., Van den Berghe, W., Plais-ance, S., et al., Glucocorticoid-mediated repression ofnuclear factor-kappaB-dependent transcription involvesdirect interference with transactivation, Proc. Natl. Acad. Sci. USA 1997, 94, 13504-13509.
37. Chinetti, G., Fruchart, J. C., Staels, B., Peroxisome proliferator-activated receptors (PPARs): New targets for the pharmacological modulation of macrophage gene expression andfunction, Curr. Opin. Cell Biol. 2003, 14, 459-468.
38. Verzele, M., De Keukeleire, D., Chemistry and Analysis ofHop and Beer Bitter Acids, Elsevier, Amsterdam 1991.
39. Plaisance, S., Vandenberghe, W., Boone, E., Fiers, W., Haegeman, G., Recombination signal sequence binding protein Jkappa is constitutively bound to the NF-kappa B site of theinterleukin-6 promoter and acts as a negative regulatory fac-tor, Mol. Cell Biol. 1997, 17, 3733-3743.
40. De Bosscher, K., Van den Berghe, W., Vermeulen, L., Plais-ance, S. et al., Glucocorticoids repress NF-kappaB-drivengenes by disturbing the interaction of p65 with the basal tran-scription machinery, irrespective of coactivator levels in thecell, Proc. Natl. Acad. Sci. USA 2000, 97, 3919-3924.
41. Van den Berghe, W., Plaisance, S., Boone, E., De Bosscher, K., et al., p38 and extracellular signal-regulated kinase mito-gen-activated protein kinase pathways are required fornuclear factor kappa B p65 transactivation mediated by tumornecrosis factor, J. Biol. Chem. 1998, 273, 3285-3290.
42. Van den Berghe, W., Vermeulen, L., De Wilde, G., De Bosscher, K., et al., Signal transduction by tumor necrosis factor and gene regulation of the inflammatory cytokineinterleukin-6, Biochem. Pharmacol. 2000, 60, 1185-1195.
43. Kishimoto, T., Interleukin-6: Discovery of a pleiotropic cytokine, Arthritis Res. Ther. 2006, 8, S2.
44. Goodman, R. H., Smolik, S., CBP/p300 in cell growth, transformation, and development, Genes Dev. 2000, 14, 1553-1577.
45. Shaulian, E., Karin, M., AP-1 as a regulator of cell life and death, Nat. Cell Biol. 2002, 4, E131-E136.
46. Shaulian, E., Karin, M., AP-1 in cell proliferation and survival, Oncogene 2001, 20, 2390-2400.
47. Van den Berghe, W., De Bosscher, K., Boone, E., Plaisance, S., Haegeman, G., The nuclear factor-kappa B engages CBP/p300 and histone acetyltransferase activity for transcriptionalactivation of the interleukin-6 gene promoter, J. Biol. Chem.1999, 274, 32091-32098.
48. Van den Berghe, W., Francesconi, E., De Bosscher, K., Resche-Rigon, M., Haegeman, G., Dissociated glucocorticoids with anti-inflammatory potential repress interleukin-6gene expression by a nuclear factor-kappa B-dependentmechanism, Mol. Pharmacol. 1999, 56, 797-806.
49. Marx, N., Kehrle, B., Kohlhammer, K., Grub, M., et al., PPAR activators as antiinflammatory mediators in human Tlymphocytes - Implications for atherosclerosis and trans-plantation-associated arteriosclerosis, Circ. Res. 2002, 90, 703-710.
50. Milligan, S. R., Kalita, J. C., Pocock, V., Van de Kauter, V. et al., The endocrine activities of 8-prenylnaringenin andrelated hop (Humulus lupulus L.) flavonoids, J. Clin. Endocrinol. Metab. 2000, 85, 4912-4915.
51. Hougee, S., Faber, J., Sanders, A., van den Berg, W. B., et al., Selective inhibition of COX-2 by a standardized CO2 extractof Humulus lupulus in vitro and its activity in a mouse modelof zymosan-induced arthritis, Planta Med. 2006, 72, 228-233.
52. Yasukawa, K., Yamaguchi, A., Arita, J., Sakurai, S., et al., Inhibitory effect of edible plant-extracts on 12-0-tetradecanoylphorbol-13-acetate-induced ear edema in mice. Phytother. Res. 1993, 7, 185-189.
53. Dijsselbloem, N., Van den Berghe, W., De Naeyer, A., Haegeman, G., Soy isoflavone phyto-pharmaceuticals in interleukin-6 affections multi-purpose nutraceuticals at the crossroadof hormone replacement, anti-cancer and anti-inflammatorytherapy, Biochem. Pharmacol. 2004, 68, 1171-1185.
54. Glass, C. K., Ogawa, S., Combinatorial roles of nuclearreceptors in inflammation and immunity, Immunology 2005, 6, 44-55.
55. De Bosscher, K., Van den Berghe, W., Haegeman, G., Theinterplay between the glucocorticoid receptor and nuclearfactor-kappa B or activator protein-1: Molecular mechanismsfor gene repression, Endocr. Rev. 2003, 24, 488-522.
56. Bachert, C., Watelet, J. B., Gevaert, P., Van Cauwenberge, P., Pharmacological management of nasal polyposis, Drugs 2005, 65, 1537-1552.