Allose Gallates Suppress Expression of Pro-Inflammatory Cytokines through Attenuation of NF-κB in Human Mast Cells

Abstract

Gallotannins are plant-derived, water-soluble polyphenols with wide-ranging biological activities. Mast cell-mediated allergic inflammation is known to cause many diseases such as asthma, sinusitis, and rheumatoid arthritis. Mast cells induce synthesis and production of pro-inflammatory cytokines including tumor necrosis factor (TNF)-α, interleukin (IL)-1β, and IL-6 with immune regulatory properties. Expression of inflammatory cytokines is mainly regulated by a transcription factor, nuclear factor (NF)-κB. In the present study, the effect of eight gallotannins on the level of pro-inflammatory cytokines and NF-κB activation was investigated in human mast cell line (HMC-1). HMC-1 cells were sensitized by phorbol 12-myristate 13-acetate (PMA) and calcium ionophore (A23187). Among the eight gallotannins from Euphorbia species, three gallotannins such as 1,2,3,4,6-penta-O-galloyl-β-D-glucose, 1,2,6-tri-O-galloyl-β-D-allopyanose, and 1,2,3,6-tetra-O-galloyl-β-D-allopyranose suppressed the gene expression and secretion of pro-inflammatory cytokines in a dose-dependent manner. In addition, these three gallotannins blocked the activation of NF-κB as indicated by an NF-κB-dependent gene reporter assay. We conclude that these gallotannins may have potential for the treatment of inflammatory diseases through the down-regulation of NF-κB-mediated activation of mast cells.

Abbreviations

HMC-1:human mast cell

IL:interleukin

NF-κB:nuclear factor-κB

PMA:phorbol 12-myristate 13-acetate

PMACI:PMA and calcium ionophore A23187

Key words

Allose gallates - Euphorbia species - Euphorbiaceae - mast cells - pro-inflammatory cytokines - nuclear factor-κB

References

• 1 Church M K, Levi-Schaffer F. The human mast cell.  J Allergy Clin Immunol. 1997;  99 155-60.
• 2 Metcalfe D D, Baram D, Mekori Y A. Mast cells.  Physiol Rev. 1997;  77 1033-79.
• 3 Galli S J, Kalesnikoff J, Grimbaldeston M A, Piliponsky A M, Williams C M, Tsai M. Mast cells as ”tunable” effector and immunoregulatory cells: recent advances.  Annu Rev Immunol. 2005;  23 749-86.
• 4 Tsang C M, Wong C K, Ip W K, Lam C W. Synergistic effect of SCF and TNF-alpha on the up-regulation of cell-surface expression of ICAM-1 on human leukemic mast cell line (HMC)-1 cells.  J Leukoc Biol. 2005;  78 239-47.
• 5 Kim S H, Shin T Y. Effect of Dracocephalum argunense on mast-cell-mediated hypersensitivity.  Int Arch Allergy Immunol. 2006;  139 87-95.
• 6 Schoonbroodt S, Legrand-Poels S, Best-Belpomme M, Piette J. Activation of the NF-kappaB transcription factor in a T-lymphocytic cell line by hypochlorous acid.  Biochem J. 1997;  321 777-85.
• 7 Kim S H, Choi C H, Kim S Y, Eun J S, Shin T Y. Anti-allergic effects of Artemisia iwayomogi on mast cell-mediated allergy model.  Exp Biol Med. 2005;  230 82-8.
• 8 Erdelyi K, Kiss A, Bakondi E, Bai P, Szabo C, Gergely P. et al . Gallotannin inhibits the expression of chemokines and inflammatory cytokines in A549 cells.  Mol Pharmacol. 2005;  68 895-904.
• 9 Li M, Kai Y, Qiang H, Dongying J. Biodegradation of gallotannins and ellagitannins.  J Basic Microbiol. 2006;  46 68-84.
• 10 Hagerman A E, Riedl K M, Rice R E. Tannins as biological antioxidants.  Basic Life Sci. 1999;  66 495-505.
• 11 Rapizzi E, Fossati S, Moroni F, Chiarugi A. Inhibition of poly(ADP-ribose) glycohydrolase by gallotannin selectively up-regulates expression of proinflammatory genes.  Mol Pharmacol. 2004;  66 890-8.
• 12 Feldman K S, Sahasrabudhe K, Lawlor M D, Wilson S L, Lang C H, Scheuchenzuber W J. In vitro and in vivo inhibition of LPS-stimulated tumor necrosis factor-alpha secretion by the gallotannin beta-D-pentagalloylglucose.  Bioorg Med Chem Lett. 2001;  11 1813-5.
• 13 Lee S H, Tanaka T, Nonaka G I, Nishioka I. Tannins and related compounds CV. Monomeric and dimeric hydrolysable tannins having a dehydrohexahydroxydiphenoyl group, supinanin, euphorscopin, euphorhelin and jolkianin from Euphorbia species.  Chem Pharm Bull. 1991;  39 630-8.
• 14 Lee S H, Tanaka T, Nonaka G I, Nishioka I. Allose gallates from E. fisheriana .  Phytochemistry. 1991;  30 1251-3.
• 15 Choi C H, Kim S H. Role of gallic acid on the inflammatory allergic process.  Korean J Physiol Pharmacol. 2006;  10 101-8.
• 16 Azzolina A, Bongiovanni A, Lampiasi N. Substance P induces TNF-alpha and IL-6 production through NF kappa B in peritoneal mast cells.  Biochim Biophys Acta. 2003;  1643 75-83.
• 17 Shin T Y, Oh J M, Choi B J, Park W H, Kim C H, Jun C D. et al . Anti-inflammatory effect of Poncirus trifoliata fruit through inhibition of NF-kappaB activation in mast cells.  Toxicol In Vitro. 2006;  20 1071-6.
• 18 Rohrbach M S, Kreofsky T, Rolstad R A, Russell J A. Tannin-mediated secretion of a neutrophil chemotactic factor from alveolar macrophages. Potential contribution to the acute pulmonary inflammatory reaction associated with byssinosis.  Am Rev Respir Dis. 1989;  139 39-45.
• 19 Galli S J, Gordon J R, Wershil B K. Cytokine production by mast cells and basophils.  Curr Opin Immunol. 1991;  3 865-72.
• 20 Cromwell O, Hamid Q, Corrigan C J, Barkans J, Meng Q, Collins P D. et al . Expression and generation of interleukin-8, IL-6 and granulocyte-macrophage colony-stimulating factor by bronchial epithelial cells and enhancement by IL-1 beta and tumour necrosis factor-alpha.  Immunology. 1992;  77 330-7.
• 21 Siebenlist U, Franzoso G, Brown K. Structure, regulation and function of NF-kappa B.  Annu Rev Cell Biol. 1994;  10 405-55.
• 22 Sen R, Baltimore D. Multiple nuclear factors interact with the immunoglobulin enhancer sequences.  Cell. 1986;  46 705-16.
• 23 Blackwell T S, Blackwell T R, Christman J W. Impaired activation of nuclear factor-kappaB in endotoxin-tolerant rats is associated with down-regulation of chemokine gene expression and inhibition of neutrophilic lung inflammation.  J Immunol. 1997;  158 5934-40.
• 24 Kang D G, Moon M K, Choi D H, Lee J K, Kwon T O, Lee H S. Vasodilatory and anti-inflammatory effects of the 1,2,3,4,6-penta-O-galloyl-beta-D-glucose (PGG) via a nitric oxide-cGMP pathway.  Eur J Pharmacol. 2005;  524 111-9.
• 25 Oh G S, Pae H O, Choi B M, Lee H S, Kim I K, Yun Y G. et al . Penta-O-galloyl-beta-D-glucose inhibits phorbol myristate acetate-induced interleukin-8 (correction of intereukin-8) gene expression in human monocytic U937 cells through its inactivation of nuclear factor-kappaB.  Int Immunopharmacol. 2004;  4 377-86.
• 26 Lee S J, Lee I S, Mar W. Inhibition of inducible nitric oxide synthase and cyclooxygenase-2 activity by 1,2,3,4,6-penta-O-galloyl-beta-D-glucose in murine macrophage cells.  Arch Pharm Res. 2003;  26 832-9.
• 27 Lee J, Lee S H, Min K R, Lee K S, Ro J S, Ryu J C, Kim Y. Inhibitory effects of hydrolyzable tannins on Ca²⁺-activated hyaluronidase.  Planta Med. 1993;  59 381-2.

1 These authors contributed equally to this work