Gallotannin causes differentiation and inflammation via ERK‑1/‑2 and p38 kinase pathways in rabbit articular chondrocytes

Lee,Won‑Kil; Chung,Ki‑Wha; Kim,Gwang‑Hoon; Kim,Song‑Ja

doi:10.3892/mmr.2012.1204

Gallotannin causes differentiation and inflammation via ERK‑1/‑2 and p38 kinase pathways in rabbit articular chondrocytes

Authors:
- Won‑Kil Lee
- Ki‑Wha Chung
- Gwang‑Hoon Kim
- Song‑Ja Kim
View Affiliations

Affiliations: Department of Biological Sciences, College of Natural Sciences, Kongju National University, Gongju, Chungnam 314‑701, Republic of Korea
Published online on: November 27, 2012 https://doi.org/10.3892/mmr.2012.1204
Pages: 701-707

Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )

Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )

Cited By (CrossRef): 0 citations Loading Articles...

Abstract

Gallotannin (GT) is a type of tannic acid, derived from plant polyphenols, that is an agonist of plant defense mechanisms. Tannins have two types of structure; condensed tannins are a polymer of flavonoid units, while hydrolysable tannins are carbohydrates. GT is used in medical agents for its anti‑viral, anti‑bacterial and anti‑parasitic effects. The present study investigated the effects of GT on differentiation and inflammation in rabbit articular chondrocytes. GT caused differentiation and inflammatory responses in the rabbit articular chondrocytes. GT treatment induced the expression of type Ⅱ collagen and sulfated proteoglycan, as determined by western blot analysis and alcian blue staining, respectively, in a dose‑ and time‑dependent manner. Additionally, treatment with GT increased the expression of cyclooxygenase‑2 (COX‑2) and the production of prostaglandin E2 (PGE2), as determined by western blot analysis and PGE2 assay. GT was confirmed to cause phosphorylation of ERK‑1/‑2 and p38 kinase. Inhibition of pERK with PD98059 promoted GT‑induced type Ⅱ collagen expression. However, the inhibition of p38 with SB203580 suppressed GT‑induced COX‑2 expression and PGE2 production. In summary, the results demonstrated that GT‑induced ERK‑1/‑2 and p38 kinase have opposite effects on differentiation and inflammation in rabbit articular chondrocytes.

View Figures

View References

1	DeLise AM, Fischer L and Tuan RS: Cellular interactions and signaling in cartilage development. Osteoarthritis Cartilage. 8:309–334. 2000. View Article : Google Scholar : PubMed/NCBI
2	Sandell LJ and Adler P: Developmental patterns of cartilage. Front Biosci. 4:D731–D742. 1999. View Article : Google Scholar : PubMed/NCBI
3	Sandell LJ and Aigner T: Articular cartilage and changes in arthritis. An introduction: cell biology of osteoarthritis. Arthritis Res. 3:107–113. 2001. View Article : Google Scholar : PubMed/NCBI
4	Feldmann M: Pathogenesis of arthritis: recent research progress. Nat Immunol. 2:771–773. 2001. View Article : Google Scholar : PubMed/NCBI
5	Feldmann M, Brennan FM and Maini RN: Rheumatoid arthritis. Cell. 85:307–310. 1996. View Article : Google Scholar
6	Erdèlyi K, Kiss A, Bakondi E, Bai P, Szabó C, Gergely P, Erdödi F and Virag L: Gallotannin inhibits the expression of chemokines and inflammatory cytokines in A549 cells. Mol Pharmacol. 68:895–904. 2005.PubMed/NCBI
7	Li W, Zhang J, Flechner L, Hyun T, Yam A, Franke TF and Pierce JH: Protein kinase C-alpha overexpression stimulates Akt activity and suppresses apoptosis induced by interleukin 3 withdrawal. Oncogene. 18:6564–6572. 1999. View Article : Google Scholar : PubMed/NCBI
8	Rapizzi E, Fossati S, Moroni F and Chiarugi A: Inhibition of poly(ADP-ribose) glycohydrolase by gallotannin selectively up-regulates expression of proinflammatory genes. Mol Pharmacol. 66:890–898. 2004. View Article : Google Scholar : PubMed/NCBI
9	Feldman KS, Sahasrabudhe K, Lawlor MD, Wilson SL, Lang CH and Scheuchenzuber WJ: In vitro and in vivo inhibition of LPS-stimulated tumor necrosis factor-alpha secretion by the gallotannin beta-D-pentagalloylglucose. Bioorg Med Chem Lett. 11:1813–1815. 2001. View Article : Google Scholar : PubMed/NCBI
10	Hagerman AE, Riedl KM and Rice RE: Tannins as biological antioxidants. Basic Life Sci. 66:495–505. 1999.PubMed/NCBI
11	Smith WL, DeWitt DL and Garavito RM: Cyclooxygenases: structural, cellular, and molecular biology. Annu Rev Biochem. 69:145–182. 2000. View Article : Google Scholar : PubMed/NCBI
12	Dubois RN, Abramson SB, Crofford L, Gupta RA, Simon LS, Van De Putte LB and Lipsky PE: Cyclooxygenase in biology and disease. FASEB J. 12:1063–1073. 1998.PubMed/NCBI
13	Wu KK: Inducible cyclooxygenase and nitric oxide synthase. Adv Pharmacol. 33:179–207. 1995. View Article : Google Scholar : PubMed/NCBI
14	Goldring MB and Berenbaum F: Human chondrocyte culture models for studying cyclooxygenase expression and prostaglandin regulation of collagen gene expression. Osteoarthritis Cartilage. 7:386–388. 1999. View Article : Google Scholar
15	Namkoong S, Lee SJ, Kim CK and Kim YM, Chung HT, Lee H, Han JA, Ha KS, Kwon YG and Kim YM: Prostaglandin E2 stimulates angiogenesis by activating the nitric oxide/cGMP pathway in human umbilical vein endothelial cells. Exp Mol Med. 37:588–600. 2005. View Article : Google Scholar : PubMed/NCBI
16	Smith WL, Garavito RM and DeWitt DL: Prostaglandin endoperoxide H synthases (cyclooxygenases)-1 and -2. J Biol Chem. 271:33157–33160. 1996. View Article : Google Scholar : PubMed/NCBI
17	Okada Y, Lorenzo JA, Freeman AM, Tomita M, Morham SG, Raisz LG and Pilbeam CC: Prostaglandin G/H synthase-2 is required for maximal formation of osteoclast-like cells in culture. J Clin Invest. 105:823–832. 2000. View Article : Google Scholar : PubMed/NCBI
18	Suponitzky I and Weinreb M: Differential effects of systemic prostaglandin E2 on bone mass in rat long bones and calvariae. J Endocrinol. 156:51–57. 1998. View Article : Google Scholar : PubMed/NCBI
19	Weinreb M, Suponitzky I and Keila S: Systemic administration of an anabolic dose of PGE₂ in young rats increases the osteogenic capacity of bone marrow. Bone. 20:521–526. 1997. View Article : Google Scholar : PubMed/NCBI
20	Duncan RL and Turner CH: Mechanotransduction and the functional response of bone to mechanical strain. Calcif Tissue Int. 57:344–358. 1995. View Article : Google Scholar : PubMed/NCBI
21	Forwood MR: Inducible cyclo-oxygenase (COX-2) mediates the induction of bone formation by mechanical loading in vivo. J Bone Miner Res. 11:1688–1693. 1996. View Article : Google Scholar : PubMed/NCBI
22	Park EH, Kang SS, Lee YS, Kim SJ, Jin EJ, Tak EN and Sonn JK: Integrity of the cortical actin ring is required for activation of the PI3K/Akt and p38 MAPK signaling pathways in redifferentiation of chondrocytes on chitosan. Cell Biol Int. 32:1272–1278. 2008. View Article : Google Scholar : PubMed/NCBI
23	Kim SJ, Kim HG, Oh CD, Hwang SG, Song WK, Yoo YJ, Kang SS and Chun JS: p38 kinase-dependent and -independent Inhibition of protein kinase C zeta and -alpha regulates nitric oxide-induced apoptosis and dedifferentiation of articular chondrocytes. J Biol Chem. 277:30375–30381. 2002. View Article : Google Scholar
24	Kim SJ, Ju JW, Oh CD, Yoon YM, Song WK, Kim JH, Yoo YJ, Bang OS, Kang SS and Chun JS: ERK-1/2 and p38 kinase oppositely regulate nitric oxide-induced apoptosis of chondrocytes in association with p53, caspase-3, and differentiation status. J Biol Chem. 277:1332–1339. 2002. View Article : Google Scholar : PubMed/NCBI
25	Yoon YM, Kim SJ, Oh CD, Ju JW, Song WK, Yoo YJ, Huh TL and Chun JS: Maintenance of differentiated phenotype of articular chondrocytes by protein kinase C and extracellular signal-regulated protein kinase. J Biol Chem. 277:8412–8420. 2002. View Article : Google Scholar : PubMed/NCBI
26	Ryu JH, Kim SJ, Kim SH, Oh CD, Hwang SG, Chun CH, Oh SH, Seong JK, Huh TL and Chun JS: Regulation of the chondrocyte phenotype by beta-catenin. Development. 129:5541–5550. 2002. View Article : Google Scholar : PubMed/NCBI
27	Lü L, Liu SW, Jiang SB and Wu SG: Tannin inhibits HIV-1 entry by targeting gp41. Acta Pharmacol Sin. 25:213–218. 2004.PubMed/NCBI
28	Lu Y, Jiang F, Jiang H, Wu K, Zheng X, Cai Y, Katakowski M, Chopp M and To SS: Gallic acid suppresses cell viability, proliferation, invasion and angiogenesis in human glioma cells. Eur J Pharmacol. 641:102–107. 2010. View Article : Google Scholar : PubMed/NCBI
29	Akiyama H, Fujii K, Yamasaki O, Oono T and Iwatsuki K: Antibacterial action of several tannins against Staphylococcus aureus. J Antimicrob Chemother. 48:487–491. 2001. View Article : Google Scholar : PubMed/NCBI
30	Yu SM, Gweon EJ, Chung KW, Kim KH, Cho HS and Kim SJ: Gallotannin regulates apoptosis and COX-2 expression via Akt and p38kinase pathway in human lung cancer cell line, A549. Animal Cells and Systems. 16:366–375. 2012. View Article : Google Scholar
31	Keller J: Effects of indomethacin and local prostaglandin E2 on fracture healing in rabbits. Dan Med Bull. 43:317–329. 1996.PubMed/NCBI
32	Norrdin RW and Shih MS: Systemic effects of prostaglandin E2 on vertebral trabecular remodeling in beagles used in a healing study. Calcif Tissue Int. 42:363–368. 1988. View Article : Google Scholar : PubMed/NCBI
33	Amin AR, Dave M, Attur M and Abramson SB: COX-2, NO, and cartilage damage and repair. Curr Rheumatol Rep. 2:447–453. 2000. View Article : Google Scholar : PubMed/NCBI
34	Schwartz Z, Gilley RM, Sylvia VL, Dean DD and Boyan BD: The effect of prostaglandin E2 on costochondral chondrocyte differentiation is mediated by cyclic adenosine 3′,5′-monophosphate and protein kinase C. Endocrinology. 139:1825–1834. 1998.PubMed/NCBI
35	Abramson SB: The role of COX-2 produced by cartilage in arthritis. Osteoarthritis Cartilage. 7:380–381. 1999. View Article : Google Scholar : PubMed/NCBI
36	Goldring MB, Birkhead JR, Suen LF, Yamin R, Mizuno S, Glowacki J, Arbiser JL and Apperley JF: Interleukin-1 beta-modulated gene expression in immortalized human chondrocytes. J Clin Invest. 94:2307–2316. 1994. View Article : Google Scholar : PubMed/NCBI
37	Goldring MB, Suen LF, Yamin R and Lai WF: Regulation of collagen gene expression by prostaglandins and interleukin-1beta in cultured chondrocytes and fibroblasts. Am J Ther. 3:9–16. 1996. View Article : Google Scholar : PubMed/NCBI
38	Lee WK, Yu SM, Cheong SW, Sonn JK and Kim SJ: Ectopic expression of cyclooxygenase-2-induced dedifferentiation in articular chondrocytes. Exp Mol Med. 40:721–727. 2008. View Article : Google Scholar : PubMed/NCBI
39	Kim MS, Park SB, Suk K, Kim IK, Kim SY, Kim JA, Lee SH and Kim SH: Gallotannin isolated from Euphorbia species, 1,2,6-tri-O-galloyl-beta-D-allose, decreases nitric oxide production through inhibition of nuclear factor-kappa B and downstream inducible nitric oxide synthase expression in macrophages. Biol Pharm Bull. 32:1053–1056. 2009. View Article : Google Scholar
40	Widmann C, Gibson S, Jarpe MB and Johnson GL: Mitogen- activated protein kinase: conservation of a three-kinase module from yeast to human. Physiol Rev. 79:143–180. 1999.PubMed/NCBI
41	Zhang W and Liu HT: MAPK signal pathways in the regulation of cell proliferation in mammalian cells. Cell Res. 12:9–18. 2002. View Article : Google Scholar : PubMed/NCBI
42	Houde M, Laprise P, Jean D, Blais M, Asselin C and Rivard N: Intestinal epithelial cell differentiation involves activation of p38 mitogen-activated protein kinase that regulates the homeobox transcription factor CDX2. J Biol chem. 276:21885–21894. 2001. View Article : Google Scholar
43	Guan Z, Buckman SY, Miller BW, Springer LD and Morrison AR: Interleukin-1beta-induced cyclooxygenase-2 expression requires activation of both c-Jun NH2-terminal kinase and p38 MAPK signal pathways in rat renal mesangial cells. J Biol Chem. 273:28670–28676. 1998. View Article : Google Scholar
44	Matsuura H, Sakaue M, Subbaramaiah K, Kamitani H, Eling TE, Dannenberg AJ, Tanabe T, Inoue H, Arata J and Jetten AM: Regulation of cyclooxygenase-2 by interferon gamma and transforming growth factor alpha in normal human epidermal keratinocytes and squamous carcinoma cells. Role of mitogen-activated protein kinases. J Biol Chem. 274:29138–29148. 1999. View Article : Google Scholar