Prostaglandin E2 induces interleukin-6 expression in human chondrocytes via cAMP/protein kinase A- and phosphatidylinositol 3-kinase-dependent NF-κB activation

American Journal of Physiology - Cell Physiology

Volumn 298, Issue 6, 2010, Pages

  Wang, Pu ^a   Zhu, Fei ^a   Konstantopoulos, Konstantinos ^a,b  

^a Johns Hopkins University   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

Arthritic disorders; Arthritis; Chondrocytes; Protein expression; Signal transduction

Indexed keywords

CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; FORSKOLIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 6; MESSENGER RNA; PHOSPHATIDYLINOSITOL 3 KINASE; PROSTAGLANDIN E2; TRANSCRIPTION FACTOR RELA; 2 MORPHOLINO 8 PHENYLCHROMONE; 2-(4-MORPHOLINYL)-8-PHENYL-4H-1-BENZOPYRAN-4-ONE; ADENYLATE CYCLASE; ANDROSTANE DERIVATIVE; CHROMONE DERIVATIVE; CREB1 PROTEIN, HUMAN; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; ENZYME ACTIVATOR; IL6 PROTEIN, HUMAN; MORPHOLINE DERIVATIVE; PROTEIN KINASE INHIBITOR; RELA PROTEIN, HUMAN; WORTMANNIN;

ARTICLE; CARTILAGE CELL; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; ENZYME ACTIVITY; HUMAN; HUMAN CELL; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; UPREGULATION; BINDING SITE; BIOSYNTHESIS; CELL CULTURE; DRUG ANTAGONISM; DRUG EFFECT; ENZYME ACTIVATION; ENZYMOLOGY; GENETICS; IMMUNOLOGY; METABOLISM; PROMOTER REGION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TIME; TRANSCRIPTION INITIATION;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ADENYLATE CYCLASE; ANDROSTADIENES; BINDING SITES; CELLS, CULTURED; CHONDROCYTES; CHROMONES; CYCLIC AMP; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; CYCLIC AMP-DEPENDENT PROTEIN KINASES; DINOPROSTONE; ENZYME ACTIVATION; ENZYME ACTIVATORS; FORSKOLIN; HUMANS; INTERLEUKIN-6; MORPHOLINES; NF-KAPPA B; PROMOTER REGIONS, GENETIC; PROTEIN KINASE INHIBITORS; RNA INTERFERENCE; RNA, MESSENGER; SIGNAL TRANSDUCTION; TIME FACTORS; TRANSCRIPTION FACTOR RELA; TRANSCRIPTIONAL ACTIVATION; UP-REGULATION;

EID: 77952657476     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00508.2009     Document Type: Article

References (39)

1. Abulencia JP, Gaspard R, Healy ZR, Gaarde WA, Quackenbush J, Konstantopoulos K. Shear-induced cyclooxygenase-2 via a JNK2/c-Jun-dependent pathway regulates prostaglandin receptor expression in chondrocytic cells. J Biol Chem 278: 28388-28394, 2003. (Pubitemid 36935739)
2. Amin AR, Attur M, Patel RN, Thakker GD, Marshall PJ, Rediske J, Stuchin SA, Patel IR, Abramson SB. Superinduction of cyclooxygenase-2 activity in human osteoarthritis-affected cartilage. Influence of nitric oxide. J Clin Invest 99: 1231-1237, 1997. (Pubitemid 27142759)
3. Anderson GD, Hauser SD, McGarity KL, Bremer ME, Isakson PC, Gregory SA. Selective inhibition of cyclooxygenase (COX)-2 reverses inflammation and expression of COX-2 and interleukin 6 in rat adjuvant arthritis. J Clin Invest 97: 2672-2679, 1996.
4. Aoyama T, Liang B, Okamoto T, Matsusaki T, Nishijo K, Ishibe T, Yasura K, Nagayama S, Nakayama T, Nakamura T, Toguchida J. PGE2 signal through EP2 promotes the growth of articular chondrocytes. J Bone Miner Res 20: 377-389, 2005. (Pubitemid 40293486)
5. Attur M, Al-Mussawir HE, Patel J, Kitay A, Dave M, Palmer G, Pillinger MH, Abramson SB. Prostaglandin E2 exerts catabolic effects in osteoarthritis cartilage: evidence for signaling via the EP4 receptor. J Immunol 181: 5082-5088, 2008.
6. Blom MA, van Twillert MG, de Vries SC, Engels F, Finch CE, Veerhuis R, Eikelenboom P. NSAIDS inhibit the IL-1 beta-induced IL-6 release from human post-mortem astrocytes: the involvement of prostaglandin E2. Brain Res 777: 210-218, 1997. (Pubitemid 28015749)
7. Chen BC, Liao CC, Hsu MJ, Liao YT, Lin CC, Sheu JR, Lin CH. Peptidoglycan-induced IL-6 production in RAW 264.7 macrophages is mediated by cyclooxygenase-2, PGE2/PGE4 receptors, protein kinase A, I kappa B kinase, and NF-kappa B. J Immunol 177: 681-693, 2006.
8. Ciullo I, Diez-Roux G, Di Domenico M, Migliaccio A, Avvedimento EV. cAMP signaling selectively influences Ras effectors pathways. Oncogene 20: 1186-1192, 2001. (Pubitemid 32226244)
9. DiBattista JA, Martel-Pelletier J, Fujimoto N, Obata K, Zafarullah M, Pelletier JP. Prostaglandins E2 and E1 inhibit cytokine-induced metalloprotease expression in human synovial fibroblasts. Mediation by cyclic-AMP signalling pathway. Lab Invest 71: 270-278, 1994. (Pubitemid 2143043)
10. Goldring MB, Birkhead JR, Suen LF, Yamin R, Mizuno S, Glowacki J, Arbiser JL, Apperley JF. Interleukin-1 beta-modulated gene expression in immortalized human chondrocytes. J Clin Invest 94: 2307-2316, 1994. (Pubitemid 24379603)
11. 2 downregulates Kupffer cell production of IL-1 and IL-6 during hepatic regeneration. Am J Physiol Gastrointest Liver Physiol 264: G601-G608, 1993.
12. Grassl C, Luckow B, Schlondorff D, Dendorfer U. Transcriptional regulation of the interleukin-6 gene in mesangial cells. J Am Soc Nephrol 10: 1466-1477, 1999. (Pubitemid 29297521)
13. Hardy MM, Seibert K, Manning PT, Currie MG, Woerner BM, Edwards D, Koki A, Tripp CS. Cyclooxygenase 2-dependent prostaglandin E2 modulates cartilage proteoglycan degradation in human osteoarthritis explants. Arthritis Rheum 46: 1789-1803, 2002.
14. Healy ZR, Lee NH, Gao X, Goldring MB, Talalay P, Kensler TW, Konstantopoulos K. Divergent responses of chondrocytes and endothelial cells to shear stress: cross-talk among COX-2, the phase 2 response, and apoptosis. Proc Natl Acad Sci USA 102: 14010-14015, 2005. (Pubitemid 41377694)
15. Healy ZR, Zhu F, Stull JD, Konstantopoulos K. Elucidation of the signaling network of COX-2 induction in sheared chondrocytes: COX-2 is induced via a Rac/MEKK1/MKK7/JNK2/c-Jun-C/EBPβ-dependent pathway. Am J Physiol Cell Physiol 294: C1146-C1157, 2008.
16. Hidaka H, Kobayashi R. Pharmacology of protein kinase inhibitors. Annu Rev Pharmacol Toxicol 32: 377-397, 1992.
17. Houssiau FA, Devogelaer JP, Van Damme J, de Deuxchaisnes CN, Van Snick J. Interleukin-6 in synovial fluid and serum of patients with rheumatoid arthritis and other inflammatory arthritides. Arthritis Rheum 31: 784-788, 1988.
18. Inoue H, Takamori M, Shimoyama Y, Ishibashi H, Yamamoto S, Koshihara Y. Regulation by PGE2 of the production of interleukin-6, macrophage colony stimulating factor, and vascular endothelial growth factor in human synovial fibroblasts. Br J Pharmacol 136: 287-295, 2002. (Pubitemid 34587676)
19. Kamat SG, Turner NA, Konstantopoulos K, Hellums JD, McIntire LV, Kleiman NS, Moake JL. Effects of Integrelin on platelet function in flow models of arterial thrombosis. J Cardiovasc Pharmacol 29: 156-163, 1997. (Pubitemid 27097716)
20. Kokenyesi R, Tan L, Robbins JR, Goldring MB. Proteoglycan production by immortalized human chondrocyte cell lines cultured under conditions that promote expression of the differentiated phenotype. Arch Biochem Biophys 383: 79-90, 2000.
21. Li X, Ellman M, Muddasani P, Wang JH, Cs-Szabo G, van Wijnen AJ, Im HJ. Prostaglandin E2 and its cognate EP receptors control human adult articular cartilage homeostasis and are linked to the pathophysiology of osteoarthritis. Arthritis Rheum 60: 513-523, 2009.
22. Lowe GN, Fu YH, McDougall S, Polendo R, Williams A, Benya PD, Hahn TJ. Effects of prostaglandins on deoxyribonucleic acid and aggrecan synthesis in the RCJ 3.1C518 chondrocyte cell line: role of second messengers. Endocrinology 137: 2208-2216, 1996. (Pubitemid 26155750)
23. Lu DY, Tang CH, Yeh WL, Wong KL, Lin CP, Chen YH, Lai CH, Chen YF, Leung YM, Fu WM. SDF-1alpha up-regulates interleukin-6 through CXCR4, PI3K/Akt, ERK, and NF-kappaB-dependent pathway in microglia. Eur J Pharmacol 613: 146-154, 2009.
24. Martel-Pelletier J, Pelletier JP, Fahmi H. Cyclooxygenase-2 and prostaglandins in articular tissues. Semin Arthritis Rheum 33: 155-167, 2003.
25. McCoy JM, Wicks JR, Audoly LP. The role of prostaglandin E2 receptors in the pathogenesis of rheumatoid arthritis. J Clin Invest 110: 651-658, 2002. (Pubitemid 34988789)
26. Millet I, McCarthy TL, Vignery A. Regulation of interleukin-6 production by prostaglandin E2 in fetal rat osteoblasts: role of protein kinase A signaling pathway. J Bone Miner Res 13: 1092-1100, 1998. (Pubitemid 28311777)
27. Misra UK, Pizzo SV. Upregulation of AKT1 protein expression in forskolin-stimulated macrophage: evidence from ChIP analysis that CREB binds to and activates the AKT1 promoter. J Cell Biochem 100: 1022-1033, 2007. (Pubitemid 46273025)
28. Miyamoto M, Ito H, Mukai S, Kobayashi T, Yamamoto H, Kobayashi M, Maruyama T, Akiyama H, Nakamura T. Simultaneous stimulation of EP2 and EP4 is essential to the effect of prostaglandin E2 in chondrocyte differentiation. Osteoarthritis Cartilage 11: 644-652, 2003. (Pubitemid 37045683)
29. Noguchi K, Shitashige M, Endo H, Kondo H, Ishikawa I. Binary regulation of interleukin (IL)-6 production by EP1 and EP2/EP4 subtypes of PGE2 receptors in IL-1beta-stimulated human gingival fibroblasts. J Periodontal Res 37: 29-36, 2002.
30. O'Keefe RJ, Crabb ID, Puzas JE, Rosier RN. Influence of prostaglandins on DNA and matrix synthesis in growth plate chondrocytes. J Bone Miner Res 7: 397-404, 1992.
31. Portanova JP, Zhang Y, Anderson GD, Hauser SD, Masferrer JL, Seibert K, Gregory SA, Isakson PC. Selective neutralization of prostaglandin E2 blocks inflammation, hyperalgesia, and interleukin 6 production in vivo. J Exp Med 184: 883-891, 1996. (Pubitemid 26313546)
32. Skurk T, van Harmelen V, Hauner H. Angiotensin II stimulates the release of interleukin-6 and interleukin-8 from cultured human adipocytes by activation of NF-kappaB. Arterioscler Thromb Vasc Biol 24: 1199-1203, 2004. (Pubitemid 38880008)
33. Sugimoto Y, Narumiya S. Prostaglandin E receptors. J Biol Chem 282: 11613-11617, 2007.
34. Takaoka Y, Niwa S, Nagai H. Interleukin-1beta induces interleukin-6 production through the production of prostaglandin E(2) in human osteoblasts, MG-63 cells. J Biochem 126: 553-558, 1999. (Pubitemid 29452620)
35. Tetlow LC, Woolley DE. Histamine and PGE(2) stimulate the production of interleukins -6 and -8 by human articular chondrocytes in vitro. 6 Human and clinical aspects of histamine. Inflamm Res 55, Suppl 1: S73-S74, 2006.
36. Tobe M, Isobe Y, Tomizawa H, Nagasaki T, Takahashi H, Fukazawa T, Hayashi H. Discovery of quinazolines as a novel structural class of potent inhibitors of NF-kappa B activation. Bioorg Med Chem 11: 383-391, 2003. (Pubitemid 36051028)
37. Trang LE, Granstrom E, Lovgren O. Levels of prostaglandins F2 alpha and E2 and thromboxane B2 in joint fluid in rheumatoid arthritis. Scand J Rheumatol 6: 151-154, 1977.
38. Zhu F, Massana R, Not F, Marie D, Vaulot D. Mapping of picoeucaryotes in marine ecosystems with quantitative PCR of the 18S rRNA gene. FEMS Microbiol Ecol 52: 79-92, 2005. (Pubitemid 40261301)
39. Zhu F, Wang P, Kontrogianni-Konstantopoulos A, Konstantopoulos K. Prostaglandin (PG)D2 and 15-deoxy-Δ12,14-PGJ2, but not PGE2, mediate shear-induced chondrocyte apoptosis via protein kinase a-dependent regulation of polo-like kinases. Cell Death Differ. In Press.