Nuclear factor-kappa B regulates inducible prostaglandin E synthase expression in human amnion mesenchymal cells

Biology of Reproduction

Volumn 78, Issue 1, 2008, Pages 68-76

  Ackerman IV, William E ^a   Summerfield, Taryn L S ^a   Vandre, Dale D ^a   Robinson, John M ^a   Kniss, Douglas A ^a,b  

^a OHIO STATE UNIVERSITY   (United States)

^b Ohio State University   (United States)

Author keywords

Cytokines; Gene regulation; Parturition; Placenta; Pregnancy

Indexed keywords

CYCLOOXYGENASE 2; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LUCIFERASE; MESSENGER RNA; PROSTAGLANDIN E SYNTHASE;

AMNION; ARTICLE; ATTENUATION; BIOSYNTHESIS; BIRTH; GENE CONTROL; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; MESENCHYME CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; RECEPTOR UPREGULATION;

AMNION; CELLS, CULTURED; CYTOKINES; EPITHELIAL CELLS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMANS; INTRAMOLECULAR OXIDOREDUCTASES; NF-KAPPA B; RESPONSE ELEMENTS; SIGNAL TRANSDUCTION;

ADENOVIRIDAE;

EID: 38149114638     PISSN: 00063363     EISSN: None     Source Type: Journal    
DOI: 10.1095/biolreprod.107.061663     Document Type: Article

References (60)

1. Romero R, Munoz H, Gomez R, Parra M, Polanco M, Valverde V, Hasbun J, Garrido J, Ghezzi F, Mazor M, Tolosa JE, Mitchell MD. Increase in prostaglandin bioavailability precedes the onset of human parturition. Prostaglandins Leukot Essent Fatty Acids 1996; 54:187-191.
2. Brown NL, Alvi SA, Elder MG, Bennett PR, Sullivan MH. A spontaneous induction of fetal membrane prostaglandin production precedes clinical labour. J Endocrinol 1998; 157:R1-R6.
3. Challis JRG, Matthews SG, Gibb W, Lye SJ. Endocrine and paracrine regulation of birth at term and preterm. Endocr Rev 2000; 21:514-550.
4. Romero R, Espinoza J, Goncalves LF, Kusanovic JP, Friel LA, Nien JK. Inflammation in preterm and term labour and delivery. Semin Fetal Neonatal Med 2006; 11:317-326.
5. Smith WL, DeWitt DL, Garavito RM. Cyclooxygenases: structural, cellular, and molecular biology. Annu Rev Biochem 2000; 69:145-182.
6. Slater DM, Berger LC, Newton R, Moore GE, Bennett PR. Expression of cyclooxygenase types 1 and 2 in human fetal membranes at term. Am J Obstet Gynecol 1995; 172:77-82.
7. Mijovic JE, Zakar T, Nairn TK, Olson DM. Prostaglandin endoperoxide H synthase (PGHS) activity and PGHS-1 and -2 messenger ribonucleic acid abundance in human chorion throughout gestation and with preterm labor. J Clin Endocrinol Metab 1998; 83:1358-1367.
8. Murakami M, Nakatani Y, Tanioka T, Kudo I. Prostaglandin E synthase. Prostaglandins Other Lipid Mediat 2002; 68-69:383-399.
9. Murakami M, Kudo I. Recent advances in molecular biology and physiology of the prostaglandin E2-biosynthetic pathway. Prog Lipid Res 2004; 43:3-35.
10. Jakobsson PJ, Thoren S, Morgenstern R, Samuelsson B. Identification of human prostaglandin E synthase: a microsomal, glutathione-dependent, inducible enzyme, constituting a potential novel drug target. Proc Natl Acad Sci U S A 1999; 96:7220-7225.
11. Forsberg L, Leeb L, Thoren S, Morgenstern R, Jakobsson P. Human glutathione dependent prostaglandin E synthase: gene structure and regulation. FEBS Lett 2000; 471:78-82.
12. Thoren S, Jakobsson PJ. Coordinate up- and down-regulation of glutathione-dependent prostaglandin E synthase and cyclooxygenase-2 in A549 cells. Inhibition by NS-398 and leukotriene C4. Eur J Biochem 2000; 267:6428-6434.
13. Premyslova M, Li W, Alfaidy N, Bocking AD, Campbell K, Gibb W, Challis JR. Differential expression and regulation of microsomal prostaglandin E(2) synthase in human fetal membranes and placenta with infection and in cultured trophoblast cells. J Clin Endocrinol Metab 2003; 88:6040-6047.
14. Roman AS, Schreher J, Mackenzie AP, Nathanielsz PW. Omega-3 fatty acids and decidual cell prostaglandin production in response to the inflammatory cytokine IL-1beta. Am J Obstet Gynecol 2006; 195:1693-1699.
15. Thoren S, Weinander R, Saha S, Jegerschold C, Pettersson PL, Samuelsson B, Hebert H, Hamberg M, Morgenstern R, Jakobsson PJ. Human microsomal prostaglandin E synthase-1: purification, functional characterization, and projection structure determination. J Biol Chem 2003; 278:22199-22209.
16. Murakami M, Naraba H, Tanioka T, Semmyo N, Nakatani Y, Kojima F, Ikeda T, Fueki M, Ueno A, Oh S, Kudo I. Regulation of prostaglandin E2 biosynthesis by inducible membrane-associated prostaglandin E2 synthase that acts in concert with cyclooxygenase-2. J Biol Chem 2000; 275: 32783-32792.
17. Kapoor M, Kojima F, Qian M, Yang L, Crofford LJ. Shunting of prostanoid biosynthesis in microsomal prostaglandin E synthase-1 null embryo fibroblasts: regulatory effects on inducible nitric oxide synthase expression and nitrite synthesis. FASEB J 2006; 20:E1704-E1715.
18. Uematsu S, Matsumoto M, Takeda K, Akira S. Lipopolysaccharide-dependent prostaglandin E(2) production is regulated by the glutathione-dependent prostaglandin E(2) synthase gene induced by the Toll-like receptor 4/MyD88/NF-IL6 pathway. J Immunol 2002; 168:5811-5816.
19. Boulet L, Ouellet M, Bateman KP, Ethier D, Percival MD, Riendeau D, Mancini JA, Methot N. Deletion of microsomal prostaglandin E2 (PGE2) synthase-1 reduces inducible and basal PGE2 production and alters the gastric prostanoid profile. J Biol Chem 2004; 279:23229-23237.
20. Whittle WL, Gibb W, Challis JR. The characterization of human amnion epithelial and mesenchymal cells: the cellular expression, activity and glucocorticoid regulation of prostaglandin output. Placenta 2000; 21: 394-401.
21. Yan X, Wu XC, Sun M, Tsang BK, Gibb W. Nuclear factor kappa B activation and regulation of cyclooxygenase type-2 expression in human amnion mesenchymal cells by interleukin-1beta. Biol Reprod 2002; 66: 1667-1671.
22. Okita JR, Sagawa N, Casey ML, Snyder JM. A comparison of human amnion tissue and amnion cells in primary culture by morphological and biochemical criteria. In Vitro 1983; 19:117-126.
23. Ackerman WE IV, Zhang XL, Rovin BH, Kniss DA. Modulation of cytokine-induced cyclooxygenase 2 expression by PPARG ligands through NFkappaB signal disruption in human WISH and amnion cells. Biol Reprod 2005; 73:527-535.
24. Chomczynski P, Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 1987; 162:156-159.
25. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 2001; 25:402-408.
26. Ackerman WE, Robinson JM, Kniss DA. Despite transcriptional and functional coordination, cyclooxygenase-2 and microsomal prostaglandin E synthase-1 largely reside in distinct lipid microdomains in WISH epithelial cells. J Histochem Cytochem 2005; 53:1391-1401.
27. Ackerman WE IV, Rovin BH, Kniss DA. Epidermal growth factor and interleukin-1beta utilize divergent signaling pathways to synergistically upregulate cyclooxygenase-2 gene expression in human amnion-derived WISH cells. Biol Reprod 2004; 71:2079-2086.
28. Olson DM, Skinner K, Challis JR. Prostaglandin output in relation to parturition by cells dispersed from human intrauterine tissues. J Clin Endocrinol Metab 1983; 57:694-699.
29. Gibb W, Sun M. Cellular specificity of interleukin-1 beta-stimulated expression of type-2 prostaglandin H synthase in human amnion cell cultures. Biol Reprod 1998; 59:1139-1142.
30. Chen LF, Greene WC. Shaping the nuclear action of NF-kappaB. Nat Rev Mol Cell Biol 2004; 5:392-401.
31. Perkins DJ, Kniss DA. Rapid and transient induction of cyclo-oxygenase 2 by epidermal growth factor in human amnion-derived WISH cells. Biochem J 1997; 321:677-681.
32. Hayden MS, Ghosh S. Signaling to NF-kappaB, Genes Dev 2004; 18: 2195-2224.
33. Catley MC, Chivers JE, Cambridge LM, Holden N, Slater DM, Staples KJ, Bergmann MW, Loser P, Barnes PJ, Newton R. IL-1beta-dependent activation of NF-kappaB mediates PGE2 release via the expression of cyclooxygenase-2 and microsomal prostaglandin E synthase. FEBS Lett 2003; 547:75-79.
34. Tergaonkar V, Li Q, Verma IM. Inhibitors of NF-kappaB activity: tools for treatment of human ailments. In: Liou HC (ed.), NF-kappaB/Rel Transcription Factor Family. Austin, TX: Springer US; 2006:162-178.
35. Bergelson JM, Cunningham JA, Droguett G, Kurt-Jones EA, Krithivas A, Hong JS, Horwitz MS, Crowell RL, Finberg RW. Isolation of a common receptor for Coxsackie B viruses and adenoviruses 2 and 5. Science 1997; 275:1320-1323.
36. Sampey AV, Monrad S, Crofford LJ. Microsomal prostaglandin E synthase-1: the inducible synthase for prostaglandin E2. Arthritis Res Ther 2005; 7:114-117.
37. TESS: Transcription Element Search Software, Jonathan Schug and G. Christian Overton, Technical Report CBIL-TR-1997-1001-v0.0, Computational Biology and Informatics Laboratory, School of Medicine, University of Pennsylvania. 1997. World Wide Web (URL: http://www.cbil.upenn.edu/tess). (March, 2007).
38. Maggirwar SJ, Harhaj EW, Sun S-C. Regulation of the interleukin-2 CD28-responsive element by NF-ATp and various NF-kappaB/Rel transcription factors. Mol Cell Biol 1997; 17:2605-2614.
39. Okamoto S, Mukaida N, Yasumoto K, Rice N, Ishikawa Y, Horiguchi H, Murakami S, Matsushima K. The interleukin-8 AP-1 and kappa B-like sites are genetic end targets of FK506-sensitive pathway accompanied by calcium mobilization. J Biol Chem 1994; 269:8582-8589.
40. Chen F, Demers LM, Vallyathan V, Lu Y, Castranova V, Shi X. Involvement of 5′-flanking kappaB-like sites within bcl-x gene in silica-induced Bcl-x expression. J Biol Chem 1999; 274:35591-35595.
41. Hong SY, Yoon WH, Park JH, Kang SG, Ahn JH, Lee TH. Involvement of two NF-kappa B binding elements in tumor necrosis factor alpha-, CD40-, and Epstein-Barr virus latent membrane protein 1-mediated induction of the cellular inhibitor of apoptosis protein 2 gene. J Biol Chem 2000; 275:18022-18028.
42. Romero R, Emamian M, Quintero R, Wan M, Hobbins JC, Mitchell MD. Amniotic fluid prostaglandin levels and intra-amniotic infections. Lancet 1986; 1:1380.
43. Bowen JM, Chamley L, Keelan JA, Mitchell MD. Cytokines of the placenta and extra-placental membranes: roles and regulation during human pregnancy and parturition. Placenta 2002; 23:257-273.
44. Keelan JA, Blumenstein M, Helliwell RJ, Sato TA, Marvin KW, Mitchell MD. Cytokines, prostaglandins and parturition - a review. Placenta 2003; 24(Suppl A):S33-S46.
45. Haddad R, Tromp G, Kuivaniemi H, Chaiworapongsa T, Kim YM, Mazor M, Romero R. Human spontaneous labor without histologic chorioamnionitis is characterized by an acute inflammation gene expression signature. Am J Obstet Gynecol 2006; 195:394e1-394e24.
46. Lindstrom TM, Bennett PR. The role of nuclear factor kappa B in human labour. Reproduction 2005; 130:569-581.
47. Lappas M, Rice GE. The role and regulation of the nuclear factor kappa B signalling pathway in human labour. Placenta 2006; 5-6:543-556.
48. Allport VC, Pieber D, Slater DM, Newton R, White JO, Bennett PR. Human labour is associated with nuclear factor-kappaB activity which mediates cyclo-oxygenase-2 expression and is involved with the 'functional progesterone withdrawal.' Mol Hum Reprod 2001; 7:581-586.
49. Yan X, Sun M, Gibb W. Localization of nuclear factor-kappa B (NF kappa B) and inhibitory factor-kappa B (I kappa B) in human fetal membranes and decidua at term and preterm delivery. Placenta 2002; 23:288-293.
50. Soloff MS, Cook DL Jr, Jeng YJ, Anderson GD. In situ analysis of interleukin-1-induced transcription of cox-2 and il-8 in cultured human myometrial cells. Endocrinology 2004; 145:1248-1254.
51. Mbonye UR, Wada M, Rieke CJ, Tang HY, DeWitt DL, Smith WL. The 19-amino acid cassette of cyclooxygenase-2 mediates entry of the protein into the endoplasmic reticulum-associated degradation system. J Biol Chem 2006; 281:35770-35778.
52. Elliott CL, Allport VC, Loudon JA, Wu GD, Bennett PR. Nuclear factor-kappa B is essential for up-regulation of interleukin-8 expression in human amnion and cervical epithelial cells. Mol Hum Reprod 2001; 7:787-790.
53. Sooranna SR, Engineer N, Loudon JA, Terzidou V, Bennett PR, Johnson MR. The mitogen-activated protein kinase dependent expression of prostaglandin H synthase-2 and interleukin-8 messenger ribonucleic acid by myometrial cells: the differential effect of stretch and interleukin-1{beta}. J Clin Endocrinol Metab 2005; 90:3517-3527.
54. Masuko-Hongo K, Berenbaum F, Humbert L, Salvat C, Goldring MB, Thirion S. Up-regulation of microsomal prostaglandin E synthase 1 in osteoarthritic human cartilage: critical roles of the ERK-1/2 and p38 signaling pathways. Arthritis Rheum 2004; 50:2829-2838.
55. Subbaramaiah K, Yoshimatsu K, Scherl E, Das KM, Glazier KD, Golijanin D, Soslow RA, Tanabe T, Naraba H, Dannenberg AJ. Microsomal prostaglandin E synthase-1 is overexpressed in inflammatory bowel disease. Evidence for involvement of the transcription factor Egr-1. J Biol Chem 2004; 279:12647-12658.
56. Cogswell PC, Mayo MW, Baldwin AS Jr. Involvement of Egr-1/RelA synergy in distinguishing T cell activation from tumor necrosis factor-alpha-induced NF-kappa B1 transcription. J Exp Med 1997; 185:491-497.
57. Chapman NR, Perkins ND. Inhibition of the RelA(p65) NF-kappaB subunit by Egr-1. J Biol Chem 2000; 275:4719-4725.
58. Kim JH, Kim WS, Kang JH, Lim HY, Ko YH, Park C. Egr-1, a new downstream molecule of Epstein-Barr virus latent membrane protein 1. FEBS Lett 2007; 581:623-628.
59. Alfaidy N, Sun M, Challis JR, Gibb W. Expression of membrane prostaglandin E synthase in human placenta and fetal membranes and effect of labor. Endocrine 2003; 20:219-225.
60. Meadows JW, Eis AL, Brockman DE, Myatt L. Expression and localization of prostaglandin E synthase isoforms in human fetal membranes in term and preterm labor. J Clin Endocrinol Metab 2003; 88:433-439.