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PMID: 17631291 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

The EP4 receptor antagonist, L-161,982, blocks prostaglandin E2-induced signal transduction and cell proliferation in HCA-7 colon cancer cells.

Experimental cell research ·Vol. 313 ·No. 14 ·2007-08-15 ·Pages 2969-79

Cherukuri DP, Chen XB, Goulet AC, Young RN, Han Y, Heimark RL, Regan JW, Meuillet E, Nelson MA

Abstract

Accumulating evidence indicates that elevated levels of prostaglandin E(2) (PGE(2)) can increase intestinal epithelial cell proliferation, and thus play a role in colorectal tumorigenesis. PGE(2) exerts its effects through four G-protein-coupled PGE receptor (EP) subtypes, named the EP1, EP2, EP3, and EP4. Increased phosphorylation of extracellular regulated kinases (ERK1/2) is required for PGE(2) to stimulate cell proliferation of human colon cancer cells. However, the EP receptor(s) that are involved in this process remain unknown. We provide evidence that L-161,982, a selective EP4 receptor antagonist, completely blocks PGE(2)-induced ERK phosphorylation and cell proliferation of HCA-7 cells. In order to identify downstream target genes of ERK1/2 signaling, we found that PGE(2) induces expression of early growth response gene-1 (EGR-1) downstream of ERK1/2 and regulates its expression at the level of transcription. PGE(2) treatment induces phosphorylation of cyclic AMP response element binding protein (CREB) at Ser133 residue and CRE-mediated luciferase activity in HCA-7 cells. Studies with dominant-negative CREB mutant (ACREB) provide clear evidence for the involvement of CREB in PGE(2) driven egr-1 transcription in HCA-7 cells. In conclusion, this study reveals that egr-1 is a target gene of PGE(2) in HCA-7 cells and is regulated via the newly identified EP4/ERK/CREB pathway. Finally our results support the notion that antagonizing EP4 receptors may provide a novel therapeutic approach to the treatment of colon cancer.

MeSH Terms
Animals Cell Line, Tumor Cell Proliferation Colonic Neoplasms/metabolism,pathology Cyclic AMP Response Element-Binding Protein/genetics,metabolism Dinoprostone/metabolism Early Growth Response Protein 1/genetics,metabolism Extracellular Signal-Regulated MAP Kinases/metabolism Humans Promoter Regions, Genetic Receptors, Prostaglandin E/genetics,metabolism Receptors, Prostaglandin E, EP4 Subtype Signal Transduction/physiology Thiophenes/metabolism Transcription, Genetic Triazoles/metabolism
Chemicals
Cyclic AMP Response Element-Binding Protein EGR1 protein, human Early Growth Response Protein 1 L-161982 PTGER4 protein, human Receptors, Prostaglandin E Receptors, Prostaglandin E, EP4 Subtype Thiophenes Triazoles Extracellular Signal-Regulated MAP Kinases Dinoprostone
Authors & Affiliations
9 authors, click to expand affiliations / ORCID
Cherukuri Durga Prasad
Department of Pathology, Arizona Cancer Center, University of Arizona, 1501N Campbell Avenue # 550, Tucson, AZ 85724, USA.
Chen Xiao B O
Goulet Anne-Christine
Young Robert N
Han Yongxin
Heimark Ronald L
Regan John W
Meuillet Emmanuelle
Nelson Mark A
References (46)
46 references, click to expand
  1. Increased EP4 receptor expression in colorectal cancer progression promotes cell growth and anchorage independence.
    Cancer Res. 2006 Mar 15;66(6):3106-13 PMID: 16540660
  2. Prostaglandin E2 promotes colon cancer cell growth through a Gs-axin-beta-catenin signaling axis.
    Science. 2005 Dec 2;310(5753):1504-10 PMID: 16293724
  3. Mediators of PGE2 synthesis and signalling downstream of COX-2 represent potential targets for the prevention/treatment of colorectal cancer.
    Biochim Biophys Acta. 2006 Aug;1766(1):104-19 PMID: 16859832
  4. Host and direct antitumor effects and profound reduction in tumor metastasis with selective EP4 receptor antagonism.
    Cancer Res. 2006 Oct 1;66(19):9665-72 PMID: 17018624
  5. Role of the prostaglandin E receptor subtype EP1 in colon carcinogenesis.
    Cancer Res. 1999 Oct 15;59(20):5093-6 PMID: 10537280
  6. Full promoter sequence of human early growth response factor-1 (Egr-1): demonstration of a fifth functional serum response element.
    DNA Seq. 2000;10(6):429-32 PMID: 10826704
  7. CREB: a stimulus-induced transcription factor activated by a diverse array of extracellular signals.
    Annu Rev Biochem. 1999;68:821-61 PMID: 10872467
  8. Prostaglandin E2 increases growth and motility of colorectal carcinoma cells.
    J Biol Chem. 2001 May 25;276(21):18075-81 PMID: 11278548
  9. Prostaglandin receptor EP(4) mediates the bone anabolic effects of PGE(2).
    Mol Pharmacol. 2001 Jul;60(1):36-41 PMID: 11408598
  10. Acceleration of intestinal polyposis through prostaglandin receptor EP2 in Apc(Delta 716) knockout mice.
    Nat Med. 2001 Sep;7(9):1048-51 PMID: 11533709
  11. Involvement of prostaglandin E receptor subtype EP(4) in colon carcinogenesis.
    Cancer Res. 2002 Jan 1;62(1):28-32 PMID: 11782353
  12. Prostaglandin E(2) protects intestinal tumors from nonsteroidal anti-inflammatory drug-induced regression in Apc(Min/+) mice.
    Cancer Res. 2002 Jan 15;62(2):403-8 PMID: 11809688
  13. Prostaglandin E2 transactivates EGF receptor: a novel mechanism for promoting colon cancer growth and gastrointestinal hypertrophy.
    Nat Med. 2002 Mar;8(3):289-93 PMID: 11875501
  14. Transcriptional regulation of the membrane-associated prostaglandin E2 synthase gene. Essential role of the transcription factor Egr-1.
    J Biol Chem. 2002 Aug 9;277(32):28601-8 PMID: 12034740
  15. Cytokine and chemokine profiles in autologous graft-versus-host disease (GVHD): interleukin 10 and interferon gamma may be critical mediators for the development of autologous GVHD.
    Blood. 2002 Oct 1;100(7):2650-8 PMID: 12239181
  16. Prostaglandin E2 induced functional expression of early growth response factor-1 by EP4, but not EP2, prostanoid receptors via the phosphatidylinositol 3-kinase and extracellular signal-regulated kinases.
    J Biol Chem. 2003 Apr 4;278(14):12151-6 PMID: 12566441
  17. Enhancement of colon carcinogenesis by prostaglandin E2 administration.
    Carcinogenesis. 2003 May;24(5):985-90 PMID: 12771044
  18. Prostaglandins promote colon cancer cell invasion; signaling by cross-talk between two distinct growth factor receptors.
    FASEB J. 2003 Sep;17(12):1640-7 PMID: 12958170
  19. Prostaglandin E2 regulates cell migration via the intracellular activation of the epidermal growth factor receptor.
    J Biol Chem. 2003 Sep 12;278(37):35451-7 PMID: 12824187
  20. Role of prostaglandin E2 receptors in migration of murine and human breast cancer cells.
    Exp Cell Res. 2003 Oct 1;289(2):265-74 PMID: 14499627
  21. EP2 and EP4 prostanoid receptor signaling.
    Life Sci. 2003 Dec 5;74(2-3):143-53 PMID: 14607241
  22. Colon carcinoma cell growth is associated with prostaglandin E2/EP4 receptor-evoked ERK activation.
    J Biol Chem. 2004 Jul 9;279(28):29797-804 PMID: 15123663
  23. Downregulation of prostaglandin E receptor subtype EP3 during colon cancer development.
    Gut. 2004 Aug;53(8):1151-8 PMID: 15247185
  24. Prostaglandin EP receptors: targets for treatment and prevention of colorectal cancer?
    Mol Cancer Ther. 2004 Aug;3(8):1031-9 PMID: 15299086
  25. Comprehensive gene expression profiles reveal pathways related to the pathogenesis of chronic obstructive pulmonary disease.
    Proc Natl Acad Sci U S A. 2004 Oct 12;101(41):14895-900 PMID: 15469929
  26. New colorimetric cytotoxicity assay for anticancer-drug screening.
    J Natl Cancer Inst. 1990 Jul 4;82(13):1107-12 PMID: 2359136
  27. Investigation of colonic prostaglandins in carcinogenesis in the rat colon.
    Dis Colon Rectum. 1991 Jul;34(7):572-6 PMID: 2055143
  28. Altered eicosanoid levels in human colon cancer.
    J Lab Clin Med. 1993 Nov;122(5):518-23 PMID: 8228569
  29. Up-regulation of cyclooxygenase 2 gene expression in human colorectal adenomas and adenocarcinomas.
    Gastroenterology. 1994 Oct;107(4):1183-8 PMID: 7926468
  30. 6-Isopropoxy-9-oxoxanthene-2-carboxylic acid (AH 6809), a human EP2 receptor antagonist.
    Biochem Pharmacol. 1995 Nov 9;50(10):1731-3 PMID: 7503778
  31. Increased cyclooxygenase-2 levels in carcinogen-induced rat colonic tumors.
    Gastroenterology. 1996 Apr;110(4):1259-62 PMID: 8613017
  32. Selective regulation of RNK-16 cell matrix metalloproteinases by the EP4 subtype of prostaglandin E2 receptor.
    Biochemistry. 1996 Jun 4;35(22):7159-64 PMID: 8679543
  33. Suppression of intestinal polyposis in Apc delta716 knockout mice by inhibition of cyclooxygenase 2 (COX-2).
    Cell. 1996 Nov 29;87(5):803-9 PMID: 8945508
  34. A dominant-negative inhibitor of CREB reveals that it is a general mediator of stimulus-dependent transcription of c-fos.
    Mol Cell Biol. 1998 Feb;18(2):967-77 PMID: 9447994
  35. Prostaglandin levels in human colorectal mucosa: effects of sulindac in patients with familial adenomatous polyposis.
    Dig Dis Sci. 1998 Feb;43(2):311-6 PMID: 9512123
  36. EP4/EP2 receptor-specific prostaglandin E2 regulation of interleukin-6 generation by human HSB.2 early T cells.
    J Pharmacol Exp Ther. 1998 Sep;286(3):1420-6 PMID: 9732406
  37. Egr-1 is activated by 17beta-estradiol in MCF-7 cells by mitogen-activated protein kinase-dependent phosphorylation of ELK-1.
    J Cell Biochem. 2004 Nov 15;93(5):1063-74 PMID: 15449318
  38. Prostaglandin E2 reduces radiation-induced epithelial apoptosis through a mechanism involving AKT activation and bax translocation.
    J Clin Invest. 2004 Dec;114(11):1676-85 PMID: 15578100
  39. NF-kappaB/Egr-1/Gadd45 are sequentially activated upon UVB irradiation to mediate epidermal cell death.
    EMBO J. 2005 Jan 12;24(1):128-37 PMID: 15616591
  40. Prostaglandin E receptor subtype EP(1) deficiency inhibits colon cancer development.
    Carcinogenesis. 2005 Feb;26(2):353-7 PMID: 15564292
  41. Prostaglandin E2 induces MUC8 gene expression via a mechanism involving ERK MAPK/RSK1/cAMP response element binding protein activation in human airway epithelial cells.
    J Biol Chem. 2005 Feb 25;280(8):6676-81 PMID: 15615708
  42. Early growth response factor-1 mediates prostaglandin E2-dependent transcriptional suppression of cytokine-induced tumor necrosis factor-alpha gene expression in human macrophages and rheumatoid arthritis-affected synovial fibroblasts.
    J Biol Chem. 2005 Mar 11;280(10):9536-46 PMID: 15640148
  43. Prostaglandin E2 enhances intestinal adenoma growth via activation of the Ras-mitogen-activated protein kinase cascade.
    Cancer Res. 2005 Mar 1;65(5):1822-9 PMID: 15753380
  44. PGE2-induced hypertrophy of cardiac myocytes involves EP4 receptor-dependent activation of p42/44 MAPK and EGFR transactivation.
    Am J Physiol Heart Circ Physiol. 2005 May;288(5):H2111-7 PMID: 15626689
  45. Bombesin regulates cyclin D1 expression through the early growth response protein Egr-1 in prostate cancer cells.
    Cancer Res. 2005 Nov 1;65(21):9934-42 PMID: 16267018
  46. Prostaglandin E2 promotes cell survival of glomerular epithelial cells via the EP4 receptor.
    Am J Physiol Renal Physiol. 2006 Jun;290(6):F1534-42 PMID: 16396944
Article Info
Journal
Experimental cell research
Abbr.
Exp Cell Res
ISSN
0014-4827
Published
2007-08-15
Epub
2007-00-22
Pages
2969-79
Language
English
Region
United States
NLM ID
0373226
PMCID
PMC2706013
Subset
IM
Grants
NCI NIH HHS · R01 CA097383 · United States
NCI NIH HHS · R01 CA097383-02 · United States
NCI NIH HHS · CA 097383 · United States
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