Molecules and Cells

Korean Society for Molecular and Cellular Biology (한국분자세포생물학회)
권호 표지

Activation of p38 MAPK Is Involved in Endothelin-1-stimulated COX-2 Expression in Cultured Feline Esophageal Smooth Muscle Cells

  • Song, Hyun Ju (Department of Pharmacology, College of Pharmacy, Chung Ang University) ;
  • Min, Young Sil (Department of Pharmacology, College of Pharmacy, Chung Ang University) ;
  • Shin, Chang Yell (Department of Pharmacology, College of Pharmacy, Chung Ang University) ;
  • Jeong, Ji Hoon (Department of Pharmacology, School of Medicine, Chung Ang University) ;
  • Sohn, Uy Dong (Department of Pharmacology, College of Pharmacy, Chung Ang University)
  • Received : 2006.02.27
  • Accepted : 2006.06.12
  • Published : 2006.08.31
⟨ Previous Next ⟩

Abstract

We investigated the possible role of p38 MAPK and $ET_B$ receptors in ET-1 induction of cyclooxygenase-2 (COX-2) and prostaglandin $E_2$ ($PGE_2$) in cultured feline esophageal smooth muscle cells (ESMC). Confluent layers of ESMC were stimulated with 10 nM ET-1 and expression of COX-1 and COX-2, involvement of receptors, and activation of p38 MAPK, were examined by Western blot analysis. Levels of $PGE_2$ induced by ET-1 were measured by Elisa. Using $ET_A$and $ET_B$ antagonists (BQ-123 and BQ-788, respectively), the contribution of the ET receptors to COX-1 and COX-2 expression induced by ET-1 was determined. Western blot analysis revealed that treatment of ESMC with ET-1 resulted in transient expression of COX-2 and activation of p38 MAPK. Activation of p38 MAPK was maximal after 1 h. SB202190, a p38 MAPK inhibitor, reduced expression of COX-2, but not COX-1. ET-1-induced release of $PGE_2$ was also blocked by SB202190. COX-2 expression was upregulated only via the $ET_B$ receptor, and COX-1 expression was not affected by either antagonist. Taken together, our data suggest that ET-1 causes p38 MAPK-dependent expression of COX-2 by interacting with $ET_B$ receptors on ESMC.

Keywords

Acknowledgement

Supported by : Chung Ang University

References

  1. Arai, H., Hori, S., Aramori, I., Ohkubo, H., and Nakanishi, S. (1990) Cloning and expression of a cDNA encoding an endothelin receptor. Nature 348, 730−732 https://doi.org/10.1038/348730a0
  2. Arun, C., London, N. J., and Hemingway, D. M. (2004) Prognostic significance of elevated endothelin-1 levels in patients with colorectal cancer. Int. J. Biol. Markers 19, 32−37
  3. Biancani, P., Zabinski, M., Kerstein, M., and Behar, J. (1982) Lower esophageal sphincter mechanics: anatomic and physiologic relationships of the esophagogastric junction of cat. Gastroenterology 82, 468−475
  4. Biancani, P., Hillemeier, C., Bitar, K. N., and Makhlouf, G. M. (1987) Contraction mediated by $Ca^{2+}$ influx in esophageal muscle and by $Ca^{2+}$ release in the LES. Am. J. Physiol. 253, G760−766
  5. Chen, D., Balyakina, E. V., Lawrence, M., Christman, B. W., and Meyrick, B. (2003) Cyclooxygenase is regulated by ET-1 and MAPKs in peripheral lung microvascular smooth muscle cells. Am. J. Physiol. Lung Cell Mol. Physiol. 284, L614−621
  6. Deng, L. Y., Li, J. S., and Schiffrin, E. L. (1995) Endothelin receptor subtypes in resistance arteries from humans and rats. Cardiovasc. Res. 29, 532−535
  7. Dubois, R. N., Abramson, S. B., Crofford, L., Gupta, R. A., Simon, L. S., et al. (1998) Cyclooxygenase in biology and disease. Faseb. J. 12, 1063−1073
  8. Gallois, C., Habib, A., Tao, J., Moulin, S., Maclouf, J., et al. (1998) Role of NF-kappaB in the antiproliferative effect of endothelin-1 and tumor necrosis factor-alpha in human hepatic stellate cells. Involvement of cyclooxygenase-2. J. Biol. Chem. 273, 23183−23190 https://doi.org/10.1074/jbc.273.36.23183
  9. Guan, Z., Buckman, S. Y., Miller, B. W., Springer, L. D., and Morrison, A. R. (1998) 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 https://doi.org/10.1074/jbc.273.44.28670
  10. Guo, Y. S., Hellmich, M. R., Wen, X. D., and Townsend, C. M., Jr. (2001) Activator protein-1 transcription factor mediates bombesin-stimulated cyclooxygenase-2 expression in intestinal epithelial cells. J. Biol. Chem. 276, 22941−22947 https://doi.org/10.1074/jbc.M101801200
  11. Hersch, E., Huang, J., Grider, J. R., and Murthy, K. S. (2004) Gq/G13 signaling by ET-1 in smooth muscle: MYPT1 phosphorylation via ETA and CPI-17 dephosphorylation via ETB. Am. J. Physiol. Cell Physiol. 287, C1209−1218 https://doi.org/10.1152/ajpcell.00198.2004
  12. Huang, S. C. (2005) Endothelin receptors in lower esophageal sphincter circular smooth muscle. Regul. Pept. 127, 27−35 https://doi.org/10.1016/j.regpep.2004.10.009
  13. Huang, S. C., Lee, M. C., Wei, C. K., and Huang, S. M. (2001) Endothelin receptors in human and guinea-pig gallbladder muscle. Regul. Pept. 98, 145−153 https://doi.org/10.1016/S0167-0115(00)00238-X
  14. Hundley, T. R., Prasad, A. R., and Beaven, M. A. (2001) Elevated levels of cyclooxygenase-2 in antigen-stimulated mast cells is associated with minimal activation of p38 mitogenactivated protein kinase. J. Immunol. 167, 1629−1636
  15. Inui, T., James, A. F., Fujitani, Y., Takimoto, M., Okada, T., et al. (1994) ETA and ETB receptors on single smooth muscle cells cooperate in mediating guinea pig tracheal contraction. Am. J. Physiol. 266, L113−124
  16. Kedzierski, R. M. and Yanagisawa, M. (2001) Endothelin system: the double-edged sword in health and disease. Annu. Rev. Pharmacol. Toxicol. 41, 851−876 https://doi.org/10.1146/annurev.pharmtox.41.1.851
  17. Kitsukawa, Y., Gu, Z. F., Hildebrand, P., and Jensen, R. T. (1994) Gastric smooth muscle cells possess two classes of endothelin receptors but only one alters contraction. Am. J. Physiol. 266, G713−721
  18. Koepp, J., Cardozo, A. M., D'Orleans-Juste, P., and Rae, G. A. (2002) Influence of indomethacin on effects of endothelin-1 on guinea pig isolated rings of common bile duct and sphincter of Oddi. Eur. J. Pharmacol. 435, 103−111 https://doi.org/10.1016/S0014-2999(01)01564-3
  19. Kruger, H., Carr, S., Brennand, J. C., and McLean, J. S. (1995) Activation of phospholipase A2 by the human endothelin receptor in Chinese hamster ovary cells involves Gi proteinmediated calcium influx. Biochem. Biophys. Res. Commun. 217, 52−58
  20. LaPointe, M. C. and Isenovic, E. (1999) Interleukin-1beta regulation of inducible nitric oxide synthase and cyclooxygenase- 2 involves the p42/44 and p38 MAPK signaling pathways in cardiac myocytes. Hypertension 33, 276−282 https://doi.org/10.1161/01.HYP.33.1.44
  21. Lee, S. C., Han, J. S., Seo, J. K., and Cha, Y. N. (2003) Modulation of cyclooxygenase-2 expression by phosphatidylcholine specific phospholipase C and D in macrophages stimulated with lipopolysaccharide. Mol. Cells 15, 320−326
  22. Lin, C. C., Hsiao, L. D., Chien, C. S., Lee, C. W., Hsieh, J. T., et al. (2004) Tumor necrosis factor-alpha-induced cyclooxygenase- 2 expression in human tracheal smooth muscle cells: involvement of p42/p44 and p38 mitogen-activated protein kinases and nuclear factor-kappaB. Cell. Signal. 16, 597−607 https://doi.org/10.1016/j.cellsig.2003.10.002
  23. Liu, L., Zhang, M., Luo, B., Abrams, G. A., and Fallon, M. B. (2001) Biliary cyst fluid from common bile duct-ligated rats stimulates endothelial nitric oxide synthase in pulmonary artery endothelial cells: a potential role in hepatopulmonary syndrome. Hepatology 33, 722−727 https://doi.org/10.1053/jhep.2001.22701
  24. Luo, S. F., Wang, C. C., Chien, C. S., Hsiao, L. D., and Yang, C. M. (2003) Induction of cyclooxygenase-2 by lipopolysaccharide in canine tracheal smooth muscle cells: involvement of p42/p44 and p38 mitogen-activated protein kinases and nuclear factor-kappaB pathways. Cell. Signal. 15, 497−509 https://doi.org/10.1016/S0898-6568(02)00135-3
  25. Marcinkiewicz, M., Sarosiek, J., Edmunds, M., Scheurich, J., Weiss, P., et al. (1995) Monophasic luminal release of prostaglandin E2 in patients with reflux esophagitis under the impact of acid and acid/pepsin solutions. Its potential pathogenetic significance. J. Clin. Gastroenterol. 21, 268−274
  26. Mitchell, J. A. and Warner, T. D. (1999) Cyclo-oxygenase-2: pharmacology, physiology, biochemistry and relevance to NSAID therapy. Br. J. Pharmacol. 128, 1121−1132 https://doi.org/10.1038/sj.bjp.0702897
  27. Mizuno, H., Sakamoto, C., Matsuda, K., Wada, K., Uchida, T., et al. (1997) Induction of cyclooxygenase 2 in gastric mucosal lesions and its inhibition by the specific antagonist delays healing in mice. Gastroenterology 112, 387−397
  28. Molero, L., Farre, J., Garcia-Mendez, A., Jimenez Mateos- Caceres, P., Carrasco Martin, C., et al. (2003) Endothelin-1 induced proinflammatory markers in the myocardium and leukocytes of guinea-pigs: role of glycoprotein IIB/IIIA receptors. Cardiovasc. Res. 57, 109−118 https://doi.org/10.1016/S0008-6363(02)00657-0
  29. Moore, K. (2004) Endothelin and vascular function in liver disease. Gut 53, 159−161 https://doi.org/10.1136/gut.2003.024703
  30. Nelson, J., Bagnato, A., Battistini, B., and Nisen, P. (2003) The endothelin axis: emerging role in cancer. Nat. Rev. Cancer 3, 110−116 https://doi.org/10.1038/nrc990
  31. Ohta, M., Pai, R., Kawanaka, H., Ma, T., Sugimachi, K., et al. (2000) Expression of endothelin-1, and endothelin A and B receptors in portal hypertensive esophagus of rats. J. Physiol. Pharmacol. 51, 57−67
  32. Pratt, P. F., Bokemeyer, D., Foschi, M., Sorokin, A., and Dunn, M. J. (2003) Alterations in subcellular localization of p38 MAPK potentiates endothelin-stimulated COX-2 expression in glomerular mesangial cells. J. Biol. Chem. 278, 51928−51936 https://doi.org/10.1074/jbc.M309256200
  33. Rebsamen, M. C., Capoccia, R., Vallotton, M. B., and Lang, U. (2003) Role of cyclooxygenase 2, p38 and p42/44 MAPK in the secretion of prostacyclin induced by epidermal growth factor, endothelin-1 and angiotensin II in rat ventricular cardiomyocytes. J. Mol. Cell. Cardiol. 35, 81−89 https://doi.org/10.1016/S0022-2828(02)00281-X
  34. Ristimaki, A., Honkanen, N., Jankala, H., Sipponen, P., and Harkonen, M. (1997) Expression of cyclooxygenase-2 in human gastric carcinoma. Cancer Res. 57, 1276−1280
  35. Rubanyi, G. M. and Polokoff, M. A. (1994) Endothelins: molecular biology, biochemistry, pharmacology, physiology, and pathophysiology. Pharmacol. Rev. 46, 325−415
  36. Sakurai, T., Yanagisawa, M., Takuwa, Y., Miyazaki, H., Kimura, S., et al. (1990) Cloning of a cDNA encoding a nonisopeptide- selective subtype of the endothelin receptor. Nature 348, 732−735 https://doi.org/10.1038/348732a0
  37. Schiffrin, E. L. and Touyz, R. M. (1998) Vascular biology of endothelin. J. Cardiovasc. Pharmacol. 32 (Suppl 3), S2−13
  38. Shin, C. Y., Lee, Y. P., Lee, T. S., Je, H. D., Kim, D. S., et al. (2002) The signal transduction of endothelin-1-induced circular smooth muscle cell contraction in cat esophagus. J. Pharmacol. Exp. Ther. 302, 924−934 https://doi.org/10.1124/jpet.302.3.924
  39. Shirvani, V. N., Ouatu-Lascar, R., Kaur, B. S., Omary, M. B., and Triadafilopoulos, G. (2000) Cyclooxygenase 2 expression in Barrett's esophagus and adenocarcinoma: ex vivo induction by bile salts and acid exposure. Gastroenterology 118, 487−496 https://doi.org/10.1016/S0016-5085(00)70254-X
  40. Singer, II, Kawka, D. W., Schloemann, S., Tessner, T., Riehl, T., et al. (1998) Cyclooxygenase 2 is induced in colonic epithelial cells in inflammatory bowel disease. Gastroenterology 115, 297−306
  41. Smith, W. L., Garavito, R. M., and DeWitt, D. L. (1996) Prostaglandin endoperoxide H synthases (cyclooxygenases)-1 and -2. J. Biol. Chem. 271, 33157−33160 https://doi.org/10.1074/jbc.271.52.33157
  42. Smith, W. L., DeWitt, D. L., and Garavito, R. M. (2000) Cyclooxygenases: structural, cellular, and molecular biology. Annu. Rev. Biochem. 69, 145−182
  43. Sugimoto, T., Haneda, M., Sawano, H., Isshiki, K., Maeda, S., et al. (2001) Endothelin-1 induces cyclooxygenase-2 expression via nuclear factor of activated T-cell transcription factor in glomerular mesangial cells. J. Am. Soc. Nephrol. 12, 1359−1368
  44. Sung, Y. K., Hwang, S. Y., Kim, J. O., Bae, H. I., Kim, J. C., et al. (2004) The correlation between cyclooxygenase-2 expression and hepatocellular carcinogenesis. Mol. Cells 17, 35−38
  45. Uchida, K., Yuzuki, R., and Kamikawa, Y. (1998) Pharmacological characterization of endothelin-induced contraction in the guinea-pig oesophageal muscularis mucosae. Br. J. Pharmacol. 125, 849−857 https://doi.org/10.1038/sj.bjp.0702140
  46. Vane, J. R., Bakhle, Y. S., and Botting, R. M. (1998) Cyclooxygenases 1 and 2. Annu. Rev. Pharmacol. Toxicol. 38, 97−120
  47. Vigne, P. and Frelin, C. (1994) Endothelins activate phospholipase A2 in brain capillary endothelial cells. Brain Res. 651, 342−344
  48. Wilson, K. T., Fu, S., Ramanujam, K. S., and Meltzer, S. J. (1998) Increased expression of inducible nitric oxide synthase and cyclooxygenase-2 in Barrett's esophagus and associated adenocarcinomas. Cancer Res. 58, 2929−2934
  49. Xie, W. L., Chipman, J. G., Robertson, D. L., Erikson, R. L., and Simmons, D. L. (1991) Expression of a mitogen-responsive gene encoding prostaglandin synthase is regulated by mRNA splicing. Proc. Natl. Acad. Sci. USA 88, 2692−2696
  50. Yanagisawa, M., Kurihara, H., Kimura, S., Tomobe, Y., Kobayashi, M., et al. (1988) A novel potent vasoconstrictor peptide produced by vascular endothelial cells. Nature 332, 411−415