DOI QR코드

DOI QR Code

Posttranscriptional and posttranslational determinants of cyclooxygenase expression

  • Mbonye, Uri R. (Department of Molecular Biology and Microbiology, Case Western Reserve University) ;
  • Song, In-Seok (Department of Life Science, University of Seoul)
  • Published : 2009.09.30

Abstract

Cyclooxygenases (COX-1 and COX-2) are ER-resident proteins that catalyze the committed step in prostanoid synthesis. COX-1 is constitutively expressed in many mammalian cells, whereas COX-2 is usually expressed inducibly and transiently. Abnormal expression of COX-2 has been implicated in the pathogenesis of chronic inflammation and various cancers; therefore, it is subject to tight and complex regulation. Differences in regulation of the COX enzymes at the posttranscriptional and posttranslational levels also contribute significantly to their distinct patterns of expression. Rapid degradation of COX-2 mRNA has been attributed to AU-rich elements (AREs) at its 3’UTR. Recently, microRNAs that can selectively repress COX-2 protein synthesis have been identified. The mature forms of these COX proteins are very similar in structure except that COX-2 has a unique 19-amino acid (19-aa) segment located near the C-terminus. This C-terminal 19-aa cassette plays an important role in mediation of the entry of COX-2 into the ER-associated degradation (ERAD) system, which transports ER proteins to the cytoplasm for degradation by the 26S proteasome. A second pathway for COX-2 protein degradation is initiated after the enzyme undergoes suicide inactivation following cyclooxygenase catalysis. Here, we discuss these molecular determinants of COX-2 expression in detail.

Keywords

References

  1. Smith, W. L., DeWitt, D. L. and Garavito, R. M. (2000) Cyclooxygenases: structural, cellular, and molecular biology. Annu. Rev. Biochem. 69, 145-182 https://doi.org/10.1146/annurev.biochem.69.1.145
  2. Narumiya, S. and FitzGerald, G. A. (2001) Genetic and pharmacological analysis of prostanoid receptor function. J. Clin. Invest. 108, 25-30 https://doi.org/10.1172/JCI200113455
  3. Rouzer, C. A. and Marnett, L. J. (2009) Cyclooxygenases: structural and functional insights. J. Lipid. Res. 50(Suppl), S29-34 https://doi.org/10.1194/jlr.R800042-JLR200
  4. Smith, W. L. (2008) Nutritionally essential fatty acids and biologically indispensable cyclooxygenases. Trends. Biochem. Sci. 33, 27-37 https://doi.org/10.1016/j.tibs.2007.09.013
  5. Funk, C. D. (2001) Prostaglandins and leukotrienes: advances in eicosanoid biology. Science 294, 1871-1875 https://doi.org/10.1126/science.294.5548.1871
  6. Kobayashi, T. and Narumiya, S. (2002) Function of prostanoid receptors: studies on knockout mice. Prostaglandins. Other. Lipid. Mediat. 68-69, 557-573 https://doi.org/10.1016/S0090-6980(02)00055-2
  7. Zhang, Y., Shaffer, A., Portanova, J., Seibert, K. and Isakson, P. C. (1997) Inhibition of cyclooxygenase-2 rapidly reverses inflammatory hyperalgesia and prostaglandin E2 production. J. Pharmacol. Exp. Ther. 283, 1069-1075
  8. Samad, T. A., Moore, K. A., Sapirstein, A., Billet, S., Allchorne, A., Poole, S., Bonventre, J. V. and Woolf, C. J. (2001) Interleukin-1beta-mediated induction of Cox-2 in the CNS contributes to inflammatory pain hypersensitivity. Nature 410, 471-475 https://doi.org/10.1038/35068566
  9. Leahy, K. M., Ornberg, R. L., Wang, Y., Zweifel, B. S., Koki, A. T. and Masferrer, J. L. (2002) Cyclooxygenase-2 inhibition by celecoxib reduces proliferation and induces apoptosis in angiogenic endothelial cells in vivo. Cancer Res. 62, 625-631
  10. Cao, C., Matsumura, K., Yamagata, K. and Watanabe, Y. (1998) Cyclooxygenase-2 is induced in brain blood vessels during fever evoked by peripheral or central administration of tumor necrosis factor. Brain. Res. Mol. Brain. Res. 56, 45-56 https://doi.org/10.1016/S0169-328X(98)00025-4
  11. Sinicrope, F. A. (2006) Targeting cyclooxygenase-2 for prevention and therapy of colorectal cancer. Mol. Carcinog. 45, 447-454 https://doi.org/10.1002/mc.20232
  12. van der Donk, W. A., Tsai, A. L. and Kulmacz, R. J. (2002) The cyclooxygenase reaction mechanism. Biochemistry 41, 15451-15458 https://doi.org/10.1021/bi026938h
  13. Spencer, A. G., Thuresson, E., Otto, J. C., Song, I., Smith, T., DeWitt, D. L., Garavito, R. M. and Smith, W. L. (1999) The membrane binding domains of prostaglandin endoperoxide H synthases 1 and 2. Peptide mapping and mutational analysis. J. Biol. Chem. 274, 32936-32942 https://doi.org/10.1074/jbc.274.46.32936
  14. Kiefer, J. R., Pawlitz, J. L., Moreland, K. T., Stegeman, R. A., Hood, W. F., Gierse, J. K., Stevens, A. M., Goodwin, D. C., Rowlinson, S. W., Marnett, L. J., Stallings, W. C. and Kurumbail, R. G. (2000) Structural insights into the stereochemistry of the cyclooxygenase reaction. Nature 405, 97-101 https://doi.org/10.1038/35011103
  15. Picot, D., Loll, P. J. and Garavito, R. M. (1994) The X-ray crystal structure of the membrane protein prostaglandin H2 synthase-1. Nature 367, 243-249 https://doi.org/10.1038/367243a0
  16. Yuan, C., Rieke, C. J., Rimon, G., Wingerd, B. A. and Smith, W. L. (2006) Partnering between monomers of cyclooxygenase-2 homodimers. Proc. Natl. Acad. Sci. U.S.A. 103, 6142-6147 https://doi.org/10.1073/pnas.0601805103
  17. Xiao, G., Chen, W. and Kulmacz, R. J. (1998) Comparison of structural stabilities of prostaglandin H synthase-1 and -2. J. Biol. Chem. 273, 6801-6811 https://doi.org/10.1074/jbc.273.12.6801
  18. Kurumbail, R. G., Stevens, A. M., Gierse, J. K., McDonald, J. J., Stegeman, R. A., Pak, J. Y., Gildehaus, D., Miyashiro, J. M., Penning, T. D., Seibert, K., Isakson, P. C. and Stallings, W. C. (1996) Structural basis for selective inhibition of cyclooxygenase-2 by anti-inflammatory agents. Nature 384, 644-648 https://doi.org/10.1038/384644a0
  19. MirAfzali, Z., Leipprandt, J. R., McCracken, J. L. and DeWitt, D. L. (2006) Topography of the prostaglandin endoperoxide H2 synthase-2 in membranes. J. Biol. Chem. 281, 28354-28364 https://doi.org/10.1074/jbc.M605206200
  20. Otto, J. C. and Smith, W. L. (1994) The orientation of prostaglandin endoperoxide synthases-1 and -2 in the endoplasmic reticulum. J. Biol. Chem. 269, 19868-19875
  21. Spencer, A. G., Woods, J. W., Arakawa, T., Singer, I. I. and Smith, W. L. (1998) Subcellular localization of prostaglandin endoperoxide H synthases-1 and -2 by immunoelectron microscopy. J. Biol. Chem. 273, 9886-9893 https://doi.org/10.1074/jbc.273.16.9886
  22. Mbonye, U. R., Wada, M., Rieke, C. J., Tang, H. Y., Dewitt, D. L. and Smith, W. L. (2006) The 19-amino acid cassette of cyclooxygenase-2 mediates entry of the protein into the endoplasmic reticulum-associated degradation system. J. Biol. Chem. 281, 35770-35778 https://doi.org/10.1074/jbc.M608281200
  23. DeWitt, D. L. and Meade, E. A. (1993) Serum and glucocorticoid regulation of gene transcription and expression of the prostaglandin H synthase-1 and prostaglandin H synthase-2 isozymes. Arch. Biochem. Biophys. 306, 94-102 https://doi.org/10.1006/abbi.1993.1485
  24. Miyamoto, T., Ogino, N., Yamamoto, S. and Hayaishi, O. (1976) Purification of prostaglandin endoperoxide synthetase from bovine vesicular gland microsomes. J. Biol. Chem. 251, 2629-2636
  25. Xu, X. M., Tang, J. L., Chen, X., Wang, L. H. and Wu, K. K. (1997) Involvement of two Sp1 elements in basal endothelial prostaglandin H synthase-1 promoter activity. J. Biol. Chem. 272, 6943-6950 https://doi.org/10.1074/jbc.272.11.6943
  26. Duquette, M. and Laneuville, O. (2002) Translational regulation of prostaglandin endoperoxide H synthase-1 mRNA in megakaryocytic MEG-01 cells. Specific protein binding to a conserved 20-nucleotide CIS element in the 3'-untranslated region. J. Biol. Chem. 277, 44631-44637 https://doi.org/10.1074/jbc.M207007200
  27. Xu, X. M., Tang, J. L., Hajibeigi, A., Loose-Mitchell, D. S. and Wu, K. K. (1996) Transcriptional regulation of endothelial constitutive PGHS-1 expression by phorbol ester. Am. J. Physiol. 270, C259-264 https://doi.org/10.1152/ajpcell.1996.270.1.C259
  28. Perkins, D. J. and Kniss, D. A. (1997) Rapid and transient induction of cyclo-oxygenase 2 by epidermal growth factor in human amnion-derived WISH cells. Biochem. J. 321 (Pt 3), 677-681 https://doi.org/10.1042/bj3210677
  29. Rich, G., Yoder, E. J., and Moore, S. A. (1998) Regulation of prostaglandin H synthase-2 expression in cerebromicrovascular smooth muscle by serum and epidermal growth factor. J. Cell. Physiol. 176, 495-505 https://doi.org/10.1002/(SICI)1097-4652(199809)176:3<495::AID-JCP6>3.0.CO;2-J
  30. Zaric, J. and Ruegg, C. (2005) Integrin-mediated adhesion and soluble ligand binding stabilize COX-2 protein levels in endothelial cells by inducing expression and preventing degradation. J. Biol. Chem. 280, 1077-1085 https://doi.org/10.1074/jbc.M410006200
  31. Langenbach, R., Morham, S. G., Tiano, H. F., Loftin, C. D., Ghanayem, B. I., Chulada, P. C., Mahler, J. F., Lee, C. A., Goulding, E. H., Kluckman, K. D., Kim, H. S. and Smithies, O. (1995) Prostaglandin synthase 1 gene disruption in mice reduces arachidonic acid-induced inflammation and indomethacin-induced gastric ulceration. Cell. 83, 483-492 https://doi.org/10.1016/0092-8674(95)90126-4
  32. Moncada, S. and Vane, J. R. (1979) The role of prostacyclin in vascular tissue. Fed. Proc. 38, 66-71
  33. Liou, J. Y., Shyue, S. K., Tsai, M. J., Chung, C. L., Chu, K. Y. and Wu, K. K. (2000) Colocalization of prostacyclin synthase with prostaglandin H synthase-1 (PGHS-1) but not phorbol ester-induced PGHS-2 in cultured endothelial cells. J. Biol. Chem. 275, 15314-15320 https://doi.org/10.1074/jbc.275.20.15314
  34. Bustos, M., Coffman, T. M., Saadi, S. and Platt, J. L. (1997) Modulation of eicosanoid metabolism in endothelial cells in a xenograft model. Role of cyclooxygenase-2. J. Clin. Invest. 100, 1150-1158 https://doi.org/10.1172/JCI119626
  35. Okahara, K., Sun, B. and Kambayashi, J. (1998) Upregulation of prostacyclin synthesis-related gene expression by shear stress in vascular endothelial cells. Arterioscler. Thromb. Vasc. Biol. 18, 1922-1926 https://doi.org/10.1161/01.ATV.18.12.1922
  36. Caughey, G. E., Cleland, L. G., Penglis, P. S., Gamble, J. R. and James, M. J. (2001) Roles of cyclooxygenase (COX)-1 and COX-2 in prostanoid production by human endothelial cells: selective up-regulation of prostacyclin synthesis by COX-2. J. Immunol. 167, 2831-2838 https://doi.org/10.4049/jimmunol.167.5.2831
  37. DeWitt, D. L., Day, J. S., Sonnenburg, W. K. and Smith, W. L. (1983) Concentrations of prostaglandin endoperoxide synthase and prostaglandin I2 synthase in the endothelium and smooth muscle of bovine aorta. J. Clin. Invest. 72, 1882-1888 https://doi.org/10.1172/JCI111151
  38. Schildknecht, S., Bachschmid, M., Baumann, A. and Ullrich, V. (2004) COX-2 inhibitors selectively block prostacyclin synthesis in endotoxin-exposed vascular smooth muscle cells. Faseb. J. 18, 757-759 https://doi.org/10.1096/fj.03-0609fje
  39. Wang, L. H., Hajibeigi, A., Xu, X. M., Loose-Mitchell, D. and Wu, K. K. (1993) Characterization of the promoter of human prostaglandin H synthase-1 gene. Biochem. Biophys. Res. Commun. 190, 406-411 https://doi.org/10.1006/bbrc.1993.1062
  40. Tanabe, T. and Tohnai, N. (2002) Cyclooxygenase isozymes and their gene structures and expression. Prostaglandins. Other. Lipid. Mediat. 68-69, 95-114 https://doi.org/10.1016/S0090-6980(02)00024-2
  41. Kang, Y. J., Wingerd, B. A., Arakawa, T. and Smith, W. L. (2006) Cyclooxygenase-2 gene transcription in a macrophage model of inflammation. J. Immunol. 177, 8111-8122 https://doi.org/10.4049/jimmunol.177.11.8111
  42. Kang, Y. J., Mbonye, U. R., DeLong, C. J., Wada, M. and Smith, W. L. (2007) Regulation of intracellular cyclooxygenase levels by gene transcription and protein degradation. Prog. Lipid. Res. 46, 108-125 https://doi.org/10.1016/j.plipres.2007.01.001
  43. Chen, C. Y. and Shyu, A. B. (1994) Selective degradation of early-response-gene mRNAs: functional analyses of sequence features of the AU-rich elements. Mol. Cell. Biol. 14, 8471-84820 https://doi.org/10.1128/MCB.14.12.8471
  44. Chen, C. Y., Chen, T. M. and Shyu, A. B. (1994) Interplay of two functionally and structurally distinct domains of the c-fos AU-rich element specifies its mRNA-destabilizing function. Mol. Cell. Biol. 14, 416-426 https://doi.org/10.1128/MCB.14.1.416
  45. Dixon, D. A., Tolley, N. D., King, P. H., Nabors, L. B., McIntyre, T. M., Zimmerman, G. A. and Prescott, S. M. (2001) Altered expression of the mRNA stability factor HuR promotes cyclooxygenase-2 expression in colon cancer cells. J. Clin. Invest. 108, 1657-1665 https://doi.org/10.1172/JCI12973
  46. Murmu, N., Jung, J., Mukhopadhyay, D., Houchen, C. W., Riehl, T. E., Stenson, W. F., Morrison, A. R., Arumugam, T., Dieckgraefe, B. K. and Anant, S. (2004) Dynamic antagonism between RNA-binding protein CUGBP2 and cyclooxygenase-2-mediated prostaglandin E2 in radiation damage. Proc. Natl. Acad. Sci. U.S.A. 101, 13873-13878 https://doi.org/10.1073/pnas.0406066101
  47. Mukhopadhyay, D., Houchen, C. W., Kennedy, S., Dieckgraefe, B. K. and Anant, S. (2003) Coupled mRNA stabilization and translational silencing of cyclooxygenase-2 by a novel RNA binding protein, CUGBP2. Mol. Cell. 11, 113-126 https://doi.org/10.1016/S1097-2765(03)00012-1
  48. Lasa, M., Mahtani, K. R., Finch, A., Brewer, G., Saklatvala, J. and Clark, A. R. (2000) Regulation of cyclooxygenase 2 mRNA stability by the mitogen-activated protein kinase p38 signaling cascade. Mol. Cell. Biol. 20, 4265-4274 https://doi.org/10.1128/MCB.20.12.4265-4274.2000
  49. Lasa, M., Brook, M., Saklatvala, J., and Clark, A. R. (2001) Dexamethasone destabilizes cyclooxygenase 2 mRNA by inhibiting mitogen-activated protein kinase p38. Mol. Cell. Biol. 21, 771-780 https://doi.org/10.1128/MCB.21.3.771-780.2001
  50. Lim, H., Paria, B. C., Das, S. K., Dinchuk, J. E., Langenbach, R., Trzaskos, J. M. and Dey, S. K. (1997) Multiple female reproductive failures in cyclooxygenase 2-deficient mice. Cell. 91, 197-208 https://doi.org/10.1016/S0092-8674(00)80402-X
  51. Chakrabarty, A., Tranguch, S., Daikoku, T., Jensen, K., Furneaux, H. and Dey, S. K. (2007) MicroRNA regulation of cyclooxygenase-2 during embryo implantation. Proc. Natl. Acad. Sci. U. S. A. 104, 15144-15149 https://doi.org/10.1073/pnas.0705917104
  52. Jing, Q., Huang, S., Guth, S., Zarubin, T., Motoyama, A., Chen, J., Di Padova, F., Lin, S. C., Gram, H. and Han, J. (2005) Involvement of microRNA in AU-rich elementmediated mRNA instability. Cell. 120, 623-634 https://doi.org/10.1016/j.cell.2004.12.038
  53. Jackson, R. J. and Standart, N. (2007) How do microRNAs regulate gene expression? Sci. STKE. 2007, re1
  54. Mbonye, U. R., Yuan, C., Harris, C. E., Sidhu, R. S., Song, I., Arakawa, T. and Smith, W. L. (2008) Two distinct pathways for cyclooxygenase-2 protein degradation. J. Biol. Chem. 283, 8611-8623 https://doi.org/10.1074/jbc.M710137200
  55. Rockwell, P., Yuan, H., Magnusson, R. and Figueiredo-Pereira, M. E. (2000) Proteasome inhibition in neuronal cells induces a proinflammatory response manifested by upregulation of cyclooxygenase-2, its accumulation as ubiquitin conjugates, and production of the prostaglandin PGE(2). Arch. Biochem. Biophys. 374, 325-333 https://doi.org/10.1006/abbi.1999.1646
  56. Otto, J. C., DeWitt, D. L. and Smith, W. L. (1993) N-glycosylation of prostaglandin endoperoxide synthases-1 and -2 and their orientations in the endoplasmic reticulum. J. Biol. Chem. 268, 18234-18242
  57. Sevigny, M. B., Li, C. F., Alas, M. and Hughes-Fulford, M. (2006) Glycosylation regulates turnover of cyclooxygenase-2. FEBS. Lett. 580, 6533-6536 https://doi.org/10.1016/j.febslet.2006.10.073
  58. Meusser, B., Hirsch, C., Jarosch, E. and Sommer, T. (2005) ERAD: the long road to destruction. Nat. Cell. Biol. 7, 766-772 https://doi.org/10.1038/ncb0805-766
  59. McCracken, A. A. and Brodsky, J. L. (2003) Evolving questions and paradigm shifts in endoplasmic-reticulum- associated degradation (ERAD). Bioessays 25, 868-877 https://doi.org/10.1002/bies.10320
  60. Spiro, R. G. (2004) Role of N-linked polymannose oligosaccharides in targeting glycoproteins for endoplasmic reticulum- associated degradation. Cell. Mol. Life. Sci. 61, 1025-1041 https://doi.org/10.1007/s00018-004-4037-8
  61. Hampton, R. Y. (2002) ER-associated degradation in protein quality control and cellular regulation. Curr. Opin. Cell. Biol. 14, 476-482 https://doi.org/10.1016/S0955-0674(02)00358-7
  62. Spear, E. D. and Ng, D. T. (2005) Single, context-specific glycans can target misfolded glycoproteins for ER-associated degradation. J. Cell. Biol. 169, 73-82 https://doi.org/10.1083/jcb.200411136
  63. McCracken, A. A. and Brodsky, J. L. (2005) Recognition and delivery of ERAD substrates to the proteasome and alternative paths for cell survival. Curr. Top. Microbiol. Immunol. 300, 17-40 https://doi.org/10.1007/3-540-28007-3_2
  64. Ravid, T., Doolman, R., Avner, R., Harats, D. and Roitelman, J. (2000) The ubiquitin-proteasome pathway mediates the regulated degradation of mammalian 3-hydroxy-3-methylglutaryl-coenzyme A reductase. J. Biol. Chem. 275, 35840-35847 https://doi.org/10.1074/jbc.M004793200
  65. Murray, B. P. and Correia, M. A. (2001) Ubiquitin-dependent 26S proteasomal pathway: a role in the degradation of native human liver CYP3A4 expressed in Saccharomyces cerevisiae? Arch. Biochem. Biophys. 393, 106-116 https://doi.org/10.1006/abbi.2001.2482
  66. Webster, J. M., Tiwari, S., Weissman, A. M. and Wojcikiewicz, R. J. (2003) Inositol 1,4,5-trisphosphate receptor ubiquitination is mediated by mammalian Ubc7, a component of the endoplasmic reticulum-associated degradation pathway, and is inhibited by chelation of intracellular Zn2+. J. Biol. Chem. 278, 38238-38246 https://doi.org/10.1074/jbc.M305600200
  67. Tokunaga, F., Brostrom, C., Koide, T. and Arvan, P. (2000) Endoplasmic reticulum (ER)-associated degradation of misfolded N-linked glycoproteins is suppressed upon inhibition of ER mannosidase I. J. Biol. Chem. 275, 40757-40764 https://doi.org/10.1074/jbc.M001073200
  68. Hosokawa, N., Tremblay, L. O., You, Z., Herscovics, A., Wada, I. and Nagata, K. (2003) Enhancement of endoplasmic reticulum (ER) degradation of misfolded Null Hong Kong alpha1-antitrypsin by human ER mannosidase I. J. Biol. Chem. 278, 26287-26294 https://doi.org/10.1074/jbc.M303395200
  69. Fagioli, C. and Sitia, R. (2001) Glycoprotein quality control in the endoplasmic reticulum. Mannose trimming by endoplasmic reticulum mannosidase I times the proteasomal degradation of unassembled immunoglobulin subunits. J. Biol. Chem. 276, 12885-12892 https://doi.org/10.1074/jbc.M009603200
  70. Hosokawa, N., Wada, I., Hasegawa, K., Yorihuzi, T., Tremblay, L. O., Herscovics, A. and Nagata, K. (2001) A novel ER alpha-mannosidase-like protein accelerates ER-associated degradation. EMBO. Rep. 2, 415-422 https://doi.org/10.1093/embo-reports/kve084
  71. Kitzmuller, C., Caprini, A., Moore, S. E., Frenoy, J. P., Schwaiger, E., Kellermann, O., Ivessa, N. E. and Ermonval, M. (2003) Processing of N-linked glycans during endoplasmic-reticulum-associated degradation of a short-lived variant of ribophorin I. Biochem. J. 376, 687-696 https://doi.org/10.1042/BJ20030887
  72. Wu, Y., Swulius, M. T., Moremen, K. W. and Sifers, R. N. (2003) Elucidation of the molecular logic by which misfolded alpha 1-antitrypsin is preferentially selected for degradation. Proc. Natl. Acad. Sci. U.S.A. 100, 8229-8234 https://doi.org/10.1073/pnas.1430537100
  73. Smith, W. L. and Song, I. (2002) The enzymology of prostaglandin endoperoxide H synthases-1 and -2. Prostaglandins. Other. Lipid. Mediat. 68-69, 115-128 https://doi.org/10.1016/S0090-6980(02)00025-4
  74. Song, I., Ball, T. M. and Smith, W. L. (2001) Different suicide inactivation processes for the peroxidase and cyclooxygenase activities of prostaglandin endoperoxide H synthase-1. Biochem. Biophys. Res. Commun. 289, 869-875 https://doi.org/10.1006/bbrc.2001.6071
  75. Mevkh, A. T., Miroshnikov, K. A., Igumnova, N. D. and Varfolomeev, S. D. (1993) Prostaglandin H synthase. Inactivation of the enzyme in the course of catalysis is accompanied by fast and dramatic changes in protein structure. FEBS. Lett. 321, 205-208 https://doi.org/10.1016/0014-5793(93)80109-8
  76. Reddy, S. T. and Herschman, H. R. (1994) Ligand-induced prostaglandin synthesis requires expression of the TIS10/PGS-2 prostaglandin synthase gene in murine fibroblasts and macrophages. J. Biol. Chem. 269, 15473-15480
  77. Murakami, M., Shimbara, S., Kambe, T., Kuwata, H., Winstead, M. V., Tischfield, J. A. and Kudo, I. (1998) The functions of five distinct mammalian phospholipase A2S in regulating arachidonic acid release. Type IIa and type V secretory phospholipase A2S are functionally redundant and act in concert with cytosolic phospholipase A2. J. Biol. Chem. 273, 14411-14423 https://doi.org/10.1074/jbc.273.23.14411

Cited by

  1. Prostaglandin EP1Receptor Down-regulates Expression of Cyclooxygenase-2 by Facilitating Its Proteasomal Degradation vol.287, pp.21, 2012, https://doi.org/10.1074/jbc.M111.304220
  2. Influenza A viruses suppress cyclooxygenase-2 expression by affecting its mRNA stability vol.6, pp.1, 2016, https://doi.org/10.1038/srep27275
  3. Role of cyclooxygenase-2 in Trypanosoma cruzisurvival in the early stages of parasite host-cell interaction vol.110, pp.2, 2015, https://doi.org/10.1590/0074-02760140311
  4. Prostaglandin E2and the Pathogenesis of Pulmonary Fibrosis vol.45, pp.3, 2011, https://doi.org/10.1165/rcmb.2011-0025RT
  5. EGF receptor and COX-1/COX-2 enzyme proteins as related to corresponding mRNAs in human per-operative biopsies of colorectal cancer vol.13, pp.1, 2013, https://doi.org/10.1186/1471-2407-13-511
  6. Underwater trauma causes a long-term specific increase in the expression of cyclooxygenase-2 in the ventral CA1 of the hippocampus vol.49, 2014, https://doi.org/10.1016/j.psyneuen.2014.06.015
  7. Cyclooxygenase 2: its regulation, role and impact in airway inflammation vol.46, pp.3, 2016, https://doi.org/10.1111/cea.12697
  8. Regulation of Cyclooxygenase-2 Expression by Heat: A Novel Aspect of Heat Shock Factor 1 Function in Human Cells vol.7, pp.2, 2012, https://doi.org/10.1371/journal.pone.0031304
  9. Down-regulation of Cyclooxygenase-2 by the Carboxyl Tail of the Angiotensin II Type 1 Receptor vol.289, pp.45, 2014, https://doi.org/10.1074/jbc.M114.587576
  10. Vanadium Compounds as Pro-Inflammatory Agents: Effects on Cyclooxygenases vol.16, pp.6, 2015, https://doi.org/10.3390/ijms160612648
  11. Distribution of Bioactive Lipid Mediators in Human Skin vol.135, pp.6, 2015, https://doi.org/10.1038/jid.2015.41
  12. New insights into pattern recognition receptors and their ligands in gynecologic pathologies vol.72, pp.3, 2011, https://doi.org/10.1016/j.humimm.2010.12.009
  13. β1-Adrenergic receptor downregulates the expression of cyclooxygenase-2 vol.451, pp.2, 2014, https://doi.org/10.1016/j.bbrc.2014.07.123
  14. Targeting COX-2 expression by natural compounds: A promising alternative strategy to synthetic COX-2 inhibitors for cancer chemoprevention and therapy vol.80, pp.12, 2010, https://doi.org/10.1016/j.bcp.2010.06.050
  15. FGFR1-Induced Epithelial to Mesenchymal Transition through MAPK/PLCγ/COX-2-Mediated Mechanisms vol.7, pp.6, 2012, https://doi.org/10.1371/journal.pone.0038972
  16. The Effect of Cadmium on COX-1 and COX-2 Gene, Protein Expression, and Enzymatic Activity in THP-1 Macrophages vol.165, pp.2, 2015, https://doi.org/10.1007/s12011-015-0234-6
  17. Involvement of interleukin-1 type 1 receptors in lipopolysaccharide-induced sickness responses 2017, https://doi.org/10.1016/j.bbi.2017.06.013
  18. Prostaglandin receptor EP1-mediated differential degradation of cyclooxygenases involves a specific lysine residue vol.443, pp.2, 2014, https://doi.org/10.1016/j.bbrc.2013.12.038
  19. RNA-binding protein HuR regulates RGS4 mRNA stability in rabbit colonic smooth muscle cells vol.299, pp.6, 2010, https://doi.org/10.1152/ajpcell.00093.2010
  20. MiRNA in innate immune responses: novel players in wound inflammation vol.43, pp.10, 2011, https://doi.org/10.1152/physiolgenomics.00160.2010
  21. Cyclooxygenase 2: protein-protein interactions and posttranslational modifications vol.49, pp.11, 2017, https://doi.org/10.1152/physiolgenomics.00086.2017
  22. Substrate-inactivated cyclooxygenase-2 is disposed of by exosomes through the ER–Golgi pathway vol.475, pp.19, 2018, https://doi.org/10.1042/BCJ20180530