Prostaglandin E synthases: Understanding their pathophysiological roles through mouse genetic models

Biochimie

Volumn 92, Issue 6, 2010, Pages 651-659

  Hara, Shuntaro ^a   Kamei, Daisuke ^a   Sasaki, Yuka ^a   Tanemoto, Akemi ^a   Nakatani, Yoshihito ^a   Murakami, Makoto ^b  

^a SHOWA UNIVERSITY   (Japan)

^b TOKYO METROPOLITAN INSTITUTE OF MEDICAL SCIENCE   (Japan)

Author keywords

Inflammation; Knockout mice; MPGES 1; PGE2; Prostaglandin E synthase

Indexed keywords

CYCLOOXYGENASE 1; CYCLOOXYGENASE 2; PROSTAGLANDIN E SYNTHASE; PROSTAGLANDIN E SYNTHASE 1; PROSTAGLANDIN E SYNTHASE 2; PROSTAGLANDIN E2; PROSTAGLANDIN H2; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANIMAL MODEL; BIOCHEMISTRY; CARCINOGENESIS; CARDIOVASCULAR DISEASE; DOWN REGULATION; ENZYME ACTIVITY; FEVER; GASTROINTESTINAL TRACT FUNCTION; GENETIC MODEL; GOLGI COMPLEX; HOMEOSTASIS; HYDROPHOBICITY; IN VIVO STUDY; INFLAMMATION; KIDNEY FUNCTION; KNOCKOUT MOUSE; MOUSE; NEUROLOGIC DISEASE; NONHUMAN; PAIN; PATHOPHYSIOLOGY; PROSTAGLANDIN SYNTHESIS; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; REPRODUCTION; REVIEW; TRANSCRIPTION REGULATION;

ANIMALS; DISEASE; INFLAMMATION; INTRAMOLECULAR OXIDOREDUCTASES; MICE; MODELS, BIOLOGICAL; MODELS, GENETIC; TRANSCRIPTION, GENETIC;

MUS;

EID: 77953293751     PISSN: 03009084     EISSN: 61831638     Source Type: Journal    
DOI: 10.1016/j.biochi.2010.02.007     Document Type: Review

References (94)

1. 2 enzymes. Prostaglandins Other Lipid Mediat. 2002, 68-69:3-58.
2. Smith W.I., DeWitt D.L., Garavito R.M. Cyclooxygenases: structural, cellular, and molecular biology. Annu. Rev. Biochem. 2000, 69:145-182.
3. 2 biosynthesis. J. Biochem. Mol. Biol. 2005, 38:633-638.
4. 2s and cyclooxygenases in immediate and delayed prostanoid biosynthetic pathways. J. Biol. Chem. 1999, 274:3103-3115.
5. 2 synthesis in rat 3Y1 fibroblasts following vasopressin V1a receptor stimulation. Biochem. Biophys. Res. Commun. 2007, 354:676-680.
6. Jakobsson P.J., Thorén 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.
7. 2 biosynthesis. J. Biol. Chem. 2000, 275:32775-32782.
8. 2 synthase that acts in concert with cyclooxygenase-2. J. Biol. Chem. 2000, 275:32783-32792.
9. Tanikawa N., Ohmiya Y., Ohkubo H., et al. Identification and characterization of a novel type of membrane-associated prostaglandin E synthase. Biochem. Biophys. Res. Commun. 2002, 291:884-889.
10. 2 synthase gene induced by the Toll-like receptor 4/MyD88/NF-IL6 pathway. J. Immunol. 2002, 168:5811-5816.
11. Trebino C.E., Stock J.L., Gibbons C.P., et al. Impaired inflammatory and pain responses in mice lacking an inducible prostaglandin E synthase. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:9044-9049.
12. Grad I., McKee T.A., Ludwig S.M., et al. The Hsp90 cochaperone p23 is essential for perinatal survival. Mol. Cell. Biol. 2006, 26:8976-8983.
13. 2 synthetic enzyme, are perinatally lethal. Biochem. Biophys. Res. Commun. 2007, 362:387-392.
14. 2 synthesis. Mol. Cell. Biol. 2007, 27:4416-4430.
15. 2 biosynthesis. Prostaglandins Other Lipid Mediat. 2009, 88:73-81.
16. Thorén S., Weinander R., Saha S., et al. Human microsomal prostaglandin E synthase-1: purification, functional characterization, and projection structure determination. J. Biol. Chem. 2003, 278:22199-22209.
17. Mancini J.A., Blood K., Guay J., et al. Cloning, expression, and up-regulation of inducible rat prostaglandin E synthase during lipopolysaccharide-induced pyresis and adjuvant-induced arthritis. J. Biol. Chem. 2001, 276:4469-4475.
18. Yamagata K., Matsumura K., Inoue W., et al. Coexpression of microsomal-type prostaglandin E synthase with cyclooxygenase-2 in brain endothelial cells of rats during endotoxin-induced fever. J. Neurosci. 2001, 21:2669-2677.
19. 4. Eur. J. Biochem. 2000, 267:6428-6434.
20. Soler M., Camacho M., Escudero J.R., Iñiguez M.A., Vila L. Human vascular smooth muscle cells but not endothelial cells express prostaglandin E synthase. Circ. Res. 2000, 87:504-507.
21. Stichtenoth D.O., Thorén S., Bian H., Peters-Golden M., Jakobsson P.J., Crofford L.J. Microsomal prostaglandin E synthase is regulated by proinflammatory cytokines and glucocorticoids in primary rheumatoid synovial cells. J. Immunol. 2001, 167:469-474.
22. 2 synthase gene. Essential role of the transcription factor Egr-1. J. Biol. Chem. 2002, 277:28601-28608.
23. 2 release by antisense microsomal prostaglandin E synthase 1 oligonucleotides in A549 cells. Mol. Cell. Endocrinol. 2003, 205:151-157.
24. 2-deficient mice are resistant to collagen-induced arthritis. J. Exp. Med. 2003, 197:1297-1302.
25. Myers L.K., Kang A.H., Postlethwaite A.E., et al. The genetic ablation of cyclooxygenase 2 prevents the development of autoimmune arthritis. Arthritis Rheum. 2000, 43:2687-2693.
26. 2 receptors in the pathogenesis of rheumatoid arthritis. J. Clin. Invest. 2002, 110:651-658.
27. Rocca B., Spain L.M., Pure E., Langenbach R., Patrono C., FitzGerald G.A. Distinct roles of prostaglandin H synthases 1 and 2 in T-cell development. J. Clin. Invest. 1999, 103:1469-1477.
28. Kojima F., Kapoor M., Yang L., et al. Defective generation of a humoral immune response is associated with a reduced incidence and severity of collagen-induced arthritis in microsomal prostaglandin E synthase-1 null mice. J. Immunol. 2008, 180:8361-8368.
29. Kamei D., Yamakawa K., Takegoshi Y., et al. Reduced pain hypersensitivity and inflammation in mice lacking microsomal prostaglandin E synthase-1. J. Biol. Chem. 2004, 279:33684-33695.
30. 2 synthase to bone resorption. J. Cell. Physiol. 2003, 197:348-356.
31. 2 production by osteoblast plays a critical role in lipopolysaccharide-induced bone loss associated with inflammation. J. Immunol. 2006, 177:1879-1885.
32. Yamakawa K., Kamekura S., Kawamura N., et al. Association of microsomal prostaglandin E synthase 1 deficiency with impaired fracture healing, but not with bone loss or osteoarthritis, in mouse models of skeletal disorders. Arthritis Rheum. 2008, 58:172-183.
33. Mabuchi T., Kojima H., Abe T., et al. Membrane-associated prostaglandin E synthase-1 is required for neuropathic pain. Neuroreport 2004, 15:1395-1398.
34. Li S., Wang Y., Matsumura K., Ballou L.R., Morham S.G., Blatteis C.M. The febrile response to lipopolysaccharide is blocked in cyclooxygenase-2 (-/-), but not in cyclooxygenase-1 (-/-) mice. Brain Res. 1999, 825:86-94.
35. Engblom D., Saha S., Engstrom L., et al. Microsomal prostaglandin E synthase-1 is the central switch during immune-induced pyresis. Nat. Neurosci. 2003, 6:1137-1138.
36. Saha S., Engström L., Mackerlova L., Jakobsson P.J., Blomqvist A. Impaired febrile responses to immune challenge in mice deficient in microsomal prostaglandin E synthase-1. Am. J. Physiol. 2005, 288:R1100-R1107.
37. 2 signaling for neurologic disease. Curr. Med. Chem. 2008, 15:1863-1869.
38. Ikeda-Matsuo Y., Ota A., Fukada T., Uematsu S., Akira S., Sasaki Y. Microsomal prostaglandin E synthase-1 is a critical factor of stroke-reperfusion injury. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:11790-11795.
39. Satoh K., Nagano Y., Shimomura C., Suzuki N., Saeki Y., Yokota H. Expression of prostaglandin E synthase mRNA is induced in beta-amyloid treated rat astrocytes. Neurosci. Lett. 2000, 283:221-223.
40. Pasinetti G.M., Aisen P.S. Cyclooxygenase-2 expression is increased in frontal cortex of Alzheimer's disease. Neuroscience 1998, 87:319-324.
41. 2 levels in patients with probable AD. Neurology 1999, 53:1495-1498.
42. Chaudhry U.A., Zhuang H., Crain B.J., Doré S. Elevated microsomal prostaglandin-E synthase-1 in Alzheimer's disease. Alzheimers Dement. 2008, 4:6-13.
43. Cha Y.I., DuBois R.N. NSAIDs and cancer prevention: targets downstream of COX-2. Annu. Rev. Med. 2007, 58:239-252.
44. 716 knockout mice by inhibition of cyclooxygenase 2 (COX-2). Cell 1996, 87:803-809.
45. 2 gene. J. Biol. Chem. 2002, 275:34013-34016.
46. 716 knockout mice. Nat. Med. 2001, 7:1048-1051.
47. Kamei D., Murakami M., Nakatani Y., Ishikawa Y., Ishii T., Kudo I. Potential role of microsomal prostaglandin E synthase-1 in tumorigenesis. J. Biol. Chem. 2003, 278:19396-19405.
48. Oshima H., Oshima M., Inaba K., Taketo M.M. Hyperplastic gastric tumors induced by activated macrophages in COX-2/mPGES-1 transgenic mice. EMBO J. 2004, 23:1669-1678.
49. Kamei D., Murakami M., Sasaki Y., et al. Microsomal prostaglandin E synthase-1 in both cancer cells and hosts contributes to tumor growth, invasion and metastasis. Biochem. J. 2010, 425:361-371.
50. Nakanishi M., Montrose D.C., Clark P., et al. Genetic deletion of mPGES-1 suppresses intestinal tumorigenesis. Cancer Res. 2008, 68:3251-3259.
51. Min/+ mice. Biochem. Biophys. Res. Commun. 2008, 372:249-253.
52. Cheng Y., Wang M., Yu Y., Lawson J., Funk C.D., Fitzgerald G.A. Cyclooxygenases, microsomal prostaglandin E synthase-1, and cardiovascular function. J. Clin. Invest. 2006, 116:1391-1399.
53. 2 synthase-1 deletion leads to adverse left ventricular remodeling after myocardial infarction. Circulation 2008, 117:1701-1710.
54. Wang M., Zukas A.M., Hui Y., Ricciotti E., Puré E., FitzGerald G.A. Deletion of microsomal prostaglandin E synthase-1 augments prostacyclin and retards atherogenesis. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:14507-14512.
55. Wang M., Lee E., Song W., et al. Microsomal prostaglandin E synthase-1 deletion suppresses oxidative stress and angiotensin II-induced abdominal aortic aneurysm formation. Circulation 2008, 117:1302-1309.
56. Schneider A., Zhang Y., Zhang M., et al. Membrane-associated PGE synthase-1 (mPGES-1) is coexpressed with both COX-1 and COX-2 in the kidney. Kidney Int. 2004, 65:1205-1213.
57. 2 production and alters the gastric prostanoid profile. J. Biol. Chem. 2004, 279:23229-23237.
58. Francois H., Facemire C., Kumar A., Audoly L., Koller B., Coffman T. Role of microsomal prostaglandin E synthase 1 in the kidney. J. Am. Soc. Nephrol. 2007, 18:1466-1475.
59. Jia Z., Zhang A., Zhang H., Dong Z., Yang T. Deletion of microsomal prostaglandin E synthase-1 increases sensitivity to salt loading and angiotensin II infusion. Circ. Res. 2006, 99:1243-1251.
60. Soodvilai S., Jia Z., Wang M.H., Dang Z., Yang T. mPGES-1 deletion impairs diuretic response to acute water loading. Am. J. Physiol. 2009, 296:F1129-F1135.
61. Sharon P., Ligumsky M., Rachmilewitz D., Zor U. Role of prostaglandins in ulcerative colitis: enhanced production during active disease and inhibition by sulfasalazine. Gastroenterology 1978, 75:638-640.
62. Bjarnason I., Hayllar J., MacPherson A.J., Russell A.S. Side effects of non-steroidal anti-inflammatory drugs on the small and large intestine in humans. Gastroenterology 1993, 104:1832-1847.
63. 2 in experimental inflammatory bowel disease is mediated through the IL-23 -> IL-17 axis. J. Immunol. 2007, 178:8138-8147.
64. Morteau O., Morham S.G., Sellon R., et al. Impaired mucosal defense to acute colonic injury in mice lacking cyclooxygenase-1 or cyclooxygenase-2. J. Clin. Invest. 2000, 105:469-478.
65. Kabashima K., Saji T., Murata T., et al. The prostaglandin receptor EP4 suppresses colitis, mucosal damage and CD4 cell activation in the gut. J. Clin. Invest. 2002, 109:883-893.
66. Subbaramaiah K., Yoshimatsu K., Scherl E., et al. 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.
67. Sirois J. Induction of prostaglandin endoperoxide synthase-2 by human chorionic gonadotropin in bovine preovulatory follicles in vivo. Endocrinology 1994, 135:841-848.
68. Sirois J., Doré M. The late induction of prostaglandin G/H synthase-2 in equine preovulatory follicles supports its role as a determinant of the ovulatory process. Endocrinology 1997, 138:4427-4434.
69. Lim H., Paria B.C., Das S.K., et al. Multiple female reproductive failures in cyclooxygenase 2-deficient mice. Cell 1997, 91:197-208.
70. Kennedy C.R., Zhang Y., Brandon S., et al. Salt-sensitive hypertension and reduced fertility in mice lacking the prostaglandin EP2 receptor. Nat. Med. 1999, 5:217-220.
71. 2. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:10501-10506.
72. Filion F., Bouchard N., Goff A.K., Lussier J.G., Sirois J. Molecular cloning and induction of bovine prostaglandin E synthase by gonadotropins in ovarian follicles prior to ovulation in vivo. J. Biol. Chem. 2001, 276:34323-34330.
73. Meadows J.W., Pitzer B., Brockman D.E., Myatt L. Differential localization of prostaglandin E synthase isoforms in human placental cell types. Placenta 2004, 25:259-265.
74. Meadows J.W., Eis A.L., Brockman D.E., 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.
75. Alfaidy N., Sun M., Challis J.R., Gibb W. Expression of membrane prostaglandin E synthase in human placenta and fetal membranes and effect of labor. Endocrine 2003, 20:219-225.
76. Kubota K., Kubota T., Kamei D., et al. Change in prostaglandin E synthases (PGESs) in microsomal PGES-1 knockout mice in a preterm delivery model. J. Endocrinol. 2005, 187:339-345.
77. 2 synthase in porcine ductus arteriosus. Am. J. Physiol. 2004, 286:R903-R909.
78. Segi E., Sugimoto Y., Yamasaki A., et al. Patent ductus arteriosus and neonatal death in prostaglandin receptor EP4-deficient mice. Biochem. Biophys. Res. Commun. 1998, 246:7-12.
79. 2 in patency of the ductus arteriosus in the mouse. Pediatr. Res. 2008, 64:523-527.
80. Johnson J.L., Beito T.G., Krco C.J., Toft D.O. Characterization of a novel 23-kilodalton protein of unactive progesterone receptor complexes. Mol. Cell. Biol. 1994, 14:1956-1963.
81. Hutchison K.A., Stancato L.F., Owens-Grillo J.K., et al. The 23-kDa acidic protein in reticulocyte lysate is the weakly bound component of the hsp foldosome that is required for assembly of the glucocorticoid receptor into a functional heterocomplex with hsp90. J. Biol. Chem. 1995, 270:18841-18847.
82. Johnson J.A., el Barbary A., Kornguth S.E., Brugge J.F., Siegel F.L. Glutathione S-transferase isoenzymes in rat brain neurons and glia. J. Neurosci. 1993, 13:2013-2023.
83. Kobayashi T., Nakatani Y., Tanioka T., et al. Regulation of cytosolic prostaglandin E synthase by phosphorylation. Biochem. J. 2004, 381:59-69.
84. 2 synthase by 90-kDa heat shock protein. Biochem. Biophys. Res. Commun. 2003, 303:1018-1023.
85. Moore A.H., Olschowka J.A., O'Banion M.K. Intraparenchymal administration of interleukin-1β induces cyclooxygenase-2-mediated expression of membrane- and cytosolic-associated prostaglandin E synthases in mouse brain. J. Neuroimmunol. 2004, 148:32-40.
86. Ni H., Sun T., Ma X.H., Yang Z.M. Expression and regulation of cytosolic prostaglandin E synthase in mouse uterus during the peri-implantation period. Biol. Reprod. 2003, 68:744-750.
87. 2 synthase gene. Biochim. Biophys. Acta 2003, 1634:15-23.
88. 2 synthase results in decreased nociceptive behavior in rats. J. Neurosci. 2005, 25:9005-9009.
89. Watanabe K., Kurihara K., Suzuki T. Purification and characterization of membrane-bound prostaglandin E synthase from bovine heart. Biochim. Biophys. Acta 1999, 1439:406-414.
90. 110Cys in active site of membrane-associated prostaglandin E synthase-2. Biochem. Biophys. Res. Commun. 2003, 306:577-581.
91. Yamada T., Komoto J., Watanabe K., Ohmiya Y., Takusagawa F. Crystal structure and possible catalytic mechanism of microsomal prostaglandin E synthase type 2 (mPGES-2). J. Mol. Biol. 2005, 348:1163-1176.
92. 2 production by membrane-bound prostaglandin E synthase-2 via both cyclooxygenases-1 and -2. J. Biol. Chem. 2003, 278:37937-37947.
93. Ueno N., Takegoshi Y., Kamei D., Kudo I., Murakami M. Coupling between cyclooxygenases and terminal prostanoid synthases. Biochem. Biophys. Res. Commun. 2005, 338:70-76.
94. Hara S., Kudo I. COX-2 inhibitors and the risk of cardiovascular events. Jpn. Med. Assoc. J. 2006, 49:276-278.