COX-2 but not mPGES-1 contributes to renal PGE2 induction and diabetic proteinuria in mice with type-1 diabetes

PLoS ONE

Volumn 9, Issue 7, 2014, Pages

  Jia, Zhanjun ^a   Sun, Ying ^a   Liu, Shanshan ^a   Liu, Ying ^a   Yang, Tianxin ^a,b  

^a UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^b SUN YAT SEN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

15 HYDROXYPROSTAGLANDIN DEHYDROGENASE; ALBUMIN; CELECOXIB; CYCLOOXYGENASE 2; CYTOSOLIC PROSTAGLANDIN E SYNTHASE; GLUCOSE; MESSENGER RNA; MICROSOMAL PROSTAGLANDIN E SYNTHASE 2; PROSTAGLANDIN E SYNTHASE 1; PROSTAGLANDIN E2; PROSTAGLANDIN SYNTHASE; UNCLASSIFIED DRUG; ISOMERASE; PROSTAGLANDIN E SYNTHASE; PTGS2 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DIABETIC NEPHROPATHY; GLUCOSE BLOOD LEVEL; INSULIN DEPENDENT DIABETES MELLITUS; KIDNEY MASS; KNOCKOUT MOUSE; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PROSTAGLANDIN SYNTHESIS; PROTEINURIA; STREPTOZOTOCIN-INDUCED DIABETES MELLITUS; URINE VOLUME; ALBUMINURIA; ANIMAL; BIOSYNTHESIS; EXPERIMENTAL DIABETES MELLITUS; GENETICS; KIDNEY; METABOLISM; PATHOLOGY;

ALBUMINURIA; ANIMALS; CYCLOOXYGENASE 2; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 1; DIABETIC NEPHROPATHIES; DINOPROSTONE; INTRAMOLECULAR OXIDOREDUCTASES; KIDNEY; MICE; MICE, KNOCKOUT;

EID: 84903640824     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0093182     Document Type: Article

References (41)

1. Breyer MD, Jacobson HR, Breyer RM (1996) Functional and molecular aspects of renal prostaglandin receptors. J Am Soc Nephrol 7: 8-17.
2. Craven PA, DeRubertis FR (1989) Role for local prostaglandin and thromboxane production in the regulation of glomerular filtration rate in the rat with streptozocin-induced diabetes. J Lab Clin Med 113: 674-681.
3. DeRubertis FR, Craven PA (1993) Eicosanoids in the pathogenesis of the functional and structural alterations of the kidney in diabetes. Am J Kidney Dis 22: 727-735.
4. Gerrard JM, Stuart MJ, Rao GH, Steffes MW, Mauer SM, et al. (1980) Alteration in the balance of prostaglandin and thromboxane synthesis in diabetic rats. J Lab Clin Med 95: 950-958.
5. Ishibashi R, Tanaka I, Kotani M, Muro S, Goto M, et al. (1999) Roles of prostaglandin E receptors in mesangial cells under high-glucose conditions. Kidney Int 56: 589-600.
6. Komers R, Lindsley JN, Oyama TT, Schutzer WE, Reed JF, et al. (2001) Immunohistochemical and functional correlations of renal cyclooxygenase-2 in experimental diabetes. J Clin Invest 107: 889-898.
7. Schambelan M, Blake S, Sraer J, Bens M, Nivez MP, et al. (1985) Increased prostaglandin production by glomeruli isolated from rats with streptozotocin-induced diabetes mellitus. J Clin Invest 75: 404-412.
8. Williams B, Schrier RW (1993) Glucose-induced protein kinase C activity regulates arachidonic acid release and eicosanoid production by cultured glomerular mesangial cells. J Clin Invest 92: 2889-2896.
9. Komers R, Lindsley JN, Oyama TT, Anderson S (2007) Cyclo-oxygenase-2 inhibition attenuates the progression of nephropathy in uninephrectomized diabetic rats. Clin Exp Pharmacol Physiol 34: 36-41.
10. Quilley J, Santos M, Pedraza P (2011) Renal protective effect of chronic inhibition of COX-2 with SC-58236 in streptozotocin-diabetic rats. Am J Physiol Heart Circ Physiol 300: H2316-2322.
11. Nasrallah R, Xiong H, Hebert RL (2007) Renal prostaglandin E2 receptor (EP) expression profile is altered in streptozotocin and B6-Ins2Akita type I diabetic mice. Am J Physiol Renal Physiol 292: F278-284.
12. Makino H, Tanaka I, Mukoyama M, Sugawara A, Mori K, et al. (2002) Prevention of diabetic nephropathy in rats by prostaglandin E receptor EP1-selective antagonist. J Am Soc Nephrol 13: 1757-1765.
13. Mohamed R, Jayakumar C, Ramesh G (2013) Chronic administration of EP4-selective agonist exacerbates albuminuria and fibrosis of the kidney in streptozotocin-induced diabetic mice through IL-6. Lab Invest 93: 933-945.
14. Francois H, Athirakul K, Howell D, Dash R, Mao L, et al. (2005) Prostacyclin protects against elevated blood pressure and cardiac fibrosis. Cell Metab 2: 201-207.
15. Grosser T, Fries S, FitzGerald GA (2006) Biological basis for the cardiovascular consequences of COX-2 inhibition: therapeutic challenges and opportunities. J Clin Invest 116: 4-15.
16. Mancini JA, Blood K, Guay J, Gordon R, Claveau D, et al. (2001) Cloning, expression, and up-regulation of inducible rat prostaglandin e synthase during lipopolysaccharide-induced pyresis and adjuvant-induced arthritis. J Biol Chem 276: 4469-4475.
17. Murakami M, Naraba H, Tanioka T, Semmyo N, Nakatani Y, et al. (2000) Regulation of prostaglandin E2 biosynthesis by inducible membrane-associated prostaglandin E2 synthase that acts in concert with cyclooxygenase-2. J Biol Chem 275: 32783-32792.
18. Jia Z, Wang N, Aoyagi T, Wang H, Liu H, et al. (2011) Amelioration of cisplatin nephrotoxicity by genetic or pharmacologic blockade of prostaglandin synthesis. Kidney Int 79: 77-88.
19. Jia Z, Aoyagi T, Kohan DE, Yang T (2010) mPGES-1 deletion impairs aldosterone escape and enhances sodium appetite. Am J Physiol Renal Physiol 299: F155-166.
20. Jia Z, Aoyagi T, Yang T (2010) mPGES-1 protects against DOCA-salt hypertension via inhibition of oxidative stress or stimulation of NO/cGMP. Hypertension 55: 539-546.
21. Jia Z, Wang H, Yang T (2009) Mice lacking mPGES-1 are resistant to lithium-induced polyuria. Am J Physiol Renal Physiol 297: F1689-1696.
22. Soodvilai S, Jia Z, Wang MH, Dong Z, Yang T (2009) mPGES-1 deletion impairs diuretic response to acute water loading. Am J Physiol Renal Physiol 296: F1129-1135.
23. Jia Z, Guo X, Zhang H, Wang MH, Dong Z, et al. (2008) Microsomal prostaglandin synthase-1-derived prostaglandin E2 protects against angiotensin II-induced hypertension via inhibition of oxidative stress. Hypertension 52: 952-959.
24. Jia Z, Zhang A, Zhang H, Dong Z, Yang T (2006) Deletion of microsomal prostaglandin E synthase-1 increases sensitivity to salt loading and angiotensin II infusion. Circ Res 99: 1243-1251.
25. Jania LA, Chandrasekharan S, Backlund MG, Foley NA, Snouwaert J, et al. (2009) Microsomal prostaglandin E synthase-2 is not essential for in vivo prostaglandin E2 biosynthesis. Prostaglandins Other Lipid Mediat 88: 73-81.
26. Lovgren AK, Kovarova M, Koller BH (2007) cPGES/p23 is required for glucocorticoid receptor function and embryonic growth but not prostaglandin E2 synthesis. Mol Cell Biol 27: 4416-4430.
27. Nakatani Y, Hokonohara Y, Kakuta S, Sudo K, Iwakura Y, et al. (2007) Knockout mice lacking cPGES/p23, a constitutively expressed PGE2 synthetic enzyme, are peri-natally lethal. Biochem Biophys Res Commun 362: 387-392.
28. Trebino CE, Stock JL, Gibbons CP, Naiman BM, Wachtmann TS, et al. (2003) Impaired inflammatory and pain responses in mice lacking an inducible prostaglandin E synthase. Proc Natl Acad Sci U S A 100: 9044-9049.
29. Paliege A, Mizel D, Medina C, Pasumarthy A, Huang YG, et al. (2004) Inhibition of nNOS expression in the macula densa by COX-2-derived prostaglandin E(2). Am J Physiol Renal Physiol 287: F152-159.
30. Kudo I, Murakami M (2005) Prostaglandin E synthase, a terminal enzyme for prostaglandin E2 biosynthesis. J Biochem Mol Biol 38: 633-638.
31. Wang J, Limburg D, Carter J, Mbalaviele G, Gierse J, et al. (2010) Selective inducible microsomal prostaglandin E(2) synthase-1 (mPGES-1) inhibitors derived from an oxicam template. Bioorg Med Chem Lett 20: 1604-1609.
32. Chiasson JF, Boulet L, Brideau C, Chau A, Claveau D, et al. (2011) Trisubstituted ureas as potent and selective mPGES-1 inhibitors. Bioorg Med Chem Lett 21: 1488-1492.
33. Xu D, Rowland SE, Clark P, Giroux A, Cote B, et al. (2008) MF63 [2-(6-chloro-1H-phenanthro [9,10-d] imidazol-2-yl)-isophthalonitrile], a selective microsomal prostaglandin E synthase-1 inhibitor, relieves pyresis and pain in preclinical models of inflammation. J Pharmacol Exp Ther 326: 754-763.
34. Nasrallah R, Robertson SJ, Hebert RL (2009) Chronic COX inhibition reduces diabetes-induced hyperfiltration, proteinuria, and renal pathological markers in 36-week B6-Ins2(Akita) mice. Am J Nephrol 30: 346-353.
35. Hommel E, Mathiesen E, Arnold-Larsen S, Edsberg B, Olsen UB, et al. (1987) Effects of indomethacin on kidney function in type 1 (insulin-dependent) diabetic patients with nephropathy. Diabetologia 30: 78-81.
36. Schneider A, Zhang Y, Zhang M, Lu WJ, Rao R, et al. (2004) Membrane-associated PGE synthase-1 (mPGES-1) is coexpressed with both COX-1 and COX-2 in the kidney. Kidney Int 65: 1205-1213.
37. Parazzoli S, Harmon JS, Vallerie SN, Zhang T, Zhou H, et al. (2012) Cyclooxygenase-2, not microsomal prostaglandin E synthase-1, is the mechanism for interleukin-1beta-induced prostaglandin E2 production and inhibition of insulin secretion in pancreatic islets. J Biol Chem 287: 32246-32253.
38. Murakami M, Nakashima K, Kamei D, Masuda S, Ishikawa Y, et al. (2003) Cellular prostaglandin E2 production by membrane-bound prostaglandin E synthase-2 via both cyclooxygenases-1 and -2. J Biol Chem 278: 37937-37947.
39. Tanioka T, Nakatani Y, Semmyo N, Murakami M, Kudo I (2000) Molecular identification of cytosolic prostaglandin E2 synthase that is functionally coupled with cyclooxygenase-1 in immediate prostaglandin E2 biosynthesis. J Biol Chem 275: 32775-32782.
40. Moore AH, Olschowka JA, O'Banion MK (2004) Intraparenchymal administration of interleukin-1beta induces cyclooxygenase-2-mediated expression of membrane- and cytosolic-associated prostaglandin E synthases in mouse brain. J Neuroimmunol 148: 32-40.
41. Ensor CM, Tai HH (1995) 15-Hydroxyprostaglandin dehydrogenase. J Lipid Mediat Cell Signal 12: 313-319.