The prostaglandin F synthase activity of the human aldose reductase AKR1B1 brings new lenses to look at pathologic conditions

Frontiers in Pharmacology

Volumn 3 MAY, Issue , 2012, Pages

  Bresson, Eva ^a   Lacroix Pépin, Nicolas ^a   Boucher Kovalik, Sofia ^a   Chapdelaine, Pierre ^a   Fortier, Michel A ^a  

^a LAVAL UNIVERSITY   (Canada)

Author keywords

Biosynthesis; Endometrium; Menstrual cycle; Prostaglandins; Regulation

Indexed keywords

ALDEHYDE REDUCTASE; ALDOSE REDUCTASE INHIBITOR; ALRESTATIN; CYCLOOXYGENASE 2; INTERLEUKIN 1BETA; N (2 CYCLOHEXYLOXY 4 NITROPHENYL)METHANESULFONAMIDE; PONALRESTAT; PROSTAGLANDIN E2; PROSTAGLANDIN F; PROSTAGLANDIN F2 ALPHA; PROSTAGLANDIN SYNTHASE; PROTEIN AKR1B1; UNCLASSIFIED DRUG;

ADULT; ANTIOXIDANT RESPONSIVE ELEMENT; ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; ENDOMETRIUM CELL; ENDOTHELIUM CELL; ENZYME ACTIVITY; ENZYME LOCALIZATION; ENZYME REGULATION; FEMALE; GENE ACTIVITY; GLUCOSE BLOOD LEVEL; HEART MUSCLE CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VIVO STUDY; INFLAMMATION; ISCHEMIA; NUCLEOTIDE SEQUENCE; PROMOTER REGION; PROSTAGLANDIN RELEASE; PROSTAGLANDIN SYNTHESIS; PROSTAGLANDIN SYNTHESIS INHIBITION; PROSTATE EPITHELIUM; SMOOTH MUSCLE FIBER; VASCULAR SMOOTH MUSCLE;

EID: 84866044957     PISSN: None     EISSN: 16639812     Source Type: Journal    
DOI: 10.3389/fphar.2012.00098     Document Type: Article

References (54)

1. Abera, A. B., Sales, K. J., Catalano, R. D., Katz, A. A., and Jabbour, H. N. (2010). EP2 receptor mediated cAMP release is augmented by PGF 2 alpha activation of the FP receptor via the calciumcalmodulin pathway. Cell. Signal. 22, 71-79.
2. Alexiou, P., Pegklidou, K., Chatzopoulou, M., Nicolaou, I., and Demopoulos, V. J. (2009). Aldose reductase enzyme and its implication to major health problems of the 21(st) century. Curr. Med. Chem. 16, 734-752.
3. Asselin, E., Goff, A. K., Bergeron, H., and Fortier, M. A. (1996). Influence of sex steroids on the production of prostaglandins F2 alpha and E2 and response to oxytocin in cultured epithelial and stromal cells of the bovine endometrium. Biol. Reprod. 54, 371-379.
4. Baron, J. A., Sandler, R. S., Bresalier, R. S., Lanas, A., Morton, D. G., Riddell, R., Iverson, E. R., and Demets, D. L. (2008). Cardiovascular events associated with rofecoxib: final analysis of the APPROVe trial. Lancet 372, 1756-1764.
5. Bresson, E., Boucher-Kovalik, S., Chapdelaine, P., Madore, E., Harvey, N., Laberge, P. Y., Leboeuf, M., and Fortier, M. A. (2011). The human aldose reductase AKR1B1 qualifies as the primary prostaglandin F synthase in the endometrium. J. Clin. Endocrinol. Metab. 96, 210-219.
6. Breuiller-Fouche, M., Leroy, M. J., Dubois, O., Reinaud, P., Chissey, A., Qi, H., Germain, G., Fortier, M. A., and Charpigny, G. (2010). Differential expression of the enzymatic system controlling synthesis, metabolism, and transport of PGF2 alpha in human fetal membranes. Biol. Reprod. 83, 155-162.
7. Catalano, R.D., Wilson, M. R., Boddy, S. C., and Jabbour, H. N. (2011). Com-prehensive expression analysis of prostanoid enzymes and receptors in the human endometrium across themenstrual cycle. Mol. Hum. Reprod. 17, 182-192.
8. Chapdelaine, P., Kang, J., Boucher-Kovalik, S., Caron, N., Tremblay, J. P., and Fortier,M. A. (2006). Decid-ualization and maintenance of a functional prostaglandin system in human endometrial cell lines follow-ing transformation with SV40 large T antigen. Mol. Hum. Reprod. 12, 309-319.
9. Del Corso, A., Cappiello,M., and Mura, U. (2008). From a dull enzyme to something else: facts and per-spectives regarding aldose reductase. Curr. Med. Chem. 15, 1452-1461.
10. Downie, J., Poyser, N. L., and Wunderlich, M. (1974). Lev-els of prostaglandins in human endometrium during the normal menstrual cycle. J. Physiol. (Lond.) 236, 465-472.
11. Huang, J. C., Liu, D. Y., Yadollahi, S., Wu, K. K., and Dawood, M. Y. (1998). Interleukin-1 beta induces cyclooxygenase-2 gene expression in cultured endometrial stromal cells. J. Clin. Endocrinol. Metab. 83, 538-541.
12. Jabbour, H. N., and Sales, K. J. (2004). Prostaglandin receptor signalling and function in human endometrial pathology. Trends Endocrinol. Metab. 15, 398-404.
13. Jabbour, H. N., Sales, K. J., Boddy, S. C., Anderson, R. A., and Williams, A. R. (2005). A positive feedback loop that regulates cyclooxygenase-2 expression and prostaglandin F2alpha synthesis via the F-series-prostanoid receptor and extracellular signalregulated kinase 1/2 signaling pathway. Endocrinology 146, 4657-4664
14. Jabbour, H. N., Sales, K. J., Smith, O. P., Battersby, S., and Boddy, S. C. (2006). Prostaglandin receptors are mediators of vascular function in endometrial pathologies. Mol. Cell. Endocrinol. 252, 191-200.
15. Jin, Y., and Penning, T. M. (2007). Aldo-keto reductases and bioactivation/detoxication. Annu. Rev. Pharmacol. Toxicol. 47, 263-292.
16. Kabututu, Z., Manin, M., Pointud, J. C., Maruyama, T., Nagata, N., Lambert, S., Lefrancois-Martinez, A. M., Martinez, A., and Urade, Y. (2009). Prostaglandin F2alpha synthase activities of aldo-keto reductase 1B1, 1B3 and 1B7. J. Biochem. 145, 161-168.
17. Kang, J., Akoum, A., Chapdelaine, P., Laberge, P., Poubelle, P. E., and Fortier, M. A. (2004). Independent regulation of prostaglandins and monocyte chemoattractant protein1 by interleukin-1beta and hCG in human endometrial cells. Hum. Reprod. 19, 2465-2473.
18. Kang, J., Chapdelaine, P., Laberge, P. Y., and Fortier, M. A. (2006). Functional characterization of prostaglandin transporter and terminal prostaglandin synthases during decidualization of human endometrial stromal cells. Hum. Reprod. 21, 592-599.
19. Kennedy, C. R., Zhang, Y., Brandon, S., Guan, Y., Coffee, K., Funk, C. D., Magnuson, M. A., Oates, J. A., Breyer, M. D., and Breyer, R. M. (1999). Salt-sensitive hypertension and reduced fertility in mice lacking the prostaglandin EP2 receptor. Nat. Med. 5, 217-220.
20. Komoto, J., Yamada, T., Watanabe, K., Woodward, D. F., and Takusagawa, F. (2006). Prostaglandin F2alpha formation from prostaglandin H2 by prostaglandin F synthase (PGFS): crystal structure of PGFS containing bimatoprost. Biochemistry 45, 1987-1996.
21. Krishnaswamy, N., Danyod, G., Chapdelaine, P., and Fortier, M. A. (2009). Oxytocin receptor down-regulation is not necessary for reducing oxytocin-induced prostaglandin F(2alpha) accumulation by interferon-tau in a bovine endometrial epithelial cell line. Endocrinology 150, 897-905.
22. Krishnaswamy, N., Lacroix-Pepin, N., Chapdelaine, P., Taniguchi, H., Kauffenstein, G., Chakravarti, A., Danyod, G., and Fortier, M. A. (2010). Epidermal growth factor receptor is an obligatory intermediate for oxytocin-induced cyclooxygenase 2 expression and prostaglandin F2 alpha production in bovine endometrial epithelial cells. Endocrinology 151, 1367-1374.
23. Lacroix-Pepin, N., Danyod, G., Krishnaswamy, N., Mondal, S., Rong, P. M., Chapdelaine, P., and Fortier, M. A. (2011). The multidrug resistance-associated protein 4 (MRP4) appears as a functional carrier of prostaglandins regulated by oxytocin in the bovine endometrium. Endocrinology 152, 4993-5004.
24. Lai, J., Jin, H., Yang, R., Winer, J., Li, W., Yen, R., King, K. L., Zeigler, F., Ko, A., Cheng, J., Bunting, S., and Paoni, N. F. (1996). Prostaglandin F2 alpha induces cardiac myocyte hypertrophy in vitro and cardiac growth in vivo. Am. J. Physiol. 271, H2197-H2208.
25. 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.
26. Lockwood, C. J., and Schatz, F. (1996). A biological model for the regulation of peri-implantational hemostasis and menstruation. J. Soc. Gynecol. Investig. 3, 159-165.
27. Madore, E., Harvey, N., Parent, J., Chapdelaine, P., Arosh, J. A., and Fortier, M. A. (2003). An aldose reductase with 20 alphahydroxysteroid dehydrogenase activity is most likely the enzyme responsible for the production of prostaglandin f2 alpha in the bovine endometrium. J. Biol. Chem. 278, 11205-11212.
28. Mandal, A. K., Zhang, Z., Kim, S. J., Tsai, P. C., and Mukherjee, A. B. (2005). Yin-yang: balancing act of prostaglandins with opposing functions to regulate inflammation. J. Immunol. 175, 6271-6273.
29. Milne, S. A., and Jabbour, H. N. (2003). Prostaglandin (PG) F(2alpha) receptor expression and signaling in human endometrium: role of PGF(2alpha) in epithelial cell proliferation. J. Clin. Endocrinol. Metab. 88, 1825-1832.
30. Nagata, N., Kusakari, Y., Fukunishi, Y., Inoue, T., and Urade, Y. (2011). Catalytic mechanism of the primary human prostaglandin F2alpha synthase, aldo-keto reductase 1B1 - prostaglandin D2 synthase activity in the absence of NADP(H). FEBS J. 278, 1288-1298.
31. Narumiya, S., and FitzGerald, G. A. (2001). Genetic and pharmacological analysis of prostanoid receptor function. J. Clin. Invest. 108, 25-30
32. Nishinaka, T., and Yabe-Nishimura, C. (2005). Transcription factor Nrf2 regulates promoter activity of mouse aldose reductase (AKR1B3) gene. J. Pharmacol. Sci. 97, 43-51.
33. Okazaki, M., Matsuyama, T., Kohno, T., Shindo, H., Koji, T., Morimoto, Y., and Ishimaru, T. (2005). Induction of epithelial cell apoptosis in the uterus by a mouse uterine ischemiareperfusion model: possible involvement of tumor necrosis factor-alpha. Biol. Reprod. 72, 1282-1288.
34. Olson, D. M., and Ammann, C. (2007). Role of the prostaglandins in labour and prostaglandin receptor inhibitors in the prevention of preterm labour. Front. Biosci. 12, 1329-1343.
35. Park, J. Y., Pillinger, M. H., and Abramson, S. B. (2006). Prostaglandin E2 synthesis and secretion: the role of PGE2 synthases. Clin. Immunol. 119, 229-240.
36. Pelletier, G., Luu-the, V., Tetu, B., and Labrie, F. (1999). Immunocytochemical localization of type 5 17beta-hydroxysteroid dehydrogenase in human reproductive tissues. J. Histochem. Cytochem. 47, 731-738.
37. Phillips, R. J., Al-Zamil, H., Hunt, L. P., Fortier, M. A., and Lopez Bernal, A. (2011). Genes for prostaglandin synthesis, transport and inactivation are differentially expressed in human uterine tissues, and the prostaglandin F synthase AKR1B1 is induced in myometrial cells by inflammatory cytokines. Mol. Hum. Reprod. 17, 1-13.
38. Sakamoto, A., and Sugamoto, Y. (2011). Identification of a novel aldose reductase-like gene upregulated in the failing heart of cardiomyopathic hamster. Mol. Cell. Biochem. 353, 275-281.
39. Sales, K. J., Grant, V., and Jabbour, H. N. (2008). Prostaglandin E2 and F2alpha activate the FP receptor and up-regulate cyclooxygenase-2 expression via the cyclic AMP response element. Mol. Cell. Endocrinol. 285, 51-61.
40. Sales, K. J., and Jabbour, H. N. (2003a). Cyclooxygenase enzymes and prostaglandins in pathology of the endometrium. Reproduction 126, 559-567.
41. Sales, K. J., and Jabbour, H. N. (2003b). Cyclooxygenase enzymes and prostaglandins in reproductive tract physiology and pathology. Prostaglandins Other Lipid Mediat. 71, 97-117.
42. Sales, K. J., Milne, S. A., Williams, A. R., Anderson, R. A., and Jabbour, H. N. (2004). Expression, localization, and signaling of prostaglandin F2 alpha receptor in human endometrial adenocarcinoma: regulation of proliferation by activation of the epidermal growth factor receptor and mitogenactivated protein kinase signaling pathways. J. Clin. Endocrinol. Metab. 89, 986-993.
43. Smith, S. K., and Kelly, R. W. (1988). The release of PGF2 alpha and PGE2 from separated cells of human endometrium and decidua. Prostaglandins Leukot. Essent. Fatty Acids 33, 91-96.
44. 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.
45. Smith, W. L., Urade, Y., and Jakobsson, P. J. (2011). Enzymes of the cyclooxygenase pathways of prostanoid biosynthesis. Chem. Rev. 111, 5821-5865.
46. Srivastava, S. K., Ramana, K. V., and Bhatnagar, A. (2005). Role of aldose reductase and oxidative damage in diabetes and the consequent potential for therapeutic options. Endocr. Rev. 26, 380-392.
47. Suzuki-Yamamoto, T., Nishizawa, M., Fukui, M., Okuda-Ashitaka, E., Nakajima, T., Ito, S., and Watanabe, K. (1999). cDNA cloning, expression and characterization of human prostaglandin F synthase. FEBS Lett. 462, 335-340.
48. Tschugguel, W., Schneeberger, C., Unfried, G., Brautigam, G., Stonek, F., Wieser, F., Vytiska-Binstorfer, E., Czerwenka,K.,Weninger,W.,Kaider, A., Bursch, W., Breitschopf, H., and Huber, J. C. (1999). Elevation of inducible nitric oxide synthase activity in human endometrium during menstruation. Biol. Reprod. 60, 297-304.
49. Watanabe, K. (2002). Prostaglandin F synthase. Prostaglandins Other Lipid Mediat. 69, 401-407.
50. Watanabe, K. (2011). Recent reports about enzymes related to the synthesis of prostaglandin (PG) F(2) (PGF(2alpha) and 9alpha, 11beta-PGF(2)). J. Biochem. 150, 593-596.
51. Wu, K. K., and Liou, J. Y. (2005). Cellular and molecular biology of prostacyclin synthase. Biochem. Biophys. Res. Commun. 338, 45-52.
52. Yuhki, K., Kashiwagi, H., Kojima, F., Kawabe, J., and Ushikubi, F. (2010). Roles of prostanoids in the pathogenesis of cardiovascular diseases. Int. Angiol. 29, 19-27.
53. Zakharov, V., Lin, H. K., Azzarello, J., Mcmeekin, S., Moore, K. N., Penning, T. M., and Fung, K. M. (2010). Suppressed expression of type 2 3alpha/type 5 17beta-hydroxysteroid dehydrogenase (AKR1C3) in endometrial hyperplasia and carcinoma. Int. J. Clin. Exp. Pathol. 3, 608-617.
54. Zhou, Y., Shaw, N., Li, Y., Zhao, Y., Zhang, R., and Liu, Z. J. (2010). Structure-function analysis of human l-prostaglandin D synthase bound with fatty acid molecules. FASEB J. 24, 4668-4677.