Augmented epithelial multidrug resistance-associated protein 4 expression in peritoneal endometriosis: Regulation by lipoxin A4

Fertility and Sterility

Volumn 99, Issue 7, 2013, Pages

  Gori, Ilaria ^a,f   Rodriguez, Yoima ^a,d   Pellegrini, Chiara ^a,b   Achtari, Chahin ^a   Hornung, Daniela ^e   Chardonnens, Eric ^c   Wunder, Dorothea ^a   Fiche, Maryse ^a   Canny, Geraldine O ^g  

^a LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

^b UNIVERSITY OF LAUSANNE   (Switzerland)

^c Clinique Cecil   (Switzerland)

^d INSTITUTO NACIONAL DE ENDOCRINOLOGÍA   (Cuba)

^e UNIVERSITY HOSPITAL SCHLESWIG HOLSTEIN   (Germany)

^f IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^g WHO Collaborating Centre in Education and Research in Human Reproduction   (Switzerland)

Author keywords

endometriosis; estrogen receptor; MRP4

Indexed keywords

ESTROGEN RECEPTOR ALPHA; LIPOXIN A; MESSENGER RNA; MULTIDRUG RESISTANCE PROTEIN 4; PROSTAGLANDIN E2;

ADULT; ARTICLE; BODY MASS; CELL LINE; CONTROLLED STUDY; ECTOPIC TISSUE; ENDOMETRIOSIS; ENDOMETRIUM; ENZYME IMMUNOASSAY; EPITHELIUM CELL; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; LAPAROSCOPY; MAJOR CLINICAL STUDY; MENSTRUAL CYCLE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

EID: 84878474656     PISSN: 00150282     EISSN: 15565653     Source Type: Journal    
DOI: 10.1016/j.fertnstert.2013.01.146     Document Type: Article

References (80)

1. S.E. Bulun Endometriosis N Engl J Med 360 2009 268 279
2. S.A. Missmer Commentary: endometriosis - epidemiologic considerations for a potentially "high-risk" population Int J Epidemiol 38 2009 1154 1155
3. J. Kitawaki, N. Kado, H. Ishihara, H. Koshiba, Y. Kitaoka, and H. Honjo Endometriosis: the pathophysiology as an estrogen-dependent disease J Steroid Biochem Mol Biol 83 2002 149 155
4. C. Parente Barbosa, A.M. Bentes de Souza, B. Bianco, and D.M. Christofolini The effect of hormones on endometriosis development Minerva Ginecol 63 2011 375 386
5. N. Heldring, A. Pike, S. Andersson, J. Matthews, G. Cheng, and J. Hartman Estrogen receptors: how do they signal and what are their targets? Physiol Rev 87 2007 905 931
6. M.H. Wu, C.W. Lu, P.C. Chuang, and S.J. Tsai Prostaglandin E2: the master of endometriosis? Exp Biol Med (Maywood) 235 2010 668 677
7. K. Sacco, M. Portelli, J. Pollacco, P. Schembri-Wismayer, and J. Calleja-Agius The role of prostaglandin E2 in endometriosis Gynecol Endocrinol 28 2012 134 138
8. K.N. Khan, M. Kitajima, N. Yamaguchi, A. Fujishita, M. Nakashima, and T. Ishimaru Role of prostaglandin E2 in bacterial growth in women with endometriosis Hum Reprod 27 2012 3417 3424
9. M.H. Wu, H.S. Sun, C.C. Lin, K.Y. Hsiao, P.C. Chuang, and H.A. Pan Distinct mechanisms regulate cyclooxygenase-1 and -2 in peritoneal macrophages of women with and without endometriosis Mol Hum Reprod 8 2002 1103 1110
10. F. Chishima, S. Hayakawa, K. Sugita, N. Kinukawa, S. Aleemuzzaman, and N. Nemoto Increased expression of cyclooxygenase-2 in local lesions of endometriosis patients Am J Reprod Immunol 48 2002 50 56
11. M.H. Wu, Y. Shoji, M.C. Wu, P.C. Chuang, C.C. Lin, and M.F. Huang Suppression of matrix metalloproteinase-9 by prostaglandin E(2) in peritoneal macrophage is associated with severity of endometriosis Am J Pathol 167 2005 1061 1069
12. U. Karck, F. Reister, W. Schafer, H.P. Zahradnik, and M. Breckwoldt PGE2 and PGF2 alpha release by human peritoneal macrophages in endometriosis Prostaglandins 51 1996 49 60
13. P.C. Chuang, Y.J. Lin, M.H. Wu, L.Y. Wing, Y. Shoji, and S.J. Tsai Inhibition of CD36-dependent phagocytosis by prostaglandin E2 contributes to the development of endometriosis Am J Pathol 176 2010 850 860
14. P. Borst, C. de Wolf, and K. van de Wetering Multidrug resistance-associated proteins 3, 4, and 5 Pflugers Arch 453 2007 661 673
15. G. Reid, P. Wielinga, N. Zelcer, I. van der Heijden, A. Kuil, and M. de Haas The human multidrug resistance protein MRP4 functions as a prostaglandin efflux transporter and is inhibited by nonsteroidal antiinflammatory drugs Proc Natl Acad Sci U S A 100 2003 9244 9249
16. Z.P. Lin, Y.L. Zhu, D.R. Johnson, K.P. Rice, T. Nottoli, and B.C. Hains Disruption of cAMP and prostaglandin E2 transport by multidrug resistance protein 4 deficiency alters cAMP-mediated signaling and nociceptive response Mol Pharmacol 73 2008 243 251
17. L.L. Ho, J.G. Kench, D.J. Handelsman, G.L. Scheffer, P.D. Stricker, and J.G. Grygiel Androgen regulation of multidrug resistance-associated protein 4 (MRP4/ABCC4) in prostate cancer Prostate 68 2008 1421 1429
18. S. Copsel, C. Garcia, F. Diez, M. Vermeulem, A. Baldi, and L.G. Bianciotti Multidrug resistance protein 4 (MRP4/ABCC4) regulates cAMP cellular levels and controls human leukemia cell proliferation and differentiation J Biol Chem 286 2011 6979 6988
19. V.R. Holla, M.G. Backlund, P. Yang, R.A. Newman, and R.N. DuBois Regulation of prostaglandin transporters in colorectal neoplasia Cancer Prev Res (Phila) 1 2008 93 99
20. R. Russell, I. Gori, C. Pellegrini, R. Kumar, C. Achtari, and G.O. Canny Lipoxin A4 is a novel estrogen receptor modulator FASEB J 25 2011 4326 4337
21. Q.H. Chen, W.D. Zhou, D.M. Pu, Q.S. Huang, T. Li, and Q.X. Chen 15-Epi-lipoxin A(4) inhibits the progression of endometriosis in a murine model Fertil Steril 93 2010 1440 1447
22. Q. Chen, W. Zhou, D. Pu, Z. Li, Q. Huang, and Q. Chen The inhibitory effect of 15-R-LXA4 on experimental endometriosis Eur J Obstet Gynecol Reprod Biol 145 2009 200 204
23. Z. Xu, F. Zhao, F. Lin, J. Chen, and Y. Huang Lipoxin A4 inhibits the development of endometriosis in mice: the role of antiinflammation and antiangiogenesis Am J Reprod Immunol 67 2012 491 497
24. American Society for Reproductive Medicine Revised American Society for Reproductive Medicine classification of endometriosis: 1996 Fertil Steril 67 1997 817 821
25. J.A. Rock ZOLADEX Endometriosis Study Group The revised American Fertility Society classification of endometriosis: reproducibility of scoring Fertil Steril 63 1995 1108 1110
26. S. Fiore, M. Romano, E.M. Reardon, and C.N. Serhan Induction of functional lipoxin A4 receptors in HL-60 cells Blood 81 1993 3395 3403
27. S. Fiore, J.F. Maddox, H.D. Perez, and C.N. Serhan Identification of a human cDNA encoding a functional high affinity lipoxin A4 receptor J Exp Med 180 1994 253 260
28. A.E. Wakeling, M. Dukes, and J. Bowler A potent specific pure antiestrogen with clinical potential Cancer Res 51 1991 3867 3873
29. A. Walther, K. Riehemann, and V. Gerke A novel ligand of the formyl peptide receptor: annexin I regulates neutrophil extravasation by interacting with the FPR Mol Cell 5 2000 831 840
30. F.S. Machado, J.E. Johndrow, L. Esper, A. Dias, A. Bafica, and C.N. Serhan Anti-inflammatory actions of lipoxin A4 and aspirin-triggered lipoxin are SOCS-2 dependent Nat Med 12 2006 330 334
31. L.C. Giudice, and L.C. Kao Endometriosis Lancet 364 2004 1789 1799
32. J.A. Sampson Metastatic or embolic endometriosis, due to the menstrual dissemination of endometrial tissue into the venous circulation Am J Pathol 3 1927 93 110.43
33. J.C. Lousse, A. van Langendonckt, S. Defrere, R.G. Ramos, S. Colette, and J. Donnez Peritoneal endometriosis is an inflammatory disease Front Biosci (Elite Ed) 4 2012 23 40
34. D.L. Olive, and L.B. Schwartz Endometriosis N Engl J Med 328 1993 1759 1769
35. J.A. Rock, N.H. Dubin, R.B. Ghodgaonkar, C.A. Bergquist, Y.S. Erozan, and A.W. Kimball Jr. Cul-de-sac fluid in women with endometriosis: fluid volume and prostanoid concentration during the proliferative phase of the cycle - days 8 to 12 Fertil Steril 37 1982 747 750
36. K. Seibert, Y. Zhang, K. Leahy, S. Hauser, J. Masferrer, and W. Perkins Pharmacological and biochemical demonstration of the role of cyclooxygenase 2 in inflammation and pain Proc Natl Acad Sci U S A 91 1994 12013 12017
37. A. Fagotti, G. Ferrandina, F. Fanfani, F. Legge, L. Lauriola, and M. Gessi Analysis of cyclooxygenase-2 (COX-2) expression in different sites of endometriosis and correlation with clinico-pathological parameters Hum Reprod 19 2004 393 397
38. H. Ota, S. Igarashi, M. Sasaki, and T. Tanaka Distribution of cyclooxygenase-2 in eutopic and ectopic endometrium in endometriosis and adenomyosis Hum Reprod 16 2001 561 566
39. B.S. Fletcher, D.A. Kujubu, D.M. Perrin, and H.R. Herschman Structure of the mitogen-inducible TIS10 gene and demonstration that the TIS10-encoded protein is a functional prostaglandin G/H synthase J Biol Chem 267 1992 4338 4344
40. W.L. Smith, R.M. Garavito, and D.L. DeWitt Prostaglandin endoperoxide H synthases (cyclooxygenases)-1 and -2 J Biol Chem 271 1996 33157 33160
41. M. Tamura, S. Sebastian, B. Gurates, S. Yang, Z. Fang, and S.E. Bulun Vascular endothelial growth factor up-regulates cyclooxygenase-2 expression in human endothelial cells J Clin Endocrinol Metab 87 2002 3504 3507
42. K.J. Sales, and H.N. Jabbour Cyclooxygenase enzymes and prostaglandins in reproductive tract physiology and pathology Prostaglandins Other Lipid Mediat 71 2003 97 117
43. H. Koike, H. Egawa, T. Ohtsuka, M. Yamaguchi, T. Ikenoue, and N. Mori Correlation between dysmenorrheic severity and prostaglandin production in women with endometriosis Prostaglandins Leukot Essent Fatty Acids 46 1992 133 137
44. H. Koike, H. Egawa, T. Ohtsuka, M. Yamaguchi, T. Ikenoue, and N. Mori Eicosanoids production in endometriosis Prostaglandins Leukot Essent Fatty Acids 45 1992 313 317
45. Z.G. Li, J.H. Lang, J.H. Leng, and D.Y. Liu [Increased levels of prostaglandin E2 and bcl-2 in peritoneal fluid and serum of patients with endometriosis] Zhonghua Fu Chan Ke Za Zhi 40 2005 598 600 Chinese
46. P.C. Chuang, H.S. Sun, T.M. Chen, and S.J. Tsai Prostaglandin E2 induces fibroblast growth factor 9 via EP3-dependent protein kinase Cdelta and Elk-1 signaling Mol Cell Biol 26 2006 8281 8292
47. S.K. Banu, J. Lee, V.O. Speights Jr., A. Starzinski-Powitz, and J.A. Arosh Cyclooxygenase-2 regulates survival, migration, and invasion of human endometriotic cells through multiple mechanisms Endocrinology 149 2008 1180 1189
48. D.W. Gilroy, P.R. Colville-Nash, D. Willis, J. Chivers, M.J. Paul-Clark, and D.A. Willoughby Inducible cyclooxygenase may have antiinflammatory properties Nat Med 5 1999 698 701
49. E.C. Hayes, and J.A. Rock COX-2 inhibitors and their role in gynecology Obstet Gynecol Surv 57 2002 768 780
50. J. Reese, X. Zhao, W.G. Ma, N. Brown, T.J. Maziasz, and S.K. Dey Comparative analysis of pharmacologic and/or genetic disruption of cyclooxygenase-1 and cyclooxygenase-2 function in female reproduction in mice Endocrinology 142 2001 3198 3206
51. J. Couzin Clinical trials. Nail-biting time for trials of COX-2 drugs Science 306 2004 1673 1675
52. J. Couzin Medicine. Estrogen's ties to COX-2 may explain heart disease gender gap Science 306 2004 1277
53. M.D. Breyer, and R.M. Breyer Prostaglandin E receptors and the kidney Am J Physiol Renal Physiol 279 2000 F12 F23
54. S. Narumiya, and G.A. FitzGerald Genetic and pharmacological analysis of prostanoid receptor function J Clin Invest 108 2001 25 30
55. S.K. Banu, J. Lee, A. Starzinski-Powitz, and J.A. Arosh Gene expression profiles and functional characterization of human immortalized endometriotic epithelial and stromal cells Fertil Steril 90 2008 972 987
56. Y. Bao, M.L. Pucci, B.S. Chan, R. Lu, S. Ito, and V.L. Schuster Prostaglandin transporter PGT is expressed in cell types that synthesize and release prostanoids Am J Physiol Renal Physiol 282 2002 F1103 F1110
57. S. Endo, T. Nomura, B.S. Chan, R. Lu, M.L. Pucci, and Y. Bao Expression of PGT in MDCK cell monolayers: polarized apical localization and induction of active PG transport Am J Physiol Renal Physiol 282 2002 F618 F622
58. Z.S. Chen, K. Lee, and G.D. Kruh Transport of cyclic nucleotides and estradiol 17-beta-D-glucuronide by multidrug resistance protein 4. Resistance to 6-mercaptopurine and 6-thioguanine J Biol Chem 276 2001 33747 33754
59. Z.S. Chen, K. Lee, S. Walther, R.B. Raftogianis, M. Kuwano, and H. Zeng Analysis of methotrexate and folate transport by multidrug resistance protein 4 (ABCC4): MRP4 is a component of the methotrexate efflux system Cancer Res 62 2002 3144 3150
60. M. Rius, A.T. Nies, J. Hummel-Eisenbeiss, G. Jedlitschky, and D. Keppler Cotransport of reduced glutathione with bile salts by MRP4 (ABCC4) localized to the basolateral hepatocyte membrane Hepatology 38 2003 374 384
61. N. Zelcer, G. Reid, P. Wielinga, A. Kuil, I. van der Heijden, and J.D. Schuetz Steroid and bile acid conjugates are substrates of human multidrug-resistance protein (MRP) 4 (ATP-binding cassette C4) Biochem J 371 Pt 2 2003 361 367
62. C.A. Ritter, G. Jedlitschky, zu Meyer, H. Schwabedissen, M. Grube, and K. Kock Cellular export of drugs and signaling molecules by the ATP-binding cassette transporters MRP4 (ABCC4) and MRP5 (ABCC5) Drug Metab Rev 37 2005 253 278
63. F.G. Russel, J.B. Koenderink, and R. Masereeuw Multidrug resistance protein 4 (MRP4/ABCC4): a versatile efflux transporter for drugs and signalling molecules Trends Pharmacol Sci 29 2008 200 207
64. W. Wu, A.V. Dnyanmote, and S.K. Nigam Remote communication through solute carriers and ATP binding cassette drug transporter pathways: an update on the remote sensing and signaling hypothesis Mol Pharmacol 79 2011 795 805
65. R.G. Deeley, C. Westlake, and S.P. Cole Transmembrane transport of endo- and xenobiotics by mammalian ATP-binding cassette multidrug resistance proteins Physiol Rev 86 2006 849 899
66. M.D. Norris, J. Smith, K. Tanabe, P. Tobin, C. Flemming, and G.L. Scheffer Expression of multidrug transporter MRP4/ABCC4 is a marker of poor prognosis in neuroblastoma and confers resistance to irinotecan in vitro Mol Cancer Ther 4 2005 547 553
67. J. Konig, M. Hartel, A.T. Nies, M.E. Martignoni, J. Guo, and M.W. Buchler Expression and localization of human multidrug resistance protein (ABCC) family members in pancreatic carcinoma Int J Cancer 115 2005 359 367
68. Z. Zhang, J. Wang, B. Shen, C. Peng, and M. Zheng The ABCC4 gene is a promising target for pancreatic cancer therapy Gene 491 2012 194 199
69. C.N. Serhan, S. Yacoubian, and R. Yang Anti-inflammatory and proresolving lipid mediators Annu Rev Pathol 3 2008 279 312
70. E. Motohashi, H. Kawauchi, H. Endo, H. Kondo, H. Kitasato, and H. Kuramoto Regulatory expression of lipoxin A4 receptor in physiologically estrus cycle and pathologically endometriosis Biomed Pharmacother 59 2005 330 338
71. L.J. Macdonald, S.C. Boddy, F.C. Denison, K.J. Sales, and H.N. Jabbour A role for lipoxin A(4) as an antiinflammatory mediator in the human endometrium Reproduction 142 2011 345 352
72. 4 inhibit tumor necrosis factor 1alpha-initiated neutrophil responses and trafficking: regulators of a cytokine-chemokine axis J Exp Med 189 1999 1923 1930
73. 4's antiinflammatory actions on intestinal epithelium Am J Physiol Cell Physiol 284 2003 C888 C896
74. S. Sodin-Semrl, A. Spagnolo, R. Mikus, B. Barbaro, J. Varga, and S. Fiore Opposing regulation of interleukin-8 and NF-kappaB responses by lipoxin A4 and serum amyloid A via the common lipoxin A receptor Int J Immunopathol Pharmacol 17 2004 145 156
75. C. Bonnans, and B.D. Levy Lipid mediators as agonists for the resolution of acute lung inflammation and injury Am J Respir Cell Mol Biol 36 2007 201 205
76. C. Bonnans, D. Gras, C. Chavis, B. Mainprice, I. Vachier, and P. Godard Synthesis and antiinflammatory effect of lipoxins in human airway epithelial cells Biomed Pharmacother 61 2007 261 267
77. 4 of production of interleukins induced in endothelial cells by lipopolysaccharide Inflamm Res 57 2008 430 437
78. S. Matsuzaki, T. Murakami, S. Uehara, M. Canis, H. Sasano, and K. Okamura Expression of estrogen receptor alpha and beta in peritoneal and ovarian endometriosis Fertil Steril 75 2001 1198 1205
79. C. Pellegrini, I. Gori, C. Achtari, D. Hornung, E. Chardonnens, and D. Wunder The expression of estrogen receptors as well as GREB1, c-MYC, and cyclin D1, estrogen-regulated genes implicated in proliferation, is increased in peritoneal endometriosis Fertil Steril 98 2012 1200 1208
80. 4 analogues inhibit leukocyte recruitment to Porphyromonas gingivalis: a role for cyclooxygenase-2 and lipoxins in periodontal disease Biochemistry 39 2000 4761 4768