MiR-199a-5p regulates urothelial permeability and may play a role in bladder pain syndrome

American Journal of Pathology

Volumn 182, Issue 2, 2013, Pages 431-448

  Monastyrskaya, Katia ^a   Sánchez Freire, Verónica ^c   Hashemi Gheinani, Ali ^a   Klumpp, David J ^d   Babiychuk, Eduard B ^b   Draeger, Annette ^b   Burkhard, Fiona C ^a  

^a UNIVERSITY OF BERN   (Switzerland)

^b UNIVERSITY OF BERN   (Switzerland)

^c STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARHGAP12 PROTEIN; CYCLIC AMP; LIN7C PROTEIN; MESSENGER RNA; MICRORNA; MICRORNA 199A 5P; NECTIN 1; PALS1 PROTEIN; RND1 PROTEIN; UNCLASSIFIED DRUG;

ADULT; AGED; ARTICLE; BLADDER PAIN SYNDROME; CELL CULTURE; CELL JUNCTION; CELL MATURATION; CELL MEMBRANE PERMEABILITY; CELL POLARITY; CHRONIC PAIN; CLINICAL ARTICLE; CONTROLLED STUDY; CYSTALGIA; ENZYME ACTIVATION; FEMALE; GENE EXPRESSION REGULATION; GENE OVEREXPRESSION; GENE TARGETING; GENETIC CODE; HUMAN; HUMAN CELL; HUMAN TISSUE; LASER MICRODISSECTION; MALE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SMOOTH MUSCLE; TIGHT JUNCTION; UPREGULATION; UROTHELIAL PERMEABILITY;

3' UNTRANSLATED REGIONS; BASE SEQUENCE; BINDING SITES; CELL DIFFERENTIATION; CELL LINE; CYCLIC AMP; CYSTITIS, INTERSTITIAL; DOWN-REGULATION; ELECTRIC IMPEDANCE; EPITHELIAL CELLS; HUMANS; LUCIFERASES; MICRORNAS; MOLECULAR SEQUENCE DATA; MUSCLE, SMOOTH; PERMEABILITY; PROTEIN BINDING; RAC1 GTP-BINDING PROTEIN; RHOA GTP-BINDING PROTEIN; RNA, MESSENGER; RNA, SMALL INTERFERING; TIGHT JUNCTION PROTEINS; UP-REGULATION; URINARY BLADDER; UROTHELIUM;

EID: 84872690808     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2012.10.020     Document Type: Article

References (57)

1. L.A. Birder More than just a barrier: urothelium as a drug target for urinary bladder pain Am J Physiol Renal Physiol 289 2005 F489 F495
2. G. Apodaca The uroepithelium: not just a passive barrier Traffic 5 2004 117 128
3. P. Acharya, J. Beckel, W.G. Ruiz, E. Wang, R. Rojas, L. Birder, and G. Apodaca Distribution of the tight junction proteins ZO-1, occludin, and claudin-4, -8, and -12 in bladder epithelium Am J Physiol Renal Physiol 287 2004 F305 F318
4. S.A. Lewis Everything you wanted to know about the bladder epithelium but were afraid to ask Am J Physiol Renal Physiol 278 2000 F867 F874
5. J.D. Lilly, and C.L. Parsons Bladder surface glycosaminoglycans is a human epithelial permeability barrier Surg Gynecol Obstet 171 1990 493 496
6. L.A. Birder, and W.C. de Groat Mechanisms of disease: involvement of the urothelium in bladder dysfunction Nat Clin Pract Urol 4 2007 46 54
7. C.L. Parsons The role of the urinary epithelium in the pathogenesis of interstitial cystitis/prostatitis/urethritis Urology 69 2007 9 16
8. J.P. van de Merwe, J. Nordling, P. Bouchelouche, K. Bouchelouche, M. Cervigni, L.K. Daha, S. Elneil, M. Fall, G. Hohlbrugger, P. Irwin, S. Mortensen, A. van Ophoven, J.L. Osborne, R. Peeker, B. Richter, C. Riedl, J. Sairanen, M. Tinzl, and J.J. Wyndaele Diagnostic criteria, classification, and nomenclature for painful bladder syndrome/interstitial cystitis: an ESSIC proposal Eur Urol 53 2008 60 67
9. J.E. Tomaszewski, J.R. Landis, V. Russack, T.M. Williams, L.P. Wang, C. Hardy, C. Brensinger, Y.L. Matthews, S.T. Abele, J.W. Kusek, and L.M. Nyberg Biopsy features are associated with primary symptoms in interstitial cystitis: results from the interstitial cystitis database study Urology 57 2001 67 81
10. G. Slobodov, M. Feloney, C. Gran, K.D. Kyker, R.E. Hurst, and D.J. Culkin Abnormal expression of molecular markers for bladder impermeability and differentiation in the urothelium of patients with interstitial cystitis J Urol 171 2004 1554 1558
11. C.O. Zhang, J.Y. Wang, K.R. Koch, and S. Keay Regulation of tight junction proteins and bladder epithelial paracellular permeability by an antiproliferative factor from patients with interstitial cystitis J Urol 174 2005 2382 2387
12. V. Sanchez Freire, F.C. Burkhard, T.M. Kessler, A. Kuhn, A. Draeger, and K. Monastyrskaya MicroRNAs may mediate the down-regulation of neurokinin-1 receptor in chronic bladder pain syndrome Am J Pathol 176 2010 288 303
13. D.P. Bartel MicroRNAs: target recognition and regulatory functions Cell 136 2009 215 233
14. T.A. Farazi, J.I. Spitzer, P. Morozov, and T. Tuschl miRNAs in human cancer J Pathol 223 2011 102 115
15. M. Lagos-Quintana, R. Rauhut, W. Lendeckel, and T. Tuschl Identification of novel genes coding for small expressed RNAs Science 294 2001 853 858
16. D.W. Thomson, C.P. Bracken, and G.J. Goodall Experimental strategies for microRNA target identification Nucleic Acids Res 39 2011 6845 6853
17. S. Valastyan, and R.A. Weinberg Roles for microRNAs in the regulation of cell adhesion molecules J Cell Sci 124 2011 999 1006
18. S. Huang, and X. He microRNAs: tiny RNA molecules, huge driving forces to move the cell Protein Cell 1 2010 916 926
19. Y. Tang, A. Banan, C.B. Forsyth, J.Z. Fields, C.K. Lau, L.J. Zhang, and A. Keshavarzian Effect of alcohol on miR-212 expression in intestinal epithelial cells and its potential role in alcoholic liver disease Alcohol Clin Exp Res 32 2008 355 364
20. D. Ye, S. Guo, R. Al-Sadi, and T.Y. Ma MicroRNA regulation of intestinal epithelial tight junction permeability Gastroenterology 141 2011 1323 1333
21. Q. Zhou, W.W. Souba, C.M. Croce, and G.N. Verne MicroRNA-29a regulates intestinal membrane permeability in patients with irritable bowel syndrome Gut 59 2010 775 784
22. A. Rickard, N. Dorokhov, J. Ryerse, D.J. Klumpp, and J. McHowat Characterization of tight junction proteins in cultured human urothelial cells In Vitro Cell Dev Biol Anim 44 2008 261 267
23. D.J. Klumpp, A.C. Weiser, S. Sengupta, S.G. Forrestal, R.A. Batler, and A.J. Schaeffer Uropathogenic Escherichia coli potentiates type 1 pilus-induced apoptosis by suppressing NF-κB Infect Immun 69 2001 6689 6695
24. V. Sanchez Freire, F.C. Burkhard, A. Schmitz, T.M. Kessler, and K. Monastyrskaya Structural differences between the bladder dome and trigone revealed by mRNA expression analysis of cold-cut biopsies BJU Int 108 2011 E126 E135
25. J. Eldrup, J. Thorup, S.L. Nielsen, T. Hald, and B. Hainau Permeability and ultrastructure of human bladder epithelium Br J Urol 55 1983 488 492
26. C.L. Parsons, J.D. Lilly, and P. Stein Epithelial dysfunction in nonbacterial cystitis (interstitial cystitis) J Urol 145 1991 732 735
27. A.L. Cozens, M.J. Yezzi, K. Kunzelmann, T. Ohrui, L. Chin, K. Eng, W.E. Finkbeiner, J.H. Widdicombe, and D.C. Gruenert CFTR expression and chloride secretion in polarized immortal human bronchial epithelial cells Am J Respir Cell Mol Biol 10 1994 38 47
28. H. Wan, H.L. Winton, C. Soeller, G.A. Stewart, P.J. Thompson, D.C. Gruenert, M.B. Cannell, D.R. Garrod, and C. Robinson Tight junction properties of the immortalized human bronchial epithelial cell lines Calu-3 and 16HBE14o Eur Respir J 15 2000 1058 1068
29. A.J. Giraldez, Y. Mishima, J. Rihel, R.J. Grocock, S. Van Dongen, K. Inoue, A.J. Enright, and A.F. Schier Zebrafish MiR-430 promotes deadenylation and clearance of maternal mRNAs Science 312 2006 75 79
30. S. Rane, M. He, D. Sayed, L. Yan, D. Vatner, and M. Abdellatif An antagonism between the AKT and β-adrenergic signaling pathways mediated through their reciprocal effects on miR-199a-5p Cell Signal 22 2010 1054 1062
31. J. Pieczynski, and B. Margolis Protein complexes that control renal epithelial polarity Am J Physiol Renal Physiol 300 2011 F589 F601
32. S.W. Straight, K. Shin, V.C. Fogg, S. Fan, C.J. Liu, M. Roh, and B. Margolis Loss of PALS1 expression leads to tight junction and polarity defects Mol Biol Cell 15 2004 1981 1990
33. M.R. Popoff, and B. Geny Multifaceted role of Rho, Rac, Cdc42 and Ras in intercellular junctions, lessons from toxins Biochim Biophys Acta 1788 2009 797 812
34. S. Terry, M. Nie, K. Matter, and M.S. Balda Rho signaling and tight junction functions Physiology (Bethesda) 25 2010 16 26
35. S. Massari, C. Perego, V. Padovano, A. D'Amico, A. Raimondi, M. Francolini, and G. Pietrini LIN7 mediates the recruitment of IRSp53 to tight junctions Traffic 10 2009 246 257
36. L. Lozovatsky, N. Abayasekara, S. Piawah, and Z. Walther CASK deletion in intestinal epithelia causes mislocalization of LIN7C and the DLG1/Scrib polarity complex without affecting cell polarity Mol Biol Cell 20 2009 4489 4499
37. A.M. Turner, R. Subramaniam, D.F. Thomas, and J. Southgate Generation of a functional, differentiated porcine urothelial tissue in vitro Eur Urol 54 2008 1423 1432
38. V. Sanchez-Freire, M.G. Blanchard, F.C. Burkhard, T.M. Kessler, S. Kellenberger, and K. Monastyrskaya Acid-sensing channels in human bladder: expression, function and alterations during bladder pain syndrome J Urol 186 2011 1509 1516
39. A. Otsuka, H. Shinbo, R. Matsumoto, Y. Kurita, and S. Ozono Expression and functional role of β-adrenoceptors in the human urinary bladder urothelium Naunyn Schmiedebergs Arch Pharmacol 377 2008 473 481
40. S.M. Kaech, C.W. Whitfield, and S.K. Kim The LIN-2/LIN-7/LIN-10 complex mediates basolateral membrane localization of the C. elegans EGF receptor LET-23 in vulval epithelial cells Cell 94 1998 761 771
41. S.W. Straight, J.N. Pieczynski, E.L. Whiteman, C.J. Liu, and B. Margolis Mammalian lin-7 stabilizes polarity protein complexes J Biol Chem 281 2006 37738 37747
42. P. Khandelwal, W.G. Ruiz, and G. Apodaca Compensatory endocytosis in bladder umbrella cells occurs through an integrin-regulated and RhoA- and dynamin-dependent pathway EMBO J 29 2009 1961 1975
43. Z. Zhang, C. Wu, S. Wang, W. Huang, Z. Zhou, K. Ying, Y. Xie, and Y. Mao Cloning and characterization of ARHGAP12, a novel human rhoGAP gene Int J Biochem Cell Biol 34 2002 325 331
44. M. Matsuda, Y. Kobayashi, S. Masuda, M. Adachi, T. Watanabe, J.K. Yamashita, E. Nishi, S. Tsukita, and M. Furuse Identification of adherens junction-associated GTPase activating proteins by the fluorescence localization-based expression cloning Exp Cell Res 314 2008 939 949
45. A. Gentile, L. D'Alessandro, L. Lazzari, B. Martinoglio, A. Bertotti, A. Mira, L. Lanzetti, P.M. Comoglio, and E. Medico Met-driven invasive growth involves transcriptional regulation of Arhgap12 Oncogene 27 2008 5590 5598
46. M.H. Roh, O. Makarova, C.J. Liu, K. Shin, S. Lee, S. Laurinec, M. Goyal, R. Wiggins, and B. Margolis The Maguk protein, Pals1, functions as an adapter, linking mammalian homologues of Crumbs and Discs Lost J Cell Biol 157 2002 161 172
47. Q. Wang, X.W. Chen, and B. Margolis PALS1 regulates E-cadherin trafficking in mammalian epithelial cells Mol Biol Cell 18 2007 874 885
48. P. Riou, P. Villalonga, and A.J. Ridley Rnd proteins: multifunctional regulators of the cytoskeleton and cell cycle progression BioEssays 32 2010 986 992
49. G. Loirand, C. Cario-Toumaniantz, P. Chardin, and P. Pacaud The Rho-related protein Rnd1 inhibits Ca2+ sensitization of rat smooth muscle J Physiol 516 Pt 3 1999 825 834
50. C.D. Nobes, I. Lauritzen, M.G. Mattei, S. Paris, A. Hall, and P. Chardin A new member of the Rho family, Rnd1, promotes disassembly of actin filament structures and loss of cell adhesion J Cell Biol 141 1998 187 197
51. A. Mizoguchi, H. Nakanishi, K. Kimura, K. Matsubara, K. Ozaki-Kuroda, T. Katata, T. Honda, Y. Kiyohara, K. Heo, M. Higashi, T. Tsutsumi, S. Sonoda, C. Ide, and Y. Takai Nectin: an adhesion molecule involved in formation of synapses J Cell Biol 156 2002 555 565
52. S. Rane, M. He, D. Sayed, H. Vashistha, A. Malhotra, J. Sadoshima, D.E. Vatner, S.F. Vatner, and M. Abdellatif Downregulation of miR-199a derepresses hypoxia-inducible factor-1α and Sirtuin 1 and recapitulates hypoxia preconditioning in cardiac myocytes Circ Res 104 2009 879 886
53. X.W. Song, Q. Li, L. Lin, X.C. Wang, D.F. Li, G.K. Wang, A.J. Ren, Y.R. Wang, Y.W. Qin, W.J. Yuan, and Q. Jing MicroRNAs are dynamically regulated in hypertrophic hearts, and miR-199a is essential for the maintenance of cell size in cardiomyocytes J Cell Physiol 225 2010 437 443
54. H.H. Cheung, A.J. Davis, T.L. Lee, A.L. Pang, S. Nagrani, O.M. Rennert, and W.Y. Chan Methylation of an intronic region regulates miR-199a in testicular tumor malignancy Oncogene 30 2011 3404 3415
55. Q. Shen, V.R. Cicinnati, X. Zhang, S. Iacob, F. Weber, G.C. Sotiropoulos, A. Radtke, M. Lu, A. Paul, G. Gerken, and S. Beckebaum Role of microRNA-199a-5p and discoidin domain receptor 1 in human hepatocellular carcinoma invasion Mol Cancer 9 2010 227
56. S. Kim, U.J. Lee, M.N. Kim, E.J. Lee, J.Y. Kim, M.Y. Lee, S. Choung, Y.J. Kim, and Y.C. Choi MicroRNA miR-199a* regulates the MET proto-oncogene and the downstream extracellular signal-regulated kinase 2 (ERK2) J Biol Chem 283 2008 18158 18166
57. P.C. Stein, A. Torri, and C.L. Parsons Elevated urinary norepinephrine in interstitial cystitis Urology 53 1999 1140 1143