MicroRNAs as regulators of drug transporters, drug-metabolizing enzymes, and tight junctions: Implication for intestinal barrier function

Pharmacology and Therapeutics

Volumn 143, Issue 2, 2014, Pages 217-224

  Ikemura, Kenji ^a   Iwamoto, Takuya ^a,b   Okuda, Masahiro ^a,b  

^a MIE UNIVERSITY HOSPITAL   (Japan)

^b MIE UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Intestinal barrier; Metabolizing enzymes; MicroRNA; Small intestine; Tight junction; Transporter

Indexed keywords

ABC TRANSPORTER; BREAST CANCER RESISTANCE PROTEIN; CYTOCHROME P450 1A1; CYTOCHROME P450 1B1; CYTOCHROME P450 2C8; CYTOCHROME P450 2E1; CYTOCHROME P450 3A4; DRUG METABOLIZING ENZYME; MICRORNA; MONOCARBOXYLATE TRANSPORTER 1; MULTIDRUG RESISTANCE ASSOCIATED PROTEIN 1; MULTIDRUG RESISTANCE ASSOCIATED PROTEIN 2; MULTIDRUG RESISTANCE ASSOCIATED PROTEIN 3; PEPTIDE TRANSPORTER 1; CARRIER PROTEIN; CYTOCHROME P450;

ARTICLE; BIOGENESIS; DRUG ABSORPTION; DRUG TRANSPORT; GENE EXPRESSION REGULATION; GENETIC POLYMORPHISM; GENETIC REGULATION; HEREDITY; HUMAN; INTESTINAL BARRIER FUNCTION; INTESTINE ABSORPTION; INTESTINE EPITHELIUM CELL; INTESTINE FUNCTION; MULTIDRUG RESISTANCE; NONHUMAN; PERSONALIZED MEDICINE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; TIGHT JUNCTION; BIOSYNTHESIS; GENETICS; METABOLISM; PHARMACOKINETICS; PHYSIOLOGY; TRANSPORT AT THE CELLULAR LEVEL;

ATP-BINDING CASSETTE TRANSPORTERS; BIOLOGICAL TRANSPORT; CARRIER PROTEINS; CYTOCHROME P-450 ENZYME SYSTEM; HUMANS; INTESTINAL ABSORPTION; MICRORNAS; PHARMACOKINETICS; TIGHT JUNCTIONS;

EID: 84902547445     PISSN: 01637258     EISSN: 1879016X     Source Type: Journal    
DOI: 10.1016/j.pharmthera.2014.03.002     Document Type: Review

References (82)

1. A. Balakrishnan, A.T. Stearns, P.J. Park, J.M. Dreyfuss, S.W. Ashley, and D.B. Rhoads et al. Upregulation of proapoptotic microRNA mir-125a after massive small bowel resection in rats Ann Surg 255 2012 747 753
2. L. Bao, S. Hazari, S. Mehra, D. Kaushal, K. Moroz, and S. Dash Increased expression of P-glycoprotein and doxorubicin chemoresistance of metastatic breast cancer is regulated by miR-298 Am J Pathol 180 2012 2490 2503
3. M. Bazett, A. Paun, and C.K. Haston MicroRNA profiling of cystic fibrosis intestinal disease in mice Mol Genet Metab 103 2011 38 43
4. E. Berezikov, V. Guryev, J. van de Belt, E. Wienholds, R.H. Plasterk, and E. Cuppen Phylogenetic shadowing and computational identification of human microRNA genes Cell 120 2005 21 24
5. D. Betel, M. Wilson, A. Gabow, D.S. Marks, and C. Sander The microRNA.org resource: targets and expression Nucleic Acids Res 36 2008 D149 D153
6. F. Borel, R. Han, A. Visser, H. Petry, S.J. van Deventer, and P.L. Jansen et al. Adenosine triphosphate-binding cassette transporter genes up-regulation in untreated hepatocellular carcinoma is mediated by cellular microRNAs Hepatology 55 2012 821 832
7. L.Y. Bourguignon, C.C. Spevak, G. Wong, W. Xia, and E. Gilad Hyaluronan-CD44 interaction with protein kinase C(epsilon) promotes oncogenic signaling by the stem cell marker Nanog and the production of microRNA-21, leading to down-regulation of the tumor suppressor protein PDCD4, anti-apoptosis, and chemotherapy resistance in breast tumor cells J Biol Chem 284 2009 26533 26546
8. H. Cheng, and C.P. Leblond Origin, differentiation and renewal of the four main epithelial cell types in the mouse small intestine. V. Unitarian Theory of the origin of the four epithelial cell types Am J Anat 141 1974 537 561
9. H. Chiba, M. Osanai, M. Murata, T. Kojima, and N. Sawada Transmembrane proteins of tight junctions Biochim Biophys Acta 1778 2008 588 600
10. L.J. Chin, E. Ratner, S. Leng, R. Zhai, S. Nallur, and I. Babar et al. A SNP in a let-7 microRNA complementary site in the KRAS 3′ untranslated region increases non-small cell lung cancer risk Cancer Res 68 2008 8535 8540
11. Y.M. Choi, S. An, E.M. Lee, K. Kim, S.J. Choi, and J.S. Kim et al. CYP1A1 is a target of miR-892a-mediated post-transcriptional repression Int J Oncol 41 2012 331 336
12. C. Cordon-Cardo, J.P. O'Brien, J. Boccia, D. Casals, J.R. Bertino, and M.R. Melamed Expression of the multidrug resistance gene product (P-glycoprotein) in human normal and tumor tissues J Histochem Cytochem 38 1990 1277 1287
13. G. Dalmasso, H.T. Nguyen, Y. Yan, H. Laroui, M.A. Charania, and T.S. Obertone et al. MicroRNA-92b regulates expression of the oligopeptide transporter PepT1 in intestinal epithelial cells Am J Physiol Gastrointest Liver Physiol 300 2011 G52 G59
14. G. Dalmasso, H.T. Nguyen, Y. Yan, H. Laroui, S. Srinivasan, and S.V. Sitaraman et al. MicroRNAs determine human intestinal epithelial cell fate Differentiation 80 2010 147 154
15. X. Ding, and L.S. Kaminsky Human extrahepatic cytochromes P450: function in xenobiotic metabolism and tissue-selective chemical toxicity in the respiratory and gastrointestinal tracts Annu Rev Pharmacol Toxicol 43 2003 149 173
16. R. Duan, C. Pak, and P. Jin Single nucleotide polymorphism associated with mature miR-125a alters the processing of pri-miRNA Hum Mol Genet 16 2007 1124 1131
17. A. Esquela-Kerscher, and F.J. Slack Oncomirs - microRNAs with a role in cancer Nat Rev Cancer 6 2006 259 269
18. A. Eulalio, E. Huntzinger, and E. Izaurralde Getting to the root of miRNA-mediated gene silencing Cell 132 2008 9 14
19. D.D. Feng, H. Zhang, P. Zhang, Y.S. Zheng, X.J. Zhang, and B.W. Han et al. Down-regulated miR-331-5p and miR-27a are associated with chemotherapy resistance and relapse in leukaemia J Cell Mol Med 15 2011 2164 2175
20. W. Filipowicz, S.N. Bhattacharyya, and N. Sonenberg Mechanisms of post-transcriptional regulation by microRNAs: are the answers in sight? Nat Rev Genet 9 2008 102 114
21. M. Furuse, K. Fujita, T. Hiiragi, K. Fujimoto, and S. Tsukita Claudin-1 and -2: novel integral membrane proteins localizing at tight junctions with no sequence similarity to occludin J Cell Biol 141 1998 1539 1550
22. M. Furuse, T. Hirase, M. Itoh, A. Nagafuchi, S. Yonemura, and S. Tsukita Occludin: a novel integral membrane protein localizing at tight junctions J Cell Biol 123 1993 1777 1788
23. C.K. Garcia, M.S. Brown, R.K. Pathak, and J.L. Goldstein cDNA cloning of MCT2, a second monocarboxylate transporter expressed in different cells than MCT1 J Biol Chem 270 1995 1843 1849
24. N. Gassler, C. Rohr, A. Schneider, J. Kartenbeck, A. Bach, and N. Obermuller et al. Inflammatory bowel disease is associated with changes of enterocytic junctions Am J Physiol Gastrointest Liver Physiol 281 2001 G216 G228
25. M.M. Gottesman, T. Fojo, and S.E. Bates Multidrug resistance in cancer: role of ATP-dependent transporters Nat Rev Cancer 2 2002 48 58
26. K. Hino, K. Tsuchiya, T. Fukao, K. Kiga, R. Okamoto, and T. Kanai et al. Inducible expression of microRNA-194 is regulated by HNF-1alpha during intestinal epithelial cell differentiation RNA 14 2008 1433 1442
27. J. Hou, and D. Zhao MicroRNA regulation in renal pathophysiology Int J Mol Sci 14 2013 13078 13092
28. K. Ikemura, K. Inoue, H. Mizutani, H. Oka, T. Iwamoto, and M. Okuda An antioxidant Trolox restores decreased oral absorption of cyclosporine A after liver ischemia-reperfusion through distinct mechanisms between CYP3A and P-glycoprotein in the small intestine Eur J Pharmacol 690 2012 192 201
29. K. Ikemura, T. Iwamoto, and M. Okuda Altered functions and expressions of drug transporters in liver, kidney and intestine in disorders of local and remote organs: possible role of oxidative stress in the pathogenesis Expert Opin Drug Metab Toxicol 5 2009 907 920
30. K. Ikemura, K. Urano, H. Matsuda, H. Mizutani, T. Iwamoto, and M. Okuda Decreased oral absorption of cyclosporine A after liver ischemia-reperfusion injury in rats: the contribution of CYP3A and P-glycoprotein to the first-pass metabolism in intestinal epithelial cells J Pharmacol Exp Ther 328 2009 249 255
31. K. Ikemura, M. Yamamoto, S. Miyazaki, H. Mizutani, T. Iwamoto, and M. Okuda MicroRNA-145 post-transcriptionally regulates the expression and function of P-glycoprotein in intestinal epithelial cells Mol Pharmacol 83 2013 399 405
32. J. Ikenouchi, M. Furuse, K. Furuse, H. Sasaki, and S. Tsukita Tricellulin constitutes a novel barrier at tricellular contacts of epithelial cells J Cell Biol 171 2005 939 945
33. M. Ingelman-Sundberg, S.C. Sim, A. Gomez, and C. Rodriguez-Antona Influence of cytochrome P450 polymorphisms on drug therapies: pharmacogenetic, pharmacoepigenetic and clinical aspects Pharmacol Ther 116 2007 496 526
34. N. Iwai, and H. Naraba Polymorphisms in human pre-miRNAs Biochem Biophys Res Commun 331 2005 1439 1444
35. X. Jiao, L. Zhao, M. Ma, X. Bai, M. He, and Y. Yan et al. MiR-181a enhances drug sensitivity in mitoxantone-resistant breast cancer cells by targeting breast cancer resistance protein (BCRP/ABCG2) Breast Cancer Res Treat 139 2013 717 730
36. M. Jin, T. Shimada, K. Yokogawa, M. Nomura, J. Ishizaki, and Y. Piao et al. Site-dependent contributions of P-glycoprotein and CYP3A to cyclosporin A absorption, and effect of dexamethasone in small intestine of mice Biochem Pharmacol 72 2006 1042 1050
37. V.N. Kim MicroRNA biogenesis: coordinated cropping and dicing Nat Rev Mol Cell Biol 6 2005 376 385
38. L.T. Kaaij, M. van de Wetering, F. Fang, B. Decato, A. Molaro, and H.J. van de Werken et al. DNA methylation dynamics during intestinal stem cell differentiation reveals enhancers driving gene expression in the villus Genome Biol 14 2013 R50
39. I. Koturbash, F.A. Beland, and I.P. Pogribny Role of microRNAs in the regulation of drug metabolizing and transporting genes and the response to environmental toxicants Expert Opin Drug Metab Toxicol 8 2012 597 606
40. O. Kovalchuk, J. Filkowski, J. Meservy, Y. Ilnytskyy, V.P. Tryndyak, and V.F. Chekhun et al. Involvement of microRNA-451 in resistance of the MCF-7 breast cancer cells to chemotherapeutic drug doxorubicin Mol Cancer Ther 7 2008 2152 2159
41. E.J. Lee, M. Baek, Y. Gusev, D.J. Brackett, G.J. Nuovo, and T.D. Schmittgen Systematic evaluation of microRNA processing patterns in tissues, cell lines, and tumors RNA 14 2008 35 42
42. X. Li, Y.Z. Pan, G.M. Seigel, Z.H. Hu, M. Huang, and A.M. Yu Breast cancer resistance protein BCRP/ABCG2 regulatory microRNAs (hsa-miR-328, -519c and -520h) and their differential expression in stem-like ABCG2+ cancer cells Biochem Pharmacol 81 2011 783 792
43. Q. Li, F. Zhu, and P. Chen MiR-7 and miR-218 epigenetically control tumor suppressor genes RASSF1A and Claudin-6 by targeting HoxB3 in breast cancer Biochem Biophys Res Commun 424 2012 28 33
44. Z. Liang, H. Wu, J. Xia, Y. Li, Y. Zhang, and K. Huang et al. Involvement of miR-326 in chemotherapy resistance of breast cancer through modulating expression of multidrug resistance-associated protein 1 Biochem Pharmacol 79 2010 817 824
45. I. Martin-Padura, S. Lostaglio, M. Schneemann, L. Williams, M. Romano, and P. Fruscella et al. Junctional adhesion molecule, a novel member of the immunoglobulin superfamily that distributes at intercellular junctions and modulates monocyte transmigration J Cell Biol 142 1998 117 127
46. L.B. McKenna, J. Schug, A. Vourekas, J.B. McKenna, N.C. Bramswig, and J.R. Friedman et al. MicroRNAs control intestinal epithelial differentiation, architecture, and barrier function Gastroenterology 139 2010 1654 1664 (1664 e1651)
47. T. Mohri, M. Nakajima, T. Fukami, M. Takamiya, Y. Aoki, and T. Yokoi Human CYP2E1 is regulated by miR-378 Biochem Pharmacol 79 2010 1045 1052
48. M. Nakajima, and T. Yokoi MicroRNAs from biology to future pharmacotherapy: regulation of cytochrome P450s and nuclear receptors Pharmacol Ther 131 2011 330 337
49. T. Nakano, S. Sekine, K. Ito, and T. Horie Ezrin regulates the expression of Mrp2/Abcc2 and Mdr1/Abcb1 along the rat small intestinal tract Am J Physiol Gastrointest Liver Physiol 305 2013 G807 G817
50. D.R. Nelson, L. Koymans, T. Kamataki, J.J. Stegeman, R. Feyereisen, and D.J. Waxman et al. P450 superfamily: update on new sequences, gene mapping, accession numbers and nomenclature Pharmacogenetics 6 1996 1 42
51. H.T. Nguyen, G. Dalmasso, Y. Yan, H. Laroui, S. Dahan, and L. Mayer et al. MicroRNA-7 modulates CD98 expression during intestinal epithelial cell differentiation J Biol Chem 285 2010 1479 1489
52. H. Ogihara, H. Saito, B.C. Shin, T. Terado, S. Takenoshita, and Y. Nagamachi et al. Immuno-localization of H+/peptide cotransporter in rat digestive tract Biochem Biophys Res Commun 220 1996 848 852
53. M. Onizuka, N. Kunii, M. Toyosaki, S. Machida, D. Ohgiya, and Y. Ogawa et al. Cytochrome P450 genetic polymorphisms influence the serum concentration of calcineurin inhibitors in allogeneic hematopoietic SCT recipients Bone Marrow Transplant 46 2011 1113 1117
54. Y.Z. Pan, W. Gao, and A.M. Yu MicroRNAs regulate CYP3A4 expression via direct and indirect targeting Drug Metab Dispos 37 2009 2112 2117
55. Y.Z. Pan, M.E. Morris, and A.M. Yu MicroRNA-328 negatively regulates the expression of breast cancer resistance protein (BCRP/ABCG2) in human cancer cells Mol Pharmacol 75 2009 1374 1379
56. Y.Z. Pan, A. Zhou, Z. Hu, and A.M. Yu Small nucleolar RNA-derived microRNA hsa-Mir-1291 modulates cellular drug disposition through direct targeting of ABC transporter ABCC1 Drug Metab Dispos 41 2013 1744 1751
57. I.P. Pogribny, J.N. Filkowski, V.P. Tryndyak, A. Golubov, S.I. Shpyleva, and O. Kovalchuk Alterations of microRNAs and their targets are associated with acquired resistance of MCF-7 breast cancer cells to cisplatin Int J Cancer 127 2010 1785 1794
58. T.J. Pullen, G. da Silva Xavier, G. Kelsey, and G.A. Rutter MiR-29a and miR-29b contribute to pancreatic beta-cell-specific silencing of monocarboxylate transporter 1 (Mct1) Mol Cell Biol 31 2011 3182 3194
59. T. Rezen, D. Rozman, J.M. Pascussi, and K. Monostory Interplay between cholesterol and drug metabolism Biochim Biophys Acta 1814 2011 146 160
60. J.K. Rieger, K. Klein, S. Winter, and U.M. Zanger Expression variability of absorption, distribution, metabolism, excretion-related microRNAs in human liver: influence of nongenetic factors and association with gene expression Drug Metab Dispos 41 2013 1752 1762
61. J. Saito, T. Hirota, S. Furuta, D. Kobayashi, H. Takane, and I. Ieiri Association between DNA methylation in the miR-328 5′-flanking region and inter-individual differences in miR-328 and BCRP expression in human placenta PLoS One 8 2013 e72906
62. M.A. Saunders, H. Liang, and W.H. Li Human polymorphism at microRNAs and microRNA target sites Proc Natl Acad Sci U S A 104 2007 3300 3305
63. A.E. Senior, M.K. al-Shawi, and I.L. Urbatsch The catalytic cycle of P-glycoprotein FEBS Lett 377 1995 285 289
64. S. Takagi, M. Nakajima, T. Mohri, and T. Yokoi Post-transcriptional regulation of human pregnane X receptor by micro-RNA affects the expression of cytochrome P450 3A4 J Biol Chem 283 2008 9674 9680
65. T. Terada, and K. Inui Peptide transporters: structure, function, regulation and application for drug delivery Curr Drug Metab 5 2004 85 94
66. M. Thorn, N. Finnstrom, S. Lundgren, A. Rane, and L. Loof Cytochromes P450 and MDR1 mRNA expression along the human gastrointestinal tract Br J Clin Pharmacol 60 2005 54 60
67. Y. Tsuchiya, M. Nakajima, S. Takagi, T. Taniya, and T. Yokoi MicroRNA regulates the expression of human cytochrome P450 1B1 Cancer Res 66 2006 9090 9098
68. A. Tsuji Transporter-mediated drug interactions Drug Metab Pharmacokinet 17 2002 253 274
69. E. Turrini, S. Haenisch, S. Laechelt, T. Diewock, O. Bruhn, and I. Cascorbi MicroRNA profiling in K-562 cells under imatinib treatment: influence of miR-212 and miR-328 on ABCG2 expression Pharmacogenet Genomics 22 2012 198 205
70. E. Vreugdenhil, C.S. Verissimo, R. Mariman, J.T. Kamphorst, J.S. Barbosa, and T. Zweers et al. MicroRNA 18 and 124a down-regulate the glucocorticoid receptor: implications for glucocorticoid responsiveness in the brain Endocrinology 150 2009 2220 2228
71. X.W. Wang, N.H. Heegaard, and H. Orum MicroRNAs in liver disease Gastroenterology 142 2012 1431 1443
72. R. Wei, F. Yang, T.J. Urban, L. Li, N. Chalasani, and D.A. Flockhart et al. Impact of the interaction between 3′-UTR SNPs and microRNA on the expression of human xenobiotic metabolism enzyme and transporter genes Front Genet 3 2012 248
73. F. Wu, S. Zhang, T. Dassopoulos, M.L. Harris, T.M. Bayless, and S.J. Meltzer et al. Identification of microRNAs associated with ileal and colonic Crohn's disease Inflamm Bowel Dis 16 2010 1729 1738
74. F. Wu, M. Zikusoka, A. Trindade, T. Dassopoulos, M.L. Harris, and T.M. Bayless et al. MicroRNAs are differentially expressed in ulcerative colitis and alter expression of macrophage inflammatory peptide-2 alpha Gastroenterology 135 2008 1624 1635 (e1624)
75. K. Xu, X. Liang, K. Shen, D. Cui, Y. Zheng, and J. Xu et al. MiR-297 modulates multidrug resistance in human colorectal carcinoma by down-regulating MRP-2 Biochem J 446 2012 291 300
76. Y. Xu, S.J. Ohms, Z. Li, Q. Wang, G. Gong, and Y. Hu et al. Changes in the expression of miR-381 and miR-495 are inversely associated with the expression of the MDR1 gene and development of multi-drug resistance PLoS One 8 2013 e82062
77. L. Yang, N. Li, H. Wang, X. Jia, X. Wang, and J. Luo Altered microRNA expression in cisplatin-resistant ovarian cancer cells and upregulation of miR-130a associated with MDR1/P-glycoprotein-mediated drug resistance Oncol Rep 28 2012 592 600
78. Y. Yang, Y. Ma, C. Shi, H. Chen, H. Zhang, and N. Chen et al. Overexpression of miR-21 in patients with ulcerative colitis impairs intestinal epithelial barrier function through targeting the Rho GTPase RhoB Biochem Biophys Res Commun 434 2013 746 752
79. D. Ye, S. Guo, R. Al-Sadi, and T.Y. Ma MicroRNA regulation of intestinal epithelial tight junction permeability Gastroenterology 141 2011 1323 1333
80. S. Zeissig, N. Burgel, D. Gunzel, J. Richter, J. Mankertz, and U. Wahnschaffe et al. Changes in expression and distribution of claudin 2, 5 and 8 lead to discontinuous tight junctions and barrier dysfunction in active Crohn's disease Gut 56 2007 61 72
81. Q.Y. Zhang, D. Dunbar, A. Ostrowska, S. Zeisloft, J. Yang, and L.S. Kaminsky Characterization of human small intestinal cytochromes P-450 Drug Metab Dispos 27 1999 804 809
82. S.Y. Zhang, S. Surapureddi, S. Coulter, S.S. Ferguson, and J.A. Goldstein Human CYP2C8 is post-transcriptionally regulated by microRNAs 103 and 107 in human liver Mol Pharmacol 82 2012 529 540