Translational repression of SLC26A3 by miR-494 in intestinal epithelial cells

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 306, Issue 2, 2014, Pages

  Anbazhagan, Arivarasu N ^a   Priyamvada, Shubha ^a   Kumar, Anoop ^a   Maher, Daniel B ^a   Borthakur, Alip ^a   Alrefai, Waddah A ^a,b   Malakooti, Jaleh ^a   Kwon, John H ^c   Dudeja, Pradeep K ^a,b  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^b JESSE BROWN VA MEDICAL CENTER   (United States)

^c UNIVERSITY OF CHICAGO   (United States)

Author keywords

3' UTR; DRA; microRNA

Indexed keywords

DOWNREGULATED IN ADENOMA PROTEIN; LUCIFERASE; MEMBRANE PROTEIN; MICRORNA; MICRORNA 31; MICRORNA 494; PROTEIN; SLC26A3 PROTEIN; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ANIMAL CELL; ARTICLE; CELL STRAIN CACO 2; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME REPRESSION; GENETIC TRANSFECTION; INFECTIOUS DIARRHEA; INTESTINE EPITHELIUM CELL; NONHUMAN; NUCLEOTIDE BINDING SITE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REGULATORY MECHANISM; SITE DIRECTED MUTAGENESIS; SPECTROPHOTOMETRY;

3′-UTR; DRA; MICRORNA;

3' UNTRANSLATED REGIONS; BLOTTING, WESTERN; CACO-2 CELLS; CHLORIDE-BICARBONATE ANTIPORTERS; CLONING, MOLECULAR; COMPUTATIONAL BIOLOGY; DIARRHEA; EPITHELIAL CELLS; HUMANS; INTESTINAL MUCOSA; MICRORNAS; POLYMERASE CHAIN REACTION; PROTEIN PROCESSING, POST-TRANSLATIONAL; REAL-TIME POLYMERASE CHAIN REACTION; RNA, MESSENGER;

EID: 84892624108     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00222.2013     Document Type: Article

References (51)

1. Alexiou P, Maragkakis M, Papadopoulos GL, Reczko M, Hatzigeorgiou AG. Lost in translation: an assessment and perspective for computational microRNA target identification. Bioinformatics 25: 3049-3055, 2009.
2. Alrefai WA, Wen X, Jiang W, Katz JP, Steinbrecher KA, Cohen MB, Williams IR, Dudeja PK, Wu GD. Molecular cloning and promoter analysis of downregulated in adenoma (DRA). Am J Physiol Gastrointest Liver Physiol 293: G923-G934, 2007.
3. Asano K, Matsushita T, Umeno J, Hosono N, Takahashi A, Kawaguchi T, Matsumoto T, Matsui T, Kakuta Y, Kinouchi Y, Shimosegawa T, Hosokawa M, Arimura Y, Shinomura Y, Kiyohara Y, Tsunoda T, Kamatani N, Iida M, Nakamura Y, Kubo M. A genome-wide association study identifies three new susceptibility loci for ulcerative colitis in the Japanese population. Nat Genet 41: 1325-1329, 2009.
4. Borenshtein D, Schlieper KA, Rickman BH, Chapman JM, Schweinfest CW, Fox JG, Schauer DB. Decreased expression of colonic Slc26a3 and carbonic anhydrase iv as a cause of fatal infectious diarrhea in mice. Infect Immun 77: 3639-3650, 2009.
5. Brennecke J, Hipfner DR, Stark A, Russell RB, Cohen SM. Bantam encodes a developmentally regulated microRNA that controls cell proliferation and regulates the proapoptotic gene hid in Drosophila. Cell 113: 25-36, 2003.
6. Chernova MN, Jiang L, Shmukler BE, Schweinfest CW, Blanco P, Freedman SD, Stewart AK, Alper SL. Acute regulation of the SLC26A3 congenital chloride diarrhoea anion exchanger (DRA) expressed in Xenopus oocytes. J Physiol 549: 3-19, 2003.
7. Dalal SR, Kwon JH. The role of MicroRNA in inflammatory bowel disease. Gastroenterol Hepatol (NY) 6: 714-722, 2010.
8. Dalmasso G, Nguyen HT, Yan Y, Laroui H, Charania MA, Obertone TS, Sitaraman SV, Merlin D. MicroRNA-92b regulates expression of the oligopeptide transporter PepT1 in intestinal epithelial cells. Am J Physiol Gastrointest Liver Physiol 300: G52-G59, 2011.
9. Dudeja PK, Gill RK, Ramaswamy K. Absorption-secretion and epithelial cell function. In: Colonic Diseases, edited by Koch T. New York: Humana, 2003, p. 3-23.
10. Enright AJ, John B, Gaul U, Tuschl T, Sander C, Marks DS. MicroRNA targets in Drosophila. Genome Biol 5: R1, 2003.
11. Filipowicz W, Bhattacharyya SN, Sonenberg N. Mechanisms of posttranscriptional regulation by microRNAs: are the answers in sight? Nat Rev Genet 9: 102-114, 2008.
12. Friedman RC, Farh KK, Burge CB, Bartel DP. Most mammalian mRNAs are conserved targets of microRNAs. Genome Res 19: 92-105, 2009.
13. Gill RK, Alrefai WA, Ramaswamy A, Dudeja PK. Mechanisms and regulation of NaCl absorption in the human intestine. Res Signpost 1: 643-677, 2003.
14. Gill RK, Borthakur A, Hodges K, Turner JR, Clayburgh DR, Saksena S, Zaheer A, Ramaswamy K, Hecht G, Dudeja PK. Mechanism underlying inhibition of intestinal apical Cl/OH exchange following infection with enteropathogenic E. coli. J Clin Invest 117: 428-437, 2007.
15. Gillen AE, Gosalia N, Leir SH, Harris A. MicroRNA regulation of expression of the cystic fibrosis transmembrane conductance regulator gene. Biochem J 438: 25-32, 2011.
16. Griffiths-Jones S, Saini HK, van Dongen S, Enright AJ. miRBase: tools for microRNA genomics. Nucleic Acids Res 36: D154-158, 2008.
17. Grimson A, Farh KK, Johnston WK, Garrett-Engele P, Lim LP, Bartel DP. MicroRNA targeting specificity in mammals: determinants beyond seed pairing. Mol Cell 27: 91-105, 2007.
18. Iborra M, Bernuzzi F, Invernizzi P, Danese S. MicroRNAs in autoimmunity and inflammatory bowel disease: crucial regulators in immune response. Autoimmun Rev 11: 305-314, 2010.
19. Iwasaki S, Kawamata T, Tomari Y. Drosophila argonaute1 and argonaute2 employ distinct mechanisms for translational repression. Mol Cell 34: 58-67, 2009.
20. Jacob P, Rossmann H, Lamprecht G, Kretz A, Neff C, Lin-Wu E, Gregor M, Groneberg DA, Kere J, Seidler U. Down-regulated in adenoma mediates apical Cl-/HCO3 exchange in rabbit, rat, and human duodenum. Gastroenterology 122: 709-724, 2002.
21. John B, Enright AJ, Aravin A, Tuschl T, Sander C, Marks DS. Human microRNA targets. PLoS Biol 2: e363, 2004.
22. Kiriakidou M, Nelson PT, Kouranov A, Fitziev P, Bouyioukos C, Mourelatos Z, Hatzigeorgiou A. A combined computational-experimental approach predicts human microRNA targets. Genes Dev 18: 1165-1178, 2004.
23. Kong YW, Cannell IG, de Moor CH, Hill K, Garside PG, Hamilton TL, Meijer HA, Dobbyn HC, Stoneley M, Spriggs KA, Willis AE, Bushell M. The mechanism of micro-RNA-mediated translation repression is determined by the promoter of the target gene. Proc Natl Acad Sci USA 105: 8866-8871, 2008.
24. Lai EC. Micro RNAs are complementary to 3 UTR sequence motifs that mediate negative post-transcriptional regulation. Nat Genet 30: 363-364, 2002.
25. Lamprecht G, Baisch S, Schoenleber E, Gregor M. Transport properties of the human intestinal anion exchanger DRA (down-regulated in adenoma) in transfected HEK293 cells. Pflügers Arch 449: 479-490, 2005.
26. Lamprecht G, Gaco V, Turner JR, Natour D, Gregor M. Regulation of the intestinal anion exchanger DRA (downregulated in adenoma). Ann NY Acad Sci 1165: 261-266, 2009.
27. Lee MG, Choi JY, Luo X, Strickland E, Thomas PJ, Muallem S. Cystic fibrosis transmembrane conductance regulator regulates luminal Cl-/HCO3 exchange in mouse submandibular and pancreatic ducts. J Biol Chem 274: 14670-14677, 1999.
28. Lewis BP, Shih IH, Jones-Rhoades MW, Bartel DP, Burge CB. Prediction of mammalian microRNA targets. Cell 115: 787-798, 2003.
29. Liao Y, Lonnerdal B. Global microRNA characterization reveals that miR-103 is involved in IGF-1 stimulated mouse intestinal cell proliferation. PLoS One 5: e12976, 2010.
30. Liao Y, Lonnerdal B. miR-584 mediates post-transcriptional expression of lactoferrin receptor in Caco-2 cells and in mouse small intestine during the perinatal period. Int J Biochem Cell Biol 42: 1363-1369, 2009.
31. Liu L, Jiang Y, Zhang H, Greenlee AR, Han Z. Overexpressed miR-494 down-regulates PTEN gene expression in cells transformed by anti-benzo-(a)pyrene-trans-7,8-dihydrodiol-9,10-epoxide. Life Sci 86: 192-198, 2010.
32. Malakooti J, Saksena S, Gill RK, Dudeja PK. Transcriptional regulation of the intestinal luminal Na(+) and Cl(-) transporters. Biochem J 435: 313-325, 2011.
33. McKenna LB, Schug J, Vourekas A, McKenna JB, Bramswig NC, Friedman JR, Kaestner KH. MicroRNAs control intestinal epithelial differentiation, architecture, and barrier function. Gastroenterology 139: 1654-1664, 1664. e1651, 2010.
34. Megiorni F, Cialfi S, Dominici C, Quattrucci S, Pizzuti A. Synergistic post-transcriptional regulation of the cystic fibrosis transmembrane conductance regulator (CFTR) by miR-101 and miR-494 specific binding. PLoS One 6: e26601, 2011.
35. Melvin JE, Park K, Richardson L, Schultheis PJ, Shull GE. Mouse down-regulated in adenoma (DRA) is an intestinal Cl(-)/HCO(3) (-)/ exchanger and is up-regulated in colon of mice lacking the NHE3 Na(+)/H(+) exchanger. J Biol Chem 274: 22855-22861, 1999.
36. Mosakhani N, Lahti L, Borze I, Karjalainen-Lindsberg ML, Sundstrom J, Ristamaki R, Osterlund P, Knuutila S, Sarhadi VK. MicroRNA profiling predicts survival in anti-EGFR treated chemorefractory metastatic colorectal cancer patients with wild-type KRAS and BRAF. Cancer Genet 205: 545-551, 2012.
37. Moseley RH, Hoglund P, Wu GD, Silberg DG, Haila S, de la Chapelle A, Holmberg C, Kere J. Downregulated in adenoma gene encodes a chloride transporter defective in congenital chloride diarrhea. Am J Physiol Gastrointest Liver Physiol 276: G185-G192, 1999.
38. Mount DB, Romero MF. The SLC26 gene family of multifunctional anion exchangers. Pflügers Arch 447: 710-721, 2004.
39. Raheja G, Singh V, Ma K, Boumendjel R, Borthakur A, Gill RK, Saksena S, Alrefai WA, Ramaswamy K, Dudeja PK. Lactobacillus acidophilus stimulates the expression of SLC26A3 via a transcriptional mechanism. Am J Physiol Gastrointest Liver Physiol 298: G395-G401, 2010.
40. Saksena S, Gill RK, Tyagi S, Alrefai WA, Sarwar Z, Ramaswamy K, Dudeja PK. Involvement of c-Src and protein kinase C delta in the inhibition of Cl(-)/OH(-) exchange activity in Caco-2 cells by serotonin. J Biol Chem 280: 11859-11868, 2005.
41. Saksena S, Singla A, Goyal S, Katyal S, Bansal N, Gill RK, Alrefai WA, Ramaswamy K, Dudeja PK. Mechanisms of transcriptional modulation of the human anion exchanger SLC26A3 gene expression by IFN-γ. Am J Physiol Gastrointest Liver Physiol 298: G159-G166, 2010.
42. Schweinfest CW, Spyropoulos DD, Henderson KW, Kim JH, Chapman JM, Barone S, Worrell RT, Wang Z, Soleimani M. Slc26a3 (dra)-deficient mice display chloride-losing diarrhea, enhanced colonic proliferation, and distinct up-regulation of ion transporters in the colon. J Biol Chem 281: 37962-37971, 2006.
43. Singla A, Dwivedi A, Saksena S, Gill RK, Alrefai WA, Ramaswamy K, Dudeja PK. Mechanisms of lysophosphatidic acid (LPA) mediated stimulation of intestinal apical Cl-/OH-exchange. Am J Physiol Gastrointest Liver Physiol 298: G182-G189, 2010.
44. Wang X. miRDB: a microRNA target prediction and functional annotation database with a wiki interface. RNA 14: 1012-1017, 2008.
45. Wang X, El Naqa IM. Prediction of both conserved and nonconserved microRNA targets in animals. Bioinformatics 24: 325-332, 2008.
46. Wheat VJ, Shumaker H, Burnham C, Shull GE, Yankaskas JR, Soleimani M. CFTR induces the expression of DRA along with Cl-/ HCO3 exchange activity in tracheal epithelial cells. Am J Physiol Cell Physiol 279: C62-C71, 2000.
47. Wu F, Zhang S, Dassopoulos T, Harris ML, Bayless TM, Meltzer SJ, Brant SR, Kwon JH. Identification of microRNAs associated with ileal and colonic Crohn's disease. Inflamm Bowel Dis 16: 1729-1738, 2010.
48. Xiao F, Juric M, Li J, Riederer B, Yeruva S, Singh AK, Zheng L, Glage S, Kollias G, Dudeja P, Tian DA, Xu G, Zhu J, Bachmann O, Seidler U. Loss of downregulated in adenoma (DRA) impairs mucosal HCO3(-) secretion in murine ileocolonic inflammation. Inflamm Bowel Dis 18: 101-111, 2012.
49. Yang H, Jiang W, Furth EE, Wen X, Katz JP, Sellon RK, Silberg DG, Antalis TM, Schweinfest CW, Wu GD. Intestinal inflammation reduces expression of DRA, a transporter responsible for congenital chloride diarrhea. Am J Physiol Gastrointest Liver Physiol 275: G1445-G1453, 1998.
50. Ye D, Guo S, Al-Sadi R, Ma TY. MicroRNA regulation of intestinal epithelial tight junction permeability. Gastroenterology 141: 1323-1333, 2011.
51. Yoda M, Kawamata T, Paroo Z, Ye X, Iwasaki S, Liu Q, Tomari Y. ATP-dependent human RISC assembly pathways. Nat Struct Mol Biol 17: 17-23, 2010.