Post-transcriptional regulation of cystic fibrosis transmembrane conductance regulator expression and function by MicroRNAs

American Journal of Respiratory Cell and Molecular Biology

Volumn 49, Issue 4, 2013, Pages 544-551

  Ramachandran, Shyam ^a   Karp, Philip H ^a   Osterhaus, Samantha R ^a   Jiang, Peng ^a   Wohlford Lenane, Christine ^a   Lennox, Kim A ^b   Jacobi, Ashley M ^b   Praekh, Kal ^a   Rose, Scott D ^b   Behlke, Mark A ^b   Xing, Yi ^a,b   Welsh, Michael J ^a   McCray Jr , Paul B ^a  

^a UNIVERSITY OF IOWA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

39 UTR; ATP binding cassette protein; Cystic fibrosis transmembrane conductance regulator; Epithelial fluid and electrolyte transport

Indexed keywords

CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; MICRORNA; MICRORNA 494; MICRORNA 509 3P; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; CYSTIC FIBROSIS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE TARGETING; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; PROTEIN FUNCTION; PROTEIN PROCESSING; RESPIRATORY EPITHELIUM; SIGNAL TRANSDUCTION; STAPHYLOCOCCUS AUREUS;

CELL LINE; CYSTIC FIBROSIS; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; EPITHELIAL CELLS; GENE EXPRESSION; HUMANS; INFLAMMATION MEDIATORS; INTERLEUKIN-1BETA; MICRORNAS; NF-KAPPA B; RESPIRATORY MUCOSA; RNA PROCESSING, POST-TRANSCRIPTIONAL; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84886530607     PISSN: 10441549     EISSN: 15354989     Source Type: Journal    
DOI: 10.1165/rcmb.2012-0430OC     Document Type: Article

References (54)

1. Friedman RC, Farh KK, Burge CB, Bartel DP. Most mammalian mRNAs are conserved targets of microRNAs. Genome Res 2009;19: 92-105.
2. Guo H, Ingolia NT, Weissman JS, Bartel DP. Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature 2010;466: 835-840.
3. Bushati N, Cohen SM. MicroRNA functions. Annu Rev Cell Dev Biol 2007;23:175-205.
4. Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell 2009;136:215-233.
5. Shkumatava A, Stark A, Sive H, Bartel DP. Coherent but overlapping expression of microRNAs and their targets during vertebrate development. Genes Dev 2009;23:466-481.
6. Marcet B, Chevalier B, Luxardi G, Coraux C, Zaragosi LE, Cibois M, Robbe-Sermesant K, Jolly T, Cardinaud B, Moreilhon C, et al. Control of vertebrate multiciliogenesis by miR-449 through direct repression of the Delta/Notch pathway. Nat Cell Biol 2011;13:693-699.
7. Harris KS, Zhang Z, McManus MT, Harfe BD, Sun X. Dicer function is essential for lung epithelium morphogenesis. Proc Natl Acad Sci USA 2006;103:2208-2213.
8. Williams AE, Larner-Svensson H, Perry MM, Campbell GA, Herrick SE, Adcock IM, Erjefalt JS, Chung KF, Lindsay MA. MicroRNA expression profiling in mild asthmatic human airways and effect of corticosteroid therapy. PLoS ONE 2009;4:e5889.
9. Moschos SA, Williams AE, Perry MM, Birrell MA, Belvisi MG, Lindsay MA. Expression profiling in vivo demonstrates rapid changes in lung microRNA levels following lipopolysaccharide-induced inflammation but not in the anti-inflammatory action of glucocorticoids. BMC Genomics 2007;8:240.
10. Williams AE, PerryMM,Moschos SA, LindsayMA.MicroRNA expression in the aging mouse lung. BMC Genomics 2007;8:172.
11. Riordan JR, Rommens JM, Kerem B, Alon N, Rozmahel R, Grzelczak Z, Zielenski J, Lok S, Plavsic N, Chou JL, et al. Identification of the cystic fibrosis gene: cloning and characterization of complementary DNA. Science 1989;245:1066-1073.
12. Rowe SM, Miller S, Sorscher EJ. Cystic fibrosis. N Engl J Med 2005;352: 1992-2001.
13. Koehler DR, Downey GP, Sweezey NB, Tanswell AK, Hu J. Lung inflammation as a therapeutic target in cystic fibrosis. Am J Respir Cell Mol Biol 2004;31:377-381.
14. Muir A, Soong G, Sokol S, Reddy B, Gomez MI, Van Heeckeren A, Prince A. Toll-like receptors in normal and cystic fibrosis airway epithelial cells. Am J Respir Cell Mol Biol 2004;30:777-783.
15. Zhang Z, Ott CJ, Lewandowsa MA, Leir SH, Harris A. Molecular mechanisms controlling CFTR gene expression in the airway. J Cell Mol Med 2012;16:1321-1330.
16. Lewandowska MA, Costa FF, Bischof JM, Williams SH, Soares MB, Harris A. Multiple mechanisms influence regulation of the cystic fibrosis transmembrane conductance regulator gene promoter. Am J Respir Cell Mol Biol 2010;43:334-341.
17. Trapnell BC, Chu C-S, Paakko PK, Banks TC, Yoshimura K, Ferrans VJ, Chernick MS, Crystal RG. Expression of the cystic fibrosis transmembrane conductance regulator gene in the respiratory tract of normal individuals and individuals with cystic fibrosis. Proc Natl Acad Sci USA 1991;88:6565-6569.
18. Mukherji S, EbertMS, Zheng GX, Tsang JS, Sharp PA, van Oudenaarden A. MicroRNAs can generate thresholds in target gene expression. Nat Genet 2011;43:854-859.
19. Gillen AE, Gosalia N, Leir SH, Harris A. MicroRNA regulation of expression of the cystic fibrosis transmembrane conductance regulator gene. Biochem J 2011;438:25-32.
20. Megiorni F, Cialfi S, Dominici C, Quattrucci S, Pizzuti A. Synergistic posttranscriptional regulation of the cystic fibrosis transmembrane conductance regulator (CFTR) by miR-101 and miR-494 specific binding. PLoS ONE 2011;6:e26601.
21. Ramachandran S, Karp PH, Jiang P, Ostedgaard LS, Walz AE, Fisher JT, Keshavjee S, Lennox KA, Jacobi AM, Rose SD, et al. A microRNA network regulates expression and biosynthesis of wild-type and DeltaF508 mutant cystic fibrosis transmembrane conductance regulator. Proc Natl Acad Sci USA 2012;109:13362- 13367.
22. Ramachandran S, Clarke LA, Scheetz TE, Amaral MD, McCray PB Jr. Microarray mRNA expression profiling to study cystic fibrosis. Methods Mol Biol 2011;742:193-212.
23. Karp PH, Moninger TO, Weber SP, Nesselhauf TS, Launspach JL, Zabner J,WelshMJ. An in vitro model of differentiated human airway epithelia: methods for establishing primary cultures. Methods Mol Biol 2002;188: 115-137.
24. Yamaya M, Finkbeiner WE, Chun SY, Widdicombe JH. Differentiated structure and function of cultures from human tracheal epithelium. Am J Physiol 1992;262:L713-L724.
25. Haws C, Finkbeiner WE, Widdicombe JH, Wine JJ. CFTR in Calu-3 human airway cells: channel properties and role in cAMP-activated Cl2 conductance. Am J Physiol 1994;266:L502-L512.
26. Varga K, Jurkuvenaite A, Wakefield J, Hong JS, Guimbellot JS, Venglarik CJ, Niraj A, MazurM, Sorscher EJ, Collawn JF, et al. Efficient intracellular processing of the endogenous cystic fibrosis transmembrane conductance regulator in epithelial cell lines. J Biol Chem 2004;279:22578-22584.
27. Ostedgaard LS,Meyerholz DK, Chen JH, Pezzulo AA, Karp PH, Rokhlina T, Ernst SE, Hanfland RA, Reznikov LR, Ludwig PS, et al. The DF508 mutation causes CFTR misprocessing and cystic fibrosis-like disease in pigs. Sci Transl Med 2011;3:74ra24.
28. Farmen SL, Karp PH, Ng P, Palmer DJ, Koehler DR, Hu J, Beaudet AL, Zabner J, Welsh MJ. Gene transfer of CFTR to airway epithelia: low levels of expression are sufficient to correct Cl2 transport and overexpression can generate basolateral CFTR. Am J Physiol Lung Cell Mol Physiol 2005;289:L1123-L1130.
29. Szaff M, H'iby N. Antibiotic treatment of Staphylococcus aureus infection in cystic fibrosis. Acta Paediatr Scand 1982;71:821-826.
30. Baudouin-Legros M, Hinzpeter A, Jaulmes A, Brouillard F, Costes B, Fanen P, Edelman A. Cell-specific posttranscriptional regulation of CFTR gene expression via influence of MAPK cascades on 39UTR part of transcripts. Am J Physiol Cell Physiol 2005;289:C1240-C1250.
31. Cafferata EG, Gonzelez-Guerrico AM, Giordano L, Pivetta OH, Santa-Coloma TA. Interleukin-1beta regulates CFTR expression in human intestinal T84 cells. Biochim Biophys Acta 2000;1500:241-248.
32. Cafferata EG, Guerrico AM, Pivetta OH, Santa-Coloma TA. NF-kappaB activation is involved in regulation of cystic fibrosis transmembrane conductance regulator (CFTR) by interleukin-1beta. J Biol Chem2001; 276:15441-15444.
33. Nakamura H, Yoshimura K, Bajocchi G, Trapnell BC, Pavirani A, Crystal RG. Tumor necrosis factor modulation of expression of the cystic fibrosis transmembrane conductance regulator gene. FEBS Lett 1992; 314:366-370.
34. Besancon F, Przewlocki G, Baró I, Hongre AS, Escande D, Edelman A. Interferon-gamma downregulates CFTR gene expression in epithelial cells. Am J Physiol 1994;267:C1398-C1404.
35. Brouillard F, Bouthier M, Leclerc T, Clement A, Baudouin-Legros M, Edelman A. NF-kappa B mediates up-regulation of CFTR gene expression in Calu-3 cells by interleukin-1beta. J Biol Chem2001;276:9486-9491.
36. Galietta LJ, Folli C, Marchetti C, Romano L, Carpani D, Conese M, Zegarra-Moran O. Modification of transepithelial ion transport in human cultured bronchial epithelial cells by interferon-gamma. Am J Physiol Lung Cell Mol Physiol 2000;278:L1186-L1194.
37. Gray T, Coakley R, Hirsh A, Thornton D, Kirkham S, Koo JS, Burch L, Boucher R, Nettesheim P. Regulation of MUC5AC mucin secretion and airway surface liquid metabolism by IL-1beta in human bronchial epithelia. Am J Physiol Lung Cell Mol Physiol 2004;286:L320-L330.
38. Muller-Anstett MA, Muller P, Albrecht T, Nega M, Wagener J, Gao Q, Kaesler S, Schaller M, Biedermann T, Gotz F. Staphylococcal peptidoglycan co-localizes with NOD2 and TLR2 and activates innate immune response via both receptors in primary murine keratinocytes. PLoS ONE 2010;5:e13153.
39. Viemann D, Goebeler M, Schmid S, Klimmek K, Sorg C, Ludwig S, Roth J. Transcriptional profiling of IKK2/NF-kappa B-and p38 MAP kinase-dependent gene expression in TNF-alpha-stimulated primary human endothelial cells. Blood 2004;103:3365-3373.
40. Lin FS, Lin CC, Chien CS, Luo SF, Yang CM. Involvement of p42/p44 MAPK, JNK, and NF-kappaB in IL-1beta-induced ICAM-1 expression in human pulmonary epithelial cells. J Cell Physiol 2005;202:464-473.
41. Udalova IA, Mott R, Field D, Kwiatkowski D. Quantitative prediction of NF-kappa B DNA-protein interactions. Proc Natl Acad Sci USA 2002;99:8167-8172.
42. Fan C, Yang J, Engelhardt JF. Temporal pattern of NFkappaB activation influences apoptotic cell fate in a stimuli-dependent fashion. J Cell Sci 2002;115:4843-4853.
43. Kolin N, Claass A, Sommer M, Puchelle E, Tommler B. DeltaF508 CFTR protein expression in tissues from patients with cystic fibrosis. J Clin Invest 1999;103:1379-1389.
44. Blackledge NP, Ott CJ, Gillen AE, Harris A. An insulator element 39 to the CFTR gene binds CTCF and reveals an active chromatin hub in primary cells. Nucleic Acids Res 2009;37:1086-1094.
45. Ott CJ, Bischof JM, Unti KM, Gillen AE, Leir SH, Harris A. Nucleosome occupancy reveals regulatory elements of the CFTR promoter. Nucleic Acids Res 2012;40:625-637.
46. Ott CJ, Blackledge NP, Kerschner JL, Leir SH, Crawford GE, Cotton CU, Harris A. Intronic enhancers coordinate epithelial-specific looping of the active CFTR locus. Proc Natl Acad Sci USA 2009; 106:19934-19939.
47. Bartoszewski RA, Jablonsky M, Bartoszewska S, Stevenson L, Dai Q, Kappes J, Collawn JF, Bebok Z. A synonymous single nucleotide polymorphism in DeltaF508 CFTR alters the secondary structure of the mRNA and the expression of the mutant protein. J Biol Chem 2010;285:28741-28748.
48. Baek D, Villin J, Shin C, Camargo FD, Gygi SP, Bartel DP. The impact of microRNAs on protein output. Nature 2008;455:64-71.
49. Long D, Lee R, Williams P, Chan CY, Ambros V, Ding Y. Potent effect of target structure on microRNA function. Nat Struct Mol Biol 2007; 14:287-294.
50. Kertesz M, Iovino N, Unnerstall U, Gaul U, Segal E. The role of site accessibility in microRNA target recognition. Nat Genet 2007;39: 1278-1284.
51. Ott CJ, Blackledge NP, Leir SH, Harris A. Novel regulatory mechanisms for the CFTR gene. Biochem Soc Trans 2009;37:843-848.
52. Oglesby IK, Bray IM, Chotirmall SH, Stallings RL, O'Neill SJ, McElvaney NG, Greene CM. MiR-126 is downregulated in cystic fibrosis airway epithelial cells and regulates TOM1 expression. J Immunol 2010;184:1702-1709.
53. Granio O, Norez C, Ashbourne Excoffon KJ, Karp PH, Lusky M, Becq F, Boulanger P, Zabner J, Hong SS. Cellular localization and activity of Ad-delivered GFP-CFTR in airway epithelial and tracheal cells. Am J Respir Cell Mol Biol 2007;37:631-639.
54. Pezzulo AA, Tang XX, Hoegger MJ, Alaiwa MH, Ramachandran S, Moninger TO, Karp PH, Wohlford-Lenane CL, Haagsman HP, van Eijk M, et al. Reduced airway surface pH impairs bacterial killing in the porcine cystic fibrosis lung. Nature 2012;487:109-113.