XHigh-content siRNA screen reveals global ENaC regulators and potential cystic fibrosis therapy targets

Cell

Volumn 154, Issue 6, 2013, Pages 1390-

  Almaça, Joana ^a   Faria, Diana ^a,b   Sousa, Marisa ^a   Uliyakina, Inna ^a   Conrad, Christian ^c   Sirianant, Lalida ^b   Clarke, Luka A ^a   Martins, José Paulo ^d   Santos, Miguel ^d   Heriché, Jean Karim ^c   Huber, Wolfgang ^c   Schreiber, Rainer ^b   Pepperkok, Rainer ^c   Kunzelmann, Karl ^b   Amaral, Margarida D ^a  

^a UNIVERSITY OF LISBON   (Portugal)

^b UNIVERSITY OF REGENSBURG   (Germany)

^c EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^d ECBio RandD in Biotechnology SA   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

APROTININ; BUTYRIC ACID; CILIARY NEUROTROPHIC FACTOR RECEPTOR; DOXYCYCLINE; EPITHELIAL SODIUM CHANNEL; PHOSPHATIDYLINOSITOL; SMALL INTERFERING RNA;

APICAL MEMBRANE; ARTICLE; BIOINFORMATICS; CELL MEMBRANE; CONTROLLED STUDY; CYSTIC FIBROSIS; DRUG TARGETING; ENDOCYTOSIS; ENZYME INHIBITION; EPITHELIUM CELL; EX VIVO STUDY; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; SHORT CIRCUIT CURRENT; WATER ABSORPTION;

EID: 84884266668     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2013.08.045     Document Type: Article

References (65)

1. J. Almaça, S. Dahimène, N. Appel, C. Conrad, K. Kunzelmann, R. Pepperkok, and M.D. Amaral Functional genomics assays to study CFTR traffic and ENaC function Methods Mol. Biol. 742 2011 249 264
2. M. Althaus, W.G. Clauss, and M. Fronius Amiloride-sensitive sodium channels and pulmonary edema Pulm. Med. 2011 2011 830320
3. M.D. Amaral, and K. Kunzelmann Molecular targeting of CFTR as a therapeutic approach to cystic fibrosis Trends Pharmacol. Sci. 28 2007 334 341
4. Y. Berthiaume, and M.A. Matthay Alveolar edema fluid clearance and acute lung injury Respir. Physiol. Neurobiol. 159 2007 350 359
5. O. Bonny, and E. Hummler Dysfunction of epithelial sodium transport: from human to mouse Kidney Int. 57 2000 1313 1318
6. R.C. Boucher Cystic fibrosis: a disease of vulnerability to airway surface dehydration Trends Mol. Med. 13 2007 231 240
7. + permeability in cystic fibrosis human primary cell cultures J. Physiol. 405 1988 77 103
8. D.M. Bryant, and K.E. Mostov From cells to organs: building polarized tissue Nat. Rev. Mol. Cell Biol. 9 2008 887 901
9. M.B. Butterworth, R.S. Edinger, R.A. Frizzell, and J.P. Johnson Regulation of the epithelial sodium channel by membrane trafficking Am. J. Physiol. Renal Physiol. 296 2009 F10 F24
10. + channel is made of three homologous subunits Nature 367 1994 463 467
11. S. Carbon, A. Ireland, C.J. Mungall, S. Shu, B. Marshall, S. Lewis AmiGO Hub Web Presence Working Group AmiGO: online access to ontology and annotation data Bioinformatics 25 2009 288 289
12. J.H. Chen, D.A. Stoltz, P.H. Karp, S.E. Ernst, A.A. Pezzulo, T.O. Moninger, M.V. Rector, L.R. Reznikov, J.L. Launspach, and K. Chaloner Loss of anion transport without increased sodium absorption characterizes newborn porcine cystic fibrosis airway epithelia Cell 143 2010 911 923
13. N. Chung, X.D. Zhang, A. Kreamer, L. Locco, P.F. Kuan, S. Bartz, P.S. Linsley, M. Ferrer, and B. Strulovici Median absolute deviation to improve hit selection for genome-scale RNAi screens J. Biomol. Screen. 13 2008 149 158
14. L.A. Clarke, L. Sousa, C. Barreto, and M.D. Amaral Changes in transcriptome of native nasal epithelium expressing F508del-CFTR and intersecting data from comparable studies Respir. Res. 14 2013 38
15. L.A. Clunes, C.M. Davies, R.D. Coakley, A.A. Aleksandrov, A.G. Henderson, K.L. Zeman, E.N. Worthington, M. Gentzsch, S.M. Kreda, and D. Cholon Cigarette smoke exposure induces CFTR internalization and insolubility, leading to airway surface liquid dehydration FASEB J. 26 2012 533 545
16. +) channel cell surface expression EMBO J. 20 2001 7052 7059
17. S.H. Donaldson, and R.C. Boucher Sodium channels and cystic fibrosis Chest 132 2007 1631 1636
18. S.H. Donaldson, W.D. Bennett, K.L. Zeman, M.R. Knowles, R. Tarran, and R.C. Boucher Mucus clearance and lung function in cystic fibrosis with hypertonic saline N. Engl. J. Med. 354 2006 241 250
19. H. Erfle, B. Neumann, U. Liebel, P. Rogers, M. Held, T. Walter, J. Ellenberg, and R. Pepperkok Reverse transfection on cell arrays for high content screening microscopy Nat. Protoc. 2 2007 392 399
20. N. Filigheddu, S. Sampietro, F. Chianale, P.E. Porporato, M. Gaggianesi, I. Gregnanin, E. Rainero, M. Ferrara, B. Perego, and F. Riboni Diacylglycerol kinase α mediates 17-β-estradiol-induced proliferation, motility, and anchorage-independent growth of Hec-1A endometrial cancer cell line through the G protein-coupled estrogen receptor GPR30 Cell. Signal. 23 2011 1988 1996
21. + channel and airway surface liquid volume by serine proteases Pflugers Arch. 460 2010 1 17
22. M. Gálvez-Santisteban, A.E. Rodriguez-Fraticelli, D.M. Bryant, S. Vergarajauregui, T. Yasuda, I. Bañón-Rodríguez, I. Bernascone, A. Datta, N. Spivak, and K. Young Synaptotagmin-like proteins control the formation of a single apical membrane domain in epithelial cells Nat. Cell Biol. 14 2012 838 849
23. + channel J. Biol. Chem. 285 2010 32227 32232
24. A.J. Hirsh, B.F. Molino, J. Zhang, N. Astakhova, W.B. Geiss, B.J. Sargent, B.D. Swenson, A. Usyatinsky, M.J. Wyle, and R.C. Boucher Design, synthesis, and structure-activity relationships of novel 2-substituted pyrazinoylguanidine epithelial sodium channel blockers: drugs for cystic fibrosis and chronic bronchitis J. Med. Chem. 49 2006 4098 4115
25. N.J. Holden, C.O. Savage, S.P. Young, M.J. Wakelam, L. Harper, and J.M. Williams A dual role for diacylglycerol kinase generated phosphatidic acid in autoantibody-induced neutrophil exocytosis Mol. Med. 17 2011 1242 1252
26. W. Huang, B.T. Sherman, and R.A. Lempicki Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources Nat. Protoc. 4 2009 44 57
27. +) transport is associated with regulated ENaC and sgk1 expression Am. J. Physiol. Lung Cell. Mol. Physiol. 282 2002 L631 L641
28. H.L. Ji, X.F. Su, S. Kedar, J. Li, P. Barbry, P.R. Smith, S. Matalon, and D.J. Benos Delta-subunit confers novel biophysical features to alpha beta gamma-human epithelial sodium channel (ENaC) via a physical interaction J. Biol. Chem. 281 2006 8233 8241
29. T. Kimura, H. Kawabe, C. Jiang, W. Zhang, Y.Y. Xiang, C. Lu, M.W. Salter, N. Brose, W.Y. Lu, and D. Rotin Deletion of the ubiquitin ligase Nedd4L in lung epithelia causes cystic fibrosis-like disease Proc. Natl. Acad. Sci. USA 108 2011 3216 3221
30. M.R. Knowles, N.L. Church, W.E. Waltner, J.R. Yankaskas, P. Gilligan, M. King, L.J. Edwards, R.W. Helms, and R.C. Boucher A pilot study of aerosolized amiloride for the treatment of lung disease in cystic fibrosis N. Engl. J. Med. 322 1990 1189 1194
31. (Min/+) mice Oncogene 29 2010 1553 1560
32. K. Kunzelmann, and R. Schreiber Airway epithelial cells - hyperabsorption in CF? Int. J. Biochem. Cell Biol. 44 2012 1232 1235
33. + conductance in cystic fibrosis Pflugers Arch. 431 1995 1 9
34. 2 FASEB J. 19 2005 142 143
35. R.P. Lifton, A.G. Gharavi, and D.S. Geller Molecular mechanisms of human hypertension Cell 104 2001 545 556
36. M. Lu, J. Wang, K.T. Jones, H.E. Ives, M.E. Feldman, L.J. Yao, K.M. Shokat, K. Ashrafi, and D. Pearce mTOR complex-2 activates ENaC by phosphorylating SGK1 J. Am. Soc. Nephrol. 21 2010 811 818
37. + conductance is reduced by the cystic fibrosis transmembrane conductance regulator in normal but not in cystic fibrosis airways J. Clin. Invest. 102 1998 15 21
38. + absorption produces cystic fibrosis-like lung disease in mice Nat. Med. 10 2004 487 493
39. 2+ influx in platelets by R59949, an inhibitor of diacylglycerol kinase J. Pharm. Pharmacol. 64 2012 855 861
40. S. Moniz, M. Sousa, B. Moraes, A.I. Mendes, M. Palma, C. Barreto, J.I. Fragata, M.D. Amaral, and P. Matos HGF stimulation of Rac1 signaling enhances pharmacological correction of the most prevalent cystic fibrosis mutant F508del-CFTR ACS Chem. Biol. 8 2013 432 442
41. B. Neumann, T. Walter, J.K. Hériché, J. Bulkescher, H. Erfle, C. Conrad, P. Rogers, I. Poser, M. Held, and U. Liebel Phenotypic profiling of the human genome by time-lapse microscopy reveals cell division genes Nature 464 2010 721 727
42. H. O'Brodovich Epithelial ion transport in the fetal and perinatal lung Am. J. Physiol. 261 1991 C555 C564
43. V. Ogilvie, M. Passmore, L. Hyndman, L. Jones, B. Stevenson, A. Wilson, H. Davidson, R.R. Kitchen, R.D. Gray, and P. Shah Differential global gene expression in cystic fibrosis nasal and bronchial epithelium Genomics 98 2011 327 336
44. G. Otulakowski, W. Duan, S. Gandhi, and H. O'brodovich Steroid and oxygen effects on eIF4F complex, mTOR, and ENaC translation in fetal lung epithelia Am. J. Respir. Cell Mol. Biol. 37 2007 457 466
45. (Min/+) mice Pflugers Arch. 456 2008 847 855
46. + channel J. Gen. Physiol. 130 2007 399 413
47. O. Pochynyuk, V. Bugaj, and J.D. Stockand Physiologic regulation of the epithelial sodium channel by phosphatidylinositides Curr. Opin. Nephrol. Hypertens. 17 2008 533 540
48. J.R. Riordan CFTR function and prospects for therapy Annu. Rev. Biochem. 77 2008 701 726
49. J. Ritzerfeld, S. Remmele, T. Wang, K. Temmerman, B. Brügger, S. Wegehingel, S. Tournaviti, J.R. Strating, F.T. Wieland, and B. Neumann Phenotypic profiling of the human genome reveals gene products involved in plasma membrane targeting of SRC kinases Genome Res. 21 2011 1955 1968
50. A.J. Ross, L.A. Dailey, L.E. Brighton, and R.B. Devlin Transcriptional profiling of mucociliary differentiation in human airway epithelial cells Am. J. Respir. Cell Mol. Biol. 37 2007 169 185
51. D. Ruffieux-Daidié, O. Poirot, S. Boulkroun, F. Verrey, S. Kellenberger, and O. Staub Deubiquitylation regulates activation and proteolytic cleavage of ENaC J. Am. Soc. Nephrol. 19 2008 2170 2180
52. J.C. Simpson, B. Joggerst, V. Laketa, F. Verissimo, C. Cetin, H. Erfle, M.G. Bexiga, V.R. Singan, J.K. Hériché, and B. Neumann Genome-wide RNAi screening identifies human proteins with a regulatory function in the early secretory pathway Nat. Cell Biol. 14 2012 764 774
53. J.N. Snouwaert, K.K. Brigman, A.M. Latour, N.N. Malouf, R.C. Boucher, O. Smithies, and B.H. Koller An animal model for cystic fibrosis made by gene targeting Science 257 1992 1083 1088
54. + channel (ENaC) by ubiquitination EMBO J. 16 1997 6325 6336
55. + channel subunit proteins J. Biol. Chem. 275 2000 25760 25765
56. X. Wang, J. Venable, P. LaPointe, D.M. Hutt, A.V. Koulov, J. Coppinger, C. Gurkan, W. Kellner, J. Matteson, and H. Plutner Hsp90 cochaperone Aha1 downregulation rescues misfolding of CFTR in cystic fibrosis Cell 127 2006 803 815
57. K. Yokogami, S. Wakisaka, J. Avruch, and S.A. Reeves Serine phosphorylation and maximal activation of STAT3 during CNTF signaling is mediated by the rapamycin target mTOR Curr. Biol. 10 2000 47 50
58. 2) stimulates epithelial sodium channel activity in A6 cells J. Biol. Chem. 277 2002 11965 11969
59. F. Bard, L. Casano, A. Mallabiabarrena, E. Wallace, K. Saito, H. Kitayama, G. Guizzunti, Y. Hu, F. Wendler, and R. Dasgupta Functional genomics reveals genes involved in protein secretion and Golgi organization Nature 439 2006 604 607
60. S. Benabderrahmane, M. Smail-Tabbone, O. Poch, A. Napoli, and M.D. Devignes IntelliGO: a new vector-based semantic similarity measure including annotation origin BMC Bioinformatics 11 2010 588
61. J.G. Lees, J.K. Heriche, I. Morilla, J.A. Ranea, and C.A. Orengo Systematic computational prediction of protein interaction networks Phys. Biol. 8 2011 035008
62. J. Moffat, D.A. Grueneberg, X. Yang, S.Y. Kim, A.M. Kloepfer, G. Hinkle, B. Piqani, T.M. Eisenhaure, B. Luo, and J.K. Grenier A lentiviral RNAi library for human and mouse genes applied to an arrayed viral high-content screen Cell 124 2006 1283 1298
63. S.H. Randell, L. Walstad, U.E. Schwab, B.R. Grubb, and J.R. Yankaskas Isolation and culture of airway epithelial cells from chronically infected human lungs In Vitro Cell. Dev. Biol. Anim. 37 2001 480 489
64. S.H. Randell, M.L. Fulcher, W. O'Neal, and J.C. Olsen Primary epithelial cell models for cystic fibrosis research Methods Mol. Biol. 742 2011 285 310
65. +) dendritic cells Immunity 30 2009 544 555