Regulatory insertion removal restores maturation, stability and function of ΔF508 CFTR

Journal of Molecular Biology

Volumn 401, Issue 2, 2010, Pages 194-210

  Aleksandrov, Andrei A ^a,b   Kota, Pradeep ^b,c   Aleksandrov, Luba A ^b   He, Lihua ^b   Jensen, Tim ^b   Cui, Liying ^b   Gentzsch, Martina ^b,c   Dokholyan, Nikolay V ^b,c   Riordan, John R ^b  

^a NORTH CAROLINA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

ABC transporters; CFTR; Cystic fibrosis; DMD simulations; Ion channel

Indexed keywords

ADENOSINE TRIPHOSPHATE; CHLORIDE CHANNEL; NUCLEOTIDE BINDING PROTEIN; TRANSMEMBRANE CONDUCTANCE REGULATOR;

ANIMAL CELL; ANION TRANSPORT; ARTICLE; CELL SURFACE; CHANNEL GATING; CONTROLLED STUDY; GENE DELETION; GENE INSERTION; HUMAN; HUMAN CELL; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN TRANSPORT; WILD TYPE;

EID: 77955086020     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2010.06.019     Document Type: Article

References (54)

1. Aleksandrov A.A., Aleksandrov L.A., Riordan J.R. CFTR (ABCC7) is a hydrolyzable-ligand-gated channel. Pflugers Arch. 2007, 453:693-702.
2. Wang W., Wu J., Bernard K., Li G., Wang G., Bevensee M.O., Kirk K.L. ATP-independent CFTR channel gating and allosteric modulation by phosphorylation. Proc. Natl Acad. Sci. USA 2010, 107:3888-3893.
3. Riordan J.R. CFTR function and prospects for therapy. Annu. Rev. Biochem. 2008, 77:701-726.
4. Denning G.M., Anderson M.P., Amara J.F., Marshall J., Smith A.E., Welsh M.J. Processing of mutant cystic fibrosis transmembrane conductance regulator is temperature-sensitive. Nature 1992, 358:761-764.
5. Howard M., Fischer H., Roux J., Santos B.C., Gullans S.R., Yancey P.H., Welch W.J. Mammalian osmolytes and S-nitrosoglutathione promote Delta F508 cystic fibrosis transmembrane conductance regulator (CFTR) protein maturation and function. J. Biol. Chem. 2003, 278:35159-35167.
6. Wang X., Koulov A.V., Kellner W.A., Riordan J.R., Balch W.E. Chemical and biological folding contribute to temperature-sensitive DeltaF508 CFTR trafficking. Traffic 2008, 9:1878-1893.
7. Pedemonte N., Lukacs G.L., Du K., Caci E., Zegarra-Moran O., Galietta L.J., Verkman A.S. Small-molecule correctors of defective DeltaF508-CFTR cellular processing identified by high-throughput screening. J. Clin. Invest. 2005, 115:2564-2571.
8. Pissarra L.S., Farinha C.M., Xu Z., Schmidt A., Thibodeau P.H., Cai Z., et al. Solubilizing mutations used to crystallize one CFTR domain attenuate the trafficking and channel defects caused by the major cystic fibrosis mutation. Chem. Biol. 2008, 15:62-69.
9. Teem J.L., Berger H.A., Ostedgaard L.S., Rich D.P., Tsui L.C., Welsh M.J. Identification of revertants for the cystic fibrosis ΔF508 mutation using STE6-CFTR chimeras in yeast. Cell 1993, 73:335-346.
10. DeCarvalho A.C., Gansheroff L.J., Teem J.L. Mutations in the nucleotide binding domain 1 signature motif region rescue processing and functional defects of cystic fibrosis transmembrane conductance regulator Delta F508. J. Biol. Chem. 2002, 277:35896-35905.
11. Serohijos A.W., Hegedus T., Aleksandrov A.A., He L., Cui L., Dokholyan N.V., Riordan J.R. Phenylalanine-508 mediates a cytoplasmic-membrane domain contact in the CFTR 3D structure crucial to assembly and channel function. Proc. Natl Acad. Sci. USA 2008, 105:3256-3261.
12. Lewis H.A., Zhao X., Wang C., Sauder J.M., Rooney I., Noland B.W., et al. Impact of the DeltaF508 mutation in first nucleotide-binding domain of human cystic fibrosis transmembrane conductance regulator on domain folding and structure. J. Biol. Chem. 2005, 280:1346-1353.
13. Qu B.H., Strickland E.H., Thomas P.J. Localization and suppression of a kinetic defect in cystic fibrosis transmembrane conductance regulator folding. J. Biol. Chem. 1997, 272:15739-15744.
14. Serohijos A.W., Hegedus T., Riordan J.R., Dokholyan N.V. Diminished self-chaperoning activity of the DeltaF508 mutant of CFTR results in protein misfolding. PLoS Comput. Biol. 2008, 4:e1000008.
15. Lewis H.A., Buchanan S.G., Burley S.K., Conners K., Dickey M., Dorwart M., et al. Structure of nucleotide-binding domain 1 of the cystic fibrosis transmembrane conductance regulator. EMBO J. 2004, 23:282-293.
16. Csanady L., Chan K.W., Nairn A.C., Gadsby D.C. Functional roles of nonconserved structural segments in CFTR's NH2-terminal nucleotide binding domain. J. Gen. Physiol. 2005, 125:43-55.
17. Atwell S., Brouillette C.G., Conners K., Emtage S., Gheyi T., Guggino W., et al. Structures of a minimal human CFTR first nucleotide-binding domain as a monomer, head-to-tail homodimer, and pathogenic mutant. Protein Eng. Des. Sel. 2010, 23:375-384.
18. Yang H., Shelat A.A., Guy R.K., Gopinath V.S., Ma T., Du K., et al. Nanomolar affinity small molecule correctors of defective Delta F508-CFTR chloride channel gating. J. Biol. Chem. 2003, 278:35079-35085.
19. Sharma M., Pampinella F., Nemes C., Benharouga M., So J., Du K., et al. Misfolding diverts CFTR from recycling to degradation: quality control at early endosomes. J. Cell. Biol. 2004, 164:923-933.
20. Glozman R., Okiyoneda T., Mulvihill C.M., Rini J.M., Barriere H., Lukacs G.L. N-Glycans are direct determinants of CFTR folding and stability in secretory and endocytic membrane traffic. J. Cell. Biol. 2009, 184:847-862.
21. Du K., Sharma M., Lukacs G.L. The DeltaF508 cystic fibrosis mutation impairs domain-domain interactions and arrests post-translational folding of CFTR. Nat. Struct. Mol. Biol. 2005, 12:17-25.
22. Aleksandrov L., Aleksandrov A.A., Chang X.B., Riordan J.R. The first nucleotide binding domain of cystic fibrosis transmembrane conductance regulator is a site of stable nucleotide interaction, whereas the second is a site of rapid turnover. J. Biol. Chem. 2002, 277:15419-15425.
23. 2-terminal nucleotide binding domain and its role in channel gating. J. Gen. Physiol. 2003, 122:333-348.
24. Cui L., Aleksandrov L., Hou Y.X., Gentzsch M., Chen J.H., Riordan J.R., Aleksandrov A.A. The role of cystic fibrosis transmembrane conductance regulator phenylalanine 508 side chain in ion channel gating. J. Physiol. 2006, 572:347-358.
25. 2+-dependent ATP occlusion at the first nucleotide-binding domain (NBD1) of CFTR does not require the second (NBD2). Biochem. J. 2008, 416:129-136.
26. He L., Aleksandrov A.A., Serohijos A.W., Hegedus T., Aleksandrov L.A., Cui L., et al. Multiple membrane-cytoplasmic domain contacts in the cystic fibrosis transmembrane conductance regulator (CFTR) mediate regulation of channel gating. J. Biol. Chem. 2008, 283:26383-26390.
27. Dalemans W., Barbry P., Champigny G., Jallat S., Dott K., Dreyer D., et al. Altered chloride-ion channel kinetics associated with the Delta-F508 cystic-fibrosis mutation. Nature 1991, 354:526-528.
28. Haws C.M., Nepomuceno I.B., Krouse M.E., Wakelee H., Law T., Xia Y., et al. DeltaF508-CFTR channels: kinetics, activation by forskolin, and potentiation by xanthines. Am. J. Physiol. 1996, 270:C1544-C1555.
29. Schultz B.D., Frizzell R.A., Bridges R.J. Rescue of dysfunctional DeltaF508-CFTR chloride channel activity by IBMX. J. Membr. Biol. 1999, 170:51-66.
30. Wang F., Zeltwanger S., Hu S., Hwang T.C. Deletion of phenylalanine 508 causes attenuated phosphorylation-dependent activation of CFTR chloride channels. J. Physiol. 2000, 524(Pt 3):637-648.
31. Hegedus T., Aleksandrov A., Cui L., Gentzsch M., Chang X.B., Riordan J.R. F508del CFTR with two altered RXR motifs escapes from ER quality control but its channel activity is thermally sensitive. Biochim. Biophys. Acta 2006, 1758:565-572.
32. Jurkuvenaite A., Chen L., Bartoszewski R., Goldstein R., Bebok Z., Matalon S., Collawn J.F. Functional stability of rescued Delta F508 cystic fibrosis transmembrane conductance regulator in airway epithelial cells. Am. J. Respir. Cell Mol. Biol. 2010, 42:363-372.
33. Van Goor F., Straley K.S., Cao D., Gonzalez J., Hadida S., Hazlewood A., et al. Rescue of DeltaF508-CFTR trafficking and gating in human cystic fibrosis airway primary cultures by small molecules. Am. J. Physiol. Lung Cell Mol. Physiol. 2006, 290:L1117-1130.
34. Dokholyan N.V., Buldyrev S.V., Stanley H.E., Shakhnovich E.I. Discrete molecular dynamics studies of the folding of a protein-like model. Fold. Des. 1998, 3:577-587.
35. Ding F., Dokholyan N.V. Emergence of protein fold families through rational design. PLoS Comput. Biol. 2006, e85:2.
36. Kanelis V., Hudson R.P., Thibodeau P.H., Thomas P.J., Forman-Kay J.D. NMR evidence for differential phosphorylation-dependent interactions in WT and DeltaF508 CFTR. EMBO J. 2010, 29:263-277.
37. Lewis H.A., Wang C., Zhao X., Hamuro Y., Conners K., Kearins M.C., et al. Structure and dynamics of NBD1 from CFTR characterized using crystallography and hydrogen/deuterium exchange mass spectrometry. J. Mol. Biol. 2010, 396:406-430.
38. Schmitt L., Benabdelhak H., Blight M.A., Holland I.B., Stubbs M.T. Crystal structure of the nucleotide-binding domain of the ABC-transporter haemolysin B: identification of a variable region within ABC helical domains. J. Mol. Biol. 2003, 330:333-342.
39. Ward C.L., Omura S., Kopito R.R. Degradation of CFTR by the ubiquitin-proteasome pathway. Cell 1995, 83:121-127.
40. Jensen T.J., Loo M.A., Pind S., Williams D.B., Goldberg A.L., Riordan J.R. Multiple proteolytic systems, including the proteasome, contribute to CFTR processing. Cell 1995, 83:129-135.
41. Grove D.E., Rosser M.F., Ren H.Y., Naren A.P., Cyr D.M. Mechanisms for rescue of correctable folding defects in CFTRDelta F508. Mol. Biol. Cell 2009, 20:4059-4069.
42. Wang X., Venable J., LaPointe P., Hutt D.M., Koulov A.V., Coppinger J., et al. Hsp90 cochaperone Aha1 downregulation rescues misfolding of CFTR in cystic fibrosis. Cell 2006, 127:803-815.
43. Wang Y., Loo T.W., Bartlett M.C., Clarke D.M. Correctors promote maturation of cystic fibrosis transmembrane conductance regulator (CFTR)-processing mutants by binding to the protein. J. Biol. Chem. 2007, 282:33247-33251.
44. Mornon J.P., Lehn P., Callebaut I. Molecular models of the open and closed states of the whole human CFTR protein. Cell. Mol. Life Sci. 2009, 66:3469-3486.
45. Wang Y., Loo T.W., Bartlett M.C., Clarke D.M. Additive effect of multiple pharmacological chaperones on maturation of CFTR processing mutants. Biochem. J. 2007, 406:257-263.
46. Loo T.W., Bartlett M.C., Clarke D.M. Introduction of the most common cystic fibrosis mutation (Delta F508) into human P-glycoprotein disrupts packing of the transmembrane segments. J. Biol. Chem. 2002, 277:27585-27588.
47. Buyse F., Vandenbranden M., Ruysschaert J.M. Mistargeted MRPDeltaF728 mutant is rescued by intracellular GSH. FEBS Lett. 2004, 578:145-151.
48. Cui L., Aleksandrov L., Chang X.B., Hou Y.X., He L., Hegedus T., et al. Domain interdependence in the biosynthetic assembly of CFTR. J. Mol. Biol. 2007, 365:981-994.
49. Chang X.B., Tabcharani J.A., Hou Y.X., Jensen T.J., Kartner N., Alon N., et al. Protein kinase A (PKA) still activates CFTR chloride channel after mutagenesis of all ten PKA consensus phosphorylation sites. J. Biol. Chem. 1993, 268:11304-11311.
50. Loo M.A., Jensen T.J., Cui L., Hou Y., Chang X.B., Riordan J.R. Perturbation of Hsp90 interaction with nascent CFTR prevents its maturation and accelerates its degradation by the proteasome. EMBO J. 1998, 17:6879-6887.
51. Aleksandrov L., Mengos A., Chang X., Aleksandrov A., Riordan J.R. Differential interactions of nucleotides at the two nucleotide binding domains of the cystic fibrosis transmembrane conductance regulator. J. Biol. Chem. 2001, 276:12918-12923.
52. Aleksandrov A.A., Cui L., Riordan J.R. Relationship between nucleotide binding and ion channel gating in cystic fibrosis transmembrane conductance regulator. J. Physiol. 2009, 587:2875-2886.
53. Sharma S., Ding F., Dokholyan N.V. Multiscale modeling of nucleosome dynamics. Biophys. J. 2007, 92:1457-1470.
54. Teotico D.G., Frazier M.L., Ding F., Dokholyan N.V., Temple B.R., Redinbo M.R. Active nuclear receptors exhibit highly correlated AF-2 domain motions. PLoS Comput. Biol. 2008, 4:e1000111.