Identification of a NBD1-binding pharmacological chaperone that corrects the trafficking defect of F508del-CFTR

Chemistry and Biology

Volumn 18, Issue 2, 2011, Pages 231-242

  Sampson, Heidi M ^a   Robert, Renaud ^a   Liao, Jie ^a   Matthes, Elizabeth ^a   Carlile, Graeme W ^a   Hanrahan, John W ^a   Thomas, David Y ^a  

^a MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

HYDRAZONE DERIVATIVE; NUCLEOTIDE; PHENYLALANINE; PHENYLHYDRAZONE; TRANSMEMBRANE CONDUCTANCE REGULATOR;

ANIMAL; ARTICLE; CELL LINE; CHEMISTRY; CYSTIC FIBROSIS; CYTOLOGY; DRUG EFFECT; DRUG SCREENING; GENE DELETION; GENETICS; HUMAN; METABOLISM; MOUSE; PROTEIN BINDING; PROTEIN STABILITY; PROTEIN TERTIARY STRUCTURE; PROTEIN TRANSPORT; RESPIRATORY TRACT MUCOSA; TEMPERATURE;

ANIMALS; CELL LINE; CYSTIC FIBROSIS; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; DRUG EVALUATION, PRECLINICAL; HUMANS; HYDRAZONES; MICE; NUCLEOTIDES; PHENYLALANINE; PROTEIN BINDING; PROTEIN STABILITY; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; RESPIRATORY MUCOSA; SEQUENCE DELETION; TEMPERATURE;

EID: 79951829938     PISSN: 10745521     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.chembiol.2010.11.016     Document Type: Article

References (56)

1. T. Ai, S.G. Bompadre, X. Wang, S. Hu, M. Li, and T.C. Hwang Capsaicin potentiates wild-type and mutant cystic fibrosis transmembrane conductance regulator chloride-channel currents Mol. Pharmacol. 65 2004 1415 1426 (Pubitemid 38668300)
2. A. Bachmann, U. Russ, S. Waldegger, and U. Quast Potent stimulation and inhibition of the CFTR Cl(-) current by phloxine B Br. J. Pharmacol. 131 2000 433 440
3. W.E. Balch, R.I. Morimoto, A. Dillin, and J.W. Kelly Adapting proteostasis for disease intervention Science 319 2008 916 919 (Pubitemid 351263754)
4. F. Becq, Y. Mettey, M.A. Gray, L.J. Galietta, R.L. Dormer, M. Merten, T. Metaye, V. Chappe, C. Marvingt-Mounir, and O. Zegarra-Moran Development of substituted Benzo[c]quinolizinium compounds as novel activators of the cystic fibrosis chloride channel J. Biol. Chem. 274 1999 27415 27425
5. J.A. Best, and P.M. Quinton Salivary secretion assay for drug efficacy for cystic fibrosis in mice Exp. Physiol. 90 2005 189 193 (Pubitemid 40364797)
6. C.R. Brown, L.Q. Hong-Brown, J. Biwersi, A.S. Verkman, and W.J. Welch Chemical chaperones correct the mutant phenotype of the delta F508 cystic fibrosis transmembrane conductance regulator protein Cell Stress Chaperones 1 1996 117 125 (Pubitemid 126670773)
7. Z. Cai, and D.N. Sheppard Phloxine B interacts with the cystic fibrosis transmembrane conductance regulator at multiple sites to modulate channel activity J. Biol. Chem. 277 2002 19546 19553 (Pubitemid 34967467)
8. Z. Cai, A. Taddei, and D.N. Sheppard Differential sensitivity of the cystic fibrosis (CF)-associated mutants G551D and G1349D to potentiators of the cystic fibrosis transmembrane conductance regulator (CFTR) Cl- channel J. Biol. Chem. 281 2006 1970 1977 (Pubitemid 43845783)
9. G.W. Carlile, R. Robert, D. Zhang, K.A. Teske, Y. Luo, J.W. Hanrahan, and D.Y. Thomas Correctors of protein trafficking defects identified by a novel high-throughput screening assay ChemBioChem 8 2007 1012 1020 (Pubitemid 47189285)
10. W. Dalemans, P. Barbry, G. Champigny, S. Jallat, K. Dott, D. Dreyer, R.G. Crystal, A. Pavirani, J.P. Lecocq, and M. Lazdunski Altered chloride ion channel kinetics associated with the delta F508 cystic fibrosis mutation Nature 354 1991 526 528 (Pubitemid 21896832)
11. G.M. Denning, M.P. Anderson, J.F. Amara, J. Marshall, A.E. Smith, and M.J. Welsh Processing of mutant cystic fibrosis transmembrane conductance regulator is temperature-sensitive Nature 358 1992 761 764
12. R.L. Dormer, R. Derand, C.M. McNeilly, Y. Mettey, L. Bulteau-Pignoux, T. Metaye, J.M. Vierfond, M.A. Gray, L.J. Galietta, and M.R. Morris Correction of delF508-CFTR activity with benzo(c)quinolizinium compounds through facilitation of its processing in cystic fibrosis airway cells J. Cell Sci. 114 2001 4073 4081 (Pubitemid 33115028)
13. R.L. Dormer, C.M. Harris, Z. Clark, M.M. Pereira, I.J. Doull, C. Norez, F. Becq, and M.A. McPherson Sildenafil (Viagra) corrects DeltaF508-CFTR location in nasal epithelial cells from patients with cystic fibrosis Thorax 60 2005 55 59 (Pubitemid 40101019)
14. J.Q. Fan, S. Ishii, N. Asano, and Y. Suzuki Accelerated transport and maturation of lysosomal alpha-galactosidase A in Fabry lymphoblasts by an enzyme inhibitor Nat. Med. 5 1999 112 115 (Pubitemid 29051008)
15. P.J. French, J.H. van Doorninck, R.H. Peters, E. Verbeek, N.A. Ameen, C.R. Marino, H.R. de Jonge, J. Bijman, and B.J. Scholte A delta F508 mutation in mouse cystic fibrosis transmembrane conductance regulator results in a temperature-sensitive processing defect in vivo J. Clin. Invest. 98 1996 1304 1312 (Pubitemid 26322055)
16. P.J. French, J. Bijman, A.G. Bot, W.E. Boomaars, B.J. Scholte, and H.R. de Jonge Genistein activates CFTR Cl- channels via a tyrosine kinase- and protein phosphatase-independent mechanism Am. J. Physiol. 273 1997 C747 C753
17. L.J. Galietta, M.F. Springsteel, M. Eda, E.J. Niedzinski, K. By, M.J. Haddadin, M.J. Kurth, M.H. Nantz, and A.S. Verkman Novel CFTR chloride channel activators identified by screening of combinatorial libraries based on flavone and benzoquinolizinium lead compounds J. Biol. Chem. 276 2001 19723 19728
18. D.M. Hutt, D. Herman, A.P. Rodrigues, S. Noel, J.M. Pilewski, J. Matteson, B. Hoch, W. Kellner, J.W. Kelly, and A. Schmidt Reduced histone deacetylase 7 activity restores function to misfolded CFTR in cystic fibrosis Nat. Chem. Biol. 6 2010 25 33
19. T.C. Hwang, F. Wang, I.C. Yang, and W.W. Reenstra Genistein potentiates wild-type and delta F508-CFTR channel activity Am. J. Physiol. 273 1997 C988 C998 (Pubitemid 27422179)
20. A. Jurkuvenaite, L. Chen, R. Bartoszewski, R. Goldstein, Z. Bebok, S. Matalon, and J.F. Collawn Functional stability of rescued {delta}f508 cystic fibrosis transmembrane conductance regulator in airway epithelial cells Am. J. Respir. Cell Mol. Biol. 42 2010 363 372
21. P. Kim Chiaw, L. Wellhauser, L.J. Huan, M. Ramjeesingh, and C. Bear A chemical corrector modifies the channel function of F508del-CFTR Mol. Pharmacol. 78 2010 411 418
22. H.A. Lewis, S.G. Buchanan, S.K. Burley, K. Conners, M. Dickey, M. Dorwart, R. Fowler, X. Gao, W.B. Guggino, and W.A. Hendrickson Structure of nucleotide-binding domain 1 of the cystic fibrosis transmembrane conductance regulator EMBO J. 23 2004 282 293 (Pubitemid 38294493)
23. G.L. Lukacs, X.B. Chang, C. Bear, N. Kartner, A. Mohamed, J.R. Riordan, and S. Grinstein The delta F508 mutation decreases the stability of cystic fibrosis transmembrane conductance regulator in the plasma membrane. Determination of functional half-lives on transfected cells J. Biol. Chem. 268 1993 21592 21598 (Pubitemid 23320650)
24. E.F. McKone, S.S. Emerson, K.L. Edwards, and M.L. Aitken Effect of genotype on phenotype and mortality in cystic fibrosis: a retrospective cohort study Lancet 361 2003 1671 1676 (Pubitemid 36577438)
25. O. Moran, L.J. Galietta, and O. Zegarra-Moran Binding site of activators of the cystic fibrosis transmembrane conductance regulator in the nucleotide binding domains Cell. Mol. Life Sci. 62 2005 446 460 (Pubitemid 40379235)
26. J.P. Morello, A. Salahpour, A. Laperriere, V. Bernier, M.F. Arthus, M. Lonergan, U. Petaja-Repo, S. Angers, D. Morin, and D.G. Bichet Pharmacological chaperones rescue cell-surface expression and function of misfolded V2 vasopressin receptor mutants J. Clin. Invest. 105 2000 887 895 (Pubitemid 30203061)
27. J.P. Mornon, P. Lehn, and I. Callebaut Atomic model of human cystic fibrosis transmembrane conductance regulator: membrane-spanning domains and coupling interfaces Cell. Mol. Life Sci. 65 2008 2594 2612
28. F.H. Niesen, H. Berglund, and M. Vedadi The use of differential scanning fluorimetry to detect ligand interactions that promote protein stability Nat. Protoc. 2 2007 2212 2221 (Pubitemid 351565860)
29. C. Norez, S. Noel, M. Wilke, M. Bijvelds, H. Jorna, P. Melin, H. DeJonge, and F. Becq Rescue of functional delF508-CFTR channels in cystic fibrosis epithelial cells by the alpha-glucosidase inhibitor miglustat FEBS Lett. 580 2006 2081 2086
30. C. Norez, F. Bilan, A. Kitzis, Y. Mettey, and F. Becq Proteasome-dependent pharmacological rescue of cystic fibrosis transmembrane conductance regulator revealed by mutation of glycine 622 J. Pharmacol. Exp. Ther. 325 2008 89 99 (Pubitemid 351439157)
31. N. Pedemonte, G.L. Lukacs, K. Du, E. Caci, O. Zegarra-Moran, L.J. Galietta, and A.S. Verkman Small-molecule correctors of defective DeltaF508-CFTR cellular processing identified by high-throughput screening J. Clin. Invest. 115 2005 2564 2571 (Pubitemid 41266219)
32. N. Pedemonte, V. Tomati, E. Sondo, and L.J. Galietta Influence of cell background on pharmacological rescue of mutant Cftr Am. J. Physiol. Cell Physiol. 298 2010 C866 C874
33. B.H. Qu, E.H. Strickland, and P.J. Thomas Localization and suppression of a kinetic defect in cystic fibrosis transmembrane conductance regulator folding J. Biol. Chem. 272 1997 15739 15744 (Pubitemid 27265548)
34. J.R. Riordan, J.M. Rommens, B. Kerem, N. Alon, R. Rozmahel, Z. Grzelczak, J. Zielenski, S. Lok, N. Plavsic, and J.L. Chou Identification of the cystic fibrosis gene: cloning and characterization of complementary DNA Science 245 1989 1066 1073 (Pubitemid 19231814)
35. R. Robert, G.W. Carlile, C. Pavel, N. Liu, S.M. Anjos, J. Liao, Y. Luo, D. Zhang, D.Y. Thomas, and J.W. Hanrahan Structural analog of sildenafil identified as a novel corrector of the F508del-CFTR trafficking defect Mol. Pharmacol. 73 2008 478 489 (Pubitemid 351159218)
36. R. Robert, G.C. Carlile, J. Liao, H. Balghi, P. Lesimple, N. Liu, B. Kus, D. Rotin, M. Wilke, and H.R. de Jonge Correction of the Delta phe508 cystic fibrosis transmembrane conductance regulator trafficking defect by the bioavailable compound glafenine Mol. Pharmacol. 77 2010 922 930
37. R.C. Rubenstein, M.E. Egan, and P.L. Zeitlin In vitro pharmacologic restoration of CFTR-mediated chloride transport with sodium 4-phenylbutyrate in cystic fibrosis epithelial cells containing delta F508-CFTR J. Clin. Invest. 100 1997 2457 2465 (Pubitemid 27514885)
38. A.R. Sawkar, W.C. Cheng, E. Beutler, C.H. Wong, W.E. Balch, and J.W. Kelly Chemical chaperones increase the cellular activity of N370S beta -glucosidase: a therapeutic strategy for Gaucher disease Proc. Natl. Acad. Sci. USA 99 2002 15428 15433 (Pubitemid 35403951)
39. A.W. Serohijos, T. Hegedus, A.A. Aleksandrov, L. He, L. Cui, N.V. Dokholyan, and J.R. Riordan Phenylalanine-508 mediates a cytoplasmic-membrane domain contact in the CFTR 3D structure crucial to assembly and channel function Proc. Natl. Acad. Sci. USA 105 2008 3256 3261 (Pubitemid 351723540)
40. D.N. Sheppard, and M.J. Welsh Structure and function of the CFTR chloride channel Physiol. Rev. 79 1999 S23 S45 (Pubitemid 29058908)
41. F.L. Stratford, M.M. Pereira, F. Becq, M.A. McPherson, and R.L. Dormer Benzo(c)quinolizinium drugs inhibit degradation of Delta F508-CFTR cytoplasmic domain Biochem. Biophys. Res. Commun. 300 2003 524 530 (Pubitemid 38375840)
42. M.B. Tropak, S.P. Reid, M. Guiral, S.G. Withers, and D. Mahuran Pharmacological enhancement of beta-hexosaminidase activity in fibroblasts from adult Tay-Sachs and Sandhoff Patients J. Biol. Chem. 279 2004 13478 13487 (Pubitemid 38468872)
43. J.H. van Doorninck, P.J. French, E. Verbeek, R.H. Peters, H. Morreau, J. Bijman, and B.J. Scholte A mouse model for the cystic fibrosis delta F508 mutation EMBO J. 14 1995 4403 4411
44. F. Van Goor, K.S. Straley, D. Cao, J. Gonzalez, S. Hadida, A. Hazlewood, J. Joubran, T. Knapp, L.R. Makings, and M. Miller Rescue of DeltaF508-CFTR trafficking and gating in human cystic fibrosis airway primary cultures by small molecules Am. J. Physiol. Lung Cell. Mol. Physiol. 290 2006 L1117 L1130 (Pubitemid 43830856)
45. M. Vedadi, F.H. Niesen, A. Allali-Hassani, O.Y. Fedorov, P.J. Finerty Jr., G.A. Wasney, R. Yeung, C. Arrowsmith, L.J. Ball, and H. Berglund Chemical screening methods to identify ligands that promote protein stability, protein crystallization, and structure determination Proc. Natl. Acad. Sci. USA 103 2006 15835 15840 (Pubitemid 44657553)
46. P. Vergani, S.W. Lockless, A.C. Nairn, and D.C. Gadsby CFTR channel opening by ATP-driven tight dimerization of its nucleotide-binding domains Nature 433 2005 876 880 (Pubitemid 40314897)
47. 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 (Pubitemid 44716255)
48. Y. Wang, M.C. Bartlett, T.W. Loo, and D.M. Clarke Specific rescue of cystic fibrosis transmembrane conductance regulator processing mutants using pharmacological chaperones Mol. Pharmacol. 70 2006 297 302
49. Y. Wang, T.W. Loo, M.C. Bartlett, and D.M. Clarke Additive effect of multiple pharmacological chaperones on maturation of CFTR processing mutants Biochem. J. 406 2007 257 263 (Pubitemid 47310956)
50. Y. Wang, T.W. Loo, M.C. Bartlett, and D.M. Clarke Correctors promote maturation of cystic fibrosis transmembrane conductance regulator (CFTR)-processing mutants by binding to the protein J. Biol. Chem. 282 2007 33247 33251 (Pubitemid 350159496)
51. Y. Wang, T.W. Loo, M.C. Bartlett, and D.M. Clarke Modulating the folding of P-glycoprotein and cystic fibrosis transmembrane conductance regulator truncation mutants with pharmacological chaperones Mol. Pharmacol. 71 2007 751 758 (Pubitemid 46294086)
52. L. Wellhauser, P. Kim Chiaw, S. Pasyk, C. Li, M. Ramjeesingh, and C.E. Bear A small-molecule modulator interacts directly with deltaPhe508-CFTR to modify its ATPase activity and conformational stability Mol. Pharmacol. 75 2009 1430 1438
53. M.J. Welsh, G.M. Denning, L.S. Ostedgaard, and M.P. Anderson Dysfunction of CFTR bearing the delta F508 mutation J. Cell Sci. Suppl. 17 1993 235 239 (Pubitemid 24041304)
54. M. Wilke, R. Buijs-Offerman, J. Aarbiou, W.H. Colledge, D.N. Sheppard, L. Touqui, A. Bot, H. Jorna, H.R. De Jonge, and B.J. Scholte Mouse models of cystic fibrosis: phenotypic analysis and research applications J. Cyst. Fibros. 2010 in press
55. O. Zegarra-Moran, M. Monteverde, L.J. Galietta, and O. Moran Functional analysis of mutations in the putative binding site for cystic fibrosis transmembrane conductance regulator potentiators. Interaction between activation and inhibition J. Biol. Chem. 282 2007 9098 9104 (Pubitemid 47093516)
56. L. Zhang, B. Button, S.E. Gabriel, S. Burkett, Y. Yan, M.H. Skiadopoulos, Y.L. Dang, L.N. Vogel, T. McKay, and A. Mengos CFTR delivery to 25% of surface epithelial cells restores normal rates of mucus transport to human cystic fibrosis airway epithelium PLoS Biol. 7 2009 e1000155