Functional Rescue of DeltaF508-CFTR by Peptides Designed to Mimic Sorting Motifs

Chemistry and Biology

Volumn 16, Issue 5, 2009, Pages 520-530

  Chiaw, Patrick Kim ^a,b   Huan, Ling Jun ^a   Gagnon, Stephane ^a   Ly, Diane ^a   Sweezey, Neil ^a,b   Rotin, Daniela ^a,b   Deber, Charles M ^a,b   Bear, Christine E ^a,b  

^a HOSPITAL FOR SICK CHILDREN RESEARCH INSTITUTE   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

CELLBIO; CHEMBIO

Indexed keywords

MUTANT PROTEIN; PEPTIDE; TRANSMEMBRANE CONDUCTANCE REGULATOR;

AMINO ACID SEQUENCE; ARTICLE; CELL LINE; GENETICS; HUMAN; METABOLISM; PROTEIN MOTIF; RESPIRATORY TRACT MUCOSA; SYNTHESIS;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; CELL LINE; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; HUMANS; MUTANT PROTEINS; PEPTIDES; RESPIRATORY MUCOSA;

EID: 65749107939     PISSN: 10745521     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.chembiol.2009.04.005     Document Type: Article

References (56)

1. Amaral M.D. Processing of CFTR: traversing the cellular maze-how much CFTR needs to go through to avoid cystic fibrosis?. Pediatr. Pulmonol. 39 (2005) 479-491
2. Bates E., Bode C., Costa M., Gibson C.M., Granger C., Green C., Grimes K., Harrington R., Huber K., Kleiman N., et al. Intracoronary KAI-9803 as an adjunct to primary percutaneous coronary intervention for acute ST-segment elevation myocardial infarction. Circulation 117 (2008) 886-896
3. Chang X.B., Cui L., Hou Y.X., Jensen T.J., Aleksandrov A.A., Mengos A., and Riordan J.R. Removal of multiple arginine-framed trafficking signals overcomes misprocessing of delta F508 CFTR present in most patients with cystic fibrosis. Mol. Cell 4 (1999) 137-142
4. Cheung J.C., Kim Chiaw P., Pasyk S., and Bear C.E. Molecular basis for the ATPase activity of CFTR. Arch. Biochem. Biophys. 476 (2008) 95-100
5. Clarke L.L., Gawenis L.R., Hwang T.C., Walker N.M., Gruis D.B., and Price E.M. A domain mimic increases DeltaF508 CFTR trafficking and restores cAMP-stimulated anion secretion in cystic fibrosis epithelia. Am. J. Physiol. Cell Physiol. 287 (2004) C192-C199
6. Denning G.M., Anderson M.P., Amara J.F., Marshall J., Smith A.E., and Welsh M.J. Processing of mutant cystic fibrosis transmembrane conductance regulator is temperature-sensitive. Nature 358 (1992) 761-764
7. Du K., Sharma M., and Lukacs G.L. The DeltaF508 cystic fibrosis mutation impairs domain-domain interactions and arrests post-translational folding of CFTR. Nat. Struct. Mol. Biol. 12 (2005) 17-25
8. Duchardt F., Fotin-Mleczek M., Schwarz H., Fischer R., and Brock R. A comprehensive model for the cellular uptake of cationic cell-penetrating peptides. Traffic 8 (2007) 848-866
9. Farmen S.L., Karp P.H., Ng P., Palmer D.J., Koehler D.R., Hu J., Beaudet A.L., Zabner J., and Welsh M.J. Gene transfer of CFTR to airway epithelia: low levels of expression are sufficient to correct Cl- transport and overexpression can generate basolateral CFTR. Am. J. Physiol. Lung Cell. Mol. Physiol. 289 (2005) L1123-L1130
10. Galietta L.J., Haggie P.M., and Verkman A.S. Green fluorescent protein-based halide indicators with improved chloride and iodide affinities. FEBS Lett. 499 (2001) 220-224
11. Haggie P.M., Kim J.K., Lukacs G.L., and Verkman A.S. Tracking of quantum dot-labeled CFTR shows near immobilization by C-terminal PDZ interactions. Mol. Biol. Cell 17 (2006) 4937-4945
12. He L., Aleksandrov A.A., Serohijos A.W., Hegedus T., Aleksandrov L.A., Cui L., Dokholyan N.V., and Riordan J.R. Multiple membrane-cytoplasmic domain contacts in the cystic fibrosis transmembrane conductance regulator (CFTR) mediate regulation of channel gating. J. Biol. Chem. 283 (2008) 26383-26390
13. Hegedus T., Aleksandrov A., Cui L., Gentzsch M., Chang X.B., and 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 1758 (2006) 565-572
14. Henriques S.T., Melo M.N., and Castanho M.A. Cell-penetrating peptides and antimicrobial peptides: how different are they?. Biochem. J. 399 (2006) 1-7
15. Jaskolski F., Coussen F., Nagarajan N., Normand E., Rosenmund C., and Mulle C. Subunit composition and alternative splicing regulate membrane delivery of kainate receptors. J. Neurosci. 24 (2004) 2506-2515
16. Jin S., Haggie P.M., and Verkman A.S. Single-particle tracking of membrane protein diffusion in a potential: simulation, detection, and application to confined diffusion of CFTR Cl- channels. Biophys. J. 93 (2007) 1079-1088
17. Kaplan I.M., Wadia J.S., and Dowdy S.F. Cationic TAT peptide transduction domain enters cells by macropinocytosis. J. Control. Release 102 (2005) 247-253
18. Lewis H.A., Zhao X., Wang C., Sauder J.M., Rooney I., Noland B.W., Lorimer D., Kearins M.C., Conners K., Condon B., 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. 280 (2005) 1346-1353
19. Loo T.W., Bartlett M.C., Wang Y., and Clarke D.M. The chemical chaperone CFcor-325 repairs folding defects in the transmembrane domains of CFTR-processing mutants. Biochem. J. 395 (2006) 537-542
20. Loo T.W., Bartlett M.C., and Clarke D.M. Processing mutations disrupt interactions between the nucleotide binding and transmembrane domains of P-glycoprotein and the cystic fibrosis transmembrane conductance regulator (CFTR). J. Biol. Chem. 283 (2008) 28190-28197
21. Lukacs G.L., Mohamed A., Kartner N., Chang X.B., Riordan J.R., and Grinstein S. Conformational maturation of CFTR but not its mutant counterpart (delta F508) occurs in the endoplasmic reticulum and requires ATP. EMBO J. 13 (1994) 6076-6086
22. Ma X., Zheng W., Wei D., Ma Y., Wang T., Wang J., Liu Q., and Yang S. High-level expression, purification and pro-apoptosis activity of HIV-TAT-survivin (T34A) mutant to cancer cells in vitro. J. Biotechnol. 123 (2006) 367-378
23. MacVinish L.J., Gill D.R., Hyde S.C., Mofford K.A., Evans M.J., Higgins C.F., Colledge W.H., Huang L., Sorgi F., Ratcliff R., and Cuthbert A.W. Chloride secretion in the trachea of null cystic fibrosis mice: the effects of transfection with pTrial10-CFTR2. J. Physiol. 499 (1997) 677-687
24. Margeta-Mitrovic M., Jan Y.N., and Jan L.Y. A trafficking checkpoint controls GABA(B) receptor heterodimerization. Neuron 27 (2000) 97-106
25. Mense M., Vergani P., White D.M., Altberg G., Nairn A.C., and Gadsby D.C. In vivo phosphorylation of CFTR promotes formation of a nucleotide-binding domain heterodimer. EMBO J. 25 (2006) 4728-4739
26. Ostedgaard L.S., Zabner J., Vermeer D.W., Rokhlina T., Karp P.H., Stecenko A.A., Randak C., and Welsh M.J. CFTR with a partially deleted R domain corrects the cystic fibrosis chloride transport defect in human airway epithelia in vitro and in mouse nasal mucosa in vivo. Proc. Natl. Acad. Sci. USA 99 (2002) 3093-3098
27. Pedemonte N., Lukacs G.L., Du K., Caci E., Zegarra-Moran O., Galietta L.J., and Verkman A.S. Small-molecule correctors of defective DeltaF508-CFTR cellular processing identified by high-throughput screening. J. Clin. Invest. 115 (2005) 2564-2571
28. Pissarra L.S., Farinha C.M., Xu Z., Schmidt A., Thibodeau P.H., Cai Z., Thomas P.J., Sheppard D.N., and Amaral M.D. Solubilizing mutations used to crystallize one CFTR domain attenuate the trafficking and channel defects caused by the major cystic fibrosis mutation. Chem. Biol. 15 (2008) 62-69
29. Potocky T.B., Menon A.K., and Gellman S.H. Cytoplasmic and nuclear delivery of a TAT-derived peptide and a beta-peptide after endocytic uptake into HeLa cells. J. Biol. Chem. 278 (2003) 50188-50194
30. Rennolds J., Tower C., Musgrove L., Fan L., Maloney K., Clancy J.P., Kirk K.L., Sztul E., and Cormet-Boyaka E. Cystic fibrosis transmembrane conductance regulator trafficking is mediated by the COPI coat in epithelial cells. J. Biol. Chem. 283 (2008) 833-839
31. Roxo-Rosa M., Xu Z., Schmidt A., Neto M., Cai Z., Soares C.M., Sheppard D.N., and Amaral M.D. Revertant mutants G550E and 4RK rescue cystic fibrosis mutants in the first nucleotide-binding domain of CFTR by different mechanisms. Proc. Natl. Acad. Sci. USA 103 (2006) 17891-17896
32. Scott D.B., Blanpied T.A., Swanson G.T., Zhang C., and Ehlers M.D. An NMDA receptor ER retention signal regulated by phosphorylation and alternative splicing. J. Neurosci. 21 (2001) 3063-3072
33. Serohijos A.W., Hegedus T., Aleksandrov A.A., He L., Cui L., Dokholyan N.V., and 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 105 (2008) 3256-3261
34. Sheppard D.N., and Welsh M.J. Structure and function of the CFTR chloride channel. Physiol. Rev. 79 (1999) S23-S45
35. Sheppard D.N., Rich D.P., Ostedgaard L.S., Gregory R.J., Smith A.E., and Welsh M.J. Mutations in CFTR associated with mild-disease-form Cl- channels with altered pore properties. Nature 362 (1993) 160-164
36. Snyder E.L., and Dowdy S.F. Cell penetrating peptides in drug delivery. Pharm. Res. 21 (2004) 389-393
37. Standley S., Roche K.W., McCallum J., Sans N., and Wenthold R.J. PDZ domain suppression of an ER retention signal in NMDA receptor NR1 splice variants. Neuron 28 (2000) 887-898
38. Sun F., Mi Z., Condliffe S.B., Bertrand C.A., Gong X., Lu X., Zhang R., Latoche J.D., Pilewski J.M., Robbins P.D., and Frizzell R.A. Chaperone displacement from mutant cystic fibrosis transmembrane conductance regulator restores its function in human airway epithelia. FASEB J. 22 (2008) 3255-3263
39. Szul T., Grabski R., Lyons S., Morohashi Y., Shestopal S., Lowe M., and Sztul E. Dissecting the role of the ARF guanine nucleotide exchange factor GBF1 in Golgi biogenesis and protein trafficking. J. Cell Sci. 120 (2007) 3929-3940
40. Teem J.L., Berger H.A., Ostedgaard L.S., Rich D.P., Tsui L.C., and Welsh M.J. Identification of revertants for the cystic fibrosis delta F508 mutation using STE6-CFTR chimeras in yeast. Cell 73 (1993) 335-346
41. Teem J.L., Carson M.R., and Welsh M.J. Mutation of R555 in CFTR-delta F508 enhances function and partially corrects defective processing. Receptors Channels 4 (1996) 63-72
42. Trzcinska-Daneluti A.M., Ly D., Huynh L., Jiang C., Fladd C., and Rotin D. High-content functional screen to identify proteins that correct F508del-CFTR function. Mol. Cell. Proteomics 8 (2009) 780-790
43. Van Goor F., Straley K.S., Cao D., Gonzalez J., Hadida S., Hazlewood A., Joubran J., Knapp T., Makings L.R., Miller M., 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. 290 (2006) L1117-L1130
44. Vergani P., Basso C., Mense M., Nairn A.C., and Gadsby D.C. Control of the CFTR channel's gates. Biochem. Soc. Trans. 33 (2005) 1003-1007
45. Wadia J.S., Stan R.V., and Dowdy S.F. Transducible TAT-HA fusogenic peptide enhances escape of TAT-fusion proteins after lipid raft macropinocytosis. Nat. Med. 10 (2004) 310-315
46. Wang X., Matteson J., An Y., Moyer B., Yoo J.S., Bannykh S., Wilson I.A., Riordan J.R., and Balch W.E. COPII-dependent export of cystic fibrosis transmembrane conductance regulator from the ER uses a di-acidic exit code. J. Cell Biol. 167 (2004) 65-74
47. Wang X., Venable J., LaPointe P., Hutt D.M., Koulov A.V., Coppinger J., Gurkan C., Kellner W., Matteson J., Plutner H., et al. Hsp90 cochaperone Aha1 downregulation rescues misfolding of CFTR in cystic fibrosis. Cell 127 (2006) 803-815
48. Wang Y., Loo T.W., Bartlett M.C., and Clarke D.M. Modulating the folding of P-glycoprotein and cystic fibrosis transmembrane conductance regulator truncation mutants with pharmacological chaperones. Mol. Pharmacol. 71 (2007) 751-758
49. Watson R.T., Khan A.H., Furukawa M., Hou J.C., Li L., Kanzaki M., Okada S., Kandror K.V., and Pessin J.E. Entry of newly synthesized GLUT4 into the insulin-responsive storage compartment is GGA dependent. EMBO J. 23 (2004) 2059-2070
50. Yoo D., Fang L., Mason A., Kim B.Y., and Welling P.A. A phosphorylation-dependent export structure in ROMK (Kir 1.1) channel overrides an endoplasmic reticulum localization signal. J. Biol. Chem. 280 (2005) 35281-35289
51. Younger J.M., Chen L., Ren H.Y., Rosser M.F., Turnbull E.L., Fan C.Y., Patterson C., and Cyr D.M. Sequential quality-control checkpoints triage misfolded cystic fibrosis transmembrane conductance regulator. Cell 126 (2006) 571-582
52. Younger J.M., Ren H.Y., Chen L., Fan C.Y., Fields A., Patterson C., and Cyr D.M. A foldable CFTR{Delta}F508 biogenic intermediate accumulates upon inhibition of the Hsc70-CHIP E3 ubiquitin ligase. J. Cell Biol. 167 (2004) 1075-1085
53. Zabner J., Zeiher B.G., Friedman E., and Welsh M.J. Adenovirus-mediated gene transfer to ciliated airway epithelia requires prolonged incubation time. J. Virol. 70 (1996) 6994-7003
54. Zerangue N., Malan M.J., Fried S.R., Dazin P.F., Jan Y.N., Jan L.Y., and Schwappach B. Analysis of endoplasmic reticulum trafficking signals by combinatorial screening in mammalian cells. Proc. Natl. Acad. Sci. USA 98 (2001) 2431-2436
55. Zerangue N., Schwappach B., Jan Y.N., and Jan L.Y. A new ER trafficking signal regulates the subunit stoichiometry of plasma membrane K(ATP) channels. Neuron 22 (1999) 537-548
56. Zhang L.N., Karp P., Gerard C.J., Pastor E., Laux D., Munson K., Yan Z., Liu X., Godwin S., Thomas C.P., et al. Dual therapeutic utility of proteasome modulating agents for pharmaco-gene therapy of the cystic fibrosis airway. Mol. Ther. 10 (2004) 990-1002