The primary folding defect and rescue of δf508 CFTR emerge during translation of the mutant domain

PLoS ONE

Volumn 5, Issue 11, 2010, Pages

  Hoelen, Hanneke ^a   Kleizen, Sbertrand ^a   Schmidt, Andre ^b   Richardson, John ^b,c   Charitou, Paraskevi ^a   Thomas, Philip J ^b   Braakman, Ineke ^a  

^a UTRECHT UNIVERSITY   (Netherlands)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^c AUSTIN COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLUTAMIC ACID; GLYCINE; ISOLEUCINE; MUTANT PROTEIN; NUCLEOTIDE BINDING PROTEIN; PHENYLALANINE; THREONINE; TRANSMEMBRANE CONDUCTANCE REGULATOR; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR DELTA F508;

ARTICLE; CELL SURFACE; CONTROLLED STUDY; CYSTIC FIBROSIS; HUMAN; HUMAN CELL; PROTEIN DEFECT; PROTEIN DEGRADATION; PROTEIN DEPLETION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN ISOLATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEIN STABILITY; PROTEIN TARGETING; AMINO ACID SEQUENCE; ANIMAL; BINDING SITE; CHEMISTRY; CHO CELL; CRICETULUS; GENE THERAPY; GENETIC COMPLEMENTATION; GENETICS; HAMSTER; HELA CELL; MOLECULAR GENETICS; MUTATION; PROTEIN SYNTHESIS; SEQUENCE HOMOLOGY; TUMOR CELL LINE;

AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; CELL LINE, TUMOR; CHO CELLS; CRICETINAE; CRICETULUS; CYSTIC FIBROSIS; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; GENE THERAPY; GENETIC COMPLEMENTATION TEST; HELA CELLS; HUMANS; MOLECULAR SEQUENCE DATA; MUTATION; PROTEIN BIOSYNTHESIS; PROTEIN FOLDING; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 78649775607     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0015458     Document Type: Article

References (50)

1. Anderson MP, Gregory RJ, Thompson S, Souza DW, Paul S, et al. (1991) Demonstration that CFTR is a chloride channel by alteration of its anion selectivity. Science 253: 202-205.
2. Riordan JR, Rommens JM, Kerem B, Alon N, Rozmahel R, et al. (1989) Identification of the cystic fibrosis gene: cloning and characterization of complementary DNA. Science 245: 1066-1073.
3. Schwiebert EM, Benos DJ, Egan ME, Stutts MJ, Guggino WB (1999) CFTR is a conductance regulator as well as a chloride channel. Physiol Rev 79: S145-166.
4. Cheng SH, Gregory RJ, Marshall J, Paul S, Souza DW, et al. (1990) Defective intracellular transport and processing of CFTR is the molecular basis of most cystic fibrosis. Cell 63: 827-834.
5. Jensen TJ, Loo MA, Pind S, Williams DB, Goldberg AL, et al. (1995) Multiple proteolytic systems, including the proteasome, contribute to CFTR processing. Cell 83: 129-135.
6. Ward CL, Omura S, Kopito RR (1995) Degradation of CFTR by the ubiquitinproteasome pathway. Cell 83: 121-127.
7. Mendoza JL, Thomas PJ (2007) Building an understanding of cystic fibrosis on the foundation of ABC transporter structures. J Bioenerg Biomembr 39: 499-505.
8. Serohijos AW, Hegedus T, Aleksandrov AA, He L, Cui L, et al. (2008) Phenylalanine-508 mediates a cytoplasmic-membrane domain contact in the CFTR 3D structure crucial to assembly and channel function. Proc Natl Acad Sci U S A 105: 3256-3261.
9. Mornon JP, Lehn P, Callebaut I (2009) Molecular models of the open and closed states of the whole human CFTR protein. Cell Mol Life Sci 66: 3469-3486.
10. Thibodeau PH, Brautigam CA, Machius M, Thomas PJ (2005) Side chain and backbone contributions of Phe508 to CFTR folding. Nat Struct Mol Biol 12: 10-16.
11. Cui L, Aleksandrov L, Chang XB, Hou YX, He L, et al. (2007) Domain interdependence in the biosynthetic assembly of CFTR. J Mol Biol 365: 981-994.
12. Du K, Sharma M, Lukacs GL (2005) The DeltaF508 cystic fibrosis mutation impairs domain-domain interactions and arrests post-translational folding of CFTR. Nat Struct Mol Biol 12: 17-25.
13. Qu BH, Thomas PJ (1996) Alteration of the cystic fibrosis transmembrane conductance regulator folding pathway. J Biol Chem 271: 7261-7264.
14. Qu BH, Strickland EH, Thomas PJ (1997) Localization and suppression of a kinetic defect in cystic fibrosis transmembrane conductance regulator folding. J Biol Chem 272: 15739-15744.
15. Denning GM, Anderson MP, Amara JF, Marshall J, Smith AE, et al. (1992) Processing of mutant cystic fibrosis transmembrane conductance regulator is temperature-sensitive. Nature 358: 761-764.
16. Brown CR, Hong-Brown LQ, Biwersi J, Verkman AS, Welch WJ (1996) Chemical chaperones correct the mutant phenotype of the delta F508 cystic fibrosis transmembrane conductance regulator protein. Cell Stress Chaperones 1: 117-125.
17. Sato S, Ward CL, Krouse ME, Wine JJ, Kopito RR (1996) Glycerol reverses the misfolding phenotype of the most common cystic fibrosis mutation. J Biol Chem 271: 635-638.
18. Zhang XM, Wang XT, Yue H, Leung SW, Thibodeau PH, et al. (2003) Organic solutes rescue the functional defect in delta F508 cystic fibrosis transmembrane conductance regulator. J Biol Chem 278: 51232-51242.
19. DeCarvalho AC, Gansheroff LJ, Teem JL (2002) 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 277: 35896-35905.
20. Roxo-Rosa M, Xu Z, Schmidt A, Neto M, Cai Z, et al. (2006) Revertant mutants G550E and 4RK rescue cystic fibrosis mutants in the first nucleotidebinding domain of CFTR by different mechanisms. Proc Natl Acad Sci U S A 103: 17891-17896.
21. He L, Aleksandrov LA, Cui L, Jensen TJ, Nesbitt KL, et al. (2010) Restoration of domain folding and interdomain assembly by second-site suppressors of the {Delta}F508 mutation in CFTR. FASEB J.
22. van Doorninck JH, French PJ, Verbeek E, Peters RH, Morreau H, et al. (1995) A mouse model for the cystic fibrosis delta F508 mutation. EMBO J 14: 4403-4411.
23. Buchner J, Kiefhaber T (2005) Protein Folding Handbook: Wiley-VCH.
24. Kleizen B, van Vlijmen T, de Jonge HR, Braakman I (2005) Folding of CFTR is predominantly cotranslational. Mol Cell 20: 277-287.
25. Zhang F, Kartner N, Lukacs GL (1998) Limited proteolysis as a probe for arrested conformational maturation of delta F508 CFTR. Nat Struct Biol 5: 180-183.
26. Sato S, Ward CL, Kopito RR (1998) Cotranslational ubiquitination of cystic fibrosis transmembrane conductance regulator in vitro. J Biol Chem 273: 7189-7192.
27. Meacham GC, Lu Z, King S, Sorscher E, Tousson A, et al. (1999) The Hdj-2/Hsc70 chaperone pair facilitates early steps in CFTR biogenesis. EMBO J 18: 1492-1505.
28. Wang X, Venable J, LaPointe P, Hutt DM, Koulov AV, et al. (2006) Hsp90 cochaperone Aha1 downregulation rescues misfolding of CFTR in cystic fibrosis. Cell 127: 803-815.
29. Sun F, Mi Z, Condliffe SB, Bertrand CA, Gong X, et al. (2008) Chaperone displacement from mutant cystic fibrosis transmembrane conductance regulator restores its function in human airway epithelia. FASEB J 22: 3255-3263.
30. Younger JM, Ren HY, Chen L, Fan CY, Fields A, et al. (2004) A foldable CFTR{Delta}F508 biogenic intermediate accumulates upon inhibition of the Hsc70-CHIP E3 ubiquitin ligase. J Cell Biol 167: 1075-1085.
31. Strickland E, Qu BH, Millen L, Thomas PJ (1997) The molecular chaperone Hsc70 assists the in vitro folding of the N-terminal nucleotide-binding domain of the cystic fibrosis transmembrane conductance regulator. J Biol Chem 272: 25421-25424.
32. Meacham GC, Patterson C, Zhang W, Younger JM, Cyr DM (2001) The Hsc70 co-chaperone CHIP targets immature CFTR for proteasomal degradation. Nat Cell Biol 3: 100-105.
33. Younger JM, Chen L, Ren HY, Rosser MF, Turnbull EL, et al. (2006) Sequential quality-control checkpoints triage misfolded cystic fibrosis transmembrane conductance regulator. Cell 126: 571-582.
34. Lewis HA, Zhao X, Wang C, Sauder JM, Rooney I, et al. (2005) 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: 1346-1353.
35. Lewis HA, Wang C, Zhao X, Hamuro Y, Conners K, et al. (2010) Structure and dynamics of NBD1 from CFTR characterized using crystallography and hydrogen/deuterium exchange mass spectrometry. J Mol Biol 396: 406-430.
36. Atwell S, Brouillette CG, Conners K, Emtage S, Gheyi T, et al. (2010) Structures of a minimal human CFTR first nucleotide-binding domain as a monomer, head-to-tail homodimer, and pathogenic mutant. Protein Eng Des Sel 23: 375-384.
37. Kanelis V, Hudson RP, Thibodeau PH, Thomas PJ, Forman-Kay JD (2009) NMR evidence for differential phosphorylation-dependent interactions in WT and DeltaF508 CFTR. EMBO J 29: 263-277.
38. Loo TW, Bartlett MC, Clarke DM (2008) 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: 28190-28197.
39. Ostedgaard LS, Rich DP, DeBerg LG, Welsh MJ (1997) Association of domains within the cystic fibrosis transmembrane conductance regulator. Biochemistry 36: 1287-1294.
40. Du K, Lukacs GL (2009) Cooperative assembly and misfolding of CFTR domains in vivo. Mol Biol Cell 20: 1903-1915.
41. Dawson RJ, Locher KP (2006) Structure of a bacterial multidrug ABC transporter. Nature 443: 180-185.
42. Vergani P, Lockless SW, Nairn AC, Gadsby DC (2005) CFTR channel opening by ATP-driven tight dimerization of its nucleotide-binding domains. Nature 433: 876-880.
43. Thibodeau PH, Richardson JM, Wang W, Millen L, Watson J, et al. (2010) The cystic fibrosis-causing mutation {Delta}F508 affects multiple steps in CFTR biogenesis. J Biol Chem.
44. Johnson LG, Olsen JC, Sarkadi B, Moore KL, Swanstrom R, et al. (1992) Efficiency of gene transfer for restoration of normal airway epithelial function in cystic fibrosis. Nat Genet 2: 21-25.
45. Sun X, Yan Z, Yi Y, Li Z, Lei D, et al. (2008) Adeno-associated virus-targeted disruption of the CFTR gene in cloned ferrets. J Clin Invest 118: 1578-1583.
46. Rogers CS, Stoltz DA, Meyerholz DK, Ostedgaard LS, Rokhlina T, et al. (2008) Disruption of the CFTR gene produces a model of cystic fibrosis in newborn pigs. Science 321: 1837-1841.
47. Picciotto MR, Cohn JA, Bertuzzi G, Greengard P, Nairn AC (1992) Phosphorylation of the cystic fibrosis transmembrane conductance regulator. J Biol Chem 267: 12742-12752.
48. Lewis HA, Buchanan SG, Burley SK, Conners K, Dickey M, et al. (2004) Structure of nucleotide-binding domain 1 of the cystic fibrosis transmembrane conductance regulator. EMBO J 23: 282-293.
49. Braakman I, Hoover-Litty H, Wagner KR, Helenius A (1991) Folding of influenza hemagglutinin in the endoplasmic reticulum. J Cell Biol 114: 401-411.
50. Wilson R, Allen AJ, Oliver J, Brookman JL, High S, et al. (1995) The translocation, folding, assembly and redox-dependent degradation of secretory and membrane proteins in semi-permeabilized mammalian cells. Biochem J 307(Pt 3): 679-687.