Side chain and backbone contributions of Phe508 to CFTR folding

Nature Structural and Molecular Biology

Volumn 12, Issue 1, 2005, Pages 10-16

  Thibodeau, Patrick H ^a,b   Brautigam, Chad A ^a   Machius, Mischa ^a,b   Thomas, Philip J ^a,b  

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

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

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE PROTEIN; NUCLEOTIDE BINDING PROTEIN; PHENYLALANINE; TRANSMEMBRANE CONDUCTANCE REGULATOR;

ARTICLE; CYSTIC FIBROSIS; HUMAN; HUMAN CELL; IN VITRO STUDY; MISSENSE MUTATION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN INTERACTION; PROTEIN PROCESSING; PROTEIN STABILITY; PROTEIN STRUCTURE;

ANIMALS; BINDING SITES; CELL LINE; CRYSTALLOGRAPHY, X-RAY; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; HUMANS; HYDROPHOBICITY; MICE; MODELS, MOLECULAR; MUTATION; PHENYLALANINE; PROTEIN DENATURATION; PROTEIN FOLDING; PROTEIN STRUCTURE, TERTIARY; TEMPERATURE; THERMODYNAMICS;

EID: 11444265307     PISSN: 15459993     EISSN: None     Source Type: Journal    
DOI: 10.1038/nsmb881     Document Type: Article

References (51)

1. Sheppard, D.N. & Welsh, M.J. Structure and function of the CFTR chloride channel. Physiol. Rev. 79, S23-S45 (1999).
2. Riordan, J.R. et al. Identification of the cystic fibrosis gene: cloning and characterization of complementary DNA. Science 245, 1066-1073 (1989).
3. Tsui, L.C. The spectrum of cystic fibrosis mutations. Trends Genet. 8, 392-398 (1992).
4. Tsui, L.C. The cystic fibrosis transmembrane conductance regulator gene. Am. J. Respir. Crit. Care Med. 151, S47-S53 (1995).
5. Cheng, S.H. et al. Defective intracellular transport and processing of CFTR is the molecular basis of most cystic fibrosis. Cell 63, 827-834 (1990).
6. Lukacs, G.L. et al. Conformational maturation of CFTR but not its mutant counterpart (ΔF508) occurs in the endoplasmic reticulum and requires ATP. EMBO J. 13, 6076-6086 (1994).
7. Denning, G.M., Ostedgaard, L.S. & Welsh, M.J. Abnormal localization of cystic fibrosis transmembrane conductance regulator in primary cultures of cystic fibrosis airway epithelia. J. Cell Biol. 118, 551-559 (1992).
8. Sharma, M., Benharouga, M., Hu, W. & Lukacs, G.L. Conformational and temperature-sensitive stability defects of the ΔF508 cystic fibrosis transmembrane conductance regulator in post-endoplasmic reticulum compartments. J. Biol. Chem. 276, 8942-8950 (2001).
9. Ward, C.L., Omura, S. & Kopito, R.R. Degradation of CFTR by the ubiquitin-proteasome pathway. Cell 83, 121-127 (1995).
10. Jensen, T.J. et al. Multiple proteolytic systems, including the proteasome, contribute to CFTR processing. Cell 83, 129-135 (1995).
11. Kartner, N., Augustinas, O., Jensen, T.J., Naismith, A.L. & Riordan, J.R. Mislocalization of ΔF508 CFTR in cystic fibrosis sweat gland. Nat. Genet. 1, 321-327 (1992).
12. Zhang, X.M. et al. Organic solutes rescue the functional defect in F508 CFTR. J. Biol. Chem. 278, 51232-51242 (2003).
13. Denning, G.M. et al. Processing of mutant cystic fibrosis transmembrane conductance regulator is temperature-sensitive. Nature 358, 761-764 (1992).
14. Sato, S., Ward, C.L., Krouse, M.E., Wine, J.J. & Kopito, R.R. Glycerol reverses the misfolding phenotype of the most common cystic fibrosis mutation. J. Biol. Chem. 271, 635-638 (1996).
15. Yang, H. et al. Nanomolar affinity small molecule correctors of defective ΔF508-CFTR chloride channel gating. J. Biol. Chem. 278, 35079-35085 (2003).
16. Brown, C.R., Hong-Brown, L.Q., Biwersi, J., Verkman, A.S. & Welch, W.J. Chemical chaperones correct the mutant phenotype of the ΔF508 cystic fibrosis transmembrane conductance regulator protein. Cell Stress Chaperones 1, 117-125 (1996).
17. Dormer, R.L. et al. Correction of delF508-CFTR activity with benzo(c)quinolizinium compounds through facilitation of its processing in cystic fibrosis airway cells. J. Cell Sci. 114, 4073-4081 (2001).
18. Howard, M. et al. Mammalian osmolytes and S-nitrosoglutathione promote ΔF508 cystic fibrosis transmembrane conductance regulator (CFTR) protein maturation and function. J. Biol. Chem. 278, 35159-35167 (2003).
19. Thomas, P.J., Ko, Y.H. & Pedersen, P.L. Altered protein folding may be the molecular basis of most cases of cystic fibrosis. FEBS Lett. 312, 7-9 (1992).
20. Zeitlin, P.L. Therapies directed at the basic defect in cystic fibrosis. Clin. Chest Med. 19, 515-525 (1998).
21. Locher, K.P., Lee, A.T. & Rees, D.C. The E. coli BtuCD structure: a framework for ABC transporter architecture and mechanism. Science 296, 1091-1098 (2002).
22. Chang, G. Structure of MsbA from Vibrio cholera: a multidrug resistance ABC transporter homolog in a closed conformation. J. Mol. Biol. 330, 419-430 (2003).
23. 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. 272, 15739-15744 (1997).
24. Qu, B.H. & Thomas, P.J. Alteration of the cystic fibrosis transmembrane conductance regulator folding pathway. J. Biol. Chem. 271, 7261-7264 (1996).
25. Myers, J.K., Pace, C.N. & Scholtz, J.M. Denaturant m values and heat capacity changes: relation to changes in accessible surface areas of protein unfolding. Protein Sci. 4, 2138-2148 (1995).
26. Lewis, H.A. et al. Structure of nucleotide-binding domain 1 of the cystic fibrosis transmembrane conductance regulator. EMBO J. 23, 282-293 (2004).
27. Karpowich, N. et al. Crystal structures of the MJ1267 ATP binding cassette reveal an induced-fit effect at the ATPase active site of an ABC transporter. Structure 9, 571-586 (2001).
28. Chen, W., Helenius, J., Braakman, I. & Helenius, A. Cotranslational folding and calnexin binding during glycoprotein synthesis. Proc. Natl. Acad. Sci. USA 92, 6229-6233 (1995).
29. Jansens, A., van Duijn, E. & Braakman, I. Coordinated nonvectorial folding in a newly synthesized multidomain protein. Science 298, 2401-2403 (2002).
30. Du, K., Sharma, L. & Lukacs, G.L. The ΔF508 cystic fibrosis mutation impairs domain-domain interactions and arrests post-translational folding of CFTR. Nat. Struct. Mol. Biol. 12, 17-25 (2005).
31. Yuan, Y.R. et al. The crystal structure of the MJ0796 ATP-binding cassette. Implications for the structural consequences of ATP hydrolysis in the active site of an ABC transporter. J. Biol. Chem. 276, 32313-32321 (2001).
32. Gaudet, R. & Wiley, D.C. Structure of the ABC ATPase domain of human TAP1, the transporter associated with antigen processing. EMBO J. 20, 4964-4972 (2001).
33. Ames, G.F. et al. Purification and characterization of the membrane-bound complex of an ABC transporter, the histidine permease. J. Bioenerg. Biomembr. 33, 79-92 (2001).
34. Liu, P.Q. & Ames, G.F. In vitro disassembly and reassembly of an ABC transporter, the histidine permease. Proc. Natl. Acad. Sci. USA 95, 3495-3500 (1998).
35. Mourez, M., Hofnung, M. & Dassa, E. Subunit interactions in ABC transporters: a conserved sequence in hydrophobic membrane proteins of periplasmic permeases defines an important site of interaction with the ATPase subunits. EMBO J. 16, 3066-3077 (1997).
36. Wilken, S., Schmees, G. & Schneider, E. A putative helical domain in the MalK subunit of the ATP-binding-cassette transport system for maltose of Salmonella typhimurium (MalFGK2) is crucial for interaction with MalF and MalG. A study using the LacK protein of Agrobacterium radiobacter as a tool. Mol. Microbiol. 22, 655-666 (1996).
37. Tector, M. & Hartl, F.U. An unstable transmembrane segment in the cystic fibrosis transmembrane conductance regulator. EMBO J. 18, 6290-6298 (1999).
38. Chen, E.Y., Bartlett, M.C., Loo, T.W. & Clarke, D.M. The ΔF508 mutation disrupts packing of the transmembrane segments of the cystic fibrosis transmembrane conductance regulator. J. Biol. Chem. 279, 39620-39627 (2004).
39. Loo, T.W., Bartlett, M.C. & Clarke, D.M. Introduction of the most common cystic fibrosis mutation (ΔF508) into human P-glycoprotein disrupts packing of the transmembrane segments. J. Biol. Chem. 277, 27585-27588 (2002).
40. Meacham, G.C. et al. The Hdj-2/Hsc70 chaperone pair facilitates early steps in CFTR biogenesis. EMBO J. 18, 1492-1505 (1999).
41. Xiong, X., Bragin, A., Widdicombe, J.H., Cohn, J. & Skach, W.R. Structural cues involved in endoplasmic reticulum degradation of G85E and G91R mutant cystic fibrosis transmembrane conductance regulator. J. Clin. Invest 100, 1079-1088 (1997).
42. Sato, S., Ward, C.L. & Kopito, R.R. Cotranslational ubiquitination of cystic fibrosis transmembrane conductance regulator in vitro. J. Biol. Chem. 273, 7189-7192 (1998).
43. Miller, S.R., Sekijima, Y. & Kelly, J.W. Native state stabilization by NSAIDs inhibits transthyretin amyloidogenesis from the most common familial disease variants. Lab Invest. 84, 545-552 (2004).
44. Fan, J.Q., Ishii, S., Asano, N. & Suzuki, Y. Accelerated transport and maturation of lysosomal α-galactosidase A in Fabry lymphoblasts by an enzyme inhibitor. Nat. Med. 5, 112-115 (1999).
45. Pace, C.N. & Shaw, K.L. Linear extrapolation method of analyzing solvent denaturation curves. Proteins, Suppl 4, 1-7 (2000).
46. Mossessova, E. & Lima, C.D. Ulp1-SUMO crystal structure and genetic analysis reveal conserved interactions and a regulatory element essential for cell growth in yeast. Mol. Cell 5, 865-876 (2000).
47. Otwinowski, Z. & Minor, W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326 (1997).
48. Brunger, A.T. et al. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D 54, 905-921 (1998).
49. McRee, D.E. A visual protein crystallographic software system for X11/Xview. J. Mol. Graph. 10, 44-46 (1992).
50. Nicholls, A., Sharp, K.A. & Honig, B. Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins 11, 281-296 (1991).
51. Lewis, H.A. et al. Impact of the Δ508 mutation in NBD1 of human CFTR on domain folding and structure. J. Biol. Chem. Epub ahead of print, 3 November 2004 (doi:10.1074/jbc.M410968200).