Nucleotide-binding domains of human cystic fibrosis transmembrane conductance regulator: Detailed sequence analysis and three-dimensional modeling of the heterodimer

Cellular and Molecular Life Sciences

Volumn 61, Issue 2, 2004, Pages 230-242

  Callebaut, I ^a   Eudes, R ^a   Mornon, J P ^a   Lehn, P ^b  

^a SORBONNE UNIVERSITÉ   (France)

^b HÔPITAL ROBERT DEBRÉ   (France)

Author keywords

ABC transporter; CFTR; Cystic fibrosis; Disease causing mutation; Hydrophobic cluster analysis; Molecular modeling; MRP1; SUR1

Indexed keywords

DIMER; NUCLEOTIDE BINDING PROTEIN; TRANSMEMBRANE CONDUCTANCE REGULATOR;

AMINO ACID SEQUENCE; ARTICLE; HUMAN; MOLECULAR MODEL; PROTEIN ANALYSIS; PROTEIN DOMAIN; SEQUENCE ANALYSIS; STRUCTURE ANALYSIS;

AMINO ACID SEQUENCE; BINDING SITES; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; DIMERIZATION; HUMANS; MOLECULAR SEQUENCE DATA; NUCLEOTIDES; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, TERTIARY; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, PROTEIN;

EID: 0842330688     PISSN: 1420682X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00018-003-3386-z     Document Type: Article

References (66)

1. Riordan J., Rommens J., Kerem B., Alon N., Rozhamel R., Grzeleczak Z. et al. (1989) Identification of the cystic fibrosis gene: cloning and characterization of complementary DNA. Science 245: 1066-1073
2. Rommens J., Iannuzzi M., Kerem B., Drumm M., Melmer G., Dean M. et al. (1989) Identification of the cystic fibrosis gene: chromosome walking and jumping. Science 245: 1059-1065
3. Sheppard D. and Welsh M. (1999) Structure and function of the CFTR chloride channel. Physiol. Rev. 79: S23-S45
4. Gadsby D. C. and Nairn A. C. (1999) Control of CFTR channel gating by phosphorylation and nucleotide hydrolysis. Physiol. Rev. 79: S77-S107
5. Stutts M., Canessa C., Olsen J., Hamrick M., Cohn J., Rossier B. et al. (1995) CFTR as a cAMP-dependent regulator of sodium channels. Science 269: 847-850
6. Akabas M. (2000) Cystic fibrosis transmembrane conductance regulator. J. Biol. Chem. 275: 3729-3732
7. 3-transport in mutations associated with cystic fibrosis. Nature 410: 94-97
8. Holland I. B. and Blight M. A. (1999) ABC-ATPases, adaptable energy generators fuelling transmembrane movement of a variety of molecules in organisms from bacteria to humans. J. Mol. Biol. 293: 381-399
9. Higgins C. (2001) ABC transporters: physiology, structure and mechanism- an overview. Res. Microbiol. 152: 205-210
10. Kerr I. (2002) Structure and association of ATP-binding cassette transporter nucleotide-binding domains. Biochem. Biophys. Acta 1561: 47-64
11. Schmitt L. and Tampe R. (2002) Structure and mechanism of ABC transporters. Curr. Opin. Struct. Biol. 12: 754-760
12. Hopfner K.-P. and Tainer J. (2003) Rad50/SMC proteins and ABC transporters: unifying concepts from high-resolution structures. Curr. Opin. Struct. Biol. 13: 249-255
13. Armstrong S., Tabernero L., Zhang H., Hermodsen M. and Stauffacher C. (1998) Powering the ABC transporter: the 2.5 A crystallographic structure of the ABC domain of RsbA. Pediatr. Pulmonol. 17: 91-92
14. Hung L., Wang I., Nikaido K., Liu P., Ames G. and Kim S. (1998) Crystal structure of the ATP-binding subunit of an ABC transporter. Nature 396: 703-707
15. Yuan Y.-R., Blecker S., Martsinkevich O., Millen L., Thomas P. J. and Hunt J. F. (2001) The crystal structure of the MJ0796 ATP-binding cassette. J. Biol. Chem. 276: 32313-32321
16. Karpowich N., Martsinkevich O., Millen L., Yuan Y.-R., Dai P. L., MacVey K. et al. (2001) Crystal structures of the MJ1267 ATP binding cassette reveal an induced-fit effect of the ATPase active site of an ABC transporter. Structure 9: 571-586
17. Jones P. and George A. (1999) Subunit interactions in ABC transporters: towards a functional architecture. FEMS Microbiol. Lett. 179: 187-202
18. Hopfner K., Karcher A., Shin D., Craig L., Arthur L. and Carney J. (2000) Structural biology of Rad50 ATPase: ATP-driven conformational control in DNA double-strand break repair and the ABC-ATPase superfamily. Cell 101: 789-800
19. Obmolova G., Ban C., Hsieh P. and Yang W. (2000) Crystal structures of DNA mismatch repair protein MutS and its complex with a substrate DNA. Nature 407: 703-710
20. Lamers M., Perrakis A., Enzlin J., Winterwerp H., Wind N. de and Sixma T. (2000) The crystal structure of DNA mismatch repair protein MutsS bound to a G x T mismatch. Nature 407: 711-717
21. Smith P., Karpowich N., Millen L., Moody J., Rosen J., Thomas P. et al. (2002) ATP binding to the motor domain of an ABC transporter drives formation of a nucleotide sandwich dimer. Mol. Cell 10: 139-149
22. Locher K. P., Lee A. T. and Rees D. C. (2002) The E. coli BtuCD structure: a framework for ABC transporter architecture and mechanism. Science 296: 1091-1098
23. Chang G. and Roth C. (2001) Structure of MsbA from E. coli: a homolog of the multidrug resistance ATP binding cassette (ABC) transporters. Science 293: 1793-1800
24. Campbell J., Biggin P., Baaden M. and Sansom M. (2003) Extending the structure of an ABC transporter to atomic resolution: modeling and simulation studies of MsbA. Biochemistry 42: 3666-3673
25. Dorwart M., Thibodeau P. and Thomas P. J. (2002) A structural view of cystic fibrosis. Cystic fibrosis Eur. Netw. 3: pp. 1-6
26. Gaudet R. and Wiley D. C. (2001) Structure of the ABC ATPase domain of human TAP1, the transporter associated with antigen processing. EMBO J. 20: 4964-4972
27. Diederichs K., Diez J., Greller G., Müller C., Breed J., Schnell C. et al. (2000) Crystal structure of MalK, the ATPase subunit of the trehalose/maltose ABC transporter of the archaeon Thermococcus litoralis. EMBO J. 19: 5951-5961
28. Gaboriaud C., Bissery V., Benchetrit T. and Mornon J. P. (1987) Hydrophobic cluster analysis: an efficient new way to compare and analyse amino-acid sequences. FEBS Lett. 224: 149-155
29. Callebaut I., Labesse G., Durand P., Poupon A., Canard L., Chomilier J. et al. (1997) Deciphering protein sequence information through hydrophobic cluster analysis (HCA): current status and perspectives. Cell. Mol. Life Sci. 53: 621-645
30. Mornon J. P., Prat K., Dupuis F., Boisset N. and Callebaut I. (2002) Structural features of prions explored by sequence analysis. II. A PrP(Sc) model. Cell. Mol. Life. Sci. 59: 2144-2154
31. Callebaut I., Curcio-Morelli C., Mornon J. P., Gereben B., Buettner C., Huang S. et al. (2003) The iodothyronine selenodeiodinases are thioredoxin-fold family proteins containing a glycoside hydrolase-clan GH-A-like structure. J. Biol. Chem. 276: 36887-36896
32. Nagel G. (1999) Differential function of the two nucleotide binding domains on cystic fibrosis transmembrane conductance regulator. Biochem. Biophys. Acta 1461: 263-274
33. Szabo K., Szakacs G., Hegedus T. and Sarkadi B. (1999) Nucleotide occlusion in the human cystic fibrosis transmembrane conductance regulator: different patterns in the two nucleotide-binding domains. J. Biol. Chem. 274: 12209-12212
34. Holm L. and Sander C. (1998) Touring protein fold space with Dali/FSSP. Nucleic Acids Res. 26: 316-319
35. Woodcock S., Mornon J. P. and Henrissat B. (1992) Detection of secondary structure elements in proteins by hydrophobic cluster analysis. Protein Eng. 5: 629-635
36. Hennetin J., LeTuan K., Canard L., Colloc'h N., Mornon J.-P. and Callebaut I. (2003) Non intertwined binary patterns of hydrophobic/non hydrophobic amino acids are considerably better markers of regular secondary structures than non constrained binary patterns. Proteins 51: 236-244
37. Altschul S. F., Madden T. L., Schaffer A. A., Zhang J., Zhang Z., Miller W. et al. (1997) Gapped-BLAST and PSI-BLAST : a new generation of protein database search programs. Nucleic Acids Res. 25: 3389-3402
38. Sali A., Potterton L., Yuan F., Vlijmen H. van and Karplus M. (1995) Evaluation of comparative protein modelling by MODELLER. Proteins 23: 318-326
39. Eisenberg D., Luthy R. and Bowie J. (1997) VERIFY3D: assessment of protein models with three-dimensional profiles. Methods Enzymol. 277: 396-404
40. Guex N. and Peitsch M. (1997) SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis 18: 2714-2723
41. Kabsch W. and Sander C. (1983) Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 22: 2577-2637
42. Poupon A. and Mornon J. P. (1998) Populations of hydrophobic amino acids within protein globular domains: identification of conserved 'topohydrophobic' positions. Proteins 33: 329-342
43. Bahadur R., Chakrabarti P., Rodier F. and Janin J. (2003) Dissecting subunit interfaces in homodimeric proteins. Proteins 53: 708-719
44. Berger A. L. and Welsh M. J. (2000) Differences between cystic fibrosis transmembrane conductance regulator and HisP in the adenine ring of ATP. J. Biol. Chem. 275: 29407-29412
45. Annereau J., Wulbrand U., Vankeerberghen A., Cuppens H., Bontems F., Tümmler B. et al. (1997) A novel model for the first nucleotide binding domain of the cystic fibrosis transmembrane conductance regulator. FEBS Lett. 407: 303-308
46. Bianchet M., Ko Y, Amzel L. and Pedersen P. (1997) Modeling of nucleotide binding domains of ABC transporter proteins based on a F1-ATPase/ RecA topology: structural model of the nucleotide binding domains of the cystic fibrosis transmembrane conductance regulator (CFTR). J. Bioenerg. Biomembr. 29: 503-524
47. Hoedemaeker F., Davidson A. and Rose D. (1998) A model for the nucleotide-binding domains of ABC transporters based on the large domain of aspartate aminotransferase. Proteins 30: 275-286
48. Chan K. W., Csanady L., Seto-Young D., Nairn A. C. and Gadsby D. C. (2000) Severed molecules functionally define the boundaries of the cystic fibrosis transmembrane conductance regulator's NH(2)-terminal nucleotide binding domain. J. Gen. Physiol. 116: 163-180
49. Chen J., Cutler C., Jacques C., Boeuf G., Denamur E., Lecointre G., Mercier B., Cramb G. and Ferec C. (2001) A combined analysis of the cystic fibrosis transmembrane conductance regulator: implications for structure and disease models. Mol. Biol. Evol. 18: 1771-1788
50. Gentzsch M., Aleksandrov A., Aleksandrov L. and Riordan J. R. (2002) Functional analysis of the C-terminal boundary of the second nucleotide binding domain of the cystic fibrosis transmembrane conductance regulator and structural implications. Biochem. J. 366: 541-548
51. Zeltwanger S., Wang F., Wang G.-T., Gillis K. and Hwang T.-C. (1999) Gating of cystic fibrosis transmembrane conductance regulator chloride channels by adenosine triphosphate hydrolysis: quantitative analysis of a cyclic gating scheme. J. Gen. Physiol. 113: 541-554
52. Hwang T.-C., Nagel G., Narin A. and Gadsby D. C. (1994) Regulation of gating of CFTR Cl channels by phosphorylation and hydrolysis. Proc. Natl. Acad. Sci. USA 91: 4698-4702
53. Gunderson K. and Kopito R. (1994) Conformational states of CFTR associated with channel gating: the role of ATP binding and hydrolysis. Cell 82: 231-239
54. Aleksandrov L., Aleksandrov A., Chang X.-B. and Riordan J. R. (2002) The first nucleotide binding domain of cystic fibrosis transmembrane conductance is a site of stable nucleotide interaction, whereas the second is a site of rapid turnover. J. Biol. Chem. 277: 15419-15425
55. Basso C., Vergani P., Nairn A. and Gadsby D. (2003) Prolonged nonhydrolytic interaction of nucleotide with CFTR's NH2-terminal nucleotide binding domain and its role in channel gating. J. Gen. Physiol. 122: 333-348
56. Ueda K., Inagaki N. and Seino S. (1997) MgADP antagonism to Mg2+ independent ATP binding of the sulfonylurea receptor SUR1. J. Biol. Chem. 272: 22983-22986
57. Matsuo M., Kioki N., Amachi T. and Ueda K. (1999) ATP-binding properties of the nucleotide-binding folds of SUR1. J. Biol. Chem. 274: 37479-37482
58. Matsuo M., Tanabe K., Kioki N., Amachi T. and Ueda K. (2000) Different binding properties and affinities for ATP and ADP among sulfonylurea receptor subtypes, SUR1, SUR2A, and SUR2B. J. Biol. Chem. 275: 21111-21114
59. Gao M., Cui H., Loe D., Grant C., Almquist K., Cole S. et al. (2000) Comparison of the functional characteristics of the nucleotide binding domains of multidrug resistance protein 1. J. Biol. Chem. 275: 13098-13108
60. Hou Y., Cui L., Riordan J. R. and Chang X.-B. (2000) Allosteric interactions between the two non-equivalent nucleotide binding domains of multidrug resistance protein MRP1. J. Biol. Chem. 275: 20280-20287
61. - channel by its R domain. J. Biol. Chem. 276: 7689-7692
62. Winter M. and Welsh M. (1997) Stimulation of CFTR activity by its phosphorylated R domain. Nature 389: 294-296
63. Wang W., He Z., O'Shaughnessy T., Rux J. and Reenstra W (2002) Domain-domain associations in cystic fibrosis transmembrane conductance regulator. Am. J. Physiol. Cell Physiol. 282: C1170-1180
64. Rowntree R. and Harris A. (2003) The phenotypic consequences of CFTR mutations. Ann. Hum. Genet. 67: 471-485
65. Logan J., Hiestand D., Daram P., Huang Z., Muccio D., Hartman J. et al. (1994) Cystic fibrosis transmembrane conductance regulator mutations that disrupt nucleotide binding. J. Clin. Invest. 94: 228-236
66. Jones P. and George A. (2002) Mechanism of ABC transporters: a molecular dynamics simulation of a well characterized nucleotide-binding subunit. Proc. Natl. Acad. Sci. USA 99: 12639-12644