Functional and pharmacological induced structural changes of the cystic fibrosis transmembrane conductance regulator in the membrane solved using SAXS

Cellular and Molecular Life Sciences

Volumn 72, Issue 7, 2015, Pages 1363-1375

  Baroni, Debora ^a   Zegarra Moran, Olga ^b   Moran, Oscar ^a  

^a CNR   (Italy)

^b G GASLINI INSTITUTE   (Italy)

Author keywords

CFTR; Cystic fibrosis; Membrane structure; Phosphorylation; Small angle X ray scattering; F508 rescue

Indexed keywords

ABC TRANSPORTER; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; MEMBRANE PROTEIN; PROTEIN; SODIUM CHLORIDE; WATER; 1,3 BENZODIOXOLE DERIVATIVE; AMINOPYRIDINE DERIVATIVE; LUMACAFTOR; MUTANT PROTEIN;

3T3 CELL LINE; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; CYSTIC FIBROSIS; ENDOPLASMIC RETICULUM MEMBRANE; GENE MUTATION; GENETIC TRANSFECTION; LIPID BILAYER; LOW TEMPERATURE; MEMBRANE STRUCTURE; MICROSOME MEMBRANE; MOUSE; NONHUMAN; PHARMACOLOGICAL PROCEDURES; PROTEIN ASSEMBLY; PROTEIN CONFORMATION; PROTEIN DEPHOSPHORYLATION; PROTEIN FAMILY; PROTEIN PHOSPHORYLATION; PROTEIN TRANSPORT; WATER TRANSPORT; X RAY CRYSTALLOGRAPHY; ALGORITHM; ANIMAL; CELL MEMBRANE; CHEMICAL STRUCTURE; CHEMISTRY; DRUG EFFECTS; ELECTRON MICROSCOPY; GENETICS; HUMAN; INTRACELLULAR MEMBRANE; METABOLISM; MICROSOME; MUTATION; PHOSPHORYLATION; PROCEDURES; SMALL ANGLE SCATTERING; ULTRASTRUCTURE; WESTERN BLOTTING; X RAY DIFFRACTION;

ALGORITHMS; AMINOPYRIDINES; ANIMALS; BENZODIOXOLES; BLOTTING, WESTERN; CELL MEMBRANE; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; HUMANS; INTRACELLULAR MEMBRANES; MICE; MICROSCOPY, ELECTRON; MICROSOMES; MODELS, MOLECULAR; MUTANT PROTEINS; MUTATION; NIH 3T3 CELLS; PHOSPHORYLATION; PROTEIN CONFORMATION; SCATTERING, SMALL ANGLE; TRANSFECTION; X-RAY DIFFRACTION;

EID: 84930913259     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-014-1747-4     Document Type: Article

References (61)

1. Awayn NH, Rosenberg MF, Kamis AB, Aleksandrov LA, Riordan JR, Ford RC (2005) Crystallographic and single-particle analyses of native- and nucleotide-bound forms of the cystic fibrosis transmembrane conductance regulator (CFTR) protein. Biochem Soc Trans 33:996-999
2. Rosenberg MF, Kamis AB, Aleksandrov LA, Ford RC, Riordan JR (2004) Purification and crystallization of the cystic fibrosis transmembrane conductance regulator (CFTR). J Biol Chem 279:39051-39057
3. Rosenberg MF, O'Ryan LP, Hughes G, Zhao Z, Aleksandrov LA, Riordan JR, Ford RC (2011) The cystic fibrosis transmembrane conductance regulator (CFTR): three-dimensional structure and localization of a channel gate. J Biol Chem 286:42647-42654
4. Zhang L, Aleksandrov LA, Zhao Z, Birtley JR, Riordan JR, Ford RC (2009) Architecture of the cystic fibrosis transmembrane conductance regulator protein and structural changes associated with phosphorylation and nucleotide binding. J Struct Biol 167:242-251
5. Marasini C, Galeno L, Moran O (2013) A SAXS-based ensemble model of the native and phosphorylated regulatory domain of the CFTR. Cell Mol Life Sci 70:923-933
6. Galeno L, Galfrè E, Moran O (2011) Small-angle X-ray scattering study of the ATP modulation of the structural features of the nucleotide binding domains of the CFTR in solution. Eur Biophys J 40:811-824
7. Galfrè E, Galeno L, Moran O (2012) A potentiator induces conformational changes on the recombinant CFTR nucleotide binding domains in solution. Cell Mol Life Sci 69:3701-3713
8. Atwell S, Brouillette CG, Conners K, Emtage S, Gheyi T, Guggino WB, Hendle J, Hunt JF, Lewis HA, Lu F, Protasevich II, Rodgers LA, Romero R, Wasserman SR, Weber PC, Wetmore D, Zhang FF, Zhao X (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
9. Lewis HA, Buchanan SG, Burley SK, Conners K, Dickey M, Dorwart M, Fowler R, Gao X, Guggino WB, Hendrickson WA, Hunt JF, Kearins MC, Lorimer D, Maloney PC, Post KW, Rajashankar KR, Rutter ME, Sauder JM, Shriver S, Thibodeau PH, Thomas PJ, Zhang M, Zhao X, Emtage S (2004) Structure of nucleotide-binding domain 1 of the cystic fibrosis transmembrane conductance regulator. EMBO J 23:282-293
10. Lewis HA, Zhao X, Wang C, Sauder JM, Rooney I, Noland BW, Lorimer D, Kearins MC, Conners K, Condon B, Maloney PC, Guggino WB, Hunt JF, Emtage S (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
11. Mertens HDT, Svergun DI (2010) Structural characterization of proteins and complexes using small-angle X-ray solution scattering. J Struct Biol 172:128-141
12. Stuhrmann HB (2008) Small-angle scattering and its interplay with crystallography, contrast variation in SAXS and SANS. Acta Crystallogr A 64:181-191
13. Sano Y, Inoue H, Kajiwara K, Hiragi Y, Isoda S (1997) Structural analysis of A-protein of cucumber green mottle mosaic virus and tobacco mosaic virus by synchrotron small-angle X-ray scattering. J Protein Chem 16:151-159
14. Svergun DI, Burkhardt N, Pedersen JS, Koch MH, Volkov VV, Kozin MB, Meerwink W, Stuhrmann HB, Diedrich G, Nierhaus KH (1997) Solution scattering structural analysis of the 70 S Escherichia coli ribosome by contrast variation. II. A model of the ribosome and its RNA at 3.5 nm resolution. J Mol Biol 271:602-618
15. Castorph S, Riedel D, Arleth L, Sztucki M, Jahn R, Holt M, Salditt T (2010) Structure parameters of synaptic vesicles quantified by small-angle x-ray scattering. Biophys J 98:1200-1208
16. Aleksandrov L, Mengos A, Chang X, Aleksandrov A, Riordan JR (2001) Differential interactions of nucleotides at the two nucleotide binding domains of the cystic fibrosis transmembrane conductance regulator. J Biol Chem 276:12918-12923
17. Gunderson KL, Kopito RR (1994) Effects of pyrophosphate and nucleotide analogs suggest a role for ATP hydrolysis in cystic fibrosis transmembrane regulator channel gating. J Biol Chem 269:19349-19353
18. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248-254
19. Körschen HG, Yildiz Y, Raju DN, Schonauer S, Bönigk W, Jansen V, Kremmer E, Kaupp UB, Wachten D (2013) The non-lysosomal β-glucosidase GBA2 is a non-integral membrane-associated protein at the endoplasmic reticulum (ER) and Golgi. J Biol Chem 288:3381-3393
20. Kong E, Peng S, Chandra G, Sarkar C, Zhang Z, Bagh MB, Mukherjee AB (2013) Dynamic palmitoylation links cytosol-membrane shuttling of acyl-protein thioesterase-1 and acyl-protein thioesterase-2 with that of proto-oncogene H-ras product and growth-associated protein-43. J Biol Chem 288:9112-9125
21. Mondini A, Sassone F, Civello DA, Garavaglia ML, Bazzini C, Rodighiero S, Vezzoli V, Conti F, Torielli L, Capasso G, Paulmichl M, Meyer G (2012) Hypertension-linked mutation of α-adducin increases CFTR surface expression and activity in HEK and cultured rat distal convoluted tubule cells. PLoS One 7:e52014
22. Nakamura N, Rabouille C, Watson R, Nilsson T, Hui N, Slusarewicz P, Kreis TE, Warren G (1995) Characterization of a cis-Golgi matrix protein, GM130. J Cell Biol 131:1715-1726
23. Guinier A (1994) X-ray Diffraction in Crystals, Imperfect Crystals, and Amorphous Bodies. Courier Dover Publications, San Francisco and London
24. Brzustowicz MR, Brunger AT (2005) X-ray scattering from unilamellar lipid vesicles. J Appl Cryst 38:126-131
25. Wibo M, Amar-Costesec A, Berthet J, Beaufay H (1971) Electron microscope examination of subcellular fractions. 3. Quantitative analysis of the microsomal fraction isolated from rat liver. J Cell Biol 51:52-71
26. Lavoie C, Lanoix J, Kan FW, Paiement J (1996) Cell-free assembly of rough and smooth endoplasmic reticulum. J Cell Sci 109(Pt 6):1415-1425
27. Castorph S, Arleth L, Sztucki M, Vainio U, Ghosh SK, Holt M, Jahn R, Salditt T (2010) Synaptic vesicles studied by SAXS: derivation and validation of a model form factor. J Phys Conf Ser 247:012015
28. Baroni D, Zegarra-Moran O, Svensson A, Moran O (2014) Direct interaction of a CFTR potentiator and a CFTR corrector with phospholipid bilayers. Eur Biophys J 43:341-346
29. Pabst G, Rappolt M, Amenitsch H, Laggner P (2000) Structural information from multilamellar liposomes at full hydration: full q-range fitting with high-quality X-ray data. Phys Rev E 62:4000-4009
30. De Duve C (1971) Tissue fractionation past and present. J Cell Biol 50:20d-55d
31. Palade GE, Siekevits P (1956) Liver microsomes: an integrated morphological and biochemical study. J Biophys Biochem Cytol. 2:171-200
32. Blouin A, Bolender RP, Weibel ER (1977) Distribution of organelles and membranes between hepatocytes and nonhepatocytes in the rat liver parenchyma. A stereological study. J Cell Biol 72:441-455
33. Croze EM, Morré DJ (1984) Isolation of plasma membrane, golgi apparatus, and endoplasmic reticulum fractions from single homogenates of mouse liver. J Cell Physiol 119:46-57
34. Saeger W, Rübenach-Gerz K, Caselitz J, Lüdecke DK (1987) Electron microscopical morphometry of GH producing pituitary adenomas in comparison with normal GH cells. Virchows Arch A Pathol Anat Histopathol 411:467-472
35. Navas P, Nowack DD, Morré DJ (1989) Isolation of purified plasma membranes from cultured cells and hepatomas by two-phase partition and preparative free-flow electrophoresis. Cancer Res 49:2147-2156
36. Moran O (2014) On the structural organization of the intracellular domains of CFTR. Int J Biochem Cell Biol 52C:7-14
37. Wang X, Venable J, LaPointe P, Hutt DM, Koulov AV, Coppinger J, Gurkan C, Kellner W, Matteson J, Plutner H, Riordan JR, Kelly JW, Yates JR, Balch WE (2006) Hsp90 cochaperone Aha1 downregulation rescues misfolding of CFTR in cystic fibrosis. Cell 127:803-815
38. Ahner A, Gong X, Frizzell RA (2013) Cystic fibrosis transmembrane conductance regulator degradation: cross-talk between the ubiquitylation and SUMOylation pathways. FEBS J 280:4430-4438
39. Edelman A (2014) Cytoskeleton and CFTR. Int J Biochem Cell Biol 52C:68-72
40. Pranke IM, Sermet-Gaudelus I (2014) Biosynthesis of cystic fibrosis transmembrane conductance regulator. Int J Biochem Cell Biol 52C:26-38
41. 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
42. Bouwstra JA, Gooris GS, Bras W, Talsma H (1993) Small angle X-ray scattering: possibilities and limitations in characterization of vesicles. Chem Phys Lipids 64:83-98
43. Hirai M, Iwase H, Hayakawa T, Koizumi M, Takahashi H (2003) Determination of asymmetric structure of ganglioside-DPPC mixed vesicle using SANS, SAXS, and DLS. Biophys J 85:1600-1610
44. Herbette L, Scarpa A, Blasie JK, Wang CT, Saito A, Fleischer S (1981) Comparison of the profile structures of isolated and reconstituted sarcoplasmic reticulum membranes. Biophys J 36:47-72
45. Chang XB, Hou YX, Riordan JR (1997) ATPase activity of purified multidrug resistance-associated protein. J Biol Chem 272:30962-30968
46. Rich DP, Berger HA, Cheng SH, Travis SM, Saxena M, Smith AE, Welsh MJ (1993) Regulation of the cystic fibrosis transmembrane conductance regulator Cl- channel by negative charge in the R domain. J Biol Chem 268:20259-20267
47. Rich DP, Gregory RJ, Anderson MP, Manavalan P, Smith AE, Welsh MJ (1991) Effect of deleting the R domain on CFTR-generated chloride channels. Science 253:205-207
48. Dulhanty AMRJ (1994) Phosphorylation by cAMP-dependent protein kinase causes a conformational change in the R domain of the cystic fibrosis transmembrane conductance regulator. Biochemistry 33:4072-4079
49. Kanelis V, Hudson RP, Thibodeau PH, Thomas PJ, Forman-Kay JD (2010) NMR evidence for differential phosphorylation-dependent interactions in WT and DeltaF508 CFTR. EMBO J 29:263-277
50. Marasini C, Galeno L, Moran O (2012) Thermodynamic study of the native and phosphorylated regulatory domain of the CFTR. Biochem Biophys Res Commun 423:549-552
51. Baker JMR, Hudson RP, Kanelis V, Choy W, Thibodeau PH, Thomas PJ, Forman-Kay JD (2007) CFTR regulatory region interacts with NBD1 predominantly via multiple transient helices. Nat Struct Mol Biol 14:738-745
52. Lukacs GL, Chang XB, Bear C, Kartner N, Mohamed A, Riordan JR, Grinstein S (1993) 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 268:21592-21598
53. Sharma M, Benharouga M, Hu W, Lukacs GL (2001) Conformational and temperature-sensitive stability defects of the delta F508 cystic fibrosis transmembrane conductance regulator in post-endoplasmic reticulum compartments. J Biol Chem 276:8942-8950
54. Thibodeau PH, Richardson JM, Wang W, Millen L, Watson J, Mendoza JL, Du K, Fischman S, Senderowitz H, Lukacs GL, Kirk K, Thomas PJ (2010) The cystic fibrosis-causing mutation deltaF508 affects multiple steps in cystic fibrosis transmembrane conductance regulator biogenesis. J Biol Chem 285:35825-35835
55. 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
56. Pedemonte N, Lukacs GL, Du K, Caci E, Zegarra-Moran O, Galietta LJ, Verkman AS (2005) Small-molecule correctors of defective DeltaF508-CFTR cellular processing identified by high-throughput screening. J Clin Invest. 115:2564-2571 Epub 2005 Aug 25
57. Jurkuvenaite A, Chen L, Bartoszewski R, Goldstein R, Bebok Z, Matalon S, Collawn JF (2010) Functional stability of rescued delta F508 cystic fibrosis transmembrane conductance regulator in airway epithelial cells. Am J Respir Cell Mol Biol 42:363-372
58. Rowe SM, Pyle LC, Jurkevante A, Varga K, Collawn J, Sloane PA, Woodworth B, Mazur M, Fulton J, Fan L, Li Y, Fortenberry J, Sorscher EJ, Clancy JP (2010) DeltaF508 CFTR processing correction and activity in polarized airway and non-airway cell monolayers. Pulm Pharmacol Ther 23:268-278
59. Dalemans W, Barbry P, Champigny G, Jallat S, Dott K, Dreyer D, Crystal RG, Pavirani A, Lecocq JP, Lazdunski M (1991) Altered chloride ion channel kinetics associated with the delta F508 cystic fibrosis mutation. Nature 354:526-528
60. Haws CM, Nepomuceno IB, Krouse ME, Wakelee H, Law T, Xia Y, Nguyen H, Wine JJ (1996) Delta F508-CFTR channels: kinetics, activation by forskolin, and potentiation by xanthines. Am J Physiol 270:C1544-C1555
61. Jih K, Li M, Hwang T, Bompadre SG (2011) The most common cystic fibrosis-associated mutation destabilizes the dimeric state of the nucleotide-binding domains of CFTR. J Physiol 589:2719-2731