Thermal stability of chicken brain a-spectrin repeat 17: A spectroscopic study

Journal of Biomolecular NMR

Volumn 53, Issue 2, 2012, Pages 71-83

  Brenner, Annette K ^a   Kieffer, Bruno ^b   Travé, Gilles ^c   Frøystein, Nils Age ^a   Raae, Arnt J ^a  

^a UNIVERSITY OF BERGEN   (Norway)

^b INSTITUT DE GÉNÉTIQUE ET DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

^c UNIVERSITÉ DE STRASBOURG   (France)

Author keywords

Conformation; Dynamics; Heteronuclear NMR spectroscopy; Spectrin repeats; Stability

Indexed keywords

FODRIN; TRYPTOPHAN; VALINE;

ALPHA HELIX; ARTICLE; BRAIN; CARBOXY TERMINAL SEQUENCE; CHICKEN; CONFORMATIONAL TRANSITION; NITROGEN NUCLEAR MAGNETIC RESONANCE; NUCLEAR OVERHAUSER EFFECT; PRIORITY JOURNAL; PROTEIN STRUCTURE; TEMPERATURE; THERMOSTABILITY; X RAY CRYSTALLOGRAPHY;

AMINO ACID SEQUENCE; ANIMALS; BRAIN; BRAIN CHEMISTRY; CHICKENS; DEUTERIUM EXCHANGE MEASUREMENT; HOT TEMPERATURE; MOLECULAR SEQUENCE DATA; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN CONFORMATION; PROTEIN STABILITY; PROTEIN STRUCTURE, TERTIARY; REPETITIVE SEQUENCES, AMINO ACID; SEQUENCE ALIGNMENT; SPECTRIN;

EID: 84865161574     PISSN: 09252738     EISSN: 15735001     Source Type: Journal    
DOI: 10.1007/s10858-012-9620-y     Document Type: Article

References (52)

1. An XL, Zhang XH, Salomao M, Guo XH, Yang Y, Wu Y, Gratzer W, Baines AJ, Mohandas N (2006) Thermal stabilities of brain spectrin and the constituent repeats of subunits. Biochemistry 45(45):13670-13676. doi:10.1021/bi061368x (Pubitemid 44748513)
2. Batey S, Scott KA, Clarke J (2006) Complex folding kinetics of a multidomain protein. Biophys J 90(6):2120-2130. doi:10.1529/biophysj.105.072710
3. Bennett V, Gilligan DM (1993) The spectrin-based membrane skeleton and micron-scala organization of the plasma-membrane. Annu Rev Cell Biol 9:27-66
4. Carugo KD, Banuelos S, Saraste M (1997) Crystal structure of a calponin homology domain. Nat Struct Biol 4(3):175-179 (Pubitemid 27111161)
5. Davis AL, Keeler J, Laue ED, Moskau D (1992) Experiments for recording pure-absorption heteronuclear correlation spectra using pulsed field gradients. J Magn Reson 98(1):207-216
6. de la Torre JG, Huertas ML, Carrasco B (2000) HYDRONMR: prediction of NMR relaxation of globular proteins from atomiclevel structures and hydrodynamic calculations. J Magn Reson 147(1):138-146. doi:10.1006/jmre.2000.2170
7. Delaglio F, Grzesiek S, Vuister GW, Zhu G, Pfeifer J, Bax A (1995) NMRPipe - A multidimensional spectral processing system based on UNIX Pipes. J Biomol NMR 6(3):277-293
8. Diercks T, Coles M, Kessler H (1999) An efficient strategy for assignment of cross-peaks in 3D heteronuclear NOESY experiments. J Biomol NMR 15(2):177-180
9. Dosset P, Hus JC, Blackledge M, Marion D (2000) Efficient analysis of macromolecular rotational diffusion from heteronuclear relaxation data. J Biomol NMR 16(1):23-28 (Pubitemid 30114721)
10. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32(5): 1792-1797. doi:10.1093/nar/gkh340 (Pubitemid 38832724)
11. Fung LWM, Lu HZ, Hjelm RP, Johnson ME (1986) Selective detection of rapid motions in spectrin by NMR. FEBS Lett 197(1-2):234-238 (Pubitemid 16037926)
12. Fung LWM, Lu HZ, Hjelm RP, Johnson ME (1989) Quantitative detection of rapid motions in spectrin by NMR. Life Sci 44(11): 735-740 (Pubitemid 19065974)
13. Grum VL, Li DN, MacDonald RI, Mondragon A (1999) Structures of two repeats of spectrin suggest models of flexibility. Cell 98(4): 523-535 (Pubitemid 29402489)
14. Grzesiek S, Bax A (1993a) Amino-acid type determination in the sequential assignment procedure of uniformly C-13/N-15- enriched proteins. J Biomol NMR 3(2):185-204
15. Grzesiek S, Bax A (1993b) The importance of not saturating H2O in protein NMR-application to sensitivity enhancement and NOE measurements. J Amer Chem Soc 115(26):12593-12594
16. Grzesiek S, Anglister J, Bax A (1993) Correlation of backbone amide and aliphatic side-chain resonances in C-13/N-15-enriched proteins by isotropic mixing of C-13 magnetization. J Magn Reson B 101(1):114-119
17. Harris RK, Becker ED, De Menezes SMC, Granger P, Hoffman RE, Zilm KW (2008) Further conventions for NMR shielding and chemical shifts (IUPAC recommendations 2008). Pure Appl Chem 80(1):59-84. doi:10.1351/pac200880010059
18. Kamath U, Shriver JW (1989) Characteriazation of thermotropic state changes in myosin subfragment-1 and heavy-meromyosin by UV difference spectroscopy. J Biol Chem 264(10):5586-5592 (Pubitemid 19098015)
19. Kay LE, Torchia DA, Bax A (1989) Backbone dynamics of proteins as studied by N-15 inverse detected heteronuclear NMRspectroscopy- application to staphylococcal nuclease. Biochemistry 28(23):8972-8979 (Pubitemid 19283459)
20. Keller RLJ (2005) Optimizing the process of nuclear magnetic resonance spectrum analysis and computer aided resonance assignment. ETH Zürich, Zürich
21. Kowalski K, Merkel AL, Booker GW (2004) H-1, C-13 and N-15 resonance assignments of the third spectrin repeat of alphaactinin- 4. J Biomol NMR 29(4):533-534. doi:10.1023/b:jnmr.0000034342.20537.01 (Pubitemid 38967365)
22. Kusunoki H, Macdonald RI, Mondragon A (2004a) Structural insights into the stability and flexibility of unusual erythroid spectrin repeats. Structure 12(4):645-656. doi:10.1016/j.str.2004.02.022 (Pubitemid 38447167)
23. Kusunoki H, Minasov G, MacDonald RI, Mondragon A (2004b) Independent movement, dimerization and stability of tandem repeats of chicken brain alpha-spectrin. J Mol Biol 344(2): 495-511. doi:10.1016/j.jmb.2004.09.019 (Pubitemid 39441220)
24. Legardinier S, Legrand B, Raguenes-Nicol C, Bondon A, Hardy S, Tascon C, Le Rumeur E, Hubert JF (2009) A two-amino acid mutation encountered in Duchenne muscular dystrophy decreases stability of the rod domain 23 (R23) spectrin-like repeat of dystrophin. J Biol Chem 284(13):8813-8823. doi:10.1074/jbc.M805846200
25. Lipari G, Szabo A (1982a) Model-free approach to the interpretation of nuclear magnetic-resonance relaxation in macromolecules. 1. Theory and range of validity. JAmChem Soc 104(17):4546-4559
26. Lipari G, Szabo A (1982b) Model-free approach to the interpretation of nuclear magnetic-resonance relaxation in macromolecules. 2. Analysis of experimental results. J Am Chem Soc 104(17): 4559-4570
27. MacDonaldRI,MusacchioA,HolmgrenRA, SarasteM(1994) Invariant tryptophan at a shielded site promotes folding of the conformational unit of spectrin. Proc Natl Acad Sci 91(4):1299-1303
28. Montelione GT, Lyons BA, Emerson SD, Tashiro M (1992) An efficient triple resonance experiments using C-13 isotropic mixing for determining sequence-specific resonance assignments of isotopically-enriched proteins. J Am Chem Soc 114(27): 10974-10975
29. Musacchio A, Noble M, Pauptit R, Wierenga R, Saraste M (1992) Crystal-structure of a src-homology-3 (SH3) domain. Nature 359(6398):851-855
30. Pantazatos DP, MacDonald RI (1997) Site-directed mutagenesis of either the highly conserved Trp-22 or the moderately conserved Trp-95 to a large, hydrophobic residue reduces the thermodynamic stability of a spectrin repeating unit. J Biol Chem 272(34):21052-21059 (Pubitemid 27373962)
31. Park S, CaffreyMS, JohnsonME, FungLWM(2003) Solution structural studies on human erythrocyte alpha-spectrin tetramerization site. J Biol Chem 278(24):21837-21844. doi:10.1074/jbc.M30061 7200 (Pubitemid 36792589)
32. Parry DAD, Dixon TW, Cohen C (1992) Analysis of the 3-alpha-helix motif in the spectrin superfamily of proteins. Biophys J 61(4):858-867
33. Pascual J, Pfuhl M, Rivas G, Pastore A, Saraste M (1996) The spectrin repeat folds into a three-helix bundle in solution. FEBS Lett 383(3):201-207 (Pubitemid 26104061)
34. Pascual J, Pfuhl M, Walther D, Saraste M, Nilges M (1997) Solution structure of the spectrin repeat: a left-handed antiparallel triplehelical coiled-coil. J Mol Biol 273:740-751 (Pubitemid 27488814)
35. Sahr KE, Laurila P, Kotula L, Scarpa AL, Coupal E, Leto TL, Linnenbach AJ, Winkelmann JC, Speicher DW, Marchesi VT, Curtis PJ, Forget BG (1990) The complete cDNA and polypeptide sequences of human erythroid alpha-spectrin. J Biol Chem 265(8):4434-4443
36. Sattler M, Schleucher J, Griesinger C (1999) Heteronuclear multidimensional NMR experiments for the structure determination of proteins in solution employing pulsed field gradients. Prog Nucl Magn Reson Spectrosc 34(2):93-158 (Pubitemid 129595216)
37. Schanda P, Kupce E, Brutscher B (2005) SOFAST-HMQC experiments for recording two-dimensional heteronuclear correlation spectra of proteins within a few seconds. J Biomol NMR 33(4): 199-211. doi:10.1007/s10858-005-4425-x (Pubitemid 43118574)
38. Schubert M, Smalla M, Schmieder P, Oschkinat H (1999) MUSIC in triple-resonance experiments: amino acid type-selective H-1-N-15 correlations. J Magn Reson 141(1):34-43 (Pubitemid 129608894)
39. Schubert M, Oschkinat H, Schmieder P (2001a) MUSIC and aromatic residues: Amino acid type-selective H-1-N-15 correlations, III. J Magn Reson 153(2):186-192. doi:10.1006/jmre.2001.2447
40. Schubert M, Oschkinat H, Schmieder P (2001b) MUSIC, selective pulses, and tuned delays: Amino acid type-selective H-1-N-15 correlations, II. J Magn Reson 148(1):61-72
41. Travé G, Lacombe PJ, Pfuhl M, Saraste M, Pastore A (1995) Molecular mechanism of the calcium-induced conformational change in the spectrin EF-hands. EMBO J 14(20):4922-4931
42. Vranken WF, Boucher W, Stevens TJ, Fogh RH, Pajon A, Llinas P, Ulrich EL, Markley JL, Ionides J, Laue ED (2005) The CCPN data model for NMR spectroscopy: development of a software pipeline. Proteins Struct Funct Bioinform 59(4):687-696. doi: 10.1002/prot.20449 (Pubitemid 40695845)
43. Vuister GW, Bax A (1993) Quantitative J correlation-a new approach for measuring homonuclear 3-bond J(H(N)H(alpha)) coupling-constants in N-15-enriched proteins. J Am Chem Soc 115(17):7772-7777
44. Wang YJ, Jardetzky O (2002) Probability-based protein secondary structure identification using combined NMR chemical-shift data. Protein Sci 11(4):852-861. doi:10.1110/ps.3180102 (Pubitemid 34241293)
45. Waterhouse AM, Procter JB, Martin DMA, Clamp M, Barton GJ (2009) Jalview Version 2-a multiple sequence alignment editor and analysis workbench. Bioinformatics 25(9):1189-1191. doi: 10.1093/bioinformatics/btp033
46. Weisemann R, Ruterjans H, Schwalbe H, Schleucher J, Bermel W, Griesinger C (1994) Determination of H(N), H-alpha and H(N), C0 coupling-constants in C-13, N-15-labeled proteins. J Biomol NMR 4(2):231-240
47. Winkelmann JC, Costa FF, Linzie BL, Forget BG (1990) Betaspectrin in human skeletal-muscle-tissue-specific differential processing of 30 beta-spectrin pre-messenger-RNA generates a beta-spectrin isoform with a unique carboxyl terminus. J Biol Chem 265(33):20449-20454 (Pubitemid 120014030)
48. Wishart DS, Sykes BD, Richards FM (1991) Relationship between nuclear-magnetic-resonance chemical-shift and protein secondary structure. J Mol Biol 222(2):311-333 (Pubitemid 121004009)
49. Wishart DS, Bigam CG, Yao J, Abildgaard F, Dyson HJ, Oldfield E, Markley JL, Sykes BD (1995) H-1, C-13 and N-15 chemical-shift referencing in biomolecular NMR. J Biomol NMR 6(2):135-140
50. Wüthrich K, Billeter M, Braun W (1984) Polypeptide secondary structure determination by nuclear magnetic-resonance observation of short proton proton distances. J Mol Biol 180(3):715-740
51. Yamazaki T, Formankay JD, Kay LE (1993) 2-Dimensional NMR experiments for correlating C-13-beta and H-1-delta/epsilon chemical-shifts of aromatic residues in C-13-labeled proteins via scalar couplings. J Am Chem Soc 115(23):11054-11055
52. Yan Y, Winograd E, Viel A, Cronin T, Harrison SC, Branton D (1993) Crystal-structure of the repetetive segments of spectrin. Science 262:2027-2030