Mechanism of assembly of the non-covalent spectrin tetramerization domain from intrinsically disordered partners

Journal of Molecular Biology

Volumn 426, Issue 1, 2014, Pages 21-35

  Hill, Stephanie A ^a,b   Kwa, Lee Gyan ^a   Shammas, Sarah L ^a   Lee, Jennifer C ^b   Clarke, Jane ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

Author keywords

IDP; natively unfolded protein; protein engineering; protein folding; value analysis

Indexed keywords

SPECTRIN; SPECTRIN BETA SUBUNIT; TETRAMER; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOSKELETON; DIMERIZATION; ERYTHROCYTE; MOLECULAR DOCKING; MOLECULAR MECHANICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ENGINEERING; POLYMERIZATION; PROTEIN STRUCTURE; TETRAMERIZATION;

EID: 84890859432     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2013.08.027     Document Type: Article

References (60)

1. M. Salomao, X.L. An, X.H. Guo, W.B. Gratzer, N. Mohandas, and A.J. Baines Mammalian alpha I-spectrin is a neofunctionalized polypeptide adapted to small highly deformable erythrocytes Proc Natl Acad Sci USA 103 2006 643 648
2. A.J. Baines Evolution of spectrin function in cytoskeletal and membrane networks Biochem Soc Trans 37 2009 796 803
3. D.M. Sridharan, L.W. McMahon, and M.W. Lambert alpha II-Spectrin interacts with five groups of functionally important proteins in the nucleus Cell Biol Int 30 2006 866 878
4. P. Gascard, and N. Mohandas New insights into functions of erythroid proteins in nonerythroid cells Curr Opin Hematol 7 2000 123 129
5. K.G. Young, and R. Kothary Spectrin repeat proteins in the nucleus BioEssays 27 2005 144 152
6. C. Ayala-Grosso, J. Tam, S. Roy, S. Xanthoudakis, D. Da Costa, and D.W. Nicholson et al. Caspase-3 cleaved spectrin colocalizes with neurofilament-immunoreactive neurons in Alzheimer's disease Neuroscience 141 2006 863 874
7. M.G. Voas, D.A. Lyons, S.G. Naylor, N. Arana, M.N. Rasband, and W.S. Talbot alpha II-spectrin is essential for assembly of the nodes of Ranvier in myelinated axons Curr Biol 17 2007 562 568
8. T.W. Tillack, S.L. Marchesi, V.T. Marchesi, and E. Steers A comparative study of spectrin. A protein isolated from red blood cell membranes Biochim Biophys Acta 200 1970 125 131
9. V. Bennett, and L.S. Chen Ankyrins and cellular targeting of diverse membrane proteins to physiological sites Curr Opin Cell Biol 13 2001 61 67
10. E. van den Akker, T.J. Satchwell, R.C. Williamson, and A.M. Toye Band 3 multiprotein complexes in the red cell membrane; of mice and men Blood Cells Mol Dis 45 2010 1 8
11. A.J. Baines Evolution of the spectrin-based membrane skeleton Transfus Clin Biol 17 2010 95 103
12. D.W. Speicher, and V.T. Marchesi Erythrocyte spectrin is comprised of many homologous triple helical segments Nature 311 1984 177 180
13. J. Pascual, M. Pfuhl, D. Walther, M. Saraste, and M. Nilges Solution structure of the spectrin repeat: a left-handed antiparallel triple-helical coiled-coil J Mol Biol 273 1997 740 751
14. V.L. Grum, D.N. Li, R.I. MacDonald, and A. Mondragon Structures of two repeats of spectrin suggest models of flexibility Cell 98 1999 523 535
15. K.E. Sahr, T.L. Coetzer, L.S. Moy, L.H. Derick, A.H. Chishti, and P. Jarolim et al. Spectrin cagliari. an Ala → Gly substitution in helix 1 of beta spectrin repeat 17 that severely disrupts the structure and self-association of the erythrocyte spectrin heterodimer J Biol Chem 268 1993 22656 22662
16. D.W. Speicher, T.M. Desilva, K.D. Speicher, J.A. Ursitti, P. Hembach, and L. Weglarz Location of the human red-cell spectrin tetramer binding-site and detection of a related closed hairpin loop dimer using proteolytic footprinting J Biol Chem 268 1993 4227 4235
17. T.M. Desilva, K.C. Peng, K.D. Speicher, and D.W. Speicher Analysis of human red-cell spectrin tetramer (head-to-head) assembly using complementary univalent peptides Biochemistry 31 1992 10872 10878
18. S. Mehboob, B.H. Luo, B.M. Patel, and L.W.M. Fung alpha beta spectrin coiled coil association at the tetramerization site Biochemistry 40 2001 12457 12464
19. J.A. Ursitti, L. Kotula, T.M. DeSilva, P.J. Curtis, and D.W. Speicher Mapping the human erythrocyte beta-spectrin dimer initiation site using recombinant peptides and correlation of its phasing with the alpha-actinin dimer site J Biol Chem 271 1996 6636 6644
20. G.E. Begg, S.L. Harper, M.B. Morris, and D.W. Speicher Initiation of spectrin dimerization involves complementary electrostatic interactions between paired triple-helical bundles J Biol Chem 275 2000 3279 3287
21. B.H. Luo, S. Mehboob, M.G. Hurtuk, N.H. Pipalia, and L.W.M. Fung Important region in the beta-spectrin C-terminus for spectrin tetramer formation Eur J Haematol 68 2002 73 79
22. F. Long, D. McElheny, S.K. Jiang, S. Park, M.S. Caffrey, and L.W.M. Fung Conformational change of erythroid alpha-spectrin at the tetramerization site upon binding beta-spectrin Protein Sci 16 2007 2519 2530
23. G. Nicolas, S. Pedroni, C. Fournier, H. Gautero, C. Craescu, and D. Dhermy et al. Spectrin self-association site: characterization and study of beta-spectrin mutations associated with hereditary elliptocytosis Biochem J 332 1998 81 89
24. S. Park, M.S. Caffrey, M.E. Johnson, and L.W.M. Fung Solution structural studies on human erythrocyte alpha-spectrin tetramerization site J Biol Chem 278 2003 21837 21844
25. J.J. Ipsaro, S.L. Harper, T.E. Messick, R. Marmorstein, A. Mondragon, and D.W. Speicher Crystal structure and functional interpretation of the erythrocyte spectrin tetramerization domain complex Blood 115 2010 4843 4852
26. S. Mehboob, Y. Song, M. Witek, F. Long, B.D. Santarsiero, and M.E. Johnson et al. Crystal structure of the nonerythroid alpha-spectrin tetramerization site reveals differences between erythroid and nonerythroid spectrin tetramer formation J Biol Chem 285 2010 14572 14584
27. Z.S. Zhang, S.A. Weed, P.G. Gallagher, and J.S. Morrow Dynamic molecular modeling pathogenic mutations spectrin self-association domain Blood 98 2001 1645 1653
28. C. Antoniou, V.Q. Lam, and L.W.M. Fung Conformational changes at the tetramerization site of erythroid alpha-spectrin upon binding beta-spectrin: a spin label EPR study Biochemistry 47 2008 10765 10772
29. V.N. Uversky, and A.K. Dunker Understanding protein non-folding Biochim Biophys Acta Proteins Proteomics 1804 2010 1231 1264
30. K.K. Turoverov, I.M. Kuznetsova, and V.N. Uversky The protein kingdom extended: ordered and intrinsically disordered proteins, their folding, supramolecular complex formation, and aggregation Prog Biophys Mol Biol 102 2010 73 84
31. K. Teilum, J.G. Olsen, and B.B. Kragelund Functional aspects of protein flexibility Cell Mol Life Sci 66 2009 2231 2247
32. P.E. Wright, and H.J. Dyson Linking folding and binding Curr Opin Struct Biol 19 2009 31 38
33. H.J. Dyson, and P.E. Wright Coupling of folding and binding for unstructured proteins Curr Opin Struct Biol 12 2002 54 60
34. M. Kjaergaard, K. Teilum, and F.M. Poulsen Conformational selection in the molten globule state of the nuclear coactivator binding domain of CBP Proc Natl Acad Sci USA 107 2010 12535 12540
35. C.J. Oldfield, Y.G. Cheng, M.S. Cortese, P. Romero, V.N. Uversky, and A.K. Dunker Coupled folding and binding with alpha-helix-forming molecular recognition elements Biochemistry 44 2005 12454 12470
36. P. Maillet, N. Alloisio, L. Morle, and J. Delaunay Spectrin mutations in hereditary elliptocytosis and hereditary spherocytosis Hum Mutat 8 1996 97 107
37. L. Morle, F. Morle, A.F. Roux, J. Godet, B.G. Forget, and L. Denoroy et al. Spectrin Tunis (Sp-alpha-I/78), an elliptocytogenic variant, is due to the CGG-TGG codon change (Arg-Tryp) at position-35 of the alpha-I domain Blood 74 1989 828 832
38. S. Mehboob, J. Jacob, M. May, L. Kotula, P. Thiyagarajan, and M.E. Johnson et al. Structural analysis of the alpha N-terminal region of erythroid and nonerythroid spectrins by small-angle X-ray scattering Biochemistry 42 2003 14702 14710
39. D.H. Li, S.L. Harper, H.Y. Tang, Y. Maksimova, P.G. Gallagher, and D.W. Speicher A comprehensive model of the spectrin divalent tetramer binding region deduced using homology modeling and chemical cross-linking of a mini-spectrin J Biol Chem 285 2010 29535 29545
40. Y.L. Song, N.H. Pipalia, and L.W.M. Fung The L49F mutation in alpha erythroid spectrin induces local disorder in the tetramer association region: fluorescence and molecular dynamics studies of free and bound alpha spectrin Protein Sci 18 2009 1916 1925
41. J.X. Kang, Y.L. Song, A. Sevinc, and L.W.M. Fung Important residue (G46) in erythroid spectrin tetramer formation Cell Mol Biol Lett 15 2010 46 54
42. M. Gaetani, S. Mootien, S. Harper, P.G. Gallagher, and D.W. Speicher Structural and functional effects of hereditary hemolytic anemia-associated point mutations in the alpha spectrin tetramer site Blood 111 2008 5712 5720
43. P.A. Bignone, and A.J. Baines Spectrin alpha II and beta II isoforms interact with high affinity at the tetramerization site Biochem J 374 2003 613 624
44. S.L. Shammas, J.M. Rogers, S.A. Hill, and J. Clarke Slow, reversible, coupled folding and binding of the spectrin tetramerization domain Biophys J 103 2012 2203 2214
45. A.A. Nickson, and J. Clarke What lessons can be learned from studying the folding of homologous proteins? Methods 52 2010 38 50
46. E.A. Shank, C. Cecconi, J.W. Dill, S. Marqusee, and C. Bustamante The folding cooperativity of a protein is controlled by its chain topology Nature 465 2010 637 640
47. B.G. Wensley, M. Gartner, W.X. Choo, S. Batey, and J. Clarke Different members of a simple three-helix bundle protein family have very different folding rate constants and fold by different mechanisms J Mol Biol 390 2009 1074 1085
48. K.A. Scott, S. Batey, K.A. Hooton, and J. Clarke The folding of spectrin domains I: wild-type domains have the same stability but very different kinetic properties J Mol Biol 344 2004 195 205
49. K.A. Scott, L.G. Randles, and J. Clarke The folding of spectrin domains II: Phi-value analysis of R16 J Mol Biol 344 2004 207 221
50. K.A. Scott, L.G. Randles, S.J. Moran, V. Daggett, and J. Clarke The folding pathway of spectrin R17 from experiment and simulation: using experimentally validated MD simulations to characterize states hinted at by experiment J Mol Biol 359 2006 159 173
51. R.I. MacDonald, and E.V. Pozharski Free energies of urea and of thermal unfolding show that two tandem repeats of spectrin are thermodynamically more stable than a single repeat Biochemistry 40 2001 3974 3984
52. L.G. Randles, S. Batey, A. Steward, and J. Clarke Distinguishing specific and nonspecific interdomain interactions in multidomain proteins Biophys J 94 2008 622 628
53. A.R. Fersht, A. Matouschek, and L. Serrano The folding of an enzyme.1. Theory of protein engineering analysis of stability and pathway of protein folding J Mol Biol 224 1992 771 782
54. X. An, X. Guo, X. Zhang, A.J. Baines, G. Debnath, and D. Moyo et al. Conformational stabilities of the structural repeats of erythroid spectrin and their functional implications J Biol Chem 281 2006 10527 10532
55. S. Batey, L.G. Randles, A. Steward, and J. Clarke Cooperative folding in a multi-domain protein J Mol Biol 349 2005 1045 1059
56. A. Borgia, B.G. Wensley, A. Soranno, D. Nettels, M.B. Borgia, and A. Hoffmann et al. Localizing internal friction along the reaction coordinate of protein folding by combining ensemble and single-molecule fluorescence spectroscopy Nat Commun 3 2012 9
57. T.L. Coetzer, K. Sahr, J. Prchal, H. Blacklock, L. Peterson, and R. Koler et al. Four different mutations in codon 28 of alpha-spectrin are associated with structurally and functionally abnormal spectrin alpha-I/74 in hereditary elliptocytosis J Clin Invest 88 1991 743 749
58. M. Garbarz, M.C. Lecomte, C. Feo, I. Devaux, C. Picat, and C. Lefebvre et al. Hereditary pyropoikilocytosis and elliptocytosis in a white French family with the spectrin-alpha-I/74 variant related to a CGT to CAT codon change (Arg to His) at position 22 of the spectrin-alpha-I domain Blood 75 1990 1691 1698
59. P.B. Floyd, P.G. Gallagher, L.A. Valentino, M. Davis, S.L. Marchesi, and B.G. Forget Heterogeneity of the molecular-basis of hereditary pyropoikilocytosis and hereditary elliptocytosis associated with increased levels of the spectrin alpha-I/72-kilodalton tryptic peptide Blood 78 1991 1364 1372
60. L. Morle, A.F. Roux, N. Alloisio, B. Pothier, J. Starck, and L. Denoroy et al. Two elliptocytogenic alpha-I/74 variants of the spectrin alpha-I domain: spectrin Culoz (GGT-GTT alpha-I-40 Gly-Val) and spectrin Lyon (CTT-TTT alpha-I-43 Leu-Phe) J Clin Invest 86 1990 548 554