The crystal structures of dystrophin and utrophin spectrin repeats: Implications for domain boundaries

PLoS ONE

Volumn 7, Issue 7, 2012, Pages

  Muthu, Muralidharan ^a   Richardson, Kylie A ^a   Sutherland Smith, Andrew J ^a  

^a MASSEY UNIVERSITY   (New Zealand)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA ACTININ; DYSTROPHIN; F ACTIN; PLECTIN; SPECTRIN; UTROPHIN;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; CRYSTAL STRUCTURE; IN VITRO STUDY; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN MOTIF; PROTEIN STABILITY; SEQUENCE ANALYSIS; STRUCTURE ACTIVITY RELATION; STRUCTURE ANALYSIS; X RAY CRYSTALLOGRAPHY;

ACTINS; AMINO ACID SEQUENCE; CRYSTALLOGRAPHY, X-RAY; DYSTROPHIN; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; SEQUENCE ALIGNMENT; SPECTRIN; UTROPHIN;

EID: 84864078710     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0040066     Document Type: Article

References (70)

1. Wallace GQ, McNally EM, (2009) Mechanisms of muscle degeneration, regeneration, and repair in the muscular dystrophies. Annu Rev Physiol 71: 37-57.
2. Blake DJ, Weir A, Newey SE, Davies KE, (2002) Function and genetics of dystrophin and dystrophin-related proteins in muscle. Physiol Rev 82: 291-329.
3. Love DR, Hill DF, Dickson G, Spurr NK, Byth BC, et al. (1989) An autosomal transcript in skeletal muscle with homology to dystrophin. Nature 339: 55-58.
4. Nguyen TM, Ellis JM, Love DR, Davies KE, Gatter KC, et al. (1991) Localization of the DMDL gene-encoded dystrophin-related protein using a panel of nineteen monoclonal antibodies: presence at neuromuscular junctions, in the sarcolemma of dystrophic skeletal muscle, in vascular and other smooth muscles, and in proliferating brain cell lines. J Cell Biol 115: 1695-1700.
5. Clerk A, Morris GE, Dubowitz V, Davies KE, Sewry CA, (1993) Dystrophin-related protein, utrophin, in normal and dystrophic human fetal skeletal muscle. Histochem J 25: 554-561.
6. Way M, Pope B, Weeds AG, (1992) Evidence for functional homology in the F-actin binding domains of gelsolin and alpha-actinin: implications for the requirements of severing and capping. J Cell Biol 119: 835-842.
7. Stone MR, O'Neill A, Catino D, Bloch RJ, (2005) Specific interaction of the actin-binding domain of dystrophin with intermediate filaments containing keratin 19. Mol Biol Cell 16: 4280-4293.
8. Ervasti JM, Campbell KP, (1993) A role for the dystrophin-glycoprotein complex as a transmembrane linker between laminin and actin. J Cell Biol 122: 809-823.
9. Rybakova IN, Patel JR, Ervasti JM, (2000) The dystrophin complex forms a mechanically strong link between the sarcolemma and costameric actin. J Cell Biol 150: 1209-1214.
10. Bhasin N, Law R, Liao G, Safer D, Ellmer J, et al. (2005) Molecular extensibility of mini-dystrophins and a dystrophin rod construct. J Mol Biol 352: 795-806.
11. England SB, Nicholson LV, Johnson MA, Forrest SM, Love DR, et al. (1990) Very mild muscular dystrophy associated with the deletion of 46% of dystrophin. Nature 343: 180-182.
12. Legardinier S, Legrand B, Raguenes-Nicol C, Bondon A, Hardy S, et al. (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: 8822-8832.
13. Koenig M, Kunkel LM, (1990) Detailed analysis of the repeat domain of dystrophin reveals four potential hinge segments that may confer flexibility. J Biol Chem 265: 4560-4566.
14. Winder SJ, Gibson TJ, Kendrick-Jones J, (1995) Dystrophin and utrophin: the missing links! FEBS Lett 369: 27-33.
15. Djinovic-Carugo K, Gautel M, Ylanne J, Young P, (2002) The spectrin repeat: a structural platform for cytoskeletal protein assemblies. FEBS Lett 513: 119-123.
16. Rybakova IN, Ervasti JM, (1997) Dystrophin-glycoprotein complex is monomeric and stabilizes actin filaments in vitro through a lateral association. J Biol Chem 272: 28771-28778.
17. Kahana E, Marsh PJ, Henry AJ, Way M, Gratzer WB, (1994) Conformation and phasing of dystrophin structural repeats. J Mol Biol 235: 1271-1277.
18. Kahana E, Gratzer WB, (1995) Minimum folding unit of dystrophin rod domain. Biochemistry 34: 8110-8114.
19. Calvert R, Kahana E, Gratzer WB, (1996) Stability of the dystrophin rod domain fold: evidence for nested repeating units. Biophys J 71: 1605-1610.
20. Menhart N, (2006) Hybrid spectrin type repeats produced by exon-skipping in dystrophin. Biochim Biophys Acta 1764: 993-999.
21. Saadat L, Pittman L, Menhart N, (2006) Structural cooperativity in spectrin type repeats motifs of dystrophin. Biochim Biophys Acta 1764: 943-954.
22. Mirza A, Sagathevan M, Sahni N, Choi L, Menhart N, (2010) A biophysical map of the dystrophin rod. Biochim Biophys Acta 1804: 1796-1809.
23. Amann KJ, Renley BA, Ervasti JM, (1998) A cluster of basic repeats in the dystrophin rod domain binds F-actin through an electrostatic interaction. J Biol Chem 273: 28419-28423.
24. Rybakova IN, Ervasti JM, (2005) Identification of spectrin-like repeats required for high affinity utrophin-actin interaction. J Biol Chem 280: 23018-23023.
25. Prochniewicz E, Henderson D, Ervasti JM, Thomas DD, (2009) Dystrophin and utrophin have distinct effects on the structural dynamics of actin. Proc Natl Acad Sci U S A 106: 7822-7827.
26. Bhosle RC, Michele DE, Campbell KP, Li Z, Robson RM, (2006) Interactions of intermediate filament protein synemin with dystrophin and utrophin. Biochem Biophys Res Commun 346: 768-777.
27. Yamashita K, Suzuki A, Satoh Y, Ide M, Amano Y, et al. (2010) The 8th and 9th tandem spectrin-like repeats of utrophin cooperatively form a functional unit to interact with polarity-regulating kinase PAR-1b. Biochem Biophys Res Commun 391: 812-817.
28. Lai Y, Thomas GD, Yue Y, Yang HT, Li D, et al. (2009) Dystrophins carrying spectrin-like repeats 16 and 17 anchor nNOS to the sarcolemma and enhance exercise performance in a mouse model of muscular dystrophy. J Clin Invest 119: 624-635.
29. Le Rumeur E, Fichou Y, Pottier S, Gaboriau F, Rondeau-Mouro C, et al. (2003) Interaction of dystrophin rod domain with membrane phospholipids. Evidence of a close proximity between tryptophan residues and lipids. J Biol Chem 278: 5993-6001.
30. Legardinier S, Raguenes-Nicol C, Tascon C, Rocher C, Hardy S, et al. (2009) Mapping of the lipid-binding and stability properties of the central rod domain of human dystrophin. J Mol Biol 389: 546-558.
31. Yan Y, Winograd E, Viel A, Cronin T, Harrison SC, et al. (1993) Crystal structure of the repetitive segments of spectrin. Science 262: 2027-2030.
32. Pascual J, Pfuhl M, Walther D, Saraste M, Nilges M, (1997) Solution structure of the spectrin repeat: a left-handed antiparallel triple-helical coiled-coil. J Mol Biol 273: 740-751.
33. Grum VL, Li D, MacDonald RI, Mondragon A, (1999) Structures of two repeats of spectrin suggest models of flexibility. Cell 98: 523-535.
34. Kusunoki H, Minasov G, Macdonald RI, Mondragon A, (2004) Independent movement, dimerization and stability of tandem repeats of chicken brain alpha-spectrin. J Mol Biol 344: 495-511.
35. Kusunoki H, MacDonald RI, Mondragon A, (2004) Structural insights into the stability and flexibility of unusual erythroid spectrin repeats. Structure 12: 645-656.
36. Djinovic-Carugo K, Young P, Gautel M, Saraste M, (1999) Structure of the alpha-actinin rod: molecular basis for cross-linking of actin filaments. Cell 98: 537-546.
37. Ylanne J, Scheffzek K, Young P, Saraste M, (2001) Crystal structure of the alpha-actinin rod reveals an extensive torsional twist. Structure 9: 597-604.
38. Jefferson JJ, Ciatto C, Shapiro L, Liem RK, (2007) Structural analysis of the plakin domain of bullous pemphigoid antigen1 (BPAG1) suggests that plakins are members of the spectrin superfamily. J Mol Biol 366: 244-257.
39. Sonnenberg A, Rojas AM, de Pereda JM, (2007) The structure of a tandem pair of spectrin repeats of plectin reveals a modular organization of the plakin domain. J Mol Biol 368: 1379-1391.
40. Choi HJ, Weis WI, (2011) Crystal structure of a rigid four-spectrin-repeat fragment of the human desmoplakin plakin domain. J Mol Biol 409: 800-812.
41. Bloch RJ, Pumplin DW, (1992) A model of spectrin as a concertina in the erythrocyte membrane skeleton. Trends Cell Biol 2: 186-189.
42. Tinsley JM, Potter AC, Phelps SR, Fisher R, Trickett JI, et al. (1996) Amelioration of the dystrophic phenotype of mdx mice using a truncated utrophin transgene. Nature 384: 349-353.
43. Miura P, Chakkalakal JV, Boudreault L, Belanger G, Hebert RL, et al. (2009) Pharmacological activation of PPARbeta/delta stimulates utrophin A expression in skeletal muscle fibers and restores sarcolemmal integrity in mature mdx mice. Hum Mol Genet 18: 4640-4649.
44. Di Certo MG, Corbi N, Strimpakos G, Onori A, Luvisetto S, et al. (2010) The artificial gene Jazz, a transcriptional regulator of utrophin, corrects the dystrophic pathology in mdx mice. Hum Mol Genet 19: 752-760.
45. Henderson DM, Belanto JJ, Li B, Heun-Johnson H, Ervasti JM, (2011) Internal deletion compromises the stability of dystrophin. Hum Mol Genet 20: 2955-2963.
46. Harper SQ, Hauser MA, DelloRusso C, Duan D, Crawford RW, et al. (2002) Modular flexibility of dystrophin: implications for gene therapy of Duchenne muscular dystrophy. Nat Med 8: 253-261.
47. Davis IW, Murray LW, Richardson JS, Richardson DC, (2004) MOLPROBITY: structure validation and all-atom contact analysis for nucleic acids and their complexes. Nucleic Acids Res 32: W615-619.
48. 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: 21052-21059.
49. Altmann SM, Grunberg RG, Lenne PF, Ylanne J, Raae A, et al. (2002) Pathways and intermediates in forced unfolding of spectrin repeats. Structure 10: 1085-1096.
50. Roy A, Kucukural A, Zhang Y, (2010) I-TASSER: a unified platform for automated protein structure and function prediction. Nat Protoc 5: 725-738.
51. Banatao DR, Cascio D, Crowley CS, Fleissner MR, Tienson HL, et al. (2006) An approach to crystallizing proteins by synthetic symmetrization. Proc Natl Acad Sci U S A 103: 16230-16235.
52. Sutherland-Smith AJ, Moores CA, Norwood FL, Hatch V, Craig R, et al. (2003) An atomic model for actin binding by the CH domains and spectrin-repeat modules of utrophin and dystrophin. J Mol Biol 329: 15-33.
53. Amann KJ, Guo AW, Ervasti JM, (1999) Utrophin lacks the rod domain actin binding activity of dystrophin. J Biol Chem 274: 35375-35380.
54. Ashkenazy H, Erez E, Martz E, Pupko T, Ben-Tal N, (2010) ConSurf 2010: calculating evolutionary conservation in sequence and structure of proteins and nucleic acids. Nucleic Acids Res 38: W529-533.
55. Rybakova IN, Humston JL, Sonnemann KJ, Ervasti JM, (2006) Dystrophin and utrophin bind actin through distinct modes of contact. J Biol Chem 281: 9996-10001.
56. Parry DA, Dixon TW, Cohen C, (1992) Analysis of the three-alpha-helix motif in the spectrin superfamily of proteins. Biophys J 61: 858-867.
57. Zuellig RA, Bornhauser BC, Knuesel I, Heller F, Fritschy JM, et al. (2000) Identification and characterisation of transcript and protein of a new short N-terminal utrophin isoform. J Cell Biochem 77: 418-431.
58. McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, et al. (2007) Phaser crystallographic software. J Appl Crystallogr 40: 658-674.
59. Murshudov GN, Vagin AA, Dodson EJ, (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr 53: 240-255.
60. Adams PD, Grosse-Kunstleve RW, Hung LW, Ioerger TR, McCoy AJ, et al. (2002) PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr D Biol Crystallogr 58: 1948-1954.
61. Emsley P, Cowtan K, (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60: 2126-2132.
62. Winn MD, Isupov MN, Murshudov GN, (2001) Use of TLS parameters to model anisotropic displacements in macromolecular refinement. Acta Crystallogr D Biol Crystallogr 57: 122-133.
63. DeLano WL, (2002) The PyMOL Molecular Graphics System. DeLano Scientific, San Carlos, CA, USA.
64. Potterton L, McNicholas S, Krissinel E, Gruber J, Cowtan K, et al. (2004) Developments in the CCP4 molecular-graphics project. Acta Crystallogr D Biol Crystallogr 60: 2288-2294.
65. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, et al. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947-2948.
66. Bond CS, Schuttelkopf AW, (2009) ALINE: a WYSIWYG protein-sequence alignment editor for publication-quality alignments. Acta Crystallogr D Biol Crystallogr 65: 510-512.
67. Holm L, Kaariainen S, Rosenstrom P, Schenkel A, (2008) Searching protein structure databases with DaliLite v.3. Bioinformatics 24: 2780-2781.
68. Krissinel E, Henrick K, (2007) Inference of macromolecular assemblies from crystalline state. J Mol Biol 372: 774-797.
69. Clark AR, Sawyer GM, Robertson SP, Sutherland-Smith AJ, (2009) Skeletal dysplasias due to filamin A mutations result from a gain-of-function mechanism distinct from allelic neurological disorders. Hum Mol Genet 18: 4791-4800.
70. Sawyer GM, Clark AR, Robertson SP, Sutherland-Smith AJ, (2009) Disease-associated substitutions in the filamin B actin binding domain confer enhanced actin binding affinity in the absence of major structural disturbance: Insights from the crystal structures of filamin B actin binding domains. J Mol Biol 390: 1030-1047.