The nonlinear structure of the desmoplakin plakin domain and the effects of cardiomyopathy-linked mutations

Journal of Molecular Biology

Volumn 411, Issue 5, 2011, Pages 1049-1061

  Al Jassar, Caezar ^a   Knowles, Timothy ^a   Jeeves, Mark ^a   Kami, Keiichiro ^a,d   Behr, Elijah ^b   Bikker, Hennie ^c   Overduin, Michael ^a   Chidgey, Martyn ^a  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^b ST GEORGE'S UNIVERSITY OF LONDON   (United Kingdom)

^c ACADEMIC MEDICAL CENTER   (Netherlands)

^d RIKEN   (Japan)

Author keywords

arrhythmogenic right ventricular cardiomyopathy; desmoplakin; desmosome; spectrin repeat

Indexed keywords

DESMOPLAKIN; DNA; PLAKIN; SPECTRIN;

ADULT; ARTICLE; CARBOXY TERMINAL SEQUENCE; CASE REPORT; CONFORMATIONAL TRANSITION; DNA SEQUENCE; GENE MUTATION; HEART RIGHT VENTRICLE DYSPLASIA; HUMAN; MALE; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN PURIFICATION; PROTEIN STABILITY; PROTEIN STRUCTURE; ULTRACENTRIFUGATION; X RAY CRYSTALLOGRAPHY;

EID: 80051669617     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2011.06.047     Document Type: Article

References (47)

1. Garrod D., and Chidgey M. Desmosome structure, composition and function Biochim. Biophys. Acta 1778 2008 572 587 (Pubitemid 351317796)
2. Sonnenberg A., and Liem R.K. Plakins in development and disease Exp. Cell Res. 313 2007 2189 2203 (Pubitemid 46842974)
3. Sonnenberg A., Rojas A.M., and de Pereda J.M. The structure of a tandem pair of spectrin repeats of plectin reveals a modular organization of the plakin domain J. Mol. Biol. 368 2007 1379 1391 (Pubitemid 46617599)
4. Choi H.J., Park-Snyder S., Pascoe L.T., Green K.J., and Weis W.I. Structures of two intermediate filament-binding fragments of desmoplakin reveal a unique repeat motif structure Nat. Struct. Biol. 9 2002 612 620 (Pubitemid 34816143)
5. Vasioukhin V., Bowers E., Bauer C., Degenstein L., and Fuchs E. Desmoplakin is essential in epidermal sheet formation Nat. Cell Biol. 3 2001 1076 1085 (Pubitemid 33130458)
6. Lai-Cheong J.E., Arita K., and McGrath J.A. Genetic diseases of junctions J. Invest. Dermatol. 127 2007 2713 2725 (Pubitemid 350134810)
7. Armstrong D.K., McKenna K.E., Purkis P.E., Green K.J., Eady R.A., Leigh I.M., and Hughes A.E. Haploinsufficiency of desmoplakin causes a striate subtype of palmoplantar keratoderma Hum. Mol. Genet. 8 1999 143 148 (Pubitemid 29039060)
8. Whittock N.V., Ashton G.H., Dopping-Hepenstal P.J., Gratian M.J., Keane F.M., Eady R.A., and McGrath J.A. Striate palmoplantar keratoderma resulting from desmoplakin haploinsufficiency J. Invest. Dermatol. 113 1999 940 946 (Pubitemid 30013335)
9. Awad M.M., Calkins H., and Judge D.P. Mechanisms of disease: molecular genetics of arrhythmogenic right ventricular dysplasia/cardiomyopathy Nat. Clin. Pract. Cardiovasc. Med. 5 2008 258 267 (Pubitemid 351593909)
10. van der Zwaag P.A., Jongbloed J.D., van den Berg M.P., van der Smagt J.J., Jongbloed R., and Bikker H. A genetic variants database for arrhythmogenic right ventricular dysplasia/cardiomyopathy Hum. Mutat. 30 2009 1278 1283
11. Yang Z., Bowles N.E., Scherer S.E., Taylor M.D., Kearney D.L., and Ge S. Desmosomal dysfunction due to mutations in desmoplakin causes arrhythmogenic right ventricular dysplasia/cardiomyopathy Circ. Res. 99 2006 646 655 (Pubitemid 44401456)
12. Yan Y., Winograd E., Viel A., Cronin T., Harrison S.C., and Branton D. Crystal structure of the repetitive segments of spectrin Science 262 1993 2027 2030 (Pubitemid 24041880)
13. Jefferson J.J., Ciatto C., Shapiro L., and Liem R.K. Structural analysis of the plakin domain of bullous pemphigoid antigen 1 (BPAG1) suggests that plakins are members of the spectrin superfamily J. Mol. Biol. 366 2007 244 257 (Pubitemid 46123339)
14. Lenne P.F., Raae A.J., Altmann S.M., Saraste M., and Horber J.K. States and transitions during forced unfolding of a single spectrin repeat FEBS Lett. 476 2000 124 128 (Pubitemid 30410802)
15. Ortega E., Buey R.M., Sonnenberg A., and de Pereda J.M. The structure of the plakin domain of plectin reveals a non-canonical SH3 domain interacting with its fourth spectrin repeat J. Biol. Chem. 286 2011 12429 12438
16. Green K.J., Parry D.A., Steinert P.M., Virata M.L., Wagner R.M., Angst B.D., and Nilles L.A. Structure of the human desmoplakins. Implications for function in the desmosomal plaque J. Biol. Chem. 265 1990 11406 11407
17. Choi H.J., and Weis W.I. Crystal structure of a rigid four-spectrin-repeat fragment of the human desmoplakin plakin domain J. Mol. Biol. 409 2011 800 812
18. Svergun D., Barberato C., and Koch M.H.J. CRYSOL-a program to evaluate X-ray solution scattering of biological macromolecules from atomic coordinates J. Appl. Crystallogr. 28 1995 768 773 (Pubitemid 3014671)
19. Kelley L.A., and Sternberg M.J. Protein structure prediction on the Web: a case study using the Phyre server Nat. Protoc. 4 2009 363 371
20. Basso C., Czarnowska E., Della Barbera M., Bauce B., Beffagna G., and Wlodarska E.K. Ultrastructural evidence of intercalated disc remodelling in arrhythmogenic right ventricular cardiomyopathy: an electron microscopy investigation on endomyocardial biopsies Eur. Heart J. 27 2006 1847 1854 (Pubitemid 44297392)
21. Ericsson U.B., Hallberg B.M., Detitta G.T., Dekker N., and Nordlund P. Thermofluor-based high-throughput stability optimization of proteins for structural studies Anal. Biochem. 357 2006 289 298 (Pubitemid 44430091)
22. Roy A., Kucukural A., and Zhang Y. I-TASSER: a unified platform for automated protein structure and function prediction Nat. Protoc. 5 2010 725 738
23. Petoukhov M.V., and Svergun D.I. Global rigid body modeling of macromolecular complexes against small-angle scattering data Biophys. J. 89 2005 1237 1250 (Pubitemid 41099005)
24. Grantcharova V.P., and Baker D. Folding dynamics of the Src SH3 domain Biochemistry 36 1997 15685 15692 (Pubitemid 28027367)
25. Viguera A.R., Martinez J.C., Filimonov V.V., Mateo P.L., and Serrano L. Thermodynamic and kinetic analysis of the SH3 domain of spectrin shows a two-state folding transition Biochemistry 33 1994 2142 2150 (Pubitemid 24099611)
26. Musacchio A., Noble M., Pauptit R., Wierenga R., and Saraste M. Crystal structure of a Src-homology 3 (SH3) domain Nature 359 1992 851 855
27. Mirza A., Sagathevan M., Sahni N., Choi L., and Menhart N. A biophysical map of the dystrophin rod Biochim. Biophys. Acta 1804 2010 1796 1809
28. Ylanne J., Scheffzek K., Young P., and Saraste M. Crystal structure of the alpha-actinin rod reveals an extensive torsional twist Structure 9 2001 597 604 (Pubitemid 32695584)
29. Grum V.L., Li D., MacDonald R.I., and Mondragon A. Structures of two repeats of spectrin suggest models of flexibility Cell 98 1999 523 535 (Pubitemid 29402489)
30. MacDonald R.I., and Cummings J.A. Stabilities of folding of clustered, two-repeat fragments of spectrin reveal a potential hinge in the human erythroid spectrin tetramer Proc. Natl Acad. Sci. USA 101 2004 1502 1507 (Pubitemid 38234184)
31. An X., Guo X., Zhang X., Baines A.J., Debnath G., and Moyo D. Conformational stabilities of the structural repeats of erythroid spectrin and their functional implications J. Biol. Chem. 281 2006 10527 10532 (Pubitemid 43864592)
32. Law R., Liao G., Harper S., Yang G., Speicher D.W., and Discher D.E. Pathway shifts and thermal softening in temperature-coupled forced unfolding of spectrin domains Biophys. J. 85 2003 3286 3293 (Pubitemid 37345816)
33. Legardinier S., Legrand B., Raguenes-Nicol C., Bondon A., Hardy S., and Tascon C. 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 2009 8822 8832
34. Park S., Johnson M.E., and Fung L.W. Nuclear magnetic resonance studies of mutations at the tetramerization region of human alpha spectrin Blood 100 2002 283 288 (Pubitemid 35177458)
35. Brown P.H., and Schuck P. Macromolecular size-and-shape distributions by sedimentation velocity analytical ultracentrifugation Biophys. J. 90 2006 4651 4661 (Pubitemid 43830909)
36. Lobley A., Whitmore L., and Wallace B.A. DICHROWEB: an interactive website for the analysis of protein secondary structure from circular dichroism spectra Bioinformatics 18 2002 211 212 (Pubitemid 34145057)
37. Konarev P.V., Volkov V.V., Sokolova A.V., Koch M.H.J., and Svergun D.I. PRIMUS: a Windows PC-based system for small-angle scattering data analysis J. Appl. Crystallogr. 36 2003 1277 1282
38. Semenyuk A.V., and Svergun D.I. GNOM-a program package for small-angle scattering data processing J. Appl. Crystallogr. 24 1991 537 540
39. Franke D., and Svergun D.I. DAMMIF, a program for rapid ab-initio shape determination in small-angle scattering J. Appl. Crystallogr. 42 2009 342 346
40. Kozin M.B., and Svergun D.I. Automated matching of high- and low-resolution structural models J. Appl. Crystallogr. 34 2001 33 41 (Pubitemid 32151714)
41. Volkov V.V., and Svergun D.I. Uniqueness of ab initio shape determination in small-angle scattering J. Appl. Crystallogr. 36 2003 860 864
42. Wriggers W., and Chacon P. Using Situs for the registration of protein structures with low-resolution bead models from X-ray solution scattering J. Appl. Crystallogr. 34 2001 773 776 (Pubitemid 33144106)
43. Chacon P., and Wriggers W. Multi-resolution contour-based fitting of macromolecular structures J. Mol. Biol. 317 2002 375 384 (Pubitemid 34722177)
44. Pettersen E.F., Goddard T.D., Huang C.C., Couch G.S., Greenblatt D.M., Meng E.C., and Ferrin T.E. UCSF Chimera-a visualization system for exploratory research and analysis J. Comput. Chem. 25 2004 1605 1612
45. Delaglio F., Grzesiek S., Vuister G.W., Zhu G., Pfeifer J., and Bax A. NMRPipe: a multidimensional spectral processing system based on UNIX pipes J. Biomol. NMR 6 1995 277 293
46. Vranken W.F., Boucher W., Stevens T.J., Fogh R.H., Pajon A., and Llinas M. The CCPN data model for NMR spectroscopy: development of a software pipeline Proteins 59 2005 687 696 (Pubitemid 40695845)
47. Kami K., Chidgey M., Dafforn T., and Overduin M. The desmoglein-specific cytoplasmic region is intrinsically disordered in solution and interacts with multiple desmosomal protein partners J. Mol. Biol. 386 2009 531 543