Crystal structures of the human Dysferlin inner DysF domain

BMC Structural Biology

Volumn 14, Issue 1, 2014, Pages

  Sula, Altin ^a   Cole, Ambrose R ^a   Yeats, Corin ^b,c   Orengo, Christine ^b   Keep, Nicholas H ^a  

^a UNIVERSITY OF LONDON   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

Arginine tryptophan stacking; Crystal structure; DysF domain; Dysferlin; Limb girdle muscular dystrophy 2B

Indexed keywords

ARGININE; DYSFERLIN; TRYPTOPHAN;

ARTICLE; CRYSTAL STRUCTURE; CRYSTALLIZATION; DYSFERLINOPATHY; HYDROGEN BOND; MISSENSE MUTATION; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; POINT MUTATION; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN SECONDARY STRUCTURE; PROTEIN STRUCTURE; STRUCTURE ANALYSIS;

ARGININE; CRYSTALLOGRAPHY, X-RAY; HUMANS; HYDROGEN BONDING; MEMBRANE PROTEINS; MODELS, MOLECULAR; MUSCLE PROTEINS; MUSCULAR DYSTROPHIES, LIMB-GIRDLE; MUTATION, MISSENSE; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; SEQUENCE ALIGNMENT; TRYPTOPHAN;

EID: 84892452960     PISSN: None     EISSN: 14726807     Source Type: Journal    
DOI: 10.1186/1472-6807-14-3     Document Type: Article

References (55)

1. A gene related to Caenorhabditis elegans spermatogenesis factor fer-1 is mutated in limb-girdle muscular dystrophy type 2B. Bashir R, Britton S, Strachan T, Keers S, Vafiadaki E, Lako M, Richard I, Marchand S, Bourg N, Argov Z, et al. Nat Genet 1998 20 37 42 10.1038/1689 9731527 (Pubitemid 28410340)
2. Dysferlin, a novel skeletal muscle gene, is mutated in Miyoshi myopathy and limb girdle muscular dystrophy. Liu J, Aoki M, Illa I, Wu C, Fardeau M, Angelini C, Serrano C, Urtizberea JA, Hentati F, Hamida MB, et al. Nat Genet 1998 20 31 36 10.1038/1682 9731526 (Pubitemid 28410339)
3. Distal anterior compartment myopathy: a dysferlin mutation causing a new muscular dystrophy phenotype. Illa I, Serrano-Munuera C, Gallardo E, Lasa A, Rojas-García R, Palmer J, Gallano P, Baiget M, Matsuda C, Brown RH, Ann Neurol 2001 49 130 134 10.1002/1531-8249(200101)49:1<130::AID-ANA22>3.0. CO;2-0 11198284 (Pubitemid 32163018)
4. Defective membrane repair in dysferlin-deficient muscular dystrophy. Bansal D, Miyake K, Vogel SS, Groh S, Chen CC, Williamson R, McNeil PL, Campbell KP, Nature 2003 423 168 172 10.1038/nature01573 12736685 (Pubitemid 36569539)
5. Dysferlin and the plasma membrane repair in muscular dystrophy. Bansal D, Campbell KP, Trends Cell Biol 2004 14 206 213 10.1016/j.tcb.2004.03.001 15066638 (Pubitemid 38447120)
6. Ferlins: regulators of vesicle fusion for auditory neurotransmission, receptor trafficking and membrane repair. Lek A, Evesson FJ, Sutton RB, North KN, Cooper ST, Traffic 2012 13 185 194 10.1111/j.1600-0854.2011.01267.x 21838746
7. Phylogenetic analysis of ferlin genes reveals ancient eukaryotic origins. Lek A, Lek M, North KN, Cooper ST, BMC Evolutionary Biology 2010 10 231 10.1186/1471-2148-10-231 20667140
8. Extending CATH: increasing coverage of the protein structure universe and linking structure with function. Cuff AL, Sillitoe I, Lewis T, Clegg AB, Rentzsch R, Furnham N, Pellegrini-Calace M, Jones D, Thornton J, Orengo CA, Nucleic Acids Res 2011 39 420 D426 10.1093/nar/gkq1001 21097779
9. SMART 7: recent updates to the protein domain annotation resource. Letunic I, Doerks T, Bork P, Nucleic Acids Res 2012 40 302 D305 10.1093/nar/gkr931 22053084
10. The Pfam protein families database. Punta M, Coggill PC, Eberhardt RY, Mistry J, Tate J, Boursnell C, Pang N, Forslund K, Ceric G, Clements J, et al. Nucleic Acids Res 2012 40 290 D301 10.1093/nar/gkr1065 22127870
11. Calcium-sensitive phospholipid binding properties of normal and mutant ferlin C2 domains. Davis DB, Doherty KR, Delmonte AJ, McNally EM, J Biol Chem 2002 277 22883 22888 10.1074/jbc.M201858200 11959863 (Pubitemid 34967270)
12. Characterization of lipid binding specificities of dysferlin C2 domains reveals vovel interactions with phosphoinositides. Therrien C, Di Fulvio S, Pickles S, Sinnreich M, Biochemistry 2009 48 2377 2384 10.1021/bi802242r 19253956
13. Dysferlin forms a dimer mediated by the C2 domains and the transmembrane domain in vitro and in living cells. Xu L, Pallikkuth S, Hou Z, Mignery GA, Robia SL, Han R, PloS one 2011 6 27884 e27884 10.1371/journal.pone.0027884 22110769
14. Alternate Splicing of Dysferlin C2A Confers Ca2+-Dependent and Ca2+-Independent Binding for Membrane Repair. Fuson K, Rice A, Mahling R, Snow A, Nayak K, Shanbhogue P, Meyer Austin G, Redpath GMI, Hinderliter A, Cooper ST, Sutton RB, Structure 2014 In press
15. Entries in the Leiden Duchenne muscular dystrophy mutation database: an overview of mutation types and paradoxical cases that confirm the reading-frame rule. Aartsma-Rus A, Van Deutekom JCT, Fokkema IF, Van Ommen GJB, Den Dunnen JT, Muscle Nerve 2006 34 135 144 10.1002/mus.20586 16770791 (Pubitemid 44167796)
16. Leiden muscular dystrophy database dysferlin sequence variants. http://www.dmd.nl/dysf-seqvar.html
17. Novel protein domains and repeats in Drosophila melanogaster: insights into structure, function, and evolution. Ponting CP, Mott R, Bork P, Copley RR, Genome Res 2001 11 1996 2008 10.1101/gr.198701 11731489 (Pubitemid 33138796)
18. Solution structure of the inner DysF domain of myoferlin and implications for limb girdle muscular dystrophy type 2b. Patel P, Harris R, Geddes SM, Strehle EM, Watson JD, Bashir R, Bushby K, Driscoll PC, Keep NH, J Mol Biol 2008 379 981 990 10.1016/j.jmb.2008.04.046 18495154
19. Presenting your structures: the CCP4mg molecular-graphics software. McNicholas S, Potterton E, Wilson KS, Noble MEM, Acta Crystallogr D Biol Crystallogr 2011 67 386 394 10.1107/S0907444911007281 21460457
20. CING: an integrated residue-based structure validation program suite. Doreleijers JF, da Silva AWS, Krieger E, Nabuurs SB, Spronk C, Stevens TJ, Vranken WF, Vriend G, Vuister GW, Journal of Biomolecular Nmr 2012 54 267 283 10.1007/s10858-012-9669-7 22986687
21. CING database RMS Data for 2k2o. http://nmr.cmbi.ru.nl/NRG-CING/data/k2/ 2k2o/2k2o.cing/2k2o/Cing/2k2o-01-cv-rms.png
22. Inference of macromolecular assemblies from crystalline state. Krissinel E, Henrick K, J Mol Biol 2007 372 774 797 10.1016/j.jmb.2007.05.022 17681537 (Pubitemid 47321791)
23. Planar stacking interactions of arginine and aromatic side-chains in proteins. Flocco MM, Mowbray SL, J Mol Biol 1994 235 709 717 10.1006/jmbi.1994.1022 8289290 (Pubitemid 24063588)
24. The cation-pi interaction. Ma JC, Dougherty DA, Chem Rev 1997 97 1303 1324 10.1021/cr9603744 11851453
25. Singh J, Thornton JM, Atlas of Protein Side-Chain Interactions Oxford: IRL Press 1992
26. Atlas of side chain interactions. http://www.ebi.ac.uk/thornton-srv/ databases/sidechains
27. A set of van der Waals and Coulombic radii of protein atoms for molecular and solvent-accessible surface calculation, packing evaluation, and docking. Li AJ, Nussinov R, Proteins-Structure Function and Genetics 1998 32 111 127 10.1002/(SICI)1097-0134(19980701)32:1<111::AID-PROT12>3.0.CO;2-H (Pubitemid 28313257)
28. Molecular analysis of LGMD-2B and MM patients: identification of novel DYSF mutations and possible founder effect in the Italian population. Cagliani R, Fortunato F, Giorda R, Rodolico C, Bonaglia MC, Sironi M, D'Angelo MG, Prelle A, Locatelli F, Toscano A, et al. Neuromuscul Disord 2003 13 788 795 10.1016/S0960-8966(03)00133-0 14678801 (Pubitemid 37532728)
29. Mutation finding in patients with dysferlin deficiency and role of the dysferlin interacting proteins annexin A1 and A2 in muscular dystrophies. Cagliani R, Magri F, Toscano A, Merlini L, Fortunato F, Lamperti C, Rodolico C, Prelle A, Sironi M, Aguennouz M, et al. Hum Mutat 2005 26 283
30. Clinical, molecular, and protein correlations in a large sample of genetically diagnosed Italian limb girdle muscular dystrophy patients. Guglieri M, Magri F, D'Angelo MG, Prelle A, Morandi L, Rodolico C, Cagliani R, Mora M, Fortunato F, Bordoni A, et al. Hum Mutat 2008 29 258 266 10.1002/humu.20642 17994539 (Pubitemid 351240598)
31. Dysferlin mutation analysis in a group of Italian patients with limb-girdle muscular dystrophy and Miyoshi myopathy. Kawabe K, Goto K, Nishino I, Angelini C, Hayashi YK, Eur J Neurol 2004 11 657 661 10.1111/j.1468-1331. 2004.00755.x 15469449 (Pubitemid 39389666)
32. New aspects on patients affected by dysferlin deficient muscular dystrophy. Klinge L, Aboumousa A, Eagle M, Hudson J, Sarkozy A, Vita G, Charlton R, Roberts M, Straub V, Barresi R, et al. J Neurol Neurosurg Psychiatry 2010 81 946 953 10.1136/jnnp.2009.178038 19528035
33. Absence of dysferlin alters myogenin expression and delays human muscle differentiation in vitro de Luna N, Gallardo E, Soriano M, Dominguez-Perles R, de la Torre C, Rojas-Garcia R, Garcia-Verdugo JM, Illa I, J Biol Chem 2006 281 17092 17098 10.1074/jbc.M601885200 16608842
34. Muscle protein analysis in the detection of heterozygotes for recessive limb girdle muscular dystrophy type 2B and 2E. Fanin M, Nascimbeni AC, Angelini C, Neuromuscul Disord 2006 16 792 799 10.1016/j.nmd.2006.06.010 16934466 (Pubitemid 44646857)
35. Dysferlin deficiency shows compensatory induction of Rab27A/Slp2a that may contribute to inflammatory onset. Kesari A, Fukuda M, Knoblach S, Bashir R, Nader GA, Rao D, Nagaraju K, Hoffman EP, Am J Pathol 2008 173 1476 1487 10.2353/ajpath.2008.080098 18832576
36. Clinical and genetic analysis of Korean patients with Miyoshi myopathy: identification of three novel mutations in the DYSF gene. Cho HJ, Sung DH, Kim EJ, Yoon CH, Ki CS, Kim JW, J Korean Med Sci 2006 21 724 727 10.3346/jkms.2006.21.4.724 16891820
37. A novel compound heterozygous dysferlin mutation in Miyoshi myopathy siblings responding to dantrolene. Hattori H, Nagata E, Oya Y, Takahashi T, Aoki M, Ito D, Suzuki N, Eur J Neurol 2007 14 1288 1291 10.1111/j.1468-1331.2007. 01958.x 17868276 (Pubitemid 47621956)
38. Protein and gene analyses of dysferlinopathy in a large group of Japanese muscular dystrophy patients. Tagawa K, Ogawa M, Kawabe K, Yamanaka G, Matsumura T, Goto K, Nonaka I, Nishino I, Hayashi YK, J Neurol Sci 2003 211 23 28 10.1016/S0022-510X(03)00041-8 12767493 (Pubitemid 36593263)
39. Dysferlin mutations in Japanese Miyoshi myopathy: relationship to phenotype. Takahashi T, Aoki M, Tateyama M, Kondo E, Mizuno T, Onodera Y, Takano R, Kawai H, Kamakura K, Mochizuki H, et al. Neurology 2003 60 1799 1804 10.1212/01.WNL.0000068333.43005.12 12796534 (Pubitemid 36737077)
40. The sarcolemmal proteins dysferlin and caveolin-3 interact in skeletal muscle. Matsuda C, Hayashi YK, Ogawa M, Aoki M, Murayama K, Nishino I, Nonaka I, Arahata K, Brown RH, Hum Mol Genet 2001 10 1761 1766 10.1093/hmg/10.17.1761 11532985 (Pubitemid 32899093)
41. Novel diagnostic features of dysferlinopathies. Rosales XQ, Gastier-Foster JM, Lewis S, Vinod M, Thrush DL, Astbury C, Pyatt R, Reshmi S, Sahenk Z, Mendell JR, Muscle Nerve 2010 42 14 21 10.1002/mus.21650 20544924
42. Partial functionality of a mini-dysferlin molecule identified in a patient affected with moderately severe primary dysferlinopathy. Krahn M, Wein N, Lostal W, Bourg-Alibert N, Nguyen K, Courrier S, Vial C, Labelle V, De Petris D, Borges A, et al. Neuromuscul Disord 2008 18 781 781
43. Dysferlin deficiency enhances monocyte phagocytosis: a model for the inflammatory onset of limb-girdle muscular dystrophy 2B. Nagaraju K, Rawat R, Veszelovszky E, Thapliyal R, Kesari A, Sparks S, Raben N, Plotz P, Hoffman EP, Am J Pathol 2008 172 774 785 10.2353/ajpath.2008.070327 18276788 (Pubitemid 351354549)
44. Absence of dysferlin alters myogenin expression and delays human muscle differentiation 'in vitro'. de Luna N, Gallardo E, Soriano M, Dominguez-Perles R, de la Torre C, Rojas-Garcia R, Garcia-Verdugo JM, Illa I, Neuromuscul Disord 2006 16 57 S57
45. Phenotypic and genetic analysis in a series of 55 patients with dysferlinopathy. Nguyen K, Bassez G, Eymard B, Levy N, Pouget J, Neurology 2005 64 413 A414
46. Mutational and clinical features of Japanese patients with dysferlinopathy (Miyoshi myopathy and limb girdle muscular dystrophy type 2B). Aoki M, Takahashi T, Rinsho shinkeigaku = Clinical neurology 2005 45 938 942 16447768 (Pubitemid 43154962)
47. Scoring residue conservation. Valdar WS, Proteins 2002 48 227 241 10.1002/prot.10146 12112692 (Pubitemid 34743413)
48. High-throughput production of human proteins for crystallization: the SGC experience. Savitsky P, Bray J, Cooper CD, Marsden BD, Mahajan P, Burgess-Brown NA, Gileadi O, J Struct Biol 2010 172 3 13 10.1016/j.jsb.2010.06.008 20541610
49. Towards rationalization of crystallization screening for small- to medium-sized academic laboratories: the PACT/JCSG+ strategy. Newman J, Egan D, Walter TS, Meged R, Berry I, Ben Jelloul M, Sussman JL, Stuart DI, Perrakis A, Acta Crystallogr D Biol Crystallogr 2005 61 1426 1431 10.1107/S0907444905024984 16204897 (Pubitemid 43943144)
50. XDS. Kabsch W, Acta Crystallogr D Biol Crystallogr 2010 66 125 132 10.1107/S0907444909047337 20124692
51. An introduction to data reduction: space-group determination, scaling and intensity statistics. Evans PR, Acta Crystallographica Section D-Biological Crystallography 2011 67 282 292 10.1107/S090744491003982X
52. MrBUMP: an automated pipeline for molecular replacement. Keegan RM, Winn MD, Acta Crystallographica Section D-Biological Crystallography 2008 64 119 124 10.1107/S0907444907037195 (Pubitemid 350308685)
53. Features and development of Coot. Emsley P, Lohkamp B, Scott WG, Cowtan K, Acta Crystallogr D Biol Crystallogr 2010 66 486 501 10.1107/S0907444910007493 20383002
54. Refinement of macromolecular structures by the maximum-likelihood method. Murshudov GN, Vagin AA, Dodson EJ, Acta Crystallogr D Biol Crystallogr 1997 53 240 255 10.1107/S0907444996012255 15299926 (Pubitemid 27235885)
55. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Adams PD, Afonine PV, Bunkóczi G, Chen VB, Davis IW, Echols N, Headd JJ, Hung LW, Kapral GJ, Grosse-Kunstleve RW, et al. Acta Crystallogr D Biol Crystallogr 2010 66 213 221 10.1107/S0907444909052925 20124702