Skip to main content
SpringerLink
Log in
Book cover

Fibrous Proteins: Structures and Mechanisms pp 373–403Cite as

Dystrophin and Spectrin, Two Highly Dissimilar Sisters of the Same Family

  • Chapter
  • First Online:

Part of the book series: Subcellular Biochemistry ((SCBI,volume 82))

Abstract

Dystrophin and Spectrin are two proteins essential for the organization of the cytoskeleton and for the stabilization of membrane cells. The comparison of these two sister proteins, and with the dystrophin homologue utrophin, enables us to emphasise that, despite a similar topology with common subdomains and a common structural basis of a three-helix coiled-coil, they show a large range of dissimilarities in terms of genetics, cell expression and higher level structural organisation. Interactions with cellular partners, including proteins and membrane phospholipids, also show both strikingly similar and very different behaviours. The differences between dystrophin and spectrin are also illustrated by the large variety of pathological anomalies emerging from the dysfunction or the absence of these proteins, showing that they are keystones in their function of providing a scaffold that sustains cell structure.

This is a preview of subscription content, log in via an institution.

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   189.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   249.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   249.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  • Aartsma-Rus A, Van Ommen GJ (2007) Antisense-mediated exon skipping: a versatile tool with therapeutic and research applications. RNA 13:1609–1624

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Amann KJ, Guo AWX, Ervasti JM (1999) Utrophin lacks the rod domain actin binding activity of dystrophin. J Biol Chem 274:35375–35380

    Article  CAS  PubMed  Google Scholar 

  • Ameziane-Le Hir S, Raguénès-Nicol C, Paboeuf G, Nicolas A, Chéron A, Le Rumeur E, Vié V (2014) Cholesterol favors higher level of insertion and organization of spectrin-like repeat 16–21 of human dystrophin in membrane. Biochim Biophys Acta 1838:1266–1273

    Article  CAS  PubMed  Google Scholar 

  • An X, Guo X, Sum H, Morrow J, Gratzer W, Mohandas N (2004a) Phosphatidylserine binding sites in erythroid spectrin: location and implications for membrane stability. Biochemistry 43:310–315

    Article  CAS  PubMed  Google Scholar 

  • An X, Guo X, Wu Y, Mohandas N (2004b) Phosphatidylserine binding sites in red cell spectrin. Blood Cells Mol Dis 32:430–432

    Article  CAS  PubMed  Google Scholar 

  • An X, Debnath G, Guo X, Liu S, Lux SE, Baines A, Gratzer W, Mohandas N (2005) Identification and functional characterization of protein 4.1R and actin-binding sites in erythrocyte beta spectrin: regulation of the interactions by phosphatidylinositol-4,5-bisphosphate. Biochemistry 44:10681–10688

    Article  CAS  PubMed  Google Scholar 

  • Bandi S, Singh SM, Mallela KM (2015) Interdomain linker determines primarily the structural stability of dystrophin and utrophin tandem calponin-homology domains rather than their actin-binding affinity. Biochemistry 54:5480–5488

    Article  CAS  PubMed  Google Scholar 

  • Banuelos S, Saraste M, Djinovic Carugo K (1998) Structural comparisons of calponin homology domains: implications for actin binding. Structure 6:1419–1431

    Article  CAS  PubMed  Google Scholar 

  • Begg GE, Harper SL, Morris MB, Speicher DW (2000) Initiation of spectrin dimerization involves complementary electrostatic interactions between paired triple-helical bundles. J Biol Chem 275:3279–3287

    Article  CAS  PubMed  Google Scholar 

  • Berghs S, Aggujaro D, Dirkx R JR., Maksimova E, Stabach P, Hermel JM, Zhang JP, Philbrick W, Slepnev V, Ort T & Solimena M (2000) betaIV spectrin, a new spectrin localized at axon initial segments and nodes of ranvier in the central and peripheral nervous system. J Cell Biol, 151, 985–1002.

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Boguslawska DM, Machnicka B, Sikorski AF (2010) Hereditary stomatocytoses--diagnostic problems and their molecular basis. Pol Merkur Lekarski 29:119–124

    PubMed  Google Scholar 

  • Boguslawska DM, Heger E, Listowski M, Wasinski D, Kuliczkowski K, Machnicka B, Sikorski AF (2014a) A novel L1340P mutation in the ANK1 gene is associated with hereditary spherocytosis? Br J Haematol 167:269–271

    Article  CAS  PubMed  Google Scholar 

  • Boguslawska DM, Machnicka B, Hryniewicz-Jankowska A, Czogalla A (2014b) Spectrin and phospholipids – the current picture of their fascinating interplay. Cell Mol Biol Lett 19:158–179

    Article  CAS  PubMed  Google Scholar 

  • Bok E, Plazuk E, Hryniewicz-Jankowska A, Chorzalska A, Szmaj A, Dubielecka PM, Stebelska K, Diakowski W, Lisowski M, Langner M, Sikorski AF (2007) Lipid-binding role of betaII-spectrin ankyrin-binding domain. Cell Biol Int 31:1482–1494

    Article  CAS  PubMed  Google Scholar 

  • Bolton-Maggs PH, Langer JC, Iolascon A, Tittensor P, King MJ (2012) Guidelines for the diagnosis and management of hereditary spherocytosis–2011 update. Br J Haematol 156:37–49

    Article  PubMed  Google Scholar 

  • Broderick MJ, Bobkov A, Winder SJ (2012) Utrophin ABD binds to F-actin in an open conformation. FEBS Open Bio 2:6–11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brown JW, Bullitt E, Sriswasdi S, Harper S, Speicher DW, Mcknight CJ (2015) The physiological molecular shape of spectrin: a compact supercoil resembling a chinese finger trap. PLoS Comput Biol 11:e1004302

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bruce LJ (2009) Hereditary stomatocytosis and cation-leaky red cells--recent developments. Blood Cells Mol Dis 42:216–222

    Article  CAS  PubMed  Google Scholar 

  • Buevich AV, Lundberg S, Sethson I, Edlund U, Backman L (2004) NMR studies of calcium-binding to mutant alpha-spectrin EF-hands. Cell Mol Biol Lett 9:167–186

    CAS  PubMed  Google Scholar 

  • Bushby KM, Gardner-Medwin D (1993) The clinical, genetic and dystrophin characteristics of Becker muscular dystrophy I natural history. J Neurol 240:98–104

    Article  CAS  PubMed  Google Scholar 

  • Bushby KM, Gardner-Medwin D, Nicholson LV, Johnson MA, Haggerty ID, Cleghorn NJ, Harris JB, Bhattacharya SS (1993) The clinical, genetic and dystrophin characteristics of Becker muscular dystrophy II correlation of phenotype with genetic and protein abnormalities. J Neurol 240:105–112

    Article  CAS  PubMed  Google Scholar 

  • Byers TJ, Lidov HG, Kunkel LM (1993) An alternative dystrophin transcript specific to peripheral nerve. Nat Genet 4:77–81

    Article  CAS  PubMed  Google Scholar 

  • Campbell K, Kahl S (1989) Association of dystrophin and an integral membrane glycoprotein. Nature 338:259–262

    Article  CAS  PubMed  Google Scholar 

  • Chelly J, Hamard G, Koulakoff A, Kaplan JC, Kahn A, Berwald-Netter Y (1990) Dystrophin gene transcribed from different promoters in neuronal and glial cells. Nature 344:64–65

    Article  CAS  PubMed  Google Scholar 

  • Cianci CD, Zhang Z, Pradhan D, Morrow JS (1999) Brain and muscle express a unique alternative transcript of alphaII spectrin. Biochemistry 38:15721–15730

    Article  CAS  PubMed  Google Scholar 

  • Czogalla A, Sikorski AF (2005) Spectrin and calpain: a ‘target’ and a ‘sniper’ in the pathology of neuronal cells. Cell Mol Life Sci 62:1913–1924

    Article  CAS  PubMed  Google Scholar 

  • Czogalla A, Sikorski AF (2010) Do we already know how spectrin attracts ankyrin? Cell Mol Life Sci 67:2679–2683

    Article  CAS  PubMed  Google Scholar 

  • Czogalla A, Jaszewski AR, Diakowski W, Bok E, Jezierski A, Sikorski AF (2007) Structural insight into an ankyrin-sensitive lipid-binding site of erythroid beta-spectrin. Mol Membr Biol 24:215–224

    Article  CAS  PubMed  Google Scholar 

  • Czogalla A, Grzymajlo K, Jezierski A, Sikorski AF (2008) Phospholipid-induced structural changes to an erythroid beta spectrin ankyrin-dependent lipid-binding site. Biochim Biophys Acta 1778:2612–2620

    Article  CAS  PubMed  Google Scholar 

  • Chorzalska A, Lach A, Borowik T, Wolny M, Hryniewicz-Jankowska A, Kolondra A, Langner M, Sikorski AF (2010) The effect of the lipid-binding site of the ankyrin-binding domain of erythroid beta-spectrin on the properties of natural membranes and skeletal structures. Cell Mol Biol Lett 15:406–423

    Article  CAS  PubMed  Google Scholar 

  • D’souza VN, Nguyen TM, Morris GE, Karges W, Pillers DA, Ray PN (1995) A novel dystrophin isoform is required for normal retinal electrophysiology. Hum Mol Genet 4:837–842

    Article  PubMed  Google Scholar 

  • Da Costa L, Galimand J, Fenneteau O, Mohandas N (2013) Hereditary spherocytosis, elliptocytosis, and other red cell membrane disorders. Blood Rev 27:167–178

    Article  CAS  PubMed  Google Scholar 

  • Das A, Base C, Manna D, Cho W, Dubreuil RR (2008) Unexpected complexity in the mechanisms that target assembly of the spectrin cytoskeleton. J Biol Chem 283:12643–12653

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Davies KE, Nowak KJ (2006) Molecular mechanisms of muscular dystrophies: old and new players. Nat Rev Mol Cell Biol 7:762–773

    Article  CAS  PubMed  Google Scholar 

  • Davis J, Bennett V (1983) Brain spectrin Isolation of subunits and formation of hybrids with erythrocyte spectrin subunits. J Biol Chem 258:7757–7766

    CAS  PubMed  Google Scholar 

  • Davis L, Abdi K, Machius M, Brautigam C, Tomchick DR, Bennett V, Michaely P (2009) Localization and structure of the ankyrin-binding site on beta2-spectrin. J Biol Chem 284:6982–6987

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dhermy D, Schrevel J, Lecomte MC (2007) Spectrin-based skeleton in red blood cells and malaria. Curr Opin Hematol 14:198–202

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Dubreuil RR, Grushko T (1998) Genetic studies of spectrin: new life for a ghost protein. BioEssays 20:875–878

    Article  CAS  PubMed  Google Scholar 

  • Eber S, Lux SE (2004) Hereditary spherocytosis – defects in proteins that connect the membrane skeleton to the lipid bilayer. Semin Hematol 41:118–141

    Article  CAS  PubMed  Google Scholar 

  • England S, Nicholson L, Johnson M, Forrest S, Love D, Zubrzycka-Gaarn E, Bulman D, Harris J, Davies K (1990) Very mild muscular dystrophy associated with the deletion of 46 % of the dystrophin. Nature 343:180–182

    Article  CAS  PubMed  Google Scholar 

  • Ervasti J, Campbell K (1991) Membrane organization of the dystrophin-glycoprotein complex. Cell 66:1121–1131

    Article  CAS  PubMed  Google Scholar 

  • Ervasti J, Campbell K (1993a) Dystrophin and the membrane skeleton. Curr Opin Cell Biol 5:82–87

    Article  CAS  PubMed  Google Scholar 

  • Ervasti J, Campbell K (1993b) A Role for the dystrophin-glycoprotein complex as aTransmembrane linker between laminin and actin. J Cell Biol 122:809–823

    Article  CAS  PubMed  Google Scholar 

  • Ervasti JM, Rybakova IN, Amann KJ (1997) A multiple site side binding model for the interaction of dystrophin with F-actin. Soc Gen Physiol Ser 52:31–44

    CAS  PubMed  Google Scholar 

  • Fairclough RJ, Wood MJ, Davies KE (2013) Therapy for duchenne muscular dystrophy: renewed optimism from genetic approaches. Nat Rev Genet 14:373–378

    Article  CAS  PubMed  Google Scholar 

  • Featherstone DE, Davis WS, Dubreuil RR, Broadie K (2001) Drosophila alpha- and beta-spectrin mutations disrupt presynaptic neurotransmitter release. J Neurosci 21:4215–4224

    CAS  PubMed  Google Scholar 

  • Flanigan KM, Dunn DM, Von Niederhausern A, Soltanzadeh P, Gappmaier E, Howard MT, Sampson JB, Mendell JR, Wall C, King WM, Pestronk A, Florence JM, Connolly AM, Mathews KD, Stephan CM, Laubenthal KS, Wong BL, Morehart PJ, Meyer A, Finkel RS, Bonnemann CG, Medne L, Day JW, Dalton JC, Margolis MK, Hinton VJ, Weiss RB (2009) Mutational spectrum of DMD mutations in dystrophinopathy patients: application of modern diagnostic techniques to a large cohort. Hum Mutat 30:1657–1666

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Foster H, Sharp PS, Athanasopoulos T, Trollet C, Graham IR, Foster K, Wells DJ, Dickson G (2008) Codon and mRNA sequence optimization of microdystrophin transgenes improves expression and physiological outcome in dystrophic mdx mice following AAV2/8 gene transfer. Mol Ther 16:1825–1832

    Article  CAS  PubMed  Google Scholar 

  • Gaetani M, Mootien S, Harper S, Gallagher PG, Speicher DW (2008) Structural and functional effects of hereditary hemolytic anemia-associated point mutations in the alpha spectrin tetramer site. Blood 111:5712–5720

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Galkin VE, Orlova A, Salmazo A, Djinovic-Carugo K, Egelman EH (2010) Opening of tandem calponin homology domains regulates their affinity for F-actin. Nat Struct Mol Biol 17:614–616

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gallagher PG (2004a) Hereditary elliptocytosis: spectrin and protein 4.1R. Semin Hematol 41:142–164

    Article  CAS  PubMed  Google Scholar 

  • Gallagher PG (2004b) Update on the clinical spectrum and genetics of red blood cell membrane disorders. Curr Hematol Rep 3:85–91

    PubMed  Google Scholar 

  • Gallagher PG, Weed SA, Tse WT, Benoit L, Morrow JS, Marchesi SL, Mohandas N, Forget BG (1995) Recurrent fatal hydrops fetalis associated with a nucleotide substitution in the erythrocyte beta-spectrin gene. J Clin Invest 95:1174–1182

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gentil C, Leturcq F, Ben Yaou R, Kaplan JC, Laforet P, Penisson-Besnier I, Espil-Taris C, Voit T, Garcia L, Pietri-Rouxel F (2012) Variable phenotype of del45-55 Becker patients correlated with nNOSmu mislocalization and RYR1 hypernitrosylation. Hum Mol Genet 21:3449–3460

    Article  CAS  PubMed  Google Scholar 

  • Giudice E, Molza A-E, Laurin Y, Nicolas A, Le Rumeur E, Delalande O (2013) Molecular clues to the dystrophin–nNOS interaction: a theoretical approach. Biochemistry 52:7777–7784

    Article  CAS  PubMed  Google Scholar 

  • Glele-Kakai C, Garbarz M, Lecomte MC, Leborgne S, Galand C, Bournier O, Devaux I, Gautero H, Zohoun I, Gallagher PG, Forget BG, Dhermy D (1996) Epidemiological studies of spectrin mutations related to hereditary elliptocytosis and spectrin polymorphisms in Benin. Br J Haematol 95:57–66

    Article  CAS  PubMed  Google Scholar 

  • Goyenvalle A, Vulin A, Fougerousse F, Leturcq F, Kaplan J, Garcia L, Danos O (2004) Rescue of dystrophic muscle through U7 snRNA-mediated exon skipping. Science 306:1796–1799

    Article  CAS  PubMed  Google Scholar 

  • Gregorevic P, Blankinship MJ, Allen JM, Chamberlain JS (2008) Systemic microdystrophin gene delivery improves skeletal muscle structure and function in old dystrophic mdx mice. Mol Ther 16:657–664

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grum VL, Li D, Macdonald RI, Mondragon A (1999) Structures of two repeats of spectrin suggest models of flexibility. Cell 98:523–535

    Article  CAS  PubMed  Google Scholar 

  • Harper SQ, Hauser MA, Dellorusso C, Duan D, Crawford RW, Phelps SF, Harper HA, Robinson AS, Engelhardt JF, Brooks SV, Chamberlain JS (2002) Modular flexibility of dystrophin: implications for gene therapy of duchenne muscular dystrophy. Nat Med 8:253–261

    Article  CAS  PubMed  Google Scholar 

  • Hayes NV, Scott C, Heerkens E, Ohanian V, Maggs AM, Pinder JC, Kordeli E, Baines AJ (2000) Identification of a novel C-terminal variant of beta II spectrin: two isoforms of beta II spectrin have distinct intracellular locations and activities. J Cell Sci 113(Pt 11):2023–2034

    CAS  PubMed  Google Scholar 

  • Helliwell TR, Man NT, Morris GE, Davies KE (1992) The dystrophin-related protein, utrophin, is expressed on the sarcolemma of regenerating human skeletal muscle fibres in dystrophies and inflammatory myopathies. Neuromuscul Disord 2:177–184

    Article  CAS  PubMed  Google Scholar 

  • Henderson DM, Lee A, Ervasti JM (2010) Disease-causing missense mutations in actin binding domain 1 of dystrophin induce thermodynamic instability and protein aggregation. Proc Natl Acad Sci U S A 107:9632–9637

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Holleran EA, Ligon LA, Tokito M, Stankewich MC, Morrow JS, Holzbaur EL (2001) beta III spectrin binds to the Arp1 subunit of dynactin. J Biol Chem 276:36598–36605

    Article  CAS  PubMed  Google Scholar 

  • Hryniewicz-Jankowska A, Bok E, Dubielecka P, Chorzalska A, Diakowski W, Jezierski A, Lisowski M, Sikorski AF (2004) Mapping of an ankyrin-sensitive, phosphatidylethanolamine/phosphatidylcholine mono- and bi-layer binding site in erythroid beta-spectrin. Biochem J 382:677–685

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang X, Poy F, Zhang R, Joachimiak A, Sudol M, Eck MJ (2000) Structure of a WW domain containing fragment of dystrophin in complex with beta-dystroglycan. Nat Struct Biol 7:634–638

    Article  CAS  PubMed  Google Scholar 

  • Hugnot JP, Gilgenkrantz H, Vincent N, Chafey P, Morris GE, Monaco AP, Berwald-Netter Y, Koulakoff A, Kaplan JC, Kahn A et al (1992) Distal transcript of the dystrophin gene initiated from an alternative first exon and encoding a 75-kDa protein widely distributed in nonmuscle tissues. Proc Natl Acad Sci U S A 89:7506–7510

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hyvonen M, Macias MJ, Nilges M, Oschkinat H, Saraste M, Wilmanns M (1995) Structure of the binding site for inositol phosphates in a PH domain. EMBO J 14:4676–4685

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ikeda Y, Dick KA, Weatherspoon MR, Gincel D, Armbrust KR, Dalton JC, Stevanin G, Durr A, Zuhlke C, Burk K, Clark HB, Brice A, Rothstein JD, Schut LJ, Day JW, Ranum LP (2006) Spectrin mutations cause spinocerebellar ataxia type 5. Nat Genet 38:184–190

    Article  CAS  PubMed  Google Scholar 

  • Ipsaro JJ, Mondragon A (2010) Structural basis for spectrin recognition by ankyrin. Blood 115:4093–5101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ipsaro JJ, Huang L, Mondragon A (2009) Structures of the spectrin-ankyrin interaction binding domains. Blood 113:5385–5393

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ipsaro JJ, Harper SL, Messick TE, Marmorstein R, Mondragon A, Speicher DW (2010) Crystal structure and functional interpretation of the erythrocyte spectrin tetramerization domain complex. Blood 115:4843–4852

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jackson M, Song W, Liu MY, Jin L, Dykes-Hoberg M, Lin CI, Bowers WJ, Federoff HJ, Sternweis PC, Rothstein JD (2001) Modulation of the neuronal glutamate transporter EAAT4 by two interacting proteins. Nature 410:89–93

    Article  CAS  PubMed  Google Scholar 

  • Jarmin S, Kymalainen H, Popplewell L, Dickson G (2014) New developments in the use of gene therapy to treat Duchenne muscular dystrophy. Expert Opin Biol Ther 14:209–230

    Article  CAS  PubMed  Google Scholar 

  • Keep NH, Norwood FLM, Moores CA, Winder SJ, Kendrick-Jones J (1999) The 2.0 a structure of the second calponin homology domain from the actin-binding region of the dystrophin homologue utrophin. J Mol Biol 285:1257–1264

    Article  CAS  PubMed  Google Scholar 

  • Khanna MR, Mattie FJ, Browder KC, Radyk MD, Crilly SE, Bakerink KJ, Harper SL, Speicher DW, Thomas GH (2015) Spectrin tetramer formation is not required for viable development in Drosophila. J Biol Chem 290:706–715

    Article  CAS  PubMed  Google Scholar 

  • Koenig M, Hoffman EP, Bertelson CJ, Monaco AP, Feener C, Kunkel LM (1987) Complete cloning of the Duchenne muscular dystrophy (DMD) cDNA and preliminary genomic organization of the DMD gene in normal and affected individuals. Cell 50:509–517

    Article  CAS  PubMed  Google Scholar 

  • Koenig M, Monaco AP, Kunkel LM (1988) The complete sequence of dystrophin predicts a rod-shaped cytoskeletal protein. Cell 53:219–226

    Article  CAS  PubMed  Google Scholar 

  • Koenig M, Beggs A, Moyer M, Scherpf S, Heindrich K, Bettecken T, Meng G, Muller C, Lindlof M, Kaariainen H (1989) The molecular basis for Duchenne versus Becker muscular dystrophy: correlation of severity with type of deletion. Am J Hum Genet 45:498–506

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kohler M, Clarenbach CF, Boni L, Brack T, Russi EW, Bloch KE (2005) Quality of life, physical disability, and respiratory impairment in Duchenne muscular dystrophy. Am J Respir Crit Care Med 172:1032–1036

    Article  PubMed  Google Scholar 

  • Korsgren C, Lux SE (2010) The carboxyterminal EF domain of erythroid alpha-spectrin is necessary for optimal spectrin-actin binding. Blood 116:2600–2607

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Korsgren C, Peters LL, Lux SE (2010) Protein 4.2 binds to the carboxyl-terminal EF-hands of erythroid alpha-spectrin in a calcium- and calmodulin-dependent manner. J Biol Chem 285:4757–4770

    Article  CAS  PubMed  Google Scholar 

  • Kotula L, Desilva TM, Speicher DW, Curtis PJ (1993) Functional characterization of recombinant human red cell alpha-spectrin polypeptides containing the tetramer binding site. J Biol Chem 268:14788–14793

    CAS  PubMed  Google Scholar 

  • Kusunoki H, Macdonald R, Mondragon A (2004a) Structural insights onto the stability and flexibility of unusual erythroid spectrin repeats. Structure 12:645–656

    Article  CAS  PubMed  Google Scholar 

  • Kusunoki H, Minasov G, Macdonald R, Mondragon A (2004b) Independent movement, dimerization and stability of tandem repeats of chicken brain alpha-spectrin. J Mol Biol 344:495–511

    Article  CAS  PubMed  Google Scholar 

  • Kwa LG, Wensley BG, Alexander CG, Browning SJ, Lichman BR, Clarke J (2014) The folding of a family of three-helix bundle proteins: spectrin R15 has a robust folding nucleus, unlike its homologous neighbours. J Mol Biol 426:1600–1610

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • La-Borde PJ, Stabach PR, Simonovic I, Morrow JS, Simonovic M (2010) Ankyrin recognizes both surface character and shape of the 14-15 di-repeat of beta-spectrin. Biochem Biophys Res Commun 392:490–494

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lai Y, Thomas GD, Yue Y, Yang HT, Li D, Long C, Judge L, Bostick B, Chamberlain JS, Terjung RL, Duan D (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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lai Y, Zhao J, Yue Y, Duan D (2013) alpha2 and alpha3 helices of dystrophin R16 and R17 frame a microdomain in the alpha1 helix of dystrophin R17 for neuronal NOS binding. Proc Natl Acad Sci U S A 110:525–530

    Article  CAS  PubMed  Google Scholar 

  • Law R, Carl P, Harper S, Dalhaimer P, Speicher DW, Discher DE (2003) Cooperativity in forced unfolding of tandem spectrin repeats. Biophys J 84:533–544

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Le Rumeur E, Fichou Y, Pottier S, Gaboriau F, Rondeau-Mouro C, Vincent M, Gallay J, Bondon A (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

    Article  CAS  PubMed  Google Scholar 

  • Le Rumeur E, Pottier S, DA Costa G, Metzinger L, Mouret L, Rocher C, Fourage M, Rondeau-Mouro C, Bondon A (2007) Binding of the dystrophin second repeat to membrane di-oleyl phospholipids is dependent upon lipid packing. Biochim Biophys Acta 1768:648–654

    Article  CAS  PubMed  Google Scholar 

  • Le Rumeur E, Winder SJ, Hubert JF (2010) Dystrophin: more than just the sum of its parts. Biochim Biophys Act 1804:1713–1722

    Article  CAS  Google Scholar 

  • Lecomte MC, Dhermy D, Garbarz M, Feo C, Gautero H, Bournier O, Picat C, Chaveroche I, Galand C, Boivin P (1987) Hereditary pyropoikilocytosis and elliptocytosis in a Caucasian family. Transmission of the same molecular defect in spectrin through three generations with different clinical expression. Hum Genet 77:329–334

    Article  CAS  PubMed  Google Scholar 

  • Lecomte MC, Garbarz M, Gautero H, Bournier O, Galand C, Boivin P, Dhermy D (1993) Molecular basis of clinical and morphological heterogeneity in hereditary elliptocytosis (HE) with spectrin alpha I variants. Br J Haematol 85:584–595

    Article  CAS  PubMed  Google Scholar 

  • Legardinier S, Hubert J-F, Le Bihan O, Tascon C, Rocher C, Raguénès-Nicol C, Bondon A, Hardy S, Le Rumeur E (2008) Sub-domains of the dystrophin rod domain display contrasting lipid-binding and stability properties. Biochim Biophys Acta 1784:672–682

    Article  CAS  PubMed  Google Scholar 

  • Legardinier S, Raguénès-Nicol C, Tascon C, Rocher C, Hardy S, Hubert JF, Le Rumeur E (2009) Mapping of the lipid-binding and stability properties of the central rod domain of human dystrophin. J Mol Biol 389:546–558

    Article  CAS  PubMed  Google Scholar 

  • Legrand B, Giudice E, Nicolas A, Delalande O, Le Rumeur E (2011) Computational study of the human dystrophin repeats: interaction properties and molecular dynamics. PLoS One 6:e23819

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leluk J, Hanus-Lorenz B, Sikorski AF (2001) Application of genetic semihomology algorithm to theoretical studies on various protein families. Acta Biochim Pol 48:21–33

    CAS  PubMed  Google Scholar 

  • Lemmon MA, Ferguson KM, Abrams CS (2002) Pleckstrin homology domains and the cytoskeleton. FEBS Lett 513:71–76

    Article  CAS  PubMed  Google Scholar 

  • Lidov HG, Selig S, Kunkel LM (1995) Dp140: a novel 140 kDa CNS transcript from the dystrophin locus. Hum Mol Genet 4:329–335

    Article  CAS  PubMed  Google Scholar 

  • Lin AY, Prochniewicz E, James ZM, Svensson B, Thomas DD (2011) Large-scale opening of utrophin’s tandem calponin homology (CH) domains upon actin binding by an induced-fit mechanism. Proc Natl Acad Sci U S A 108:12729–12733

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lorenzo DN, Li MG, Mische SE, Armbrust KR, Ranum LP, Hays TS (2010) Spectrin mutations that cause spinocerebellar ataxia type 5 impair axonal transport and induce neurodegeneration in Drosophila. J Cell Biol 189:143–158

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Machnicka B, Czogalla A, Hryniewicz-Jankowska A, Boguslawska DM, Grochowalska R, Heger E, Sikorski AF (2014) Spectrins: a structural platform for stabilization and activation of membrane channels, receptors and transporters. Biochim Biophys Acta 1838:620–634

    Article  CAS  PubMed  Google Scholar 

  • Macias MJ, Musacchio A, Ponstingl H, Nilges M, Saraste M, Oschkinat H (1994) Structure of the pleckstrin homology domain from beta-spectrin. Nature 369:675–677

    Article  CAS  PubMed  Google Scholar 

  • Mcgreevy JW, Hakim CH, Mcintosh MA, Duan D (2015) Animal models of Duchenne muscular dystrophy: from basic mechanisms to gene therapy. Dis Model Mech 8:195–213

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mehboob S, Song Y, Witek M, Long F, Santarsiero BD, Johnson ME, Fung LW (2010) Crystal structure of the nonerythroid alpha-spectrin tetramerization site reveals differences between erythroid and nonerythroid spectrin tetramer formation. J Biol Chem 285:14572–14584

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mirijanian DT, Chu JW, Ayton GS, Voth GA (2007) Atomistic and coarse-grained analysis of double spectrin repeat units: the molecular origins of flexibility. J Mol Biol 365:523–534

    Article  CAS  PubMed  Google Scholar 

  • Molza A-E, Férey N, Czjzek M, Le Rumeur E, Hubert J-F, Tek A, Laurent B, Baaden M, Delalande O (2014) Innovative interactive flexible docking method for multi-scale reconstruction elucidates dystrophin molecular assembly. Faraday Discuss 169:45–62

    Article  CAS  PubMed  Google Scholar 

  • Molza AE, Mangat K, Le Rumeur E, Hubert JF, Menhart N, Delalande O (2015) Structural basis of neuronal nitric-oxide synthase interaction with dystrophin repeats 16 and 17. J Biol Chem 290:29531–29541

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Monaco A, Bertelson C, Liechti-Gallati S, Moser H, Kunkel L (1988) An explanation for the phenotypic differences between patients bearing partial deletions of the DMD locus. Genomics 2:90–95

    Article  CAS  PubMed  Google Scholar 

  • Musacchio A, Noble M, Pauptit R, Wierenga R, Saraste M (1992) Crystal structure of a Src-homology 3 (SH3) domain. Nature 359:851–855

    Article  CAS  PubMed  Google Scholar 

  • Muthu M, Richardson KA, Sutherland-Smith AJ (2012) The crystal structures of dystrophin and utrophin spectrin repeats: implications for domain boundaries. PLoS One 7:e40066

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nans A, Mohandas N, Stokes DL (2011) Native ultrastructure of the red cell cytoskeleton by cryo-electron tomography. Biophys J 101:2341–2350

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nicolas G, Pedroni S, Fournier C, Gautero H, Craescu C, Dhermy D, Lecomte MC (1998) Spectrin self-association site: characterization and study of beta-spectrin mutations associated with hereditary elliptocytosis. Biochem J 332(Pt 1):81–89

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nicolas A, Lucchetti-Miganeh C, Ben Yaou R, Kaplan JC, Chelly J, Leturcq F, Barloy-Hubler F, Le Rumeur E (2012) Assessment of the structural and functional impact of in-frame mutations of the DMD gene, using the tools included in the eDystrophin online database. Orphanet J Rare Dis 7:45

    Article  PubMed  PubMed Central  Google Scholar 

  • Nicolas A, Delalande O, Hubert JF, Le Rumeur E (2014) The spectrin family of proteins: a unique coiled-coil fold for various molecular surface properties. J Struct Biol 186:392–401

    Article  CAS  PubMed  Google Scholar 

  • Nicolas A, Raguenes-Nicol C, Ben Yaou R, Ameziane-Le Hir S, Cheron A, Vie V, Claustres M, Leturcq F, Delalande O, Hubert JF, Tuffery-Giraud S, Giudice E, Le Rumeur E (2015) Becker muscular dystrophy severity is linked to the structure of dystrophin. Hum Mol Genet 24:1267–1279

    Article  CAS  PubMed  Google Scholar 

  • Nilges M, Macias MJ, O’donoghue SI, Oschkinat H (1997) Automated NOESY interpretation with ambiguous distance restraints: the refined NMR solution structure of the pleckstrin homology domain from beta-spectrin. J Mol Biol 269:408–422

    Article  CAS  PubMed  Google Scholar 

  • Norwood F, Sutherland-Smith A, Keep N, Kendrick-Jones J (2000) The structure of the N-terminal actin-binding domain of human dystrophin and how mutations in this domain may cause Duchenne or Becker muscular dystrophy. Structure 8:481–491

    Article  CAS  PubMed  Google Scholar 

  • Nudel U, Zuk D, Einat P, Zeelon E, Levy Z, Neuman S, Yaffe D (1989) Duchenne muscular dystrophy gene product is not identical in muscle and brain. Nature 337:76–78

    Article  CAS  PubMed  Google Scholar 

  • Ogawa Y, Schafer DP, Horresh I, Bar V, Hales K, Yang Y, Susuki K, Peles E, Stankewich MC, Rasband MN (2006) Spectrins and ankyrinB constitute a specialized paranodal cytoskeleton. J Neurosci 26:5230–5239

    Article  CAS  PubMed  Google Scholar 

  • Ohara O, Ohara R, Yamakawa H, Nakajima D, Nakayama M (1998) Characterization of a new beta-spectrin gene which is predominantly expressed in brain. Brain Res Mol Brain Res 57:181–192

    Article  CAS  PubMed  Google Scholar 

  • Parry DAD, Dixon TW, Cohen C (1992) Analysis of the three-alpha-helix motif in the spectrin superfamily of proteins. Biophys J 61:858–867

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Petrof BJ, Shrager JB, Stedmann HH, Kelly AM, Sweeney HL (1993) Dystrophin protects the sarcolemma from stresses developed during muscle contraction. Proceedings of the national academy of sciences, USA, 90, 3710–3714

    Google Scholar 

  • Prins KW, Humston JL, Mehta A, Tate V, Ralston E, Ervasti JM (2009) Dystrophin is a microtubule-associated protein. J Cell Biol 186:363–369

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rahimov F, Kunkel LM (2013) The cell biology of disease: cellular and molecular mechanisms underlying muscular dystrophy. J Cell Biol 201:499–510

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ribiero Ede A Jr, Pinotsis N, Ghisleni A, Salmazo A, Konarev PV, Kostan J, Sjöblum B, Schreiner C, Polyansky AA, Gkougkoulia EA, Holt MR, Aachnann FL, Zagrovic B, Bordignon E, Pirker KF, Svergun DI, Gautel M, Djinovic-Carugo K. (2014) The structure and regulation of human muscle α-actinin. Cell 159:1447–1460

    Google Scholar 

  • Robertsson J, Petzold K, Löfvenberg L, Backman L (2005) Folding of spectrin’s SH3 domain in the presence of spectrin repeats. Cell Mol Biol Lett 10(4):595–612, PubMed PMID: 16341269

    Google Scholar 

  • Sahr KE, Laurila P, Kotula L, Scarpa AL, Coupal E, Leto TL, Linnenbach AJ, Winkelmann JC, Speicher DW, VT M et al (1990) The complete cDNA and polypeptide sequences of human erythroid alpha-spectrin. J Biol Chem 265:4434–4443

    CAS  PubMed  Google Scholar 

  • Saitsu H, Tohyama J, Kumada T, Egawa K, Hamada K, Okada I, Mizuguchi T, Osaka H, Miyata R, Furukawa T, Haginoya K, Hoshino H, Goto T, Hachiya Y, Yamagata T, Saitoh S, Nagai T, Nishiyama K, Nishimura A, Miyake N, Komada M, Hayashi K, Hirai S, Ogata K, Kato M, Fukuda A, Matsumoto N (2010) Dominant-negative mutations in alpha-II spectrin cause west syndrome with severe cerebral hypomyelination, spastic quadriplegia, and developmental delay. Am J Hum Genet 86:881–891

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sander M, Chavoshan B, Harris SA, Iannaccone ST, Stull JT, Thomas GD, Victor RG (2000) Functional muscle ischemia in neuronal nitric oxide synthase-deficient skeletal muscle of children with Duchenne muscular dystrophy. Proc Natl Acad Sci U S A 97:13818–13823

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sarkis J, Hubert JF, Legrand B, Robert E, Cheron A, Jardin J, Hitti E, Le Rumeur E, Vie V (2011) Spectrin-like repeats 11–15 of human dystrophin show adaptations to a lipidic environment. J Biol Chem 286:30481–30491

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sato K, Yokota T, Ichioka S, Shibata M, Takeda S (2008) Vasodilation of intramuscular arterioles under shear stress in dystrophin-deficient skeletal muscle is impaired through decreased nNOS expression. Act Myol 27:30–36

    CAS  Google Scholar 

  • Seto JT, Ramos JN, Muir L, Chamberlain JS, Odom GL (2012) Gene replacement therapies for duchenne muscular dystrophy using adeno-associated viral vectors. Curr Gene Ther 12:139–151

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sikorski AF, Terlecki G, Zagon IS, Goodman SR (1991) Synapsin I-mediated interaction of brain spectrin with synaptic vesicles. J Cell Biol 114:313–318

    Article  CAS  PubMed  Google Scholar 

  • Sikorski AF, Sangerman J, Goodman SR, Critz SD (2000) Spectrin (betaSpIIsigma1) is an essential component of synaptic transmission. Brain Res 852:161–166

    Article  CAS  PubMed  Google Scholar 

  • Singh SM, Mallela KM (2012) The N-terminal actin-binding tandem calponin-homology (CH) domain of dystrophin is in a closed conformation in solution and when bound to F-actin. Biophys J 103:1970–1978

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stabach PR, Morrow JS (2000) Identification and characterization of beta V spectrin, a mammalian ortholog of Drosophila beta H spectrin. J Biol Chem 275:21385–21395

    Article  CAS  PubMed  Google Scholar 

  • Stabach PR, Simonovic I, Ranieri MA, Aboodi MS, Steitz TA, Simonovic M, Morrow JS (2009) The structure of the ankyrin-binding site of beta-spectrin reveals how tandem spectrin-repeats generate unique ligand-binding properties. Blood 113:5377–5384

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stankewich MC, Tse WT, Peters LL, Ch’ng Y, John KM, Stabach PR, Devarajan P, Morrow JS, Lux SE (1998) A widely expressed betaIII spectrin associated with Golgi and cytoplasmic vesicles. Proc Natl Acad Sci U S A 95:14158–14163

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sutherland-Smith AJ, Moores CA, Norwood FL, Hatch V, Craig R, Kendrick-Jones J, Lehman W (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

    Article  CAS  PubMed  Google Scholar 

  • Tinsley J, Blake D, Roche A, Fairbrother U, Riss J, Byth B, Knight A, Kendrick-Jones J, Suthers G, Love D, Edwards Y, Davies K (1992) Primary stucture of dystrophin- related protein. Nature 360:591–593

    Article  CAS  PubMed  Google Scholar 

  • Tuffery-Giraud S, Beroud C, Leturcq F, Yaou RB, Hamroun D, Michel-Calemard L, Moizard MP, Bernard R, Cossee M, Boisseau P, Blayau M, Creveaux I, Guiochon-Mantel A, De Martinville B, Philippe C, Monnier N, Bieth E, Khau Van Kien P, Desmet FO, Humbertclaude V, Kaplan JC, Chelly J, Claustres M (2009) Genotype-phenotype analysis in 2,405 patients with a dystrophinopathy using the UMD-DMD database: a model of nationwide knowledgebase. Hum Mutat 30:934–945

    Article  CAS  PubMed  Google Scholar 

  • Voas MG, Lyons DA, Naylor SG, Arana N, Rasband MN, Talbot WS (2007) alphaII-spectrin is essential for assembly of the nodes of Ranvier in myelinated axons. Curr Biol 17:562–568

    Article  CAS  PubMed  Google Scholar 

  • Waller KL, Nunomura W, An X, Cooke BM, Mohandas N, Coppel RL (2003) Mature parasite-infected erythrocyte surface antigen (MESA) of Plasmodium falciparum binds to the 30-kDa domain of protein 4.1 in malaria-infected red blood cells. Blood 102:1911–1914

    Article  CAS  PubMed  Google Scholar 

  • Wein N, Alfano L, Flanigan KM (2015) Genetics and emerging treatments for Duchenne and Becker muscular dystrophy. Pediatr Clin N Am 62(3):723–742

    Article  Google Scholar 

  • Wichterle H, Hanspal M, Palek J, Jarolim P (1996) Combination of two mutant alpha spectrin alleles underlies a severe spherocytic hemolytic anemia. J Clin Invest 98:2300–2307

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wilmotte R, Harper SL, Ursitti JA, Marechal J, Delaunay J, Speicher DW (1997) The exon 46-encoded sequence is essential for stability of human erythroid alpha-spectrin and heterodimer formation. Blood 90:4188–4196

    CAS  PubMed  Google Scholar 

  • Wilton SD, Veedu RN, Fletcher S (2015) The emperor’s new dystrophin: finding sense in the noise. Trends Mol Med 21(7):417–426

    Google Scholar 

  • Winder SJ, Gibson TJ, Kendrick-Jones J (1995) Dystrophin and utrophin: the missing links! FEBS Lett 369:27–33

    Article  CAS  PubMed  Google Scholar 

  • Winkelmann JC, Chang JG, Tse WT, Scarpa AL, Marchesi VT, Forget BG (1990) Full-length sequence of the cDNA for human erythroid beta-spectrin. J Biol Chem 265:11827–11832

    CAS  PubMed  Google Scholar 

  • Wolny M, Grzybek M, Bok E, Chorzalska A, Lenoir M, Czogalla A, Adamczyk K, Kolondra A, Diakowski W, Overduin M, Sikorski AF (2011) Key amino acid residues of ankyrin-sensitive phosphatidylethanolamine/phosphatidylcholine-lipid binding site of betaI-spectrin. PLoS One 6:e21538

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Writzl K, Primec ZR, Strazisar BG, Osredkar D, Pecaric-Meglic N, Kranjc BS, Nishiyama K, Matsumoto N, Saitsu H (2012) Early onset West syndrome with severe hypomyelination and coloboma-like optic discs in a girl with SPTAN1 mutation. Epilepsia 53:e106–e110

    Article  CAS  PubMed  Google Scholar 

  • Xu K, Zhong G, Zhuang X (2013) Actin, spectrin, and associated proteins form a periodic cytoskeletal structure in axons. Science 339:452–456

    Article  CAS  PubMed  Google Scholar 

  • Yan Y, Winograd E, Viel A, Cronin T, Harrison SC, Branton D (1993) Crystal structure of the repetitive segments of spectrin. Science 262:2027–2030

    Article  CAS  PubMed  Google Scholar 

  • Zhang P, Talluri S, Deng H, Branton D, Wagner G (1995) Solution structure of the pleckstrin homology domain of drosophila beta-spectrin. Structure 3:1185–1195

    Article  CAS  PubMed  Google Scholar 

  • Zhang Z, Weed SA, Gallagher PG, Morrow JS (2001) Dynamic molecular modeling of pathogenic mutations in the spectrin self-association domain. Blood 98:1645–1653

    Article  CAS  PubMed  Google Scholar 

  • Zimmer WE, Zhao Y, Sikorski AF, Critz SD, Sangerman J, Elferink LA, Xu XS, Goodman SR (2000) The domain of brain beta-spectrin responsible for synaptic vesicle association is essential for synaptic transmission. Brain Res 881:18–27

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institut de Génétique et Développement de Rennes, UMR CNRS 6290, Université de Rennes 1, Rennes, France

    Olivier Delalande, Jean-François Hubert & Elisabeth Le Rumeur

  2. Biotechnology Faculty, Department of Cytobiochemistry, University of Wrocław, ul. joliot-Curie 14a, 50-383, Wroclaw, Poland

    Aleksander Czogalla & Aleksander Sikorski

Authors
  1. Olivier Delalande
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Aleksander Czogalla
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jean-François Hubert
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Aleksander Sikorski
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Elisabeth Le Rumeur
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Olivier Delalande .

Editor information

Editors and Affiliations

  1. Institute of Fundamental Sciences and Riddet Institute, Massey University, Palmerston North, New Zealand

    David A.D. Parry

  2. Muscle Contraction Group, School of Physiology, Pharmacology and Neuroscience, University of Bristol, Bristol, United Kingdom

    John M. Squire

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer International Publishing AG

About this chapter

Cite this chapter

Delalande, O., Czogalla, A., Hubert, JF., Sikorski, A., Le Rumeur, E. (2017). Dystrophin and Spectrin, Two Highly Dissimilar Sisters of the Same Family. In: Parry, D., Squire, J. (eds) Fibrous Proteins: Structures and Mechanisms. Subcellular Biochemistry, vol 82. Springer, Cham. https://doi.org/10.1007/978-3-319-49674-0_12

Download citation

Publish with us

Policies and ethics

Search

Navigation