Skip to main content

Advertisement

Log in

Lessons from a tarantula: new insights into myosin interacting-heads motif evolution and its implications on disease

  • Review
  • Published:
Biophysical Reviews Aims and scope Submit manuscript

Abstract

Tarantula’s leg muscle thick filament is the ideal model for the study of the structure and function of skeletal muscle thick filaments. Its analysis has given rise to a series of structural and functional studies, leading, among other things, to the discovery of the myosin interacting-heads motif (IHM). Further electron microscopy (EM) studies have shown the presence of IHM in frozen-hydrated and negatively stained thick filaments of striated, cardiac, and smooth muscle of bilaterians, most showing the IHM parallel to the filament axis. EM studies on negatively stained heavy meromyosin of different species have shown the presence of IHM on sponges, animals that lack muscle, extending the presence of IHM to metazoans. The IHM evolved about 800 MY ago in the ancestor of Metazoa, and independently with functional differences in the lineage leading to the slime mold Dictyostelium discoideum (Mycetozoa). This motif conveys important functional advantages, such as Ca2+ regulation and ATP energy-saving mechanisms. Recent interest has focused on human IHM structure in order to understand the structural basis underlying various conditions and situations of scientific and medical interest: the hypertrophic and dilated cardiomyopathies, overfeeding control, aging and hormone deprival muscle weakness, drug design for schistosomiasis control, and conditioning exercise physiology for the training of power athletes.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Alamo L, Koubassova N, Pinto A, Gillilan R, Tsaturyan A, Padrón R (2017a) Lessons from a tarantula: new insights into thick filament and myosin interacting-heads motif structure and function. Biophys Rev. doi:10.1007/s12551-017-0295-1

    CAS  PubMed  PubMed Central  Google Scholar 

  • Alamo L, Qi D, Wriggers W, Pinto A, Zhu J, Bilbao A, Gillilan RE, Hu S, Padrón R (2016) Conserved intramolecular interactions maintain myosin interacting-heads motifs explaining tarantula muscle super-relaxed state structural basis. J Mol Biol 428:1142–1164

    CAS  PubMed  PubMed Central  Google Scholar 

  • Alamo L, Ware JS, Pinto A, Gillilan RE, Seidman JG, Seidman CE, Padrón R (2017b) Effects of myosin variants on interacting-heads motif explain distinct hypertrophic and dilated cardiomyopathy phenotypes. eLife 6:e24634. doi:10.7554/eLife.24634

    Article  PubMed  PubMed Central  Google Scholar 

  • Alamo L, Wriggers W, Pinto A, Bártoli F, Salazar L, Zhao FQ, Craig R, Padrón R (2008) Three-dimensional reconstruction of tarantula myosin filaments suggests how phosphorylation may regulate myosin activity. J Mol Biol 384:780–797

    CAS  PubMed  PubMed Central  Google Scholar 

  • Al-Khayat HA, Kensler RW, Squire JM, Marston SB, Morris EP (2013) Atomic model of the human cardiac muscle myosin filament. Proc Natl Acad Sci U S A 110:318–323

    CAS  PubMed  Google Scholar 

  • Al-Khayat HA, Morris EP, Kensler RW, Squire JM (2008) Myosin filament 3D structure in mammalian cardiac muscle. J Struct Biol 163:117–126

    CAS  PubMed  PubMed Central  Google Scholar 

  • Al-Khayat HA, Morris EP, Squire JM (2009) The 7-stranded structure of relaxed scallop muscle myosin filaments: support for a common head configuration in myosin-regulated muscles. J Struct Biol 166:183–194

    CAS  PubMed  Google Scholar 

  • Ashrafian H, McKenna WJ, Watkins H (2011) Disease pathways and novel therapeutic targets in hypertrophic cardiomyopathy. Circ Res 109:86–96

    CAS  PubMed  Google Scholar 

  • Ashrafian H, Redwood C, Blair E, Watkins H (2003) Hypertrophic cardiomyopathy: a paradigm for myocardial energy depletion. Trends Genet 19:263–268

    CAS  PubMed  Google Scholar 

  • Bergquist R, Utzinger J, Keiser J (2017) Controlling schistosomiasis with praziquantel: how much longer without a viable alternative? Infect Dis Poverty 6:74

    PubMed  PubMed Central  Google Scholar 

  • Blankenfeldt W, Thomä NH, Wray JS, Gautel M, Schlichting I (2006) Crystal structures of human cardiac beta-myosin II S2-delta provide insight into the functional role of the S2 subfragment. Proc Natl Acad Sci U S A 103:17713–17717

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bosgraaf L, van Haastert PJ (2006) The regulation of myosin II in Dictyostelium. Eur J Cell Biol 85:969–979

    CAS  PubMed  Google Scholar 

  • Brito R, Alamo L, Lundberg U, Guerrero JR, Pinto A, Sulbarán G, Gawinowicz MA, Craig R, Padrón R (2011) A molecular model of phosphorylation-based activation and potentiation of tarantula muscle thick filaments. J Mol Biol 414:44–61

    CAS  PubMed  PubMed Central  Google Scholar 

  • Burgess SA, Yu S, Walker ML, Hawkins RJ, Chalovich JM, Knight PJ (2007) Structures of smooth muscle myosin and heavy meromyosin in the folded, shutdown state. J Mol Biol 372:1165–1178

    CAS  PubMed  Google Scholar 

  • Cavalier-Smith T, Chao EE, Snell EA, Berney C, Fiore-Donno AM, Lewis R (2014) Multigene eukaryote phylogeny reveals the likely protozoan ancestors of opisthokonts (animals, fungi, choanozoans) and Amoebozoa. Mol Phylogenet Evol 81:71–85

    PubMed  Google Scholar 

  • Christensen K, Doblhammer G, Rau R, Vaupel JW (2009) Ageing populations: the challenges ahead. Lancet 374:1196–1208

    PubMed  PubMed Central  Google Scholar 

  • Colegrave M, Peckham M (2014) Structural implications of beta-cardiac myosin heavy chain mutations in human disease. Anat Rec (Hoboken) 297:1670–1680

    CAS  Google Scholar 

  • Colson BA, Petersen KJ, Collins BC, Lowe DA, Thomas DD (2015) The myosin super-relaxed state is disrupted by estradiol deficiency. Biochem Biophys Res Commun 456:151–155

    CAS  PubMed  Google Scholar 

  • Coluccio LM (2008) Myosin: a superfamily of molecular motors. Springer, Dordrecht

    Google Scholar 

  • Cooke R (2011) The role of the myosin ATPase activity in adaptive thermogenesis by skeletal muscle. Biophys Rev 3:33–45

    CAS  PubMed  PubMed Central  Google Scholar 

  • Craig R, Woodhead JL (2006) Structure and function of myosin filaments. Curr Opin Struct Biol 16:204–212

    CAS  PubMed  Google Scholar 

  • Doenhoff MJ, Cioli D, Utzinger J (2008) Praziquantel: mechanisms of action, resistance and new derivatives for schistosomiasis. Curr Opin Infect Dis 21:659–667

    CAS  PubMed  Google Scholar 

  • Dulyaninova NG, Bresnick AR (2013) The heavy chain has its day: regulation of myosin-II assembly. BioArchitecture 3:77–85

    PubMed  PubMed Central  Google Scholar 

  • Erwin DH (2015) Early metazoan life: divergence, environment and ecology. Philos Trans R Soc Lond Ser B Biol Sci 370:20150036

    Google Scholar 

  • Fee L, Lin W, Qiu F, Edwards RJ (2017) Myosin II sequences for Lethocerus indicus. J Muscle Res Cell Motil. doi:10.1007/s10974-017-9476-6

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fritz-Laylin LK, Prochnik SE, Ginger ML, Dacks JB, Carpenter ML, Field MC, Kuo A, Paredez A, Chapman J, Pham J, Shu S, Neupane R, Cipriano M, Mancuso J, Tu H, Salamov A, Lindquist E, Shapiro H, Lucas S, Grigoriev IV, Cande WZ, Fulton C, Rokhsar DS, Dawson SC (2010) The genome of Naegleria gruberi illuminates early eukaryotic versatility. Cell 140:631–642

    CAS  PubMed  Google Scholar 

  • Gago P (2016) Post activation potentiation: modulating factors and mechanisms for muscle performance. Ph.D. thesis. The Swedish School of Sport and Health Sciences, Stockholm

  • Gago P, Arndt A, Ekblom MM (2017) Post activation potentiation of the plantarflexors: implications of knee angle variations. J Hum Kin 57:29–38

    Google Scholar 

  • Gago P, Arndt A, Tarassova O, Ekblom MM (2014a) Post activation potentiation can be induced without impairing tendon stiffness. Eur J Appl Physiol 114:2299–2308

    PubMed  Google Scholar 

  • Gago P, Marques MC, Marinho DA, Ekblom MM (2014b) Passive muscle length changes affect twitch potentiation in power athletes. Med Sci Sports Exerc 46:1334–1342

    PubMed  Google Scholar 

  • Geisterfer-Lowrance AA, Kass S, Tanigawa G, Vosberg HP, McKenna W, Seidman CE, Seidman JG (1990) A molecular basis for familial hypertrophic cardiomyopathy: a beta cardiac myosin heavy chain gene missense mutation. Cell 62:999–1006

    CAS  PubMed  Google Scholar 

  • Gillilan RE, Kumar VS, O’Neall-Hennessey E, Cohen C, Brown JH (2013) X-ray solution scattering of squid heavy meromyosin: strengthening the evidence for an ancient compact off state. PLoS One 8:e81994

    PubMed  PubMed Central  Google Scholar 

  • Gnanasekar M, Salunkhe AM, Mallia AK, He YX, Kalyanasundaram R (2009) Praziquantel affects the regulatory myosin light chain of Schistosoma mansoni. Antimicrob Agents Chemother 53:1054–1060

    CAS  PubMed  Google Scholar 

  • González-Solá M, Al-Khayat HA, Behra M, Kensler RW (2014) Zebrafish cardiac muscle thick filaments: isolation technique and three-dimensional structure. Biophys J 106:1671–1680

    PubMed  PubMed Central  Google Scholar 

  • Green EM, Wakimoto H, Anderson RL, Evanchik MJ, Gorham JM, Harrison BC, Henze M, Kawas R, Oslob JD, Rodriguez HM, Song Y, Wan W, Leinwand LA, Spudich JA, McDowell RS, Seidman JG, Seidman CE (2016) A small-molecule inhibitor of sarcomere contractility suppresses hypertrophic cardiomyopathy in mice. Science 351:617–621

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gregorich ZR, Peng Y, Cai W, Jin Y, Wei L, Chen AJ, McKiernan SH, Aiken JM, Moss RL, Diffee GM, Ge Y (2016) Top-down targeted proteomics reveals decrease in myosin regulatory light-chain phosphorylation that contributes to sarcopenic muscle dysfunction. J Proteome Res 15:2706–2716

    CAS  PubMed  PubMed Central  Google Scholar 

  • Griffith LM, Downs SM, Spudich JA (1987) Myosin light chain kinase and myosin light chain phosphatase from Dictyostelium: effects of reversible phosphorylation on myosin structure and function. J Cell Biol 104:1309–1323

    CAS  PubMed  Google Scholar 

  • Gruen M, Gautel M (1999) Mutations in beta-myosin S2 that cause familial hypertrophic cardiomyopathy (FHC) abolish the interaction with the regulatory domain of myosin-binding protein-C. J Mol Biol 286:933–949

    CAS  PubMed  Google Scholar 

  • Hooijman P, Stewart MA, Cooke R (2011) A new state of cardiac myosin with very slow ATP turnover: a potential cardioprotective mechanism in the heart. Biophys J 100:1969–1976

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hooper SL, Thuma JB (2005) Invertebrate muscles: muscle specific genes and proteins. Physiol Rev 85:1001–1060

    CAS  PubMed  Google Scholar 

  • Hu Z, Taylor DW, Reedy MK, Edwards RJ, Taylor KA (2016) Structure of myosin filaments from relaxed Lethocerus flight muscle by cryo-EM at 6 Å resolution. Sci Adv 2:e1600058

    PubMed  PubMed Central  Google Scholar 

  • Huxley H, Hanson J (1954) Changes in the cross-striations of muscle during contraction and stretch and their structural interpretation. Nature 173:973–976

    CAS  PubMed  Google Scholar 

  • Huxley AF, Niedergerke R (1954) Structural changes in muscle during contraction; interference microscopy of living muscle fibres. Nature 173:971–973

    CAS  PubMed  Google Scholar 

  • Jung HS, Burgess SA, Billington N, Colegrave M, Patel H, Chalovich JM, Chantler PD, Knight PJ (2008a) Conservation of the regulated structure of folded myosin 2 in species separated by at least 600 million years of independent evolution. Proc Natl Acad Sci U S A 105:6022–6026

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jung HS, Komatsu S, Ikebe M, Craig R (2008b) Head–head and head–tail interaction: a general mechanism for switching off myosin II activity in cells. Mol Biol Cell 19:3234–3242

    CAS  PubMed  PubMed Central  Google Scholar 

  • Konno T, Chang S, Seidman JG, Seidman CE (2010) Genetics of hypertrophic cardiomyopathy. Curr Opin Cardiol 25:205–209

    PubMed  Google Scholar 

  • Lai DH, Hong XK, Su BX, Liang C, Hide G, Zhang X, Yu X, Lun ZR (2016) Current status of Clonorchis sinensis and clonorchiasis in China. Trans R Soc Trop Med Hyg 110:21–27

    CAS  PubMed  Google Scholar 

  • Lee K, Yang S, Liu X, Korn ED, Sarsoza F, Bernstein SI, Pollard L, Lord MJ, Trybus KM, Craig R (2016) Myosin II head interaction in primitive species. Biophys J 110(Supplement 1, issue 3):615a

    Google Scholar 

  • Liu J, Wendt T, Taylor D, Taylor K (2003) Refined model of the 10S conformation of smooth muscle myosin by cryo-electron microscopy 3D image reconstruction. J Mol Biol 329:963–972

    CAS  PubMed  Google Scholar 

  • Lorenzo-Morales J, Khan NA, Walochnik J (2015) An update on Acanthamoeba keratitis: diagnosis, pathogenesis and treatment. Parasite 22:10

    PubMed  PubMed Central  Google Scholar 

  • Moore JR, Leinwand L, Warshaw DM (2012) Understanding cardiomyopathy phenotypes based on the functional impact of mutations in the myosin motor. Circ Res 111:375–385

    CAS  PubMed  PubMed Central  Google Scholar 

  • Naber N, Cooke R, Pate E (2011) Slow myosin ATP turnover in the super-relaxed state in tarantula muscle. J Mol Biol 411:943–950

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nag S, Trivedi DV, Sarkar SS, Adhikari AS, Sunitha MS, Sutton S, Ruppel KM, Spudich JA (2017) The myosin mesa and the basis of hypercontractility caused by hypertrophic cardiomyopathy mutations. Nat Struct Mol Biol 24:525–533

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nogara L, Naber N, Pate E, Canton M, Reggiani C, Cooke R (2016a) Piperine’s mitigation of obesity and diabetes can be explained by its up-regulation of the metabolic rate of resting muscle. Proc Natl Acad Sci U S A 113:13009–13014

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nogara L, Naber N, Pate E, Canton M, Reggiani C, Cooke R (2016b) Spectroscopic studies of the super relaxed state of skeletal muscle. PLoS One 11:e0160100

    PubMed  PubMed Central  Google Scholar 

  • Parfrey LW, Lahr DJ, Knoll AH, Katz LA (2011) Estimating the timing of early eukaryotic diversification with multigene molecular clocks. Proc Natl Acad Sci U S A 108:13624–13629

    CAS  PubMed  PubMed Central  Google Scholar 

  • Peterson KJ, Lyons JB, Nowak KS, Takacs CM, Wargo MJ, McPeek MA (2004) Estimating metazoan divergence times with a molecular clock. Proc Natl Acad Sci U S A 101:6536–6541

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, Ferrin TE (2004) UCSF chimera—a visualization system for exploratory research and analysis. J Comput Chem 25:1605–1612

    CAS  PubMed  Google Scholar 

  • Pinto A, Sánchez F, Alamo L, Padrón R (2012) The myosin interacting-heads motif is present in the relaxed thick filament of the striated muscle of scorpion. J Struct Biol 180:469–478

    CAS  PubMed  Google Scholar 

  • Ross AG, Chau TN, Inobaya MT, Olveda RM, Li Y, Harn DA (2017) A new global strategy for the elimination of schistosomiasis. Int J Infect Dis 54:130–137

    CAS  PubMed  Google Scholar 

  • Schmitt JP, Debold EP, Ahmad F, Armstrong A, Frederico A, Conner DA, Mende U, Lohse MJ, Warshaw D, Seidman CE, Seidman JG (2006) Cardiac myosin missense mutations cause dilated cardiomyopathy in mouse models and depress molecular motor function. Proc Natl Acad Sci U S A 103:14525–14530

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schuchert P, Reber-Müller S, Schmid V (1993) Life stage specific expression of a myosin heavy chain in the hydrozoan Podocoryne carnea. Differentiation 54:11–18

    CAS  PubMed  Google Scholar 

  • Seidman CE, Seidman JG (1991) Mutations in cardiac myosin heavy chain genes cause familial hypertrophic cardiomyopathy. Mol Biol Med 8:159–166

    CAS  PubMed  Google Scholar 

  • Seipel K, Schmid V (2005) Evolution of striated muscle: jellyfish and the origin of triploblasty. Dev Biol 282:14–26

    CAS  PubMed  Google Scholar 

  • Sellers JR (1999) Myosins, 2nd edn. Oxford University Press, Oxford

    Google Scholar 

  • Sellers JR (2000) Myosins: a diverse superfamily. Biochim Biophys Acta 1496:3–22

    CAS  PubMed  Google Scholar 

  • Steinmetz PR, Kraus JE, Larroux C, Hammel JU, Amon-Hassenzahl A, Houliston E, Wörheide G, Nickel M, Degnan BM, Technau U (2012) Independent evolution of striated muscles in cnidarians and bilaterians. Nature 487:231–234

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sulbarán G, Alamo L, Pinto A, Márquez G, Méndez F, Padrón R, Craig R (2014) Schistosome muscles contain striated muscle-like myosin filaments in a smooth muscle-like architecture. Biophys J 106(2):159a

    Google Scholar 

  • Sulbarán G, Alamo L, Pinto A, Márquez G, Méndez F, Padrón R, Craig R (2015a) An invertebrate smooth muscle with striated muscle myosin filaments. Proc Natl Acad Sci U S A 112:E5660–E5668

    PubMed  PubMed Central  Google Scholar 

  • Sulbarán G, Biasutto A, Alamo L, Riggs C, Pinto A, Méndez F, Craig R, Padrón R (2013) Different head environments in tarantula thick filaments support a cooperative activation process. Biophys J 105:2114–2122

    PubMed  PubMed Central  Google Scholar 

  • Sulbarán G, Mun JY, Lee KH, Alamo L, Pinto A, Sato O, Ikebe M, Liu X, Korn ED, Padrón R, Craig R (2015b) The inhibited, interacting-heads motif characterizes myosin II from the earliest animals with muscle. Biophys J 108:301a

    Google Scholar 

  • Telford MJ, Budd GE, Philippe H (2015) Phylogenomic insights into animal evolution. Curr Biol 25:R876–R887

    CAS  PubMed  Google Scholar 

  • Trybus KM (1994) Role of myosin light chains. J Muscle Res Cell Motil 15:587–594

    CAS  PubMed  Google Scholar 

  • Tyska MJ, Hayes E, Giewat M, Seidman CE, Seidman JG, Warshaw DM (2000) Single-molecule mechanics of R403Q cardiac myosin isolated from the mouse model of familial hypertrophic cardiomyopathy. Circ Res 86:737–744

    CAS  PubMed  Google Scholar 

  • Waldmüller S, Erdmann J, Binner P, Gelbrich G, Pankuweit S, Geier C, Timmermann B, Haremza J, Perrot A, Scheer S, Wachter R, Schulze-Waltrup N, Dermintzoglou A, Schönberger J, Zeh W, Jurmann B, Brodherr T, Börgel J, Farr M, Milting H, Blankenfeldt W, Reinhardt R, Özcelik C, Osterziel KJ, Loeffler M, Maisch B, Regitz-Zagrosek V, Schunkert H, Scheffold T (2011) Novel correlations between the genotype and the phenotype of hypertrophic and dilated cardiomyopathy: results from the German Competence Network Heart Failure. Eur J Heart Fail 13:1185–1192

    PubMed  Google Scholar 

  • Wang Y, Steimle PA, Ren Y, Ross CA, Robinson DN, Egelhoff TT, Sesaki H, Iijima M (2011) Dictyostelium huntingtin controls chemotaxis and cytokinesis through the regulation of myosin II phosphorylation. Mol Biol Cell 22:2270–2281

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wendt T, Taylor D, Messier T, Trybus KM, Taylor KA (1999) Visualization of head–head interactions in the inhibited state of smooth muscle myosin. J Cell Biol 147:1385–1390

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wendt T, Taylor D, Trybus KM, Taylor K (2001) Three-dimensional image reconstruction of dephosphorylated smooth muscle heavy meromyosin reveals asymmetry in the interaction between myosin heads and placement of subfragment 2. Proc Natl Acad Sci U S A 98:4361–4366

    CAS  PubMed  PubMed Central  Google Scholar 

  • Woodhead JL, Zhao FQ, Craig R (2013) Structural basis of the relaxed state of a Ca2+-regulated myosin filament and its evolutionary implications. Proc Natl Acad Sci U S A 110:8561–8566

    CAS  PubMed  PubMed Central  Google Scholar 

  • Woodhead JL, Zhao FQ, Craig R, Egelman EH, Alamo L, Padrón R (2005) Atomic model of a myosin filament in the relaxed state. Nature 436:1195–1199

    CAS  PubMed  Google Scholar 

  • Yang S, Lee K, Sato O, Ikebe M, Craig R (2017) 3D Reconstruction of the folded, inhibited form of vertebrate smooth muscle myosin II by single particle analysis. Biophys J 112:266a

    Google Scholar 

  • Zhao FQ, Craig R, Woodhead JL (2009) Head–head interaction characterizes the relaxed state of Limulus muscle myosin filaments. J Mol Biol 385:423–431

    CAS  PubMed  Google Scholar 

  • Zoghbi ME, Woodhead JL, Moss RL, Craig R (2008) Three-dimensional structure of vertebrate cardiac muscle myosin filaments. Proc Natl Acad Sci U S A 105:2386–2390

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank Dr. Gustavo Márquez for help with the manuscript. Molecular graphics images were produced using the UCSF Chimera package (Pettersen et al. 2004) from the Resource for Biocomputing, Visualization, and Informatics at the University of California, San Francisco (supported by the National Institutes of Health grant P41 RR-01081). This work was supported in part by Centro de Biología Estructural del Mercosur (http://www.cebem-lat.org) (to R.P.) and the Howard Hughes Medical Institute (to R.P.).

We dedicate this review to the memory of Dr. Hugh E. Huxley.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Raúl Padrón.

Ethics declarations

Conflict of interest

Lorenzo Alamo declares that he has no conflicts of interest. Antonio Pinto declares that he has no conflicts of interest. Guidenn Sulbarán declares that he has no conflicts of interest. Jesús Mavárez declares that he has no conflicts of interest. Raúl Padrón declares that he has no conflicts of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Additional information

This article is part of a Special Issue on ‘Latin America’ edited by Pietro Ciancaglini and Rosangela Itri.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Alamo, L., Pinto, A., Sulbarán, G. et al. Lessons from a tarantula: new insights into myosin interacting-heads motif evolution and its implications on disease. Biophys Rev 10, 1465–1477 (2018). https://doi.org/10.1007/s12551-017-0292-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12551-017-0292-4

Keywords

Navigation