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Bioinformatics and Biology Insights Structural and Functional Insights Bioinformatics and Biology Insights OPEN ACCESS Full open access to this and thousands of other papers at REVIEW http://www.la-press.com. Structural and Functional Insights on the Myosin Superfamily Divya P. Syamaladevi1,2, James A. Spudich1,3,* and R. Sowdhamini1,* 1National Centre for Biological Sciences (NCBS-TIFR), GKVK Campus, Bellary Road, Bangalore, India. 2Sugarcane Breeding Institute (SBI-ICAR), Coimbatore, Tamilnadu, India. 3Department of Biochemistry, Stanford University, Stanford, California. *Corresponding authors email: [email protected]; [email protected] Abstract: The myosin superfamily is a versatile group of molecular motors involved in the transport of specific biomolecules, vesicles and organelles in eukaryotic cells. The processivity of myosins along an actin filament and transport of intracellular ‘cargo’ are achieved by generating physical force from chemical energy of ATP followed by appropriate conformational changes. The typical myosin has a head domain, which harbors an ATP binding site, an actin binding site, and a light-chain bound ‘lever arm’, followed often by a coiled coil domain and a cargo binding domain. Evolution of myosins started at the point of evolution of eukaryotes, S. cerevisiae being the simplest one known to contain these molecular motors. The coiled coil domain of the myosin classes II, V and VI in whole genomes of several model organisms display differences in the length and the strength of interactions at the coiled coil interface. Myosin II sequences have long-length coiled coil regions that are predicted to have a highly stable dimeric interface. These are interrupted, how- ever, by regions that are predicted to be unstable, indicating possibilities of alternate conformations, associations to make thick fila- ments, and interactions with other molecules. Myosin V sequences retain intermittent regions of strong and weak interactions, whereas myosin VI sequences are relatively devoid of strong coiled coil motifs. Structural deviations at coiled coil regions could be important for carrying out normal biological function of these proteins. Keywords: myosin structure, myosin domain architecture, coiled coil Bioinformatics and Biology Insights 2012:6 11–21 doi: 10.4137/BBI.S8451 This article is available from http://www.la-press.com. © the author(s), publisher and licensee Libertas Academica Ltd. This is an open access article. Unrestricted non-commercial use is permitted provided the original work is properly cited. Bioinformatics and Biology Insights 2012:6 11 Syamaladevi et al Gene Organization and Evolutionary considerably between the subtypes of myosin owing History to their functional variation.9 In conventional myosin Myosin is a family of actin based molecular motors (myosin II) the myosin tail region forms a long coiled that hydrolyze ATP and generate physical force coil that facilitates dimerization and oligomerization.10 to move different cargoes inside the cell. This Coiled coils in many unconventional myosins superfamily, divided into at least twenty four classes terminate at a globular cargo binding domain, which based on head domain sequence similarity and associates with specific cargo to be localized in the domain organization1,2 (Fig. 1), drive a large number cell (Fig. 2). of biological processes like cytokinesis,3,4 organelle Myosin genes are highly interrupted with a large transport,5,6 cell polarization and signal transduction7,8 number of introns (Fig. 3). The number of exons in eukaryotes. They are typically 1000–2000 residues in mammalian myosin can be as low as 12, as seen long and comprise of three domains: a conserved in myosins III and VII, whereas the exon number motor head with ATPase activity involved in actin shoots up to 40 and higher in certain subclasses binding and movement; a neck domain with bound like myosin V. This variation is indicative of regulatory proteins called myosin light chains; and many isoforms with different cargo specificity and a variable tail that often connects to various cargo differences in localization. Most eukaryotes rely on associated proteins. The tail domain architectures vary myosins, except a few taxonomic groups, viz. red Figure 1. Different classes of myosin superfamily: Phylogenetic tree of 114 myosin sequences showing 24 classes of myosins (Foth et al;65 Copyright (2006) National Academy of Sciences, USA.). 12 Bioinformatics and Biology Insights 2012:6 Structural and functional insights on the myosin superfamily algae and diplomonad protists1 which are not known Most of the non-muscle myosins are cytoplasmic. to possess genes with myosin head domain. No There are a number of myosins suggested to function classical myosins have been found in prokaryotes. during transcription within the nucleus by facilitating The ATPase domain of myosins along with that RNA polymerase movement, like myosin I,13 myo- of the kinesin family of microtubule based motors sin II14 and myosin VI.15 Possible roles of myosins in is believed to have evolved from the core GTPase transcription and other possible nuclear functions is domain of G-proteins through deletion of strands in need of additional research. Nuclear organization 6 and 7 and addition of two N terminal strands.11,12 and dynamics of that organization, clearly an exciting The wide distributions of myosins I and II across and important area of study, is in its infancy. Within taxonomic levels ranging from yeast to human imply the cytoplasm, myosins are localized to various spe- the early evolution of these two classes. Myosins V cialized zones, viz. myosin II in the rear of polarized and XI, which diverged to animal and plant lineages cells,16 myosin V in growth cones of neuronal cells,17 respectively, are thought to have evolved from a myosin VI at the base of stereocilia, and myosin VIII common myosin II-like ancestor.1 The most recent in plasmodesmata of plant cells.18 hypothesis put forward the evolution of present Myosin was first described in muscle cells, day variability among myosins from three ancient now known as muscle myosin II. Non-muscle myosin subfamilies (see Domain Architecture myosin II is found in the cell division furrow of many section for details): (i) the MSD subfamily standing unicellular and multicellular organisms,19 where it for the general domain architecture of MYSc-SMC- forms oligomeric thick filaments and facilitates cell DIL (MYSc-Myosin head domain, SMC-Structural division. Non-muscle myosin II isoforms are also Maintenance of Chromosomes is a chromosome localized to the leading edge of growth cones of rat segregation protein domain, DIL-DILute domain), dorsal root ganglion cells (myosin IIB isoform) and comprising myosins V and XI; (ii) the subfamily of in the perinuclear region (myosin-IIA isoform).20 the architecture MYSc-MYTH4/FERM (MYTH4- Myosin II association with Golgi-associated Myosin Tail Homology 4, FERM-band 4.1/Ezrin/ Rab6 resulting in fission of transport carriers was Radixin/Moesin-like domain) domain including recently described.21 myosin classes IV, VII, XII, and XV; and (iii) the Myosin V has three isoforms and they are primarily subfamily containing a membrane binding TH1 tail involved in transport of various cellular organelles, domain comprising myosin I.1 such as secretory vesicles (reviewed in Desnos et al., 2007).22 Myosin V in melanocytes is involved in Localization and Function melanosome transport.23 In neurons and glial cells, Myosins are localized to different organs or cell types abundant punctate staining of myosin V was found in based on their structural and functional peculiarities. the peri-nuclear region, along the cellular processes IQ Coiled coil A Myosin motor head IQ B Coiled coil Myosin motor head UI IQ ? C Coiled coil Myosin motor head Figure 2. Domain architecture. The overall length and domain organization vary considerably between the subclass members of myosin superfamily. Domain architectures of human (A) myosin II (NP_005954.3: 1939 amino acids) (B) myosin Va (NP_000250.3:1855 amino acids) and (C) myosin VI (NP_004990.3: 1285 amino acids). The length of predicted coiled coil domain using COILS program reflects the variation in length and architecture of the coiled coil domains. Lengths of coiled coil of human (A) myosin II (NP_005954.3 : residue 843 -1931), (B) myosin Va (NP_000250.3: residue 911–1104; residue 1153–1234; residue 1339–1445) and (C) myosin VI (NP_004990.3: residue 864–1030) are shown in green. Bioinformatics and Biology Insights 2012:6 13 Syamaladevi et al A B C Figure 3. Gene organization of myosin superfamily. Myosin genes are highly interrupted and contain large number of exons. (A) human myosin II (NP_005954.3: 40 exons; Transcript length: 6,023 bps), (B) human myosin Va (NP_000250.3: 41 exons; Transcript length: 12,225 bps) and (C) human myosin VI (NP_004990.3: 35 exons; Transcript length: 8,662 bps). and in the distal tips of processes.24,25 Myosin V is also heavy chains with a varying number of light chains, localized in the centrosome,26 where it is proposed to depending on the myosin type. In type II myosins, facilitate chromosomal segregation.27 The myosin Va an essential light chain (ELC) and a regulatory light isoform is also involved in acrosome formation and chain (RLC) bind at the IQ motifs.36 nuclear morphogenesis during spermatogenesis.28 The C-terminal tail of unconventional myosins Myosin VI and VII are present in the inner ear often, but not always, have a coiled coil region and a epithelial cells and hair cells.29 Myosin VI is also terminal globular cargo-binding
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