Abstract
Myosin 5 is a two-headed motor protein that moves cargoes along actin filaments. Its tail ends in paired globular tail domains (GTDs) thought to bind cargo. At nanomolar calcium levels, actin-activated ATPase is low and the molecule is folded. Micromolar calcium concentrations activate ATPase and the molecule unfolds. Here we describe the structure of folded myosin and the GTD's role in regulating activity. Electron microscopy shows that the two heads lie either side of the tail, contacting the GTDs at a lobe of the motor domain (approximately Pro 117-Pro 137) that contains conserved acidic side chains, suggesting ionic interactions between motor domain and GTD. Myosin 5 heavy meromyosin, a constitutively active fragment lacking the GTDs, is inhibited and folded by a dimeric GST-GTD fusion protein. Motility assays reveal that at nanomolar calcium levels heavy meromyosin moves robustly on actin filaments whereas few myosins bind or move. These results combine to show that with no cargo, the GTDs bind in an intramolecular manner to the motor domains, producing an inhibited and compact structure that binds weakly to actin and allows the molecule to recycle towards new cargoes.
MeSH Terms
Actins/chemistry,metabolism
Binding Sites
Microscopy, Electron
Models, Molecular
Myosin Type V/chemistry,metabolism,ultrastructure
Protein Folding
Protein Structure, Tertiary
Chemicals
Actins
Myosin Type V
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Thirumurugan Kavitha
Institute of Molecular and Cellular Biology, and Astbury Centre for Structural Molecular Biology, University of Leeds, Leeds LS2 9JT, UK.
Sakamoto Takeshi
Hammer John A
Sellers James R
Knight Peter J
References (23)
23 references, click to expand
-
Conservation within the myosin motor domain: implications for structure and function.
Structure. 1996 Aug 15;4(8):969-87
PMID: 8805581
-
Three myosin V structures delineate essential features of chemo-mechanical transduction.
EMBO J. 2004 Nov 24;23(23):4527-37
PMID: 15510214
-
Motility of myosin V regulated by the dissociation of single calmodulin.
Nat Struct Mol Biol. 2005 Feb;12(2):127-32
PMID: 15665867
-
Three-dimensional structural dynamics of myosin V by single-molecule fluorescence polarization.
Nature. 2003 Mar 27;422(6930):399-404
PMID: 12660775
-
Walking with myosin V.
Curr Opin Cell Biol. 2006 Feb;18(1):68-73
PMID: 16378722
-
Structural basis for myosin V discrimination between distinct cargoes.
EMBO J. 2006 Feb 22;25(4):693-700
PMID: 16437158
-
Ca2+-induced activation of ATPase activity of myosin Va is accompanied with a large conformational change.
Biochem Biophys Res Commun. 2004 Mar 12;315(3):538-45
PMID: 14975734
-
Regulated conformation of myosin V.
J Biol Chem. 2004 Jan 23;279(4):2333-6
PMID: 14634000
-
Myosin V motor proteins: marching stepwise towards a mechanism.
J Cell Biol. 2003 Nov 10;163(3):445-50
PMID: 14610051
-
Neck length and processivity of myosin V.
J Biol Chem. 2003 Aug 1;278(31):29201-7
PMID: 12740393
-
Myosin V walks hand-over-hand: single fluorophore imaging with 1.5-nm localization.
Science. 2003 Jun 27;300(5628):2061-5
PMID: 12791999
-
An elastically tethered viscous load imposes a regular gait on the motion of myosin-V. Simulation of the effect of transient force relaxation on a stochastic process.
J R Soc Interface. 2006 Feb 22;3(6):153-65
PMID: 16849227
-
The prepower stroke conformation of myosin V.
J Cell Biol. 2002 Dec 23;159(6):983-91
PMID: 12499355
-
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. 2001 Apr 10;98(8):4361-6
PMID: 11287639
-
Three conformational states of scallop myosin S1.
Proc Natl Acad Sci U S A. 2000 Oct 10;97(21):11238-43
PMID: 11016966
-
Direct observation of processive movement by individual myosin V molecules.
Biochem Biophys Res Commun. 2000 Jun 7;272(2):586-90
PMID: 10833456
-
Kinesin's IAK tail domain inhibits initial microtubule-stimulated ADP release.
Nat Cell Biol. 2000 May;2(5):257-60
PMID: 10806475
-
SPIDER and WEB: processing and visualization of images in 3D electron microscopy and related fields.
J Struct Biol. 1996 Jan-Feb;116(1):190-9
PMID: 8742743
-
Brain myosin-V is a two-headed unconventional myosin with motor activity.
Cell. 1993 Oct 8;75(1):13-23
PMID: 8402892
-
A folded (10 S) conformer of myosin from a striated muscle and its implications for regulation of ATPase activity.
J Mol Biol. 1991 Jan 20;217(2):323-35
PMID: 1825121
-
Use of negative stain and single-particle image processing to explore dynamic properties of flexible macromolecules.
J Struct Biol. 2004 Sep;147(3):247-58
PMID: 15450294
-
Myosin V: regulation by calcium, calmodulin, and the tail domain.
J Cell Biol. 2004 Mar 15;164(6):877-86
PMID: 15007063
-
Activation of myosin Va function by melanophilin, a specific docking partner of myosin Va.
J Biol Chem. 2005 May 6;280(18):17815-22
PMID: 15760894