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Review
. 2010 Apr;67(8):1239-54.
doi: 10.1007/s00018-009-0254-5. Epub 2010 Jan 27.

Myosin motor function: the ins and outs of actin-based membrane protrusions

Rajalakshmi Nambiar  1 , Russell E McConnell, Matthew J Tyska
Affiliations
Review

Myosin motor function: the ins and outs of actin-based membrane protrusions

Rajalakshmi Nambiar et al. Cell Mol Life Sci. 2010 Apr.

Abstract

Cells build plasma membrane protrusions supported by parallel bundles of F-actin to enable a wide variety of biological functions, ranging from motility to host defense. Filopodia, microvilli and stereocilia are three such protrusions that have been the focus of intense biological and biophysical investigation in recent years. While it is evident that actin dynamics play a significant role in the formation of these organelles, members of the myosin superfamily have also been implicated as key players in the maintenance of protrusion architecture and function. Based on a simple analysis of the physical forces that control protrusion formation and morphology, as well as our review of available data, we propose that myosins play two general roles within these structures: (1) as cargo transporters to move critical regulatory components toward distal tips and (2) as mediators of membrane-cytoskeleton adhesion.

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Figures

Fig. 1
Fig. 1
Actin-based membrane protrusions. a A cartoon depiction of branched and bundled arrays of actin protruding from a cell surface. b Three forms of PAB-supported protrusions (PSPs) depicted in their cellular context. Filopodia extend several microns from the plasma membrane of motile cells in small numbers. Microvilli extend only a couple of microns, but in large numbers, from the apical surface of polarized cells such as those found in the intestinal or kidney epithelium. Stereocilia are depicted emerging from the apical surface of a mechanosensory hair cell in rows of graded height forming a staircase pattern; stereocilia also exceed microvilli in length and diameter
Fig. 2
Fig. 2
Forces involved in deforming plasma membrane. The restoring force (F R) exerted by the plasma membrane is plotted as a function of protrusion radius (R), using the relationship shown in Eq. 2, for different levels of membrane-cytoskeleton adhesion. Here, F R is calculated assuming a membrane bending stiffness, κ = 270 pN nm, and a surface tension, σ = 0.003 pN/nm. The region shaded in light blue represents the range of protrusion radii over which the energy of the protrusion (the product of F R and protrusion length) is minimized for the different levels of adhesion. The range obtained here is in good agreement with actual values of protrusion radii observed in PSPs discussed here
Fig. 3
Fig. 3
Myosins that reside in PAB-supported protrusions. Bar diagrams representing the primary structures of the seven different myosins discussed in this review are drawn along with an indication of the protrusion(s) that each motor occupies (FP filopodia, MV microvilli, SC stereocilia). All myosins possess N-terminal motor domains (red) coupled to structurally diverse C-terminal tail domains (blue). Myosin-1 contains a tail homology domain I (THI), which directs binding to membrane lipids. Myosin-3 is unique among myosins in that it possesses an N-terminal kinase domain. Tail homology domains I (THDI) and II (THDII) are also shown; the former binds to espin 1, while the latter may mediate direct binding to actin. Myosin-5 is a dimeric and processive motor with coiled-coil forming regions throughout its tail and a cargo-binding domain at the C-terminus. Myosin-6, the sole minus-end directed motor, is depicted with a cargo-binding globular tail domain (GT), which also mediates dimerization. Myosins-7, 10 and 15 are MyTH4-FERM domain myosins containing at least one MyTH4-FERM domain in their tails. These domains are known to mediate binding to a number of important proteins and lipids: the FERM domain of myosin-7a binds the transmembrane protein vezatin and thus links it to the cadherin/α-catenin complex; the MyTH4 domain of myosin-10 binds to microtubules, whereas the FERM domain binds to the cytoplasmic NPXY domain of β-integrins; the FERM domain of myosin-15 binds to the third PDZ domain of Whirlin, its primary cargo. In the case of myosin-7, the asterisk represents a coiled-coil domain that may facilitate dimerization in myosin-7a. Myosin-10 also has a non-dimerizing stable alpha helix (SAH) and PH domain that mediates interactions with PIP3
Fig. 4
Fig. 4
Membrane protrusion coalescence. a In the case of a single protrusion, membrane tension functions to keep the plasma membrane closely associated with the underlying actin bundle. b If a second protrusion forms too close to the first, tension will force the actin bundles to coalesce into a single protrusion. c Two adjacent protrusions are stabilized by the presence of high levels of membrane-cytoskeleton adhesion (provided by red linker molecules), which serves to counter coalescence
Fig. 5
Fig. 5
Roles for myosin motor proteins in membrane protrusions. A cartoon of a generic membrane protrusion (i.e., a composite of filopodia, microvilli and stereocilia), depicting general features and possible roles for many of the myosins discussed in this review. Motors colored in red are those myosins (myosins-3a, -10 and -15a) that are likely to function in plus-end directed transport within PSPs. Myosins colored blue are plus-end directed motors (myosins-1a and -7a) that are likely contributing to membrane-cytoskeleton adhesion along the length of core actin bundles. Colored yellow is myosin-6, the sole minus-ended directed motor that may play roles in both membrane-cytoskeleton adhesion and transport of components toward, or retention at, the base of PSPs
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