The Antiparallel Dimerization of Myosin X Imparts Bundle Selectivity for Processive Motility

Caporizzo, Matthew A.; Fishman, Claire E.; Satō, Osamu; Jamiolkowski, Ryan M.; Ikebe, Mitsuo; Goldman, Yale E.

doi:10.1016/j.bpj.2018.01.038

Cited by 12 publications

(22 citation statements)

References 47 publications

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“…Myosin X and VI have also been shown to exhibit gating of ADP release from AM,ADP (31)(32)(33). Myosin VI binds ATP relatively slowly and this step also is probably gated by mechanical strain between its heads.…”

Section: Implications Of Negatively Strained Actomyosin Attachmentsmentioning

confidence: 99%

“…1 B, states d / e; (22)(23)(24)(25)(26)(27)). This is also observed when the strain becomes negative for nonmuscle myosins (28)(29)(30)(31)(32)(33). This ''gating'' of the actomyosin mechanochemical cycle, which enables load-dependent energy transduction in muscle and synchronizes the biochemical reactions in processive myosins, is thought to arise from stress-and straindependent kinetics of the underlying chemical and structural transitions.…”

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confidence: 98%

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Straightening Out the Elasticity of Myosin Cross-Bridges

Linari

Piazzesi

Pertici

et al. 2020

Biophysical Journal

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In a contracting muscle, myosin cross-bridges extending from thick filaments pull the interdigitating thin (actin-containing) filaments during cyclical ATP-driven interactions toward the center of the sarcomere, the structural unit of striated muscle. Cross-bridge attachments in the sarcomere have been reported to exhibit a similar stiffness under both positive and negative forces. However, in vitro measurements on filaments with a sparse complement of heads detected a decrease of the cross-bridge stiffness at negative forces attributed to the buckling of the subfragment 2 tail portion. Here, we review some old and new data that confirm that cross-bridge stiffness is nearly linear in the muscle filament lattice. The implications of high myosin stiffness at positive and negative strains are considered in muscle fibers and in nonmuscle intracellular cargo transport.

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Section: Implications Of Negatively Strained Actomyosin Attachmentsmentioning

confidence: 99%

mentioning

confidence: 98%

Straightening Out the Elasticity of Myosin Cross-Bridges

Linari

Piazzesi

Pertici

et al. 2020

Biophysical Journal

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“…The expressions may be derived using matrix algebra, and can also be straightforwardly implemented for fitting experimental data. Our approach shares some similarities with the strategies adopted in (27) and (47) to extract the velocity and processivity for kinetic models of myosin VI, and X, respectively. However, our results have the benefit of an analytical solution which holds regardless of the underlying structure of the kinetic network.…”

Section: Significance Statementmentioning

confidence: 99%

Processivity and Velocity for Motors Stepping on Periodic Tracks

Mugnai

Caporizzo

Goldman

et al. 2020

Biophysical Journal

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Processive molecular motors enable cargo transportation by assembling into dimers capable of taking several consecutive steps along a cytoskeletal filament. In the well-accepted hand-over-hand stepping mechanism the trailing motor detaches from the track and binds the filament again in leading position. This requires fuel consumption in the form of ATP hydrolysis, and coordination of the catalytic cycles between the leading and the trailing heads. However, alternative stepping mechanisms exist, including inchworm-like movements, backward steps, and foot stomps. Whether all of these pathways are coupled to ATP hydrolysis remains to be determined. Here, in order to establish the principles governing the dynamics of processive movement, we present a theoretical framework which includes all of the alternative stepping mechanisms. Our theory bridges the gap between the elemental rates describing the biochemical and structural transitions in each head, and the experimentally measurable quantities, such as velocity, processivity, and probability of backward stepping. Our results, obtained under the assumption that the track is periodic and infinite, provide expressions which hold regardless of the topology of the network connecting the intermediate states, and are therefore capable of describing the function of any molecular motor. We apply the theory to myosin VI, a motor that takes frequent backward steps, and moves forward with a combination of hand-over-hand and inchworm-like steps. Our model reproduces quantitatively various observables of myosin VI motility measured experimentally from two groups.The theory is used to predict the gating mechanism, the pathway for backward stepping, and the energy consumption as a function of ATP concentration.

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“…This demonstrated that oligomerization is strictly required for targeting of Myo10 in our cell system. We utilized a similar design as previously described to create a parallel dimerized Myo10 (Caporizzo et al, 2018), in which a GCN4 sequence was fused in register with its SAH motif (Figure 6A; Myo10-MN-GCN4). This form of Myo10 was shown to be active in vitro, exhibiting processive motility on both single actin filaments and fascin-bundled actin (Caporizzo et al, 2018).…”

Section: Mode Of Oligomerization and Motor Domain Identity Influence Actin Track Selectionmentioning

confidence: 99%

Comparative analysis of the MyTH4-FERM myosins reveals insights into the determinants of actin track selection in polarized epithelia

Matoo

Graves

Acharya

et al. 2021

MBoC

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MyTH4-FERM (MF) myosins evolved to play a role in the creation and function of a variety of actin-based membrane protrusions that extend from cells. Here, we performed an analysis of the MF myosins, Myo7A, Myo7B, and Myo10, to gain insight into how they select for their preferred actin networks. Using enterocytes that create spatially separated actin tracks in the form of apical microvilli and basal filopodia, we show that actin track selection is principally guided by the mode of oligomerization of the myosin along with the identity of the motor domain, with little influence from the specific composition of the lever arm. Chimeric variants of Myo7A and Myo7B fused to a leucine zipper parallel dimerization sequence in place of their native tails both selected apical microvilli as their tracks, while a truncated Myo10 used its native antiparallel coiled-coil to traffic to the tips of filopodia. Swapping lever arms between the Class 7 and 10 myosins did not change actin track preference. Surprisingly, fusing the motor-neck region of Myo10 to a leucine zipper or oligomerization sequences derived from the Myo7A and Myo7B cargo proteins USH1G and ANKS4B, respectively, re-encoded the actin track usage of Myo10 to apical microvilli with significant efficiency.

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The Antiparallel Dimerization of Myosin X Imparts Bundle Selectivity for Processive Motility

Cited by 12 publications

References 47 publications

Straightening Out the Elasticity of Myosin Cross-Bridges

Straightening Out the Elasticity of Myosin Cross-Bridges

Processivity and Velocity for Motors Stepping on Periodic Tracks

Comparative analysis of the MyTH4-FERM myosins reveals insights into the determinants of actin track selection in polarized epithelia

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