Helical Order in Tarantula Thick Filaments Requires the “Closed” Conformation of the Myosin Head

Zoghbi, Maria E.; Woodhead, John L.; Craig, Roger; Padrón, Raúl

doi:10.1016/j.jmb.2004.07.037

Cited by 30 publications

(43 citation statements)

References 59 publications

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“…The observed cross-bridge movement in the absence of the thin filament may be related to the early observation of ATP-dependent cross-bridge arrangement in insect thick filaments (16). Up to the present time, ATPdependent order-disorder transition of cross-bridge arrangement has been studied in detail (17)(18)(19).…”

Section: Discussionmentioning

confidence: 54%

Direct demonstration of the cross-bridge recovery stroke in muscle thick filaments in aqueous solution by using the hydration chamber

Sugi

Minoda

Inayoshi

et al. 2008

Proc. Natl. Acad. Sci. U.S.A.

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Despite >50 years of research work since the discovery of sliding filament mechanism in muscle contraction, structural details of the coupling of cyclic cross-bridge movement to ATP hydrolysis are not yet fully understood. An example would be whether lever arm tilting on the myosin filament backbone will occur in the absence of actin. The most direct way to elucidate such movement is to record ATP-induced cross-bridge movement in hydrated thick filaments. Using the hydration chamber, with which biological specimens can be kept in an aqueous environment in an electron microscope, we have succeeded in recording ATP-induced cross-bridge movement in hydrated thick filaments consisting of rabbit skeletal muscle myosin, with gold position markers attached to the cross-bridges. The position of individual cross-bridges did not change appreciably with time in the absence of ATP, indicating stability of time-averaged cross-bridge mean position. On application of ATP, individual cross-bridges moved nearly parallel to the filament long axis. The amplitude of the ATP-induced cross-bridge movement showed a peak at 5–7.5 nm. At both sides of the filament bare region, across which the cross-bridge polarity was reversed, the cross-bridges were found to move away from, but not toward, the bare region. Application of ADP produced no appreciable cross-bridge movement. Because ATP reacts rapidly with the cross-bridges (M) to form complex (M·ADP·Pi) with an average lifetime >10 s, the observed cross-bridge movement is associated with reaction, M + ATP → M·ADP·Pi. The cross-bridges were observed to return to their initial position after exhaustion of ATP. These results constitute direct demonstration of the cross-bridge recovery stroke.

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Section: Discussionmentioning

confidence: 54%

Direct demonstration of the cross-bridge recovery stroke in muscle thick filaments in aqueous solution by using the hydration chamber

Sugi

Minoda

Inayoshi

et al. 2008

Proc. Natl. Acad. Sci. U.S.A.

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“…In unregulated myosins, the headhead interaction may be weak and thus may not inhibit myosin function (although it might restrict head access to actin filaments in the relaxed state; ref. 31). Additional interactions present in regulated myosins (e.g., involving the regulatory light chains, or interactions with heads in other crowns or with S2; ref.…”

Section: Discussion Intramolecular Interaction Between Myosin Heads Imentioning

confidence: 99%

Three-dimensional structure of vertebrate cardiac muscle myosin filaments

Zoghbi

Woodhead

Moss

et al. 2008

Proc. Natl. Acad. Sci. U.S.A.

247

364

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Contraction of the heart results from interaction of the myosin and actin filaments. Cardiac myosin filaments consist of the molecular motor myosin II, the sarcomeric template protein, titin, and the cardiac modulatory protein, myosin binding protein C (MyBP-C). Inherited hypertrophic cardiomyopathy (HCM) is a disease caused mainly by mutations in these proteins. The structure of cardiac myosin filaments and the alterations caused by HCM mutations are unknown. We have used electron microscopy and image analysis to determine the three-dimensional structure of myosin filaments from wild-type mouse cardiac muscle and from a electron microscopy ͉ MyBP-C ͉ thick filament ͉ three-dimensional reconstruction

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“…Further EM studies using methods to isolate and visualize relaxed native thick filaments (Craig 2012) should take into account the bound nucleotide state (Clarke et al 1986;Craig and Padrón 1989), the pre-power stroke state head conformation (Zoghbi et al 2004;Llinas et al 2015) and the blebbistatin stabilizing effect . IHM detection in only one half of a single thick filament in the tarantula Gramostola rosea using electron tomography could be a quick alternative EM approach for IHM detection (Márquez et al 2014).…”

Section: The Myosin Interacting-heads Motif (Ihm)mentioning

confidence: 99%

“…Released swaying free heads (Bswinging^heads) could make crossbridges with actin on switched-on thin filaments generating powerstroke force in single twitches and twitch summation (Brito et al 2011). If [Ca 2+ ] suddenly decreases, actin-bound swaying (Zoghbi et al 2004;Llinas et al 2015) can establish the two required priming intramolecular interactions docking them onto their own S2 as Bblocked^heads (BBH-S2 precursor^, light green) and to a neighbor myosin tail (pink cylinder) on the backbone by anchoring intermolecular interactions (Alamo et al 2016). The other partner (Bfree^) head, also in pre-powerstroke state, remains disordered without making interactions with the docked blocked head as needed for establishing an IHM.…”

Section: Interactions Form Ihms and Their Helical Tracks In The Relaxmentioning

confidence: 99%

Lessons from a tarantula: new insights into muscle thick filament and myosin interacting-heads motif structure and function

et al. 2017

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The tarantula skeletal muscle X-ray diffraction pattern suggested that the myosin heads were helically arranged on the thick filaments. Electron microscopy (EM) of negatively stained relaxed tarantula thick filaments revealed four helices of heads allowing a helical 3D reconstruction. Due to its low resolution (5.0 nm), the unambiguous interpretation of densities of both heads was not possible. A resolution increase up to 2.5 nm, achieved by cryo-EM of frozen-hydrated relaxed thick filaments and an iterative helical real space reconstruction, allowed the resolving of both heads. The two heads, Bfree^and Bblocked^, formed an asymmetric structure named the Binteracting-heads motif^(IHM) which explained relaxation by self-inhibition of both heads ATPases. This finding made tarantula an exemplar system for thick filament structure and function studies. Heads were shown to be released and disordered by Ca 2+ -activation through myosin regulatory light chain phosphorylation, leading to EM, small angle X-ray diffraction and scattering, and spectroscopic and biochemical studies of the IHM structure and function. The results from these studies have consequent implications for understanding and explaining myosin super-relaxed state and thick filament activation and regulation. A cooperative phosphorylation mechanism for activation in tarantula skeletal muscle, involving swaying constitutively Ser35 mono-phosphorylated free heads, explains super-relaxation, force potentiation and posttetanic potentiation through Ser45 mono-phosphorylated blocked heads. Based on this mechanism, we propose a swaying-swinging, tilting crossbridge-sliding filament for tarantula muscle contraction.

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Helical Order in Tarantula Thick Filaments Requires the “Closed” Conformation of the Myosin Head

Cited by 30 publications

References 59 publications

Direct demonstration of the cross-bridge recovery stroke in muscle thick filaments in aqueous solution by using the hydration chamber

Direct demonstration of the cross-bridge recovery stroke in muscle thick filaments in aqueous solution by using the hydration chamber

Three-dimensional structure of vertebrate cardiac muscle myosin filaments

Lessons from a tarantula: new insights into muscle thick filament and myosin interacting-heads motif structure and function

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