The Myosin Filament Superlattice in the Flight Muscles of Flies: A-band Lattice Optimisation for Stretch-activation?

Squire, John M.; Bekyarova, Tanya; Farman, Gerrie P.; Gore, David; Rajkumar, Ganeshalingam; Knupp, Carlo; Lucaveche, Carmen; Reedy, Mary C.; Reedy, Michael K.; Irving, Thomas C.

doi:10.1016/j.jmb.2006.06.072

Cited by 23 publications

(24 citation statements)

References 39 publications

(45 reference statements)

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“…Similar splitting has also been observed for Drosophila IFM 25 and has been interpreted to originate from the superlattice structure of myosin filaments. Both species belong to Diptera, and the superlattice structure may be a common feature of this group, because Ctenacrosceris is a member of a primitive Dipteran family (Tipulidae), and it is likely that the feature was acquired early in the evolution of Dipterans.…”

Section: Effect Of Reducing Temperature and Addition Of Blebbistatinsupporting

confidence: 76%

“…23,25 Unlike in vertebrate skeletal muscle, meridional intensities are observed only at 3 × multiples of the 1/38.7 nm − 1 interval, indicating that troponin complexes on the six thin filaments surrounding a thick filament assume helical symmetry with a systematic axial shift of 38.7/3 = 12.9 nm. 25 Although the lattice sampling is not as extensive as that in Lethocerus, the structural organization of filaments in Ctenacrosceris and Bombus flight muscles seems to be basically the same as that in Lethocerus except for some modifications in Ctenacrosceris. 26 Change of the 6th ALL and other reflections upon calcium activation at 20°C: Cases of giant water bug and crane fly…”

Section: Assignment Of Reflectionsmentioning

confidence: 98%

“…As described by Tregear et al, the 1st ALL (1/38.7 nm − 1 ) and the 2nd ALL (1/19.3 nm − 1 ) overlap with MLLs. 23 It is considered that troponin has a major contribution to the inner parts of these layer lines, 23,25 and the outer diffuse part of the 2nd ALL is enhanced by tropomyosin movement as mentioned above. The first meridional reflection of actin appears at 1/ 2.74 nm − 1 .…”

Section: Assignment Of Reflectionsmentioning

confidence: 99%

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Evidence for Unique Structural Change of Thin Filaments upon Calcium Activation of Insect Flight Muscle

Iwamoto

2009

Journal of Molecular Biology

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Section: Effect Of Reducing Temperature and Addition Of Blebbistatinsupporting

confidence: 76%

Section: Assignment Of Reflectionsmentioning

confidence: 98%

Section: Assignment Of Reflectionsmentioning

confidence: 99%

See 1 more Smart Citation

Evidence for Unique Structural Change of Thin Filaments upon Calcium Activation of Insect Flight Muscle

Iwamoto

2009

Journal of Molecular Biology

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“…Third, Diptera asynchronous muscles have even greater order than that noted above, which was from Lecotherus (giant water bug), a weak flyer compared to flies and one that, unlike flies, requires a preflight warm-up period. This increased order is a superlattice in which adjacent thick filaments are axially shifted one third of the axial distance between the myosin heads, which modeling shows would increase the range of thick:thin filament displacements over which the heads can bind while still maintaining regions of increased and decreased head binding (Squire et al, 2006). Taken together, these data strongly suggest that match-mismatch likely plays a role in stretch activation and shortening inactivation (Squire et al, 2005b).…”

Section: Unique Properties Due To Acto-myosin Interaction 2: Asynchromentioning

confidence: 78%

Invertebrate muscles: Thin and thick filament structure; molecular basis of contraction and its regulation, catch and asynchronous muscle

Hooper

Hobbs

Thuma

2008

Progress in Neurobiology

131

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This is the second in a series of canonical reviews on invertebrate muscle. We cover here thin and thick filament structure, the molecular basis of force generation and its regulation, and two special properties of some invertebrate muscle, catch and asynchronous muscle. Invertebrate thin filaments resemble vertebrate thin filaments, although helix structure and tropomyosin arrangement show small differences. Invertebrate thick filaments, alternatively, are very different from vertebrate striated thick filaments and show great variation within invertebrates. Part of this diversity stems from variation in paramyosin content, which is greatly increased in very large diameter invertebrate thick filaments. Other of it arises from relatively small changes in filament backbone structure, which results in filaments with grossly similar myosin head placements (rotating crowns of heads every 14.5 nm) but large changes in detail (distances between heads in azimuthal registration varying from three to thousands of crowns). The lever arm basis of force generation is common to both vetebrates and invertebrates, and in some invertebrates this process is understood on the near atomic level. Invertebrate actomyosin is both thin (tropomyosin:troponin) and thick (primarily via direct Ca ++ binding to myosin) filament regulated, and most invertebrate muscles are dually regulated. These mechanisms are well understood on the molecular level, but the behavioral utility of dual regulation is less so. The phosphorylation state of the thick filament associated giant protein, twitchin, has been recently shown to be the molecular basis of catch. The molecular basis of the stretch activation underlying asynchronous muscle activity, however, remains unresolved.

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“…Thus, it is likely that the troponin complexes in the two species would have different properties. The lattice structure of the Drosophila and Lethocerus IFMs are different (Squire et al 2006), which may also contribute to the different mechanical properties.…”

Section: Discussionmentioning

confidence: 99%

The roles of troponin C isoforms in the mechanical function of Drosophila indirect flight muscle

Eldred

Katzemich

Patel

et al. 2014

J Muscle Res Cell Motil

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Stretch activation (SA) is a fundamental property of all muscle types that increases power output and efficiency, yet its mechanism is unknown. Recently, studies have implicated troponin isoforms as important in the SA mechanism. The highly stretch-activated Drosophila IFMs express two isoforms of the Ca2+-binding subunit of troponin (TnC). TnC1 (TnC-F2 in Lethocerus IFM) has two calcium binding sites, while an unusual isoform, TnC4 (TnC-F1 in Lethocerus IFM), has only one binding site. We investigated the roles of these two TnC isoforms in Drosophila IFM by targeting RNAi to each isoform. IFMs with TnC4 expression (normally ~90 % of total TnC) replaced by TnC1 did not generate isometric tension, power or display SA. However, TnC4 knockdown resulted in sarcomere ultrastructure disarray, which could explain the lack of mechanical function and thus make interpretation of the influence of TnC4 on SA difficult. Elimination of TnC1 expression (normally ~10 % of total TnC) by RNAi resulted in normal muscle structure. In these IFMs, fiber power generation, isometric tension, stretch-activated force and calcium sensitivity were statistically identical to wild type. When TnC1 RNAi was driven by an IFM specific driver, there was no decrease in flight ability or wing beat frequency, which supports our mechanical findings suggesting that TnC1 is not essential for the mechanical function of Drosophila IFM. This finding contrasts with previous work in Lethocerus IFM showing TnC1 is essential for maximum isometric force generation. We propose that differences in TnC1 function in Lethocerus and Drosophila contribute to the ~40-fold difference in IFM isometric tension generated between these species.

show abstract

The Myosin Filament Superlattice in the Flight Muscles of Flies: A-band Lattice Optimisation for Stretch-activation?

Cited by 23 publications

References 39 publications

Evidence for Unique Structural Change of Thin Filaments upon Calcium Activation of Insect Flight Muscle

Evidence for Unique Structural Change of Thin Filaments upon Calcium Activation of Insect Flight Muscle

Invertebrate muscles: Thin and thick filament structure; molecular basis of contraction and its regulation, catch and asynchronous muscle

The roles of troponin C isoforms in the mechanical function of Drosophila indirect flight muscle

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