Myofilin, a protein in the thick filaments of insect muscle

Qiu, Feng; Brendel, Sigrun; Cunha, Paulo; Astola, Nagore; Song, Bauzhen; Furlong, Eileen E. M.; Leonard, Kevin; Bullard, Belinda

doi:10.1242/jcs.02281

Cited by 56 publications

(48 citation statements)

References 37 publications

(44 reference statements)

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“…Note however that a visible gap remains in the M-line region, suggesting that flightin is excluded from the bare zone. This agrees with immuno-EM studies of the flightin homologue (zeelin-2) in the IFMs of the water bug Lethocerus indicus, where the protein was shown to be absent from the bare zone (Ferguson et al, 1994;Reedy et al, 2000;Qiu et al, 2005). These authors also showed that flightin was absent from the very tips of the thick filaments of the A/I junction, presumably due to the presence of the connecting filaments (consisting of sallimus and projectin) in that region (Ferguson et al, 1994), though this is not resolvable in our work due to limitations of confocal microscopy.…”

Section: Discussionsupporting

confidence: 85%

Myosin isoform switching during assembly of the Drosophila flight muscle thick filament lattice

Orfanos

Sparrow

2013

Journal of Cell Science

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SummaryDuring muscle development myosin molecules form symmetrical thick filaments, which integrate with the thin filaments to produce the regular sarcomeric lattice. In Drosophila indirect flight muscles (IFMs) the details of this process can be studied using genetic approaches. The weeP26 transgenic line has a GFP-encoding exon inserted into the single Drosophila muscle myosin heavy chain gene, Mhc. The weeP26 IFM sarcomeres have a unique MHC-GFP-labelling pattern restricted to the sarcomere core, explained by nontranslation of the GFP exon following alternative splicing. Characterisation of wild-type IFM MHC mRNA confirmed the presence of an alternately spliced isoform, expressed earlier than the major IFM-specific isoform. The two wild-type IFM-specific MHC isoforms differ by the presence of a C-terminal 'tailpiece' in the minor isoform. The sequential expression and assembly of these two MHCs into developing thick filaments suggest a role for the tailpiece in initiating A-band formation. The restriction of the MHC-GFP sarcomeric pattern in weeP26 is lifted when the IFM lack the IFM-specific myosin binding protein flightin, suggesting that it limits myosin dissociation from thick filaments. Studies of flightin binding to developing thick filaments reveal a progressive binding at the growing thick filament tips and in a retrograde direction to earlier assembled, proximal filament regions. We propose that this flightin binding restricts myosin molecule incorporation/dissociation during thick filament assembly and explains the location of the early MHC isoform pattern in the IFM A-band.

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Section: Discussionsupporting

confidence: 85%

Myosin isoform switching during assembly of the Drosophila flight muscle thick filament lattice

Orfanos

Sparrow

2013

Journal of Cell Science

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“…Flightin binds the light meromyosin region of myosin, ϳ2/3 of the way down the rod, because substituting aspartic acid 1554 for lysine abolishes flightin's interaction in vitro (1) and accumulation in vivo (18). Immunolocalization studies in Drosophila and Lethocerus IFM indicate that flightin is associated with the thick filament backbone (25,26), consistent with studies that show flightin is absent in IFM lacking thick filaments (29).Studies using Drosophila mutants demonstrate that flightin plays several important roles in maintaining muscle integrity. Flightin is required for normal thick filament assembly and for establishing or maintaining in vivo filament length and flexural rigidity (8,26).…”

supporting

confidence: 79%

supporting

confidence: 79%

COOH-terminal truncation of flightin decreases myofilament lattice organization, cross-bridge binding, and power output in Drosophila indirect flight muscle

Tanner

Miller

et al. 2011

American Journal of Physiology-Cell Physiology

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insects is characterized by a near crystalline myofilament lattice structure that likely evolved to achieve high power output. In Drosophila IFM, the myosin rod binding protein flightin plays a crucial role in thick filament organization and sarcomere integrity. Here we investigate the extent to which the COOH terminus of flightin contributes to IFM structure and mechanical performance using transgenic Drosophila expressing a truncated flightin lacking the 44 COOH-terminal amino acids (fln ⌬C44 ). Electron microscopy and Xray diffraction measurements show decreased myofilament lattice order in the fln ⌬C44 line compared with control, a transgenic flightinnull rescued line (fln ϩ ). fln ⌬C44 fibers produced roughly 1/3 the oscillatory work and power of fln ϩ , with reduced frequencies of maximum work (123 Hz vs. 154 Hz) and power (139 Hz vs. 187 Hz) output, indicating slower myosin cycling kinetics. These reductions in work and power stem from a slower rate of cross-bridge recruitment and decreased cross-bridge binding in fln ⌬C44 fibers, although the mean duration of cross-bridge attachment was not different between both lines. The decreases in lattice order and myosin kinetics resulted in fln ⌬C44 flies being unable to beat their wings. These results indicate that the COOH terminus of flightin is necessary for normal myofilament lattice organization, thereby facilitating the cross-bridge binding required to achieve high power output for flight. fiber mechanics; cross-bridge kinetics; thick filaments IN MUSCLE, THE THICK AND THIN filament lattice provides the structural and mechanical foundation for transmitting contractile forces throughout the cell. The highly ordered indirect flight muscle (IFM) of Drosophila melanogaster is an attractive model system to study the relationship between lattice structure and muscle function, because its in vivo lattice organization can be measured via X-ray diffraction in living flies (15) and its function can be measured from the whole fly to the molecule (14,20,30). In addition, the means for producing genetic alterations of specific proteins in D. melanogaster are well established, permitting precise manipulation of thick and thin filament proteins. In this study, we combine these approaches to define the role of flightin, specifically the COOH terminus, in lattice organization and its effects on cross-bridge cycling kinetics and overall muscle performance.In Drosophila, flightin is a ϳ20-kDa (182 amino acids) protein that is expressed exclusively in the IFM (33). Flightin binds the light meromyosin region of myosin, ϳ2/3 of the way down the rod, because substituting aspartic acid 1554 for lysine abolishes flightin's interaction in vitro (1) and accumulation in vivo (18). Immunolocalization studies in Drosophila and Lethocerus IFM indicate that flightin is associated with the thick filament backbone (25,26), consistent with studies that show flightin is absent in IFM lacking thick filaments (29).Studies using Drosophila mutants demonstrate that flightin plays several importa...

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“…The expressed gene set also included two isoforms of myofilin, a 20‐kDa protein associated with myosin in the core of thick filaments that make up asynchronous insect flight muscle (Qiu et al . 2005). The transcription of genes coding for proteins associated with locomotory muscles (e.g.…”

Section: Resultsmentioning

confidence: 99%

Genomewide transcriptional signatures of migratory flight activity in a globally invasive insect pest

et al. 2015

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Migration is a key life history strategy for many animals and requires a suite of behavioural, morphological and physiological adaptations which together form the ‘migratory syndrome’. Genetic variation has been demonstrated for many traits that make up this syndrome, but the underlying genes involved remain elusive. Recent studies investigating migration‐associated genes have focussed on sampling migratory and nonmigratory populations from different geographic locations but have seldom explored phenotypic variation in a migratory trait. Here, we use a novel combination of tethered flight and next‐generation sequencing to determine transcriptomic differences associated with flight activity in a globally invasive moth pest, the cotton bollworm Helicoverpa armigera. By developing a state‐of‐the‐art phenotyping platform, we show that field‐collected H. armigera display continuous variation in flight performance with individuals capable of flying up to 40 km during a single night. Comparative transcriptomics of flight phenotypes drove a gene expression analysis to reveal a suite of expressed candidate genes which are clearly related to physiological adaptations required for long‐distance flight. These include genes important to the mobilization of lipids as flight fuel, the development of flight muscle structure and the regulation of hormones that influence migratory physiology. We conclude that the ability to express this complex set of pathways underlines the remarkable flexibility of facultative insect migrants to respond to deteriorating conditions in the form of migratory flight and, more broadly, the results provide novel insights into the fundamental transcriptional changes required for migration in insects and other taxa.

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Myofilin, a protein in the thick filaments of insect muscle

Cited by 56 publications

References 37 publications

Myosin isoform switching during assembly of the Drosophila flight muscle thick filament lattice

Myosin isoform switching during assembly of the Drosophila flight muscle thick filament lattice

COOH-terminal truncation of flightin decreases myofilament lattice organization, cross-bridge binding, and power output in Drosophila indirect flight muscle

Genomewide transcriptional signatures of migratory flight activity in a globally invasive insect pest

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