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The Effect of Removing the N-Terminal Extension of the Drosophila Myosin Regulatory Light Chain upon Flight Ability and the Contractile Dynamics of Indirect Flight Muscle

Moore, Jeffrey R. and Dickinson, Michael H. and Vigoreaux, Jim O. and Maughan, David W. (2000) The Effect of Removing the N-Terminal Extension of the Drosophila Myosin Regulatory Light Chain upon Flight Ability and the Contractile Dynamics of Indirect Flight Muscle. Biophysical Journal, 78 (3). pp. 1431-1440. ISSN 0006-3495. PMCID PMC1300741. https://resolver.caltech.edu/CaltechAUTHORS:20181116-153956676

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Abstract

The Drosophila myosin regulatory light chain (DMLC2) is homologous to MLC2s of vertebrate organisms, except for the presence of a unique 46-amino acid N-terminal extension. To study the role of the DMLC2 N-terminal extension in Drosophila flight muscle, we constructed a truncated form of the Dmlc2 gene lacking amino acids 2–46 (Dmlc2^(Δ2–46)). The mutant gene was expressed in vivo, with no wild-type Dmlc2 gene expression, via P-element-mediated germline transformation. Expression of the truncated DMLC2 rescues the recessive lethality and dominant flightless phenotype of the Dmlc2 null, with no discernible effect on indirect flight muscle (IFM) sarcomere assembly. Homozygous Dmlc2^(Δ2–46) flies have reduced IFM dynamic stiffness and elastic modulus at the frequency of maximum power output. The viscous modulus, a measure of the fly's ability to perform oscillatory work, was not significantly affected in Dmlc2^(Δ2–46) IFM. In vivo flight performance measurements of Dmlc2^(Δ2–46) flies using a visual closed-loop flight arena show deficits in maximum metabolic power (P*_(CO2)), mechanical power (P*_(mech)), and flight force. However, mutant flies were capable of generating flight force levels comparable to body weight, thus enabling them to fly, albeit with diminished performance. The reduction in elastic modulus in Dmlc2^(Δ2–46) skinned fibers is consistent with the N-terminal extension being a link between the thick and thin filaments that is parallel to the cross-bridges. Removal of this parallel link causes an unfavorable shift in the resonant properties of the flight system, thus leading to attenuated flight performance.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1016/s0006-3495(00)76696-3DOIArticle
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1300741/PubMed CentralArticle
ORCID:
AuthorORCID
Dickinson, Michael H.0000-0002-8587-9936
Additional Information:© 2000 The Biophysical Society. Under an Elsevier user license. Received 10 May 1999, Revised 15 November 1999. We thank Dr. V. Mohan-Ram for many helpful comments and Dr. Amanda Simcox for help with the embryo injections. We also thank W. Barnes, J. Hurley, and Allison Cox for technical assistance. This work was supported by the National Science Foundation and the Office of Naval Research.
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Funding AgencyGrant Number
NSFUNSPECIFIED
Office of Naval Research (ONR)UNSPECIFIED
Issue or Number:3
PubMed Central ID:PMC1300741
Record Number:CaltechAUTHORS:20181116-153956676
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20181116-153956676
Official Citation:Jeffrey R. Moore, Michael H. Dickinson, Jim O. Vigoreaux, David W. Maughan, The Effect of Removing the N-Terminal Extension of the Drosophila Myosin Regulatory Light Chain upon Flight Ability and the Contractile Dynamics of Indirect Flight Muscle, Biophysical Journal, Volume 78, Issue 3, 2000, Pages 1431-1440, ISSN 0006-3495, https://doi.org/10.1016/S0006-3495(00)76696-3. (http://www.sciencedirect.com/science/article/pii/S0006349500766963)
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:90991
Collection:CaltechAUTHORS
Deposited By: George Porter
Deposited On:17 Nov 2018 00:04
Last Modified:03 Oct 2019 20:30

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