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Phosphorylation-dependent power output of transgenic flies: an integrated study

Dickinson, Michael H. and Hyatt, Christopher J. and Lehmann, Fritz-Olaf and Moore, Jeffrey R. and Reedy, Mary C. and Simcox, Amanda and Tohtong, Rutawain and Vigoreaux, Jim O. and Yamashita, Hiroshi and Maughan, David W. (1997) Phosphorylation-dependent power output of transgenic flies: an integrated study. Biophysical Journal, 73 (6). pp. 3122-3134. ISSN 0006-3495. PMCID PMC1181215. https://resolver.caltech.edu/CaltechAUTHORS:20181116-074754160

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Abstract

We examine how the structure and function of indirect flight muscle (IFM) and the entire flight system of Drosophila melanogaster are affected by phosphorylation of the myosin regulatory light chain (MLC2). This integrated study uses site-directed mutagenesis to examine the relationship between removal of the myosin light chain kinase (MLCK) phosphorylation site, in vivo function of the flight system (flight tests, wing kinematics, metabolism, power output), isolated IFM fiber mechanics, MLC2 isoform pattern, and sarcomeric ultrastructure. The MLC2 mutants exhibit graded impairment of flight ability that correlates with a reduction in both IFM and flight system power output and a reduction in the constitutive level of MLC2 phosphorylation. The MLC2 mutants have wild-type IFM sarcomere and cross-bridge structures, ruling out obvious changes in the ultrastructure as the cause of the reduced performance. We describe a viscoelastic model of cross-bridge dynamics based on sinusoidal length perturbation analysis (Nyquist plots) of skinned IFM fibers. The sinusoidal analysis suggests the high power output of Drosophila IFM required for flight results from a phosphorylation-dependent recruitment of power-generating cross-bridges rather than a change in kinetics of the power generating step. The reduction in cross-bridge number appears to affect the way mutant flies generate flight forces of sufficient magnitude to keep them airborne. In two MLC2 mutant strains that exhibit a reduced IFM power output, flies appear to compensate by lowering wingbeat frequency and by elevating wingstroke amplitude (and presumably muscle strain). This behavioral alteration is not seen in another mutant strain in which the power output and estimated number of recruited cross-bridges is similar to that of wild type.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1016/s0006-3495(97)78338-3DOIArticle
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1181215PubMed CentralArticle
ORCID:
AuthorORCID
Dickinson, Michael H.0000-0002-8587-9936
Additional Information:© 1997 The Biophysical Society. Published by Elsevier Inc. The authors are grateful to Joe Haeberle, Masataka Kawai, and Justin Molloy for their help in the initial stages of this research. We also thank William Barnes, Janet Hurley, Clifford Beall, and Michael Reedy for assistance and advice. This study was supported by the National Institutes of Health Grant RO1 AR40234 (to D.M.).
Funders:
Funding AgencyGrant Number
NIHRO1 AR40234
Issue or Number:6
PubMed Central ID:PMC1181215
Record Number:CaltechAUTHORS:20181116-074754160
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20181116-074754160
Official Citation:M.H. Dickinson, C.J. Hyatt, F.O. Lehmann, J.R. Moore, M.C. Reedy, A. Simcox, R. Tohtong, J.O. Vigoreaux, H. Yamashita, D.W. Maughan, Phosphorylation-dependent power output of transgenic flies: an integrated study, Biophysical Journal, Volume 73, Issue 6, 1997, Pages 3122-3134, ISSN 0006-3495, https://doi.org/10.1016/S0006-3495(97)78338-3. (http://www.sciencedirect.com/science/article/pii/S0006349597783383)
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:90941
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:16 Nov 2018 17:15
Last Modified:03 Oct 2019 20:30

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