The Structural and Biomechanical Properties of Insect Thick Filaments
Expressing Flightin and Cardiac Myosin Binding Protein-C
Lynda Menard
1
, Lori Nyland
2
, Jim Vigoreaux
1
Department of Biology
1
and Molecular Physiology and Biophysics
2
, University of Vermont,
Burlington, Vermont
Cardiac myosin binding protein-c (cMyBP-C) of mammalian cardiac muscle and flightin (FLN)
of invertebrate indirect flight muscle (IFM) have been shown to contribute to thick filament
stiffness, as determined by calculations of persistence length (PL), an index of flexural rigidity
[1, 2] in their corresponding muscle systems. FLN and cMyBP-C in vitro bind to a common site
in the coiled-coil region of myosin II, and both proteins are known to be regulated by
phosphorylation [3, 4]. To test the hypothesis that FLN and cMyBP-C are functionally
homologous, we have determined the extent to which cMyBP-C can rescue the phenotypes
manifested in the Drosophila FLN knockout strain fln
0
. Structural characteristics of flight muscle
sarcomeres were analyzed by transmission electron microscopy (TEM) and the contour and end-
to-end length of isolated, hydrated native thick filaments was measured by atomic force
microscopy (AFM).
Experiments were carried out on four D. melanogaster mutant and transgenic strains: (i) FLN
knockout strain (fln
0
), (ii) a knockout rescued transgenic strain (fln
0
;fln
+
), (iii) a transgenic
cMyBP-C strain without FLN expression (fln
0
;cMyBPC
+
), and (iv) a transgenic strain with FLN
expression alongside cMyBP-C expression (fln
+
;cMyBPC
+
). In preparation for TEM, thoraces
from newly eclosed (<1 hour) D. melanogaster were bisected, fixed, dehydrated, infiltrated,
embedded, sectioned and imaged by TEM [5]. The length of sarcomeres from 4-5 flies for each
Drosophila strain was measured using ImageJ. AFM data of isolated thick filaments were
evaluated using the parameters and programs described by [6]. Statistical analysis was done
using JMP 9 software.
The TEM results confirmed both the sarcomere length measurements and level of structural
order previously seen for fln
0
and fln
0
;fln
+
, while revealing shorter sarcomeres in the transgenic
lines involving cMyBP-C alone (Fig. 1, Table. 1). When cMyBP-C is expressed alongside FLN,
sarcomere length is slightly but significantly longer than sarcomere length in the control fln
0
;fln
+
.
These results support the idea of cMyBP-C binding to myosin in thick filaments of D.
melanogaster and influencing the length of the filaments. However, the length regulation exerted
by cMyBP-C is surpassed by FLN when FLN is present, either by direct binding competition to a
common myosin binding site or another regulatory mechanism.
The PL for fln
+
;cMyBPC
+
obtained by AFM was significantly higher than PL for fln
0
;fln
+
, suggesting that cMyBP-C contributes to filament
stiffness when expressed ectopically in IFM. However, the cMyBP-C effect is seen only in the
presence of FLN as PL of fln
0
;cMyBPC
+
was not different that PL of fln
0
. Our observations
suggest that the presence of FLN influences the effects that cMyBP-C has on the mechanical
properties of the thick filaments. This may possibly be due to FLN stabilizing the thick filaments
to permit a more ideal environment for cMyBP-C binding. From these studies we conclude that
80
doi:10.1017/S1431927613002390
Microsc. Microanal. 19 (Suppl 2), 2013
© Microscopy Society of America 2013
https://doi.org/10.1017/S1431927613002390
Downloaded from https://www.cambridge.org/core. IP address: 54.163.42.124, on 29 May 2020 at 22:59:45, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms.