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mechanical tension and spontaneous muscle twitching precede the formation of cross striated muscle in vivo

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Nội dung chi tiết: mechanical tension and spontaneous muscle twitching precede the formation of cross striated muscle in vivo

mechanical tension and spontaneous muscle twitching precede the formation of cross striated muscle in vivo

Development Advance Online Articles. First posted online on 7 February 2017 Í httns'//|(hothuvif*n com Access the most recent version at http:,'/dev.b

mechanical tension and spontaneous muscle twitching precede the formation of cross striated muscle in vivobiologỉsts.org/lookiip/doi/lO.lr*Mechanical tension and spontaneous muscle twitching precede the formation of cross-striated muscle ill vivoManuela We

itkunat1 . Martina Lindauer2 . Andreas Bausch2 and Frank Schnorrer1 ’1Muscle Dynamics Group. Max Planck Institute of Biochemistry. Am Klopferspitz 18. mechanical tension and spontaneous muscle twitching precede the formation of cross striated muscle in vivo

82152 Martinsried. Germany2Lehrstuhl fur Biophysik E27. Technische Universitat Munchen. James-Franck-StraBe 1.85748 Garching, GermanyDevelopmental Bio

mechanical tension and spontaneous muscle twitching precede the formation of cross striated muscle in vivo

logy Institute of Marseille (IBDM). CNRS. UMR 7288. Aix-MarseilleUniversité. Case 907, Parc Scientifique de Lummy. 13288 Marseille, FranceThese author

Development Advance Online Articles. First posted online on 7 February 2017 Í httns'//|(hothuvif*n com Access the most recent version at http:,'/dev.b

mechanical tension and spontaneous muscle twitching precede the formation of cross striated muscle in vivobrillogenesis. sarcomere, self-organisation© 2017. Published by The Company of Biologists Ltd.This is an Open Access article distributed under the ter

ms of the Creative Commons Attribution License (http://creati vecommons.org/llcenses/by/3.0), which penults unrestricted use. distribution and reprodu mechanical tension and spontaneous muscle twitching precede the formation of cross striated muscle in vivo

ctionIn any medium provided that the original work Is properly attributed.Development • Advance articleAbstractMuscle forces are produced by repetitiv

mechanical tension and spontaneous muscle twitching precede the formation of cross striated muscle in vivo

e stereotyped acto-myosin units called sarcomeres. Sarcomeres are chained into linear myofibrils spanning the entire muscle fiber. In mammalian body m

Development Advance Online Articles. First posted online on 7 February 2017 Í httns'//|(hothuvif*n com Access the most recent version at http:,'/dev.b

mechanical tension and spontaneous muscle twitching precede the formation of cross striated muscle in vivot muscle structure, it is still unclear how cross-striated myofibrils are built in vivo. Here, we investigate the morphogenesis of Drosophila abdomina

l muscles and establish them as hl vivo model for cross-striated muscle development. Using live imaging, we find that long immature myofibrils lacking mechanical tension and spontaneous muscle twitching precede the formation of cross striated muscle in vivo

a periodic acto-myosin pattern are built simultaneously in the entire muscle fiber and then align laterally to mature cross-striated myofibrils. Inte

mechanical tension and spontaneous muscle twitching precede the formation of cross striated muscle in vivo

restingly, laser micro-lesion experiments demonstrate that mechanical tension precedes the formation of the immature myofibrils. Moreover, these immat

Development Advance Online Articles. First posted online on 7 February 2017 Í httns'//|(hothuvif*n com Access the most recent version at http:,'/dev.b

mechanical tension and spontaneous muscle twitching precede the formation of cross striated muscle in vivothese results suggest a myofibrillogenesis model, in which mechanical tension and spontaneous muscle twitchings synchronise the simultaneous self-orga

nisation of different sarcomeric protein complexes to build highly regular cross-striated myofibrils spanning throughout large muscle fibers.Developme mechanical tension and spontaneous muscle twitching precede the formation of cross striated muscle in vivo

nt • Advance articleIntroductionThe muscular system is the major force-producing tissue of animals. In particular the skeletal muscles enable precise

mechanical tension and spontaneous muscle twitching precede the formation of cross striated muscle in vivo

body movements of invertebrates and vertebrates. For these accurate movements, each muscle must be properly connected to the skeleton. This is achieve

Development Advance Online Articles. First posted online on 7 February 2017 Í httns'//|(hothuvif*n com Access the most recent version at http:,'/dev.b

mechanical tension and spontaneous muscle twitching precede the formation of cross striated muscle in vivo into muscle fiber bundles that run parallel to the long axis of the muscle. Thus, muscle is a highly polar tissue, which harbours a defined contracti

on axis between both tendon attachments (Hill and Olson. 2012).The sarcomere is the contractile unit of each muscle fiber (Clark et al.. 2002; Gautel mechanical tension and spontaneous muscle twitching precede the formation of cross striated muscle in vivo

and Djinovic-Carugo. 2016). Each sarcomere is symmetrically organised between two Z-discs. which cross-link antiparallel polar actin filaments, also c

mechanical tension and spontaneous muscle twitching precede the formation of cross striated muscle in vivo

alled thin filaments. The centrally located thick filaments are comprised of bipolar myosin filaments. These thick filaments are permanently connected

Development Advance Online Articles. First posted online on 7 February 2017 Í httns'//|(hothuvif*n com Access the most recent version at http:,'/dev.b

mechanical tension and spontaneous muscle twitching precede the formation of cross striated muscle in vivos results in a stereotyped length of each sarcomere that is characteristic for the muscle type, ranging from about 3.0 to 3.4 pm in relaxed human skel

etal muscle in vivo (Ehler and Gautel. 2008; Llewellyn et al.. 2008). As individual muscle fibers can be several centimetres long, hundreds, often tho mechanical tension and spontaneous muscle twitching precede the formation of cross striated muscle in vivo

usands of sarcomeres require to assemble into long chains called myofibrils during muscle development (Hill and Olson. 2012; Sanger et al.. 2010).Desp

mechanical tension and spontaneous muscle twitching precede the formation of cross striated muscle in vivo

ite detailed textbook knowledge about mature sarcomere and myofibril architecture, our understanding of myofibril and sarcomere formation during muscl

Development Advance Online Articles. First posted online on 7 February 2017 Í httns'//|(hothuvif*n com Access the most recent version at http:,'/dev.b

mechanical tension and spontaneous muscle twitching precede the formation of cross striated muscle in vivon muscle, sets sarcomere length (Furst et al.. 1988; Tskhovrebova and Trinick. 2003; Tskhovrebova et al.. 2015; Whiting et al., 1989). However, it is

unclear how such a ruler defines the characteristic sarcomere length ofDevelopment • Advance articlethe different muscle types (Gokhin and Fowler. 201 mechanical tension and spontaneous muscle twitching precede the formation of cross striated muscle in vivo

3). The ruler hypothesis is also challenged in insect muscle, as individual insect titin homologs are too short to span across half a sarcomere. Never

mechanical tension and spontaneous muscle twitching precede the formation of cross striated muscle in vivo

theless, insect sarcomere sizes are set as precisely as in vertebrates (Bullard et al., 2005; Tskhovrebova and Trinick. 2012). Likewise, it is debated

Development Advance Online Articles. First posted online on 7 February 2017 Í httns'//|(hothuvif*n com Access the most recent version at http:,'/dev.b

mechanical tension and spontaneous muscle twitching precede the formation of cross striated muscle in vivonto regular myofibrils by exchanging nonmuscle myosin II with muscle myosin II (Rhee et al.. 1994; Sanger et al., 2010; Sparrow and Schock, 2009) or a

lternatively, thin and thick filaments assemble more independently and subsequently interdigitate (Ehler et al.. 1999; Holtzer et al., 1997; Rui et al mechanical tension and spontaneous muscle twitching precede the formation of cross striated muscle in vivo

., 2010). Data supporting these models were often acquired in vitro by analysing card io myocytes or myotubes adhering to a Petri dish. This contrasts

mechanical tension and spontaneous muscle twitching precede the formation of cross striated muscle in vivo

the in vivo situation, in which both defined muscle fiber ends attach to tendons and thus set the polarity and contraction axis of the muscle fiber.

Development Advance Online Articles. First posted online on 7 February 2017 Í httns'//|(hothuvif*n com Access the most recent version at http:,'/dev.b

mechanical tension and spontaneous muscle twitching precede the formation of cross striated muscle in vivonce (Hill and Olson. 2012). which is essential for the mechanism of muscle contraction (Huxley and Niedergerke, 1954: Huxley and Hanson, 1954). These

cross-striations are formed by a regular lateral alignment of the individual myofibrils. During this alignment the Z-bands grow significantly in width mechanical tension and spontaneous muscle twitching precede the formation of cross striated muscle in vivo

(Sanger et al.. 2010) and neighbouring Z-discs might be linked by intermediate filaments (Gautel and Djinovic-Carugo, 2016). It has been found that e

mechanical tension and spontaneous muscle twitching precede the formation of cross striated muscle in vivo

ven mature Z-disc dynamically exchange a number of Z-disc components with the cytoplasmic pool (Wang et al.. 2005). This may contribute to the Z-disc

Development Advance Online Articles. First posted online on 7 February 2017 Í httns'//|(hothuvif*n com Access the most recent version at http:,'/dev.b

mechanical tension and spontaneous muscle twitching precede the formation of cross striated muscle in vivoross-striation formation in vivo remains elusive.Recently, we have investigated myofibrillogenesis in vivo using the Drosophila indirect flight muscle

model (Weitkunat et al., 2014). We found that after myotubes haveDevelopment • Advance articleattached to tendons, myofibrils assemble simultaneously mechanical tension and spontaneous muscle twitching precede the formation of cross striated muscle in vivo

throughout the entire myofiber. This results in continuous early myofibrils that span across the entừe 200 pm long muscle fiber, suggesting a self-or

mechanical tension and spontaneous muscle twitching precede the formation of cross striated muscle in vivo

ganisation mechanism of actin, and myosin filaments, together with titin complexes. Importantly, myofibril formation is preceded by a build-up of mech

Development Advance Online Articles. First posted online on 7 February 2017 Í httns'//|(hothuvif*n com Access the most recent version at http:,'/dev.b

mechanical tension and spontaneous muscle twitching precede the formation of cross striated muscle in vivoomised. This led to an extended model of myofibrillogenesis. which proposed tension as an essential coordinator for myofibrillar selforganisation in t

he flight muscles (Lemke and Schnorrer. 2016; Weitkunat et al., 2014). Tension and myosin contractility are also components of theoretical models aimi mechanical tension and spontaneous muscle twitching precede the formation of cross striated muscle in vivo

ng at predicting the dynamics of sarcomere assembly (Friedrich et al.. 2012; Yoshinaga et al., 2010). However, the in vivo presence of tension was thu

mechanical tension and spontaneous muscle twitching precede the formation of cross striated muscle in vivo

s far only detected in indirect flight muscles of Drosophila, which display a specialised fibrillar organisation of their myofibrils that enables fast

Development Advance Online Articles. First posted online on 7 February 2017 Í httns'//|(hothuvif*n com Access the most recent version at http:,'/dev.b

mechanical tension and spontaneous muscle twitching precede the formation of cross striated muscle in vivot al., 2014).Here, we set out to investigate myofibrillogenesis and tension formation in the Drosophila adult abdominal muscles, which are cross-stria

ted, synchronously contracting muscles and thus resemble vertebrate skeletal muscles. Using in vivo imaging we detect simultaneous myofibril assembly mechanical tension and spontaneous muscle twitching precede the formation of cross striated muscle in vivo

in these muscles, and find that mechanical tension is not only present before but also during myofibril assembly. Remarkably, immature myofibrils, lac

mechanical tension and spontaneous muscle twitching precede the formation of cross striated muscle in vivo

king an obvious periodic pattern, are already contractile when stimulated by Ca2 influx, suggesting a sarcomere-like organisation of their components

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