“Muscling” Throughout Life

Goody, Michelle F.; Carter, Erin V; Kilroy, Elisabeth A; Maves, Lisa; Henry, Clarissa A.

doi:10.1016/bs.ctdb.2016.11.002

Cited by 28 publications

(12 citation statements)

References 140 publications

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“…(b) Selected features of the turquoise killifish that are conserved in human and vertebrate canonical research organisms (zebrafish and house mouse), but are missing in invertebrate canonical research organisms (round worm and fruit fly). References: nervous system: Shimeld and Holland (2000), Freeman and Doherty (2006); Lohr and Hammerschmidt (2011), Oikonomou and Shaham (2011), immune system: Langenau and Zon (2005), Engelmann and Pujol (2010), Buchon, Silverman and Cherry ( 2014); circulatory system: Lehmacher, Abeln and Paululat ( 2012); Stephenson, Adams and Vaccarezza ( 2017); respiratory system: Schottenfeld, Song and Ghabrial ( 2010); skeletal system: Shimeld and Holland (2000); muscular system: Moerman and Williams (2006), Demontis, Piccirillo, Goldberg and Perrimon ( 2013), Piccirillo, Demontis, Perrimon and Goldberg ( 2014), Goody, Carter, Kilroy, Maves and Henry ( 2017); digestive system: McKay, McKay, Avery and Graff ( 2003), Arrese and Soulages (2010), Hashmi et al. ( 2013), Kuraishi, Hori and Kurata ( 2013), Lemaitre and Miguel‐Aliaga (2013), McGhee (2013), Ritter et al.…”

Section: Research Organisms For Agingmentioning

confidence: 99%

The African turquoise killifish: A research organism to study vertebrate aging and diapause

Brunet²

2018

Aging Cell

135

118

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SummaryThe African turquoise killifish has recently gained significant traction as a new research organism in the aging field. Our understanding of aging has strongly benefited from canonical research organisms—yeast, C. elegans, Drosophila, zebrafish, and mice. Many characteristics that are essential to understand aging—for example, the adaptive immune system or the hypothalamo‐pituitary axis—are only present in vertebrates (zebrafish and mice). However, zebrafish and mice live more than 3 years and their relatively long lifespans are not compatible with high‐throughput studies. Therefore, the turquoise killifish, a vertebrate with a naturally compressed lifespan of only 4–6 months, fills an essential gap to understand aging. With a recently developed genomic and genetic toolkit, the turquoise killifish not only provides practical advantages for lifespan and longitudinal experiments, but also allows more systematic characterizations of the interplay between genetics and environment during vertebrate aging. Interestingly, the turquoise killifish can also enter a long‐term dormant state during development called diapause. Killifish embryos in diapause already have some organs and tissues, and they can last in this state for years, exhibiting exceptional resistance to stress and to damages due to the passage of time. Understanding the diapause state could give new insights into strategies to prevent the damage caused by aging and to better preserve organs, tissues, and cells. Thus, the African turquoise killifish brings two interesting aspects to the aging field—a compressed lifespan and a long‐term resistant diapause state, both of which should spark new discoveries in the field.

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Section: Research Organisms For Agingmentioning

confidence: 99%

The African turquoise killifish: A research organism to study vertebrate aging and diapause

Brunet²

2018

Aging Cell

135

118

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“…Due to the high degree of genetic and structural conservation among vertebrate muscles, a number of human myopathies (e.g. Duchenne muscular dystrophy) have an analogous phenotype in the zebrafish, making their larvae a model system of choice, based on several unique attributes (3-5, 8, 9). Importantly, larvae are transparent, enabling in vivo visualization of the underlying musculature, and are permeable to drugs, making them amenable to high-throughput studies (10-12).…”

Section: Introductionmentioning

confidence: 99%

Mechanical characteristics of ultrafast zebrafish larval swimming muscles

Mead

Kennedy

Palmer

et al. 2020

Preprint

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13Zebrafish (Danio rerio) swim within days of fertilization, powered by muscles of the axial myotomes. 14 Forces generated by these muscles can be measured rapidly in whole, intact larval tails by adapting 15 protocols developed for ex vivo muscle mechanics. But it is not known how well these measurements 16 reflect the function of the underlying muscle fibers and sarcomeres. Here we consider the anatomy of 17 the 5-day-old, wild-type larval tail, and implement technical modifications to measuring muscle 18 physiology in intact tails. Specifically, we quantify fundamental relationships between force, length, and 19 shortening velocity, and capture the extreme contractile speeds required to swim with tail-beat 20 frequencies of 80-100 Hz. Therefore, we analyze 1000 frames/second movies to track the movement of 21 structures, visible in the transparent tail, which correlate with sarcomere length. We also characterize 22 the passive viscoelastic properties of the preparation to isolate forces contributed by non-muscle 23 structures within the tail. Myotomal muscles generate more than 95% of their maximum isometric 24 stress (76±3 mN/mm 2 ) over the range of muscle lengths used in vivo. They have rapid twitch kinetics 25 (full width at half-maximum stress: 11±1 msec) and a high twitch to tetanus ratio (0.91±0.05), indicating 26 adaptations for fast excitation-contraction coupling. Although contractile stress is relatively low, 27 myotomal muscles develop high net power (134±20 W/kg at 80 Hz) in cyclical work loop experiments 28 designed to simulate the in vivo dynamics of muscle fibers during swimming. When shortening at a 29 constant speed of 7±1 muscle lengths/second, muscles develop 86±2% of isometric stress, while peak 30 instantaneous power during 100Hz work loops occurs at 18±2 muscle lengths/second. These approaches 31 can improve the usefulness of zebrafish as a model system for muscle research by providing a rapid and 32 sensitive functional readout for experimental interventions. 34Statement of significance 36The zebrafish (Danio rerio) may prove a uniquely efficient model system for characterizing vertebrate 37 muscle physiology. Transparent, drug-permeable larva -each, in essence, a fully functional muscle -can 38 be generated rapidly, inexpensively, and in large numbers. Critically, the zebrafish genome contains 39 homologs of major muscle genes and is highly amenable to manipulation. To reach its potential, reliable 40 (and preferably rapid) means are needed to observe the effects of experimental interventions on larval 41 muscle function. In the present study we show how mechanical measurements made on whole, intact 42 larval tails can provide a readout of fundamental muscle-mechanical properties. Additionally, we show 43 that these muscles are among the fastest ever measured, and therefore worthy of study in their own 44 right.45 82 contractile conditions, using a modified work loop approach. Our results suggest that the tail muscle 83 fibers generate their maximum force at the in vivo resting length ...

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“…The development of skeletal muscle is highly conserved in vertebrates, with the bulk of the musculature arising from the somitic mesoderm, which differentiates into segmented myotomes early in embryonic development [1]. Somites are patterned anterior-posteriorly by a clock-and-wave-front mechanism [2,3] and become delineated by boundaries that form at the interface between cells with high and low cadherin-mediated cell-cell adhesion, into which a fibronectin-based extracellular matrix (ECM) is deposited [4].…”

Section: Introductionmentioning

confidence: 99%

“…Somites are patterned anterior-posteriorly by a clock-and-wave-front mechanism [2,3] and become delineated by boundaries that form at the interface between cells with high and low cadherin-mediated cell-cell adhesion, into which a fibronectin-based extracellular matrix (ECM) is deposited [4]. Like many provisional fibronectin-rich matrices, the ECM between developing somites is replaced by a more complex matrix consisting of laminin-rich basement membranes flanking a core rich in fibrillar collagens as the somites mature into myotomes, and as the rectangular somite boundaries mature into chevron-shaped myotendinous junctions (MTJs) [1,[5][6][7]. This biochemical and structural remodeling of the ECM is essential for the normal development of skeletal muscle and is an ideal context in which to study developmentally regulated matrix remodeling in vivo.…”

Section: Introductionmentioning

confidence: 99%

“…While the zebrafish has duplicate paralogues of genes encoding Stromelysin-3 (designated mmp11a and mmp11b), it lacks orthologues of other members of the Stromelysin gene family [21], potentially making it a better model organism in which to study the functions of Stromelysin-3 in vivo. Furthermore, its rapid external development as a transparent embryo, amenability to molecular techniques (including specific assays for the detection of MMP activation and activity [22][23][24][25]), and various other characteristics has made the zebrafish a favorite model organism for the study of muscle development and disease, as well as MMP activity and matrix remodeling [1,7,9,21,[26][27][28][29][30].…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Paralogues of Mmp11 and Timp4 Interact during the Development of the Myotendinous Junction in the Zebrafish Embryo

Matchett

Wang

Crawford

2019

JDB

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The extracellular matrix (ECM) of the myotendinous junction (MTJ) undergoes dramatic physical and biochemical remodeling during the first 48 h of development in zebrafish, transforming from a rectangular fibronectin-dominated somite boundary to a chevron-shaped laminin-dominated MTJ. Matrix metalloproteinase 11 (Mmp11, a.k.a. Stromelysin-3) is both necessary and sufficient for the removal of fibronectin at the MTJ, but whether this protease acts directly on fibronectin and how its activity is regulated remain unknown. Using immunofluorescence, we show that both paralogues of Mmp11 accumulate at the MTJ during this time period, but with Mmp11a present early and later replaced by Mmp11b. Moreover, Mmp11a also accumulates intracellularly, associated with the Z-discs of sarcomeres within skeletal muscle cells. Using the epitope-mediated MMP activation (EMMA) assay, we show that despite having a weaker paired basic amino acid motif in its propeptide than Mmp11b, Mmp11a is activated by furin, but may also be activated by other mechanisms intracellularly. One or both paralogues of tissue inhibitors of metalloproteinase-4 (Timp4) are also present at the MTJ throughout this process, and yeast two-hybrid assays reveal distinct and specific interactions between various domains of these proteins. We propose a model in which Mmp11a activity is modulated (but not inhibited) by Timp4 during early MTJ remodeling, followed by a phase in which Mmp11b activity is both inhibited and spatially constrained by Timp4 in order to maintain the structural integrity of the mature MTJ.

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“Muscling” Throughout Life

Cited by 28 publications

References 140 publications

The African turquoise killifish: A research organism to study vertebrate aging and diapause

The African turquoise killifish: A research organism to study vertebrate aging and diapause

Mechanical characteristics of ultrafast zebrafish larval swimming muscles

Paralogues of Mmp11 and Timp4 Interact during the Development of the Myotendinous Junction in the Zebrafish Embryo

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