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Article: Cellular and molecular pathways controlling muscle size in response to exercise

Attwaters, Michael / Hughes, Simon M.

FEBS journal. 2022 Mar., v. 289, no. 6

2022

Abstract: From the discovery of ATP and motor proteins to synaptic neurotransmitters and growth factor control of cell differentiation, skeletal muscle has provided an extreme model system in which to understand aspects of tissue function. Muscle is one of the few ...

Abstract	From the discovery of ATP and motor proteins to synaptic neurotransmitters and growth factor control of cell differentiation, skeletal muscle has provided an extreme model system in which to understand aspects of tissue function. Muscle is one of the few tissues that can undergo both increase and decrease in size during everyday life. Muscle size depends on its contractile activity, but the precise cellular and molecular pathway(s) by which the activity stimulus influences muscle size and strength remain unclear. Four correlates of muscle contraction could, in theory, regulate muscle growth: nerve‐derived signals, cytoplasmic calcium dynamics, the rate of ATP consumption and physical force. Here, we summarise the evidence for and against each stimulus and what is known or remains unclear concerning their molecular signal transduction pathways and cellular effects. Skeletal muscle can grow in three ways, by generation of new syncytial fibres, addition of nuclei from muscle stem cells to existing fibres or increase in cytoplasmic volume/nucleus. Evidence suggests the latter two processes contribute to exercise‐induced growth. Fibre growth requires increase in sarcolemmal surface area and cytoplasmic volume at different rates. It has long been known that high‐force exercise is a particularly effective growth stimulus, but how this stimulus is sensed and drives coordinated growth that is appropriately scaled across organelles remains a mystery.
Keywords	calcium ; cell differentiation ; exercise ; muscle contraction ; muscles ; neurotransmitters ; organelles ; signal transduction ; skeletal muscle ; surface area
Language	English
Dates of publication	2022-03
Size	p. 1428-1456.
Publishing place	John Wiley & Sons, Ltd
Document type	Article
Note	REVIEW
ZDB-ID	2173655-8
ISSN	1742-4658 ; 1742-464X
ISSN (online)	1742-4658
ISSN	1742-464X
DOI	10.1111/febs.15820
Database	NAL-Catalogue (AGRICOLA)

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Article ; Online: Isolation, Culture, and Analysis of Zebrafish Myofibers and Associated Muscle Stem Cells to Explore Adult Skeletal Myogenesis.

Ganassi, Massimo / Zammit, Peter S / Hughes, Simon M

Methods in molecular biology (Clifton, N.J.)

2023 Volume 2640, Page(s) 21–43

Abstract: Adult skeletal musculature experiences continuous physical stress, and hence requires maintenance and repair to ensure its continued efficient functioning. The population of resident muscle stem cells (MuSCs), termed satellite cells, resides beneath the ... ...

Abstract	Adult skeletal musculature experiences continuous physical stress, and hence requires maintenance and repair to ensure its continued efficient functioning. The population of resident muscle stem cells (MuSCs), termed satellite cells, resides beneath the basal lamina of adult myofibers, contributing to both muscle hypertrophy and regeneration. Upon exposure to activating stimuli, MuSCs proliferate to generate new myoblasts that differentiate and fuse to regenerate or grow myofibers. Moreover, many teleost fish undergo continuous growth throughout life, requiring continual nuclear recruitment from MuSCs to initiate and grow new fibers, a process that contrasts with the determinate growth observed in most amniotes. In this chapter, we describe a method for the isolation, culture, and immunolabeling of adult zebrafish myofibers that permits examination of both myofiber characteristics ex vivo and the MuSC myogenic program in vitro. Morphometric analysis of isolated myofibers is suitable to assess differences among slow and fast muscles or to investigate cellular features such as sarcomeres and neuromuscular junctions. Immunostaining for Pax7, a canonical stemness marker, identifies MuSCs on isolated myofibers for study. Furthermore, the plating of viable myofibers allows MuSC activation and expansion and downstream analysis of their proliferative and differentiative dynamics, thus providing a suitable, parallel alternative to amniote models for the study of vertebrate myogenesis.
MeSH term(s)	Animals ; Zebrafish ; Muscle, Skeletal ; Cell Differentiation ; Satellite Cells, Skeletal Muscle ; Muscle Development ; Muscle Fibers, Skeletal
Language	English
Publishing date	2023-03-13
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ISSN	1940-6029
ISSN (online)	1940-6029
DOI	10.1007/978-1-0716-3036-5_3
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Article ; Online: Cellular and molecular pathways controlling muscle size in response to exercise.

Attwaters, Michael / Hughes, Simon M

The FEBS journal

2021 Volume 289, Issue 6, Page(s) 1428–1456

Abstract	From the discovery of ATP and motor proteins to synaptic neurotransmitters and growth factor control of cell differentiation, skeletal muscle has provided an extreme model system in which to understand aspects of tissue function. Muscle is one of the few tissues that can undergo both increase and decrease in size during everyday life. Muscle size depends on its contractile activity, but the precise cellular and molecular pathway(s) by which the activity stimulus influences muscle size and strength remain unclear. Four correlates of muscle contraction could, in theory, regulate muscle growth: nerve-derived signals, cytoplasmic calcium dynamics, the rate of ATP consumption and physical force. Here, we summarise the evidence for and against each stimulus and what is known or remains unclear concerning their molecular signal transduction pathways and cellular effects. Skeletal muscle can grow in three ways, by generation of new syncytial fibres, addition of nuclei from muscle stem cells to existing fibres or increase in cytoplasmic volume/nucleus. Evidence suggests the latter two processes contribute to exercise-induced growth. Fibre growth requires increase in sarcolemmal surface area and cytoplasmic volume at different rates. It has long been known that high-force exercise is a particularly effective growth stimulus, but how this stimulus is sensed and drives coordinated growth that is appropriately scaled across organelles remains a mystery.
MeSH term(s)	Adenosine Triphosphate ; Exercise ; Muscle Contraction/physiology ; Muscle Fibers, Skeletal ; Muscle, Skeletal/physiology ; Myosins
Chemical Substances	Adenosine Triphosphate (8L70Q75FXE) ; Myosins (EC 3.6.4.1)
Language	English
Publishing date	2021-03-29
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Review
ZDB-ID	2173655-8
ISSN	1742-4658 ; 1742-464X
ISSN (online)	1742-4658
ISSN	1742-464X
DOI	10.1111/febs.15820
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Article ; Online: Slow myosin heavy chain 1 is required for slow myofibril and muscle fibre growth but not for myofibril initiation.

Hau, Hoi-Ting A / Kelu, Jeffrey J / Ochala, Julien / Hughes, Simon M

Developmental biology

2023 Volume 499, Page(s) 47–58

Abstract: Slow myosin heavy chain 1 (Smyhc1) is the major sarcomeric myosin driving early contraction by slow skeletal muscle fibres in zebrafish. New mutant alleles lacking a functional smyhc1 gene move poorly, but recover motility as the later-formed fast muscle ...

Abstract	Slow myosin heavy chain 1 (Smyhc1) is the major sarcomeric myosin driving early contraction by slow skeletal muscle fibres in zebrafish. New mutant alleles lacking a functional smyhc1 gene move poorly, but recover motility as the later-formed fast muscle fibres of the segmental myotomes mature, and are adult viable. By motility analysis and inhibiting fast muscle contraction pharmacologically, we show that a slow muscle motility defect persists in mutants until about 1 month of age. Breeding onto a genetic background marking slow muscle fibres with EGFP revealed that mutant slow fibres undergo terminal differentiation, migration and fibre formation indistinguishable from wild type but fail to generate large myofibrils and maintain cellular orientation and attachments. In mutants, initial myofibrillar structures with 1.67 μm periodic actin bands fail to mature into the 1.96 μm sarcomeres observed in wild type, despite the presence of alternative myosin heavy chain molecules. The poorly-contractile mutant slow muscle cells generate numerous cytoplasmic organelles, but fail to grow and bundle myofibrils or to increase in cytoplasmic volume despite passive movements imposed by fast muscle. The data show that both slow myofibril maturation and cellular volume increase depend on the function of a specific myosin isoform and suggest that appropriate force production regulates muscle fibre growth.
MeSH term(s)	Animals ; Muscle Contraction ; Muscle Fibers, Skeletal ; Muscle, Skeletal/physiology ; Myofibrils/chemistry ; Myosin Heavy Chains/genetics ; Myosins ; Zebrafish/genetics
Chemical Substances	Myosin Heavy Chains (EC 3.6.4.1) ; Myosins (EC 3.6.4.1) ; smyhc1 protein, zebrafish (EC 3.6.4.1)
Language	English
Publishing date	2023-04-28
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	1114-9
ISSN	1095-564X ; 0012-1606
ISSN (online)	1095-564X
ISSN	0012-1606
DOI	10.1016/j.ydbio.2023.04.002
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Article ; Online: MYH13, a superfast myosin expressed in extraocular, laryngeal and syringeal muscles.

Schiaffino, Stefano / Hughes, Simon M / Murgia, Marta / Reggiani, Carlo

The Journal of physiology

2023 Volume 602, Issue 3, Page(s) 427–443

Abstract: MYH13 is a unique type of sarcomeric myosin heavy chain (MYH) first detected in mammalian extraocular (EO) muscles and later also in vocal muscles, including laryngeal muscles of some mammals and syringeal muscles of songbirds. All these muscles are ... ...

Abstract	MYH13 is a unique type of sarcomeric myosin heavy chain (MYH) first detected in mammalian extraocular (EO) muscles and later also in vocal muscles, including laryngeal muscles of some mammals and syringeal muscles of songbirds. All these muscles are specialized in generating very fast contractions while producing relatively low force, a design appropriate for muscles acting against a much lower load than most skeletal muscles inserting into the skeleton. The definition of the physiological properties of muscle fibres containing MYH13 has been complicated by the mixed fibre type composition of EO muscles and the coexistence of different MYH types within the same fibre. A major advance in this area came from studies on isolated recombinant myosin motors and the demonstration that the affinity of actin-bound human MYH13 for ADP is much weaker than those of fast-type MYH1 (type 2X) and MYH2 (type 2A). This property is consistent with a very fast detachment of myosin from actin, a major determinant of shortening velocity. The MYH13 gene arose early during vertebrate evolution but was characterized only in mammals and birds and appears to have been lost in some teleost fish. The MYH13 gene is located at the 3' end of the mammalian fast/developmental gene cluster and in a similar position to the orthologous cluster in syntenic regions of the songbird genome. MYH13 gene regulation is controlled by a super-enhancer in the mammalian locus and deletion of the neighbouring fast MYH1 and MYH4 genes leads to abnormal MYH13 expression in mouse leg muscles.
MeSH term(s)	Animals ; Humans ; Mice ; Actins/metabolism ; Mammals/metabolism ; Myosin Heavy Chains/genetics ; Myosin Heavy Chains/metabolism ; Myosins/metabolism ; Oculomotor Muscles/metabolism
Chemical Substances	Actins ; Myosin Heavy Chains (EC 3.6.4.1) ; Myosins (EC 3.6.4.1) ; MYH13 protein, human
Language	English
Publishing date	2023-12-31
Publishing country	England
Document type	Journal Article
ZDB-ID	3115-x
ISSN	1469-7793 ; 0022-3751
ISSN (online)	1469-7793
ISSN	0022-3751
DOI	10.1113/JP285714
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Article ; Online: Slow myosin heavy chain 1 is required for slow myofibril and muscle fibre growth but not for myofibril initiation

Hau, Hoi-Ting A. / Kelu, Jeffrey J. / Ochala, Julien / Hughes, Simon M.

Developmental Biology. 2023 July, v. 499 p.47-58

2023

Abstract	Slow myosin heavy chain 1 (Smyhc1) is the major sarcomeric myosin driving early contraction by slow skeletal muscle fibres in zebrafish. New mutant alleles lacking a functional smyhc1 gene move poorly, but recover motility as the later-formed fast muscle fibres of the segmental myotomes mature, and are adult viable. By motility analysis and inhibiting fast muscle contraction pharmacologically, we show that a slow muscle motility defect persists in mutants until about 1 month of age. Breeding onto a genetic background marking slow muscle fibres with EGFP revealed that mutant slow fibres undergo terminal differentiation, migration and fibre formation indistinguishable from wild type but fail to generate large myofibrils and maintain cellular orientation and attachments. In mutants, initial myofibrillar structures with 1.67 μm periodic actin bands fail to mature into the 1.96 μm sarcomeres observed in wild type, despite the presence of alternative myosin heavy chain molecules. The poorly-contractile mutant slow muscle cells generate numerous cytoplasmic organelles, but fail to grow and bundle myofibrils or to increase in cytoplasmic volume despite passive movements imposed by fast muscle. The data show that both slow myofibril maturation and cellular volume increase depend on the function of a specific myosin isoform and suggest that appropriate force production regulates muscle fibre growth.
Keywords	Danio rerio ; actin ; adults ; genes ; genetic background ; muscle contraction ; muscle fibers ; muscles ; mutants ; myosin heavy chains ; organelles ; sarcomeres ; skeletal muscle
Language	English
Dates of publication	2023-07
Size	p. 47-58.
Publishing place	Elsevier Inc.
Document type	Article ; Online
Note	Use and reproduction
ZDB-ID	1114-9
ISSN	1095-564X ; 0012-1606
ISSN (online)	1095-564X
ISSN	0012-1606
DOI	10.1016/j.ydbio.2023.04.002
Database	NAL-Catalogue (AGRICOLA)

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Article ; Online: Real Time and Repeated Measurement of Skeletal Muscle Growth in Individual Live Zebrafish Subjected to Altered Electrical Activity.

Attwaters, Michael / Kelu, Jeffrey J / Pipalia, Tapan G / Hughes, Simon M

Journal of visualized experiments : JoVE

2022 , Issue 184

Abstract: A number of methods can be used to visualize individual cells throughout the body of live embryonic, larval or juvenile zebrafish. We show that live fish with fluorescently-marked plasma membranes can be scanned in a confocal laser scanning microscope in ...

Abstract	A number of methods can be used to visualize individual cells throughout the body of live embryonic, larval or juvenile zebrafish. We show that live fish with fluorescently-marked plasma membranes can be scanned in a confocal laser scanning microscope in order to determine the volume of muscle tissue and the number of muscle fibers present. Efficient approaches for the measurement of cell number and size in live animals over time are described and validated against more arduous segmentation methods. Methods are described that permit the control of muscle electrical, and thus contractile, activity. Loss of skeletal muscle contractile activity greatly reduced muscle growth. In larvae, a protocol is described that allows reintroduction of patterned electrical-evoked contractile activity. The described methods minimize the effect of inter-individual variability and will permit analysis of the effect of electrical, genetic, drug, or environmental stimuli on a variety of cellular and physiological growth parameters in the context of the living organism. Long-term follow-up of the measured effects of a defined early-life intervention on individuals can subsequently be performed.
MeSH term(s)	Animals ; Larva ; Muscle Contraction ; Muscle Fibers, Skeletal ; Nervous System Physiological Phenomena ; Zebrafish
Language	English
Publishing date	2022-06-16
Publishing country	United States
Document type	Journal Article ; Video-Audio Media ; Research Support, Non-U.S. Gov't
ZDB-ID	2259946-0
ISSN	1940-087X ; 1940-087X
ISSN (online)	1940-087X
ISSN	1940-087X
DOI	10.3791/64063
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Article ; Online: Isolation of Myofibres and Culture of Muscle Stem Cells from Adult Zebrafish.

Ganassi, Massimo / Zammit, Peter S / Hughes, Simon M

Bio-protocol

2021 Volume 11, Issue 17, Page(s) e4149

Abstract: Skeletal muscles generate force throughout life and require maintenance and repair to ensure efficiency. The population of resident muscle stem cells (MuSCs), termed satellite cells, dwells beneath the basal lamina of adult myofibres and contributes to ... ...

Abstract	Skeletal muscles generate force throughout life and require maintenance and repair to ensure efficiency. The population of resident muscle stem cells (MuSCs), termed satellite cells, dwells beneath the basal lamina of adult myofibres and contributes to both muscle growth and regeneration. Upon exposure to activating signals, MuSCs proliferate to generate myoblasts that differentiate and fuse to grow or regenerate myofibres. This myogenic progression resembles aspects of muscle formation and development during embryogenesis. Therefore, the study of MuSCs and their associated myofibres permits the exploration of muscle stem cell biology, including the cellular and molecular mechanisms underlying muscle formation, maintenance and repair. As most aspects of MuSC biology have been described in rodents, their relevance to other species, including humans, is unclear and would benefit from comparison to an alternative vertebrate system. Here, we describe a procedure for the isolation and immunolabelling or culture of adult zebrafish myofibres that allows examination of both myofibre characteristics and MuSC biology
Language	English
Publishing date	2021-09-05
Publishing country	United States
Document type	Journal Article
ZDB-ID	2833269-6
ISSN	2331-8325 ; 2331-8325
ISSN (online)	2331-8325
ISSN	2331-8325
DOI	10.21769/BioProtoc.4149
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Article ; Online: Skeletal Muscle Regeneration in Zebrafish.

Pipalia, Tapan G / Sultan, Sami H A / Koth, Jana / Knight, Robert D / Hughes, Simon M

Methods in molecular biology (Clifton, N.J.)

2023 Volume 2640, Page(s) 227–248

Abstract: Muscle regeneration models have revealed mechanisms of inflammation, wound clearance, and stem cell-directed repair of damage, thereby informing therapy. Whereas studies of muscle repair are most advanced in rodents, the zebrafish is emerging as an ... ...

Abstract	Muscle regeneration models have revealed mechanisms of inflammation, wound clearance, and stem cell-directed repair of damage, thereby informing therapy. Whereas studies of muscle repair are most advanced in rodents, the zebrafish is emerging as an additional model organism with genetic and optical advantages. Various muscle wounding protocols (both chemical and physical) have been published. Here we describe simple, cheap, precise, adaptable, and effective wounding protocols and analysis methods for two stages of a larval zebrafish skeletal muscle regeneration model. We show examples of how muscle damage, ingression of muscle stem cells, immune cells, and regeneration of fibers can be monitored over an extended timecourse in individual larvae. Such analyses have the potential to greatly enhance understanding, by reducing the need to average regeneration responses across individuals subjected to an unavoidably variable wound stimulus.
MeSH term(s)	Animals ; Zebrafish/physiology ; Muscle Fibers, Skeletal ; Stem Cells ; Satellite Cells, Skeletal Muscle/physiology ; Cell Proliferation ; Muscle, Skeletal/physiology
Language	English
Publishing date	2023-03-13
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ISSN	1940-6029
ISSN (online)	1940-6029
DOI	10.1007/978-1-0716-3036-5_17
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Article ; Online: Circadian regulation of muscle growth independent of locomotor activity.

Kelu, Jeffrey J / Pipalia, Tapan G / Hughes, Simon M

Proceedings of the National Academy of Sciences of the United States of America

2020 Volume 117, Issue 49, Page(s) 31208–31218

Abstract: Muscle tissue shows diurnal variations in function, physiology, and metabolism. Whether such variations are dependent on the circadian clock per se or are secondary to circadian differences in physical activity and feeding pattern is unclear. By ... ...

Abstract	Muscle tissue shows diurnal variations in function, physiology, and metabolism. Whether such variations are dependent on the circadian clock per se or are secondary to circadian differences in physical activity and feeding pattern is unclear. By measuring muscle growth over 12-h periods in live prefeeding larval zebrafish, we show that muscle grows more during day than night. Expression of dominant negative CLOCK (ΔCLK), which inhibits molecular clock function, ablates circadian differences and reduces muscle growth. Inhibition of muscle contraction reduces growth in both day and night, but does not ablate the day/night difference. The circadian clock and physical activity are both required to promote higher muscle protein synthesis during the day compared to night, whereas markers of protein degradation,
MeSH term(s)	Animals ; Circadian Clocks/drug effects ; Circadian Clocks/genetics ; Circadian Rhythm/drug effects ; Circadian Rhythm/genetics ; Larva/genetics ; Larva/growth & development ; Light ; Locomotion/drug effects ; Locomotion/genetics ; Mechanistic Target of Rapamycin Complex 1/genetics ; Muscle Development/genetics ; Muscle, Skeletal/growth & development ; Muscle, Skeletal/metabolism ; Photoperiod ; Sirolimus/pharmacology ; Zebrafish/genetics ; Zebrafish/growth & development
Chemical Substances	Mechanistic Target of Rapamycin Complex 1 (EC 2.7.11.1) ; Sirolimus (W36ZG6FT64)
Language	English
Publishing date	2020-11-23
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	209104-5
ISSN	1091-6490 ; 0027-8424
ISSN (online)	1091-6490
ISSN	0027-8424
DOI	10.1073/pnas.2012450117
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