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Enhanced exercise and regenerative capacity in a mouse model that violates size constraints of oxidative muscle fibres

Enhanced exercise and regenerative capacity in a mouse model that violates size constraints of oxidative muscle fibres
Enhanced exercise and regenerative capacity in a mouse model that violates size constraints of oxidative muscle fibres

A central tenet of skeletal muscle biology is the existence of an inverse relationship between the oxidative fibre capacity and its size. However, robustness of this relationship is unknown. We show that superimposition of Estrogen-related receptor gamma (Errg) on the myostatin (Mtn) mouse null background (Mtn-/-/ErrgTg/+) results in hypertrophic muscle with a high oxidative capacity thus violating the inverse relationship between fibre size and oxidative capacity. We also examined the canonical view that oxidative muscle phenotype positively correlate with Satellite cell number, the resident stem cells of skeletal muscle. Surprisingly, hypertrophic fibres from Mtn-/-/ErrgTg/+ mouse showed satellite cell deficit which unexpectedly did not affect muscle regeneration. These observations 1) challenge the concept of a constraint between fibre size and oxidative capacity and 2) indicate the important role of the microcirculation in the regenerative capacity of a muscle even when satellite cell numbers are reduced.

Animals, Mice, Mice, Knockout, Muscle Fibers, Skeletal/physiology, Muscle, Skeletal/cytology, Myostatin/deficiency, Physical Conditioning, Animal, Regeneration, Satellite Cells, Skeletal Muscle/physiology
2050-084X
1-25
Omairi, Saleh
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Matsakas, Antonios
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Degens, Hans
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Kretz, Oliver
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Hansson, Kenth Arne
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Solbrå, Andreas Våvang
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Bruusgaard, Jo C.
b775392d-9a5a-4924-8604-0923b425c2e4
Joch, Barbara
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Sartori, Roberta
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Giallourou, Natasa
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Mitchell, Robert
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Collins-Hooper, Henry
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Foster, Keith
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Pasternack, Arja
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Ritvos, Olli
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Sandri, Marco
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Narkar, Vihang
9d82813b-8e4d-46c1-9dc3-c9bf7a93d544
Swann, Jonathan R.
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Huber, Tobias B.
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Patel, Ketan
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Omairi, Saleh
91a57408-f98a-497c-9328-f3164cafef5d
Matsakas, Antonios
9afcce5e-16e6-45a6-8031-1f755cad6a36
Degens, Hans
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Kretz, Oliver
b7826a71-f0b9-46d3-bc70-9723e6338fa9
Hansson, Kenth Arne
c49e71c8-3659-4a41-b72b-ac3619e82e3c
Solbrå, Andreas Våvang
e38ec86b-4fa0-4f61-98fd-c60c789753e4
Bruusgaard, Jo C.
b775392d-9a5a-4924-8604-0923b425c2e4
Joch, Barbara
5c203adb-8fc6-45f0-a810-8eb7eadd019e
Sartori, Roberta
b5e6664e-e9ca-4578-b654-e71a766d9823
Giallourou, Natasa
b5891ea7-98d4-49d7-b883-2c57ca2d962a
Mitchell, Robert
3b8341fb-2676-4ce0-af81-3d253405be3f
Collins-Hooper, Henry
d1b74880-833c-4797-b2de-4f4e420ffecb
Foster, Keith
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Pasternack, Arja
5b3ad191-6f1f-4cd4-8d9a-1712e7a0a9e8
Ritvos, Olli
3105c373-eb8f-4e88-a8e1-d9445b119718
Sandri, Marco
132bfe72-127e-41ea-84c2-80549cf8467e
Narkar, Vihang
9d82813b-8e4d-46c1-9dc3-c9bf7a93d544
Swann, Jonathan R.
7c11a66b-f4b8-4dbf-aa17-ad8b0561b85c
Huber, Tobias B.
08b5b275-6a2e-431c-9f3b-62048ff1df11
Patel, Ketan
b2b42f1a-599d-4747-9246-69379bf6648f

Omairi, Saleh, Matsakas, Antonios, Degens, Hans, Kretz, Oliver, Hansson, Kenth Arne, Solbrå, Andreas Våvang, Bruusgaard, Jo C., Joch, Barbara, Sartori, Roberta, Giallourou, Natasa, Mitchell, Robert, Collins-Hooper, Henry, Foster, Keith, Pasternack, Arja, Ritvos, Olli, Sandri, Marco, Narkar, Vihang, Swann, Jonathan R., Huber, Tobias B. and Patel, Ketan (2016) Enhanced exercise and regenerative capacity in a mouse model that violates size constraints of oxidative muscle fibres. eLife, 5, 1-25, [e16940]. (doi:10.7554/eLife.16940).

Record type: Article

Abstract

A central tenet of skeletal muscle biology is the existence of an inverse relationship between the oxidative fibre capacity and its size. However, robustness of this relationship is unknown. We show that superimposition of Estrogen-related receptor gamma (Errg) on the myostatin (Mtn) mouse null background (Mtn-/-/ErrgTg/+) results in hypertrophic muscle with a high oxidative capacity thus violating the inverse relationship between fibre size and oxidative capacity. We also examined the canonical view that oxidative muscle phenotype positively correlate with Satellite cell number, the resident stem cells of skeletal muscle. Surprisingly, hypertrophic fibres from Mtn-/-/ErrgTg/+ mouse showed satellite cell deficit which unexpectedly did not affect muscle regeneration. These observations 1) challenge the concept of a constraint between fibre size and oxidative capacity and 2) indicate the important role of the microcirculation in the regenerative capacity of a muscle even when satellite cell numbers are reduced.

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Accepted/In Press date: 19 July 2016
Published date: 5 August 2016
Additional Information: Funding Information: The financial support from the Biotechnology and Biological Sciences Research Council is gratefully acknowledged (Grants BB/J016454/1 to HCH and BB/I015787/1 to RM). The study was also supported by the European Union and The Royal Society (Grants: FP7-PEOPLE-PCIG14-GA-2013-631440 and RG140470 Research Grant to AM). Publisher Copyright: © Copyright Omairi et al. This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited. Copyright: Copyright 2021 Elsevier B.V., All rights reserved.
Keywords: Animals, Mice, Mice, Knockout, Muscle Fibers, Skeletal/physiology, Muscle, Skeletal/cytology, Myostatin/deficiency, Physical Conditioning, Animal, Regeneration, Satellite Cells, Skeletal Muscle/physiology

Identifiers

Local EPrints ID: 440831
URI: http://eprints.soton.ac.uk/id/eprint/440831
ISSN: 2050-084X
PURE UUID: 06e97369-16ac-4171-a31e-bdafa27a4fbf
ORCID for Jonathan R. Swann: ORCID iD orcid.org/0000-0002-6485-4529

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Date deposited: 20 May 2020 16:31
Last modified: 18 Mar 2024 03:56

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Contributors

Author: Saleh Omairi
Author: Antonios Matsakas
Author: Hans Degens
Author: Oliver Kretz
Author: Kenth Arne Hansson
Author: Andreas Våvang Solbrå
Author: Jo C. Bruusgaard
Author: Barbara Joch
Author: Roberta Sartori
Author: Natasa Giallourou
Author: Robert Mitchell
Author: Henry Collins-Hooper
Author: Keith Foster
Author: Arja Pasternack
Author: Olli Ritvos
Author: Marco Sandri
Author: Vihang Narkar
Author: Tobias B. Huber
Author: Ketan Patel

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