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Clonal characterization of rat muscle satellite cells: proliferation, metabolism and differentiation define an intrinsic heterogeneity

Clonal characterization of rat muscle satellite cells: proliferation, metabolism and differentiation define an intrinsic heterogeneity
Clonal characterization of rat muscle satellite cells: proliferation, metabolism and differentiation define an intrinsic heterogeneity
Satellite cells (SCs) represent a distinct lineage of myogenic progenitors responsible for the postnatal growth, repair and maintenance of skeletal muscle. Distinguished on the basis of their unique position in mature skeletal muscle, SCs were considered unipotent stem cells with the ability of generating a unique specialized phenotype. Subsequently, it was demonstrated in mice that opposite differentiation towards osteogenic and adipogenic pathways was also possible. Even though the pool of SCs is accepted as the major, and possibly the only, source of myonuclei in postnatal muscle, it is likely that SCs are not all multipotent stem cells and evidences for diversities within the myogenic compartment have been described both in vitro and in vivo. Here, by isolating single fibers from rat flexor digitorum brevis (FDB) muscle we were able to identify and clonally characterize two main subpopulations of SCs: the low proliferative clones (LPC) present in major proportion (approximately 75%) and the high proliferative clones (HPC), present instead in minor amount (approximately 25%). LPC spontaneously generate myotubes whilst HPC differentiate into adipocytes even though they may skip the adipogenic program if co-cultured with LPC. LPC and HPC differ also for mitochondrial membrane potential (DeltaPsi(m)), ATP balance and Reactive Oxygen Species (ROS) generation underlying diversities in metabolism that precede differentiation. Notably, SCs heterogeneity is retained in vivo. SCs may therefore be comprised of two distinct, though not irreversibly committed, populations of cells distinguishable for prominent differences in basal biological features such as proliferation, metabolism and differentiation. By these means, novel insights on SCs heterogeneity are provided and evidences for biological readouts potentially relevant for diagnostic purposes described
1932-6203
e8523
Rossi, Carlo A.
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Pozzobon, Michela
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Ditadi, Andrea
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Archacka, Karolina
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Gastaldello, Annalisa
8b15e63b-94ed-4897-95c9-bc7fe2b37282
Sanna, Marta
a2849975-c78c-4eab-8d5a-332ddbd0167a
Franzin, Chiara
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Malerba, Alberto
2cf73109-3e22-4acb-bc29-accac6022181
Milan, Gabriella
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Cananzi, Mara
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Schiaffino, Stefano
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Campanella, Michelangelo
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Vettor, Roberto
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De Coppi, Paolo
b4236c8b-8700-4797-a529-d8791b59088b
Rossi, Carlo A.
35c74721-3e89-49d7-ae44-5078ac251f7a
Pozzobon, Michela
8aa96c11-1a1b-4e70-98a0-36157c07bebe
Ditadi, Andrea
946043b5-9ba3-4d89-9e83-75750fe07950
Archacka, Karolina
7d494f8f-112e-4b82-b332-100a95f62e45
Gastaldello, Annalisa
8b15e63b-94ed-4897-95c9-bc7fe2b37282
Sanna, Marta
a2849975-c78c-4eab-8d5a-332ddbd0167a
Franzin, Chiara
3b5bcea2-682b-4a2b-a8b7-c85d0081932d
Malerba, Alberto
2cf73109-3e22-4acb-bc29-accac6022181
Milan, Gabriella
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Cananzi, Mara
b2e48d82-56ad-4e61-a56a-416bee05628c
Schiaffino, Stefano
91b66608-8463-434d-a9a7-4ef0ac9577a9
Campanella, Michelangelo
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Vettor, Roberto
3832c44a-a6b5-415b-8e37-c8b4e0009335
De Coppi, Paolo
b4236c8b-8700-4797-a529-d8791b59088b

Rossi, Carlo A., Pozzobon, Michela, Ditadi, Andrea, Archacka, Karolina, Gastaldello, Annalisa, Sanna, Marta, Franzin, Chiara, Malerba, Alberto, Milan, Gabriella, Cananzi, Mara, Schiaffino, Stefano, Campanella, Michelangelo, Vettor, Roberto and De Coppi, Paolo (2010) Clonal characterization of rat muscle satellite cells: proliferation, metabolism and differentiation define an intrinsic heterogeneity. PLoS ONE, 5 (1), e8523. (doi:10.1371/journal.pone.0008523).

Record type: Article

Abstract

Satellite cells (SCs) represent a distinct lineage of myogenic progenitors responsible for the postnatal growth, repair and maintenance of skeletal muscle. Distinguished on the basis of their unique position in mature skeletal muscle, SCs were considered unipotent stem cells with the ability of generating a unique specialized phenotype. Subsequently, it was demonstrated in mice that opposite differentiation towards osteogenic and adipogenic pathways was also possible. Even though the pool of SCs is accepted as the major, and possibly the only, source of myonuclei in postnatal muscle, it is likely that SCs are not all multipotent stem cells and evidences for diversities within the myogenic compartment have been described both in vitro and in vivo. Here, by isolating single fibers from rat flexor digitorum brevis (FDB) muscle we were able to identify and clonally characterize two main subpopulations of SCs: the low proliferative clones (LPC) present in major proportion (approximately 75%) and the high proliferative clones (HPC), present instead in minor amount (approximately 25%). LPC spontaneously generate myotubes whilst HPC differentiate into adipocytes even though they may skip the adipogenic program if co-cultured with LPC. LPC and HPC differ also for mitochondrial membrane potential (DeltaPsi(m)), ATP balance and Reactive Oxygen Species (ROS) generation underlying diversities in metabolism that precede differentiation. Notably, SCs heterogeneity is retained in vivo. SCs may therefore be comprised of two distinct, though not irreversibly committed, populations of cells distinguishable for prominent differences in basal biological features such as proliferation, metabolism and differentiation. By these means, novel insights on SCs heterogeneity are provided and evidences for biological readouts potentially relevant for diagnostic purposes described

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Accepted/In Press date: 26 November 2009
Published date: 1 January 2010
Organisations: Faculty of Medicine

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Local EPrints ID: 382946
URI: http://eprints.soton.ac.uk/id/eprint/382946
ISSN: 1932-6203
PURE UUID: edf58c1f-dbda-4049-aa39-4984a2472002
ORCID for Annalisa Gastaldello: ORCID iD orcid.org/0000-0002-4365-1191

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Date deposited: 09 Nov 2015 08:48
Last modified: 17 Dec 2019 01:33

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Contributors

Author: Carlo A. Rossi
Author: Michela Pozzobon
Author: Andrea Ditadi
Author: Karolina Archacka
Author: Annalisa Gastaldello ORCID iD
Author: Marta Sanna
Author: Chiara Franzin
Author: Alberto Malerba
Author: Gabriella Milan
Author: Mara Cananzi
Author: Stefano Schiaffino
Author: Michelangelo Campanella
Author: Roberto Vettor
Author: Paolo De Coppi

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