Tbx1 regulates inherited metabolic and myogenic abilities of progenitor cells derived from slow- and fast-type muscle.
Journal
Cell death and differentiation
ISSN: 1476-5403
Titre abrégé: Cell Death Differ
Pays: England
ID NLM: 9437445
Informations de publication
Date de publication:
06 2019
06 2019
Historique:
received:
25
03
2018
accepted:
27
07
2018
revised:
18
07
2018
pubmed:
30
8
2018
medline:
2
10
2020
entrez:
30
8
2018
Statut:
ppublish
Résumé
Skeletal muscle is divided into slow- and fast-type muscles, which possess distinct contractile and metabolic properties. Myogenic progenitors associated with each muscle fiber type are known to intrinsically commit to specific muscle fiber lineage during embryonic development. However, it is still unclear whether the functionality of postnatal adult myogenic cells is attributable to the muscle fiber in which they reside, and whether the characteristics of myogenic cells derived from slow- and fast-type fibers can be distinguished at the genetic level. In this study, we isolated adult satellite cells from slow- and fast-type muscle individually and observed that satellite cells from each type of muscle generated myotubes expressing myosin heavy chain isoforms similar to their original muscle, and showed different metabolic features. Notably, we discovered that slow muscle-derived cells had low potential to differentiate but high potential to self-renew compared with fast muscle-derived cells. Additionally, cell transplantation experiments of slow muscle-derived cells into fast-type muscle revealed that slow muscle-derived cells could better contribute to myofiber formation and satellite cell constitution than fast muscle-derived cells, suggesting that the recipient muscle fiber type may not affect the predetermined abilities of myogenic cells. Gene expression analyses identified T-box transcriptional factor Tbx1 as a highly expressed gene in fast muscle-derived myoblasts. Gain- and loss-of-function experiments revealed that Tbx1 modulated muscle fiber types and oxidative metabolism in myotubes, and that Tbx1 stimulated myoblast differentiation, but did not regulate myogenic cell self-renewal. Our data suggest that metabolic and myogenic properties of myogenic progenitor cells vary depending on the type of muscle from which they originate, and that Tbx1 expression partially explains the functional differences of myogenic cells derived from fast-type and slow-type muscles.
Identifiants
pubmed: 30154444
doi: 10.1038/s41418-018-0186-4
pii: 10.1038/s41418-018-0186-4
pmc: PMC6748120
doi:
Substances chimiques
T-Box Domain Proteins
0
Tbx1 protein, mouse
0
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1024-1036Subventions
Organisme : NIAMS NIH HHS
ID : R01 AR062142
Pays : United States
Références
Mauro A. Satellite cell of skeletal muscle fibers. J Biophys Biochem Cytol. 1961;9:493–5.
pubmed: 13768451
pmcid: 2225012
doi: 10.1083/jcb.9.2.493
Charge SB, Rudnicki MA. Cellular and molecular regulation of muscle regeneration. Physiol Rev. 2004;84:209–38.
pubmed: 14715915
doi: 10.1152/physrev.00019.2003
Collins CA, Olsen I, Zammit PS, Heslop L, Petrie A, Partridge TA, et al. Stem cell function, self-renewal, and behavioral heterogeneity of cells from the adult muscle satellite cell niche. Cell. 2005;122:289–301.
pubmed: 16051152
doi: 10.1016/j.cell.2005.05.010
Day K, Shefer G, Shearer A, Yablonka-Reuveni Z. The depletion of skeletal muscle satellite cells with age is concomitant with reduced capacity of single progenitors to produce reserve progeny. Dev Biol. 2010;340:330–43.
pubmed: 20079729
pmcid: 2854302
doi: 10.1016/j.ydbio.2010.01.006
Verdijk LB, Snijders T, Drost M, Delhaas T, Kadi F, van Loon LJ. Satellite cells in human skeletal muscle; from birth to old age. Age (Dordr). 2013;36:545–7.
doi: 10.1007/s11357-013-9583-2
Webster C, Blau HM. Accelerated age-related decline in replicative life-span of Duchenne muscular dystrophy myoblasts: implications for cell and gene therapy. Somat Cell Mol Genet. 1990;16:557–65.
pubmed: 2267630
doi: 10.1007/BF01233096
Shefer G, Van de Mark DP, Richardson JB, Yablonka-Reuveni Z. Satellite-cell pool size does matter: defining the myogenic potency of aging skeletal muscle. Dev Biol. 2006;294:50–66.
pubmed: 16554047
pmcid: 2710453
doi: 10.1016/j.ydbio.2006.02.022
Bernet JD, Doles JD, Hall JK, Kelly-Tanaka K, Carter TA, Olwin BB. p38 MAPK signaling underlies a cell-autonomous loss of stem cell self-renewal in skeletal muscle of aged mice. Nat Med. 2014;20:265–71.
pubmed: 24531379
pmcid: 4070883
doi: 10.1038/nm.3465
Cosgrove BD, Gilbert PM, Porpiglia E, Mourkioti F, Lee SP, Corbel SY, et al. Rejuvenation of the muscle stem cell population restores strength to injured aged muscles. Nat Med. 2014;20:255–64.
pubmed: 24531378
pmcid: 3949152
doi: 10.1038/nm.3464
Ono Y, Boldrin L, Knopp P, Morgan JE, Zammit PS. Muscle satellite cells are a functionally heterogeneous population in both somite-derived and branchiomeric muscles. Dev Biol. 2010;337:29–41.
pubmed: 19835858
pmcid: 2806517
doi: 10.1016/j.ydbio.2009.10.005
Rosenblatt JD, Lunt AI, Parry DJ, Partridge TA. Culturing satellite cells from living single muscle fiber explants. In Vitro Cell Dev Biol Anim. 1995;31:773–9.
pubmed: 8564066
doi: 10.1007/BF02634119
Lagord C, Soulet L, Bonavaud S, Bassaglia Y, Rey C, Barlovatz-Meimon G, et al. Differential myogenicity of satellite cells isolated from extensor digitorum longus (EDL) and soleus rat muscles revealed in vitro. Cell Tissue Res. 1998;291:455–68.
pubmed: 9477302
doi: 10.1007/s004410051015
Hughes SM, Blau HM. Muscle fiber pattern is independent of cell lineage in postnatal rodent development. Cell. 1992;68:659–71.
pubmed: 1531450
doi: 10.1016/0092-8674(92)90142-Y
Lexell J, Jarvis JC, Currie J, Downham DY, Salmons S. Fibre type composition of rabbit tibialis anterior and extensor digitorum longus muscles. J Anat. 1994;185:95–101.
pubmed: 7559119
pmcid: 1166818
Schiaffino S, Reggiani C. Fiber types in mammalian skeletal muscles. Physiol Rev. 2011;91:1447–531.
pubmed: 22013216
doi: 10.1152/physrev.00031.2010
Nicholls DG, Darley-Usmar VM, Wu M, Jensen PB, Rogers GW, Ferrick DA. Bioenergetic profile experiment using C2C12 myoblast cells. J Vis Exp. 2010;46:2511.
Bockman EL, McKenzie JE. Tissue adenosine content in active soleus and gracilis muscles of cats. Am J Physiol. 1983;244:H552–9.
pubmed: 6301292
Kushmerick MJ, Meyer RA, Brown TR. Regulation of oxygen consumption in fast- and slow-twitch muscle. Am J Physiol. 1992;263:C598–606.
pubmed: 1415510
doi: 10.1152/ajpcell.1992.263.3.C598
Wu Z, Puigserver P, Andersson U, Zhang C, Adelmant G, Mootha V, et al. Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell. 1999;98:115–24.
pubmed: 10412986
doi: 10.1016/S0092-8674(00)80611-X
Lin J, Wu H, Tarr PT, Zhang CY, Wu Z, Boss O, et al. Transcriptional co-activator PGC-1 alpha drives the formation of slow-twitch muscle fibres. Nature. 2002;418:797–801.
pubmed: 12181572
doi: 10.1038/nature00904
Baroffio A, Bochaton-Piallat ML, Gabbiani G, Bader CR. Heterogeneity in the progeny of single human muscle satellite cells. Differentiation. 1995;59:259–68.
pubmed: 8575648
doi: 10.1046/j.1432-0436.1995.5940259.x
Yoshida N, Yoshida S, Koishi K, Masuda K, Nabeshima Y. Cell heterogeneity upon myogenic differentiation: down-regulation of MyoD and Myf-5 generates ‘reserve cells’. J Cell Sci. 1998;111:769–79.
pubmed: 9472005
doi: 10.1242/jcs.111.6.769
Zammit PS, Golding JP, Nagata Y, Hudon V, Partridge TA, Beauchamp JR. Muscle satellite cells adopt divergent fates: a mechanism for self-renewal? J Cell Biol. 2004;166:347–57.
pubmed: 15277541
pmcid: 2172269
doi: 10.1083/jcb.200312007
Gayraud-Morel B, Chretien F, Jory A, Sambasivan R, Negroni E, Flamant P, et al. Myf5 haploinsufficiency reveals distinct cell fate potentials for adult skeletal muscle stem cells. J Cell Sci. 2012;125:1738–49.
pubmed: 22366456
doi: 10.1242/jcs.128678
Bassaglia Y, Gautron J. Fast and slow rat muscles degenerate and regenerate differently after whole crush injury. J Muscle Res Cell Motil. 1995;16:420–9.
pubmed: 7499482
doi: 10.1007/BF00114507
Rosenblatt JD, Parry DJ, Partridge TA. Phenotype of adult mouse muscle myoblasts reflects their fiber type of origin. Differentiation. 1996;60:39–45.
pubmed: 8935927
doi: 10.1046/j.1432-0436.1996.6010039.x
Salmons S. Exercise, stimulation and type transformation of skeletal muscle. Int J Sports Med. 1994;15:136–41.
pubmed: 8005726
doi: 10.1055/s-2007-1021035
Gambke B, Lyons GE, Haselgrove J, Kelly AM, Rubinstein NA. Thyroidal and neural control of myosin transitions during development of rat fast and slow muscles. FEBS Lett. 1983;156:335–9.
pubmed: 6852266
doi: 10.1016/0014-5793(83)80524-9
Larsson L, Biral D, Campione M, Schiaffino S. An age-related type IIB to IIX myosin heavy chain switching in rat skeletal muscle. Acta Physiol Scand. 1993;147:227–34.
pubmed: 8475750
doi: 10.1111/j.1748-1716.1993.tb09493.x
Holloszy JO, Chen M, Cartee GD, Young JC. Skeletal muscle atrophy in old rats: differential changes in the three fiber types. Mech Ageing Dev. 1991;60:199–213.
pubmed: 1745075
doi: 10.1016/0047-6374(91)90131-I
Lexell J. Human aging, muscle mass, and fiber type composition. J Gerontol A Biol Sci Med Sci. 1995;50:11–6.
pubmed: 7493202
Ciciliot S, Rossi AC, Dyar KA, Blaauw B, Schiaffino S. Muscle type and fiber type specificity in muscle wasting. Int J Biochem Cell Biol. 2013;45:2191–9.
pubmed: 23702032
doi: 10.1016/j.biocel.2013.05.016
Launay T, Noirez P, Butler-Browne G, Agbulut O. Expression of slow myosin heavy chain during muscle regeneration is not always dependent on muscle innervation and calcineurin phosphatase activity. Am J Physiol Regul Integr Comp Physiol. 2006;290:R1508–14.
pubmed: 16424085
doi: 10.1152/ajpregu.00486.2005
Chakkalakal JV, Jones KM, Basson MA, Brack AS. The aged niche disrupts muscle stem cell quiescence. Nature. 2012;490:355–60.
pubmed: 23023126
pmcid: 3605795
doi: 10.1038/nature11438
Motohashi N, Asakura A. Muscle satellite cell heterogeneity and self-renewal. Front Cell Dev Biol. 2014;2:1.
pubmed: 25364710
pmcid: 4206996
doi: 10.3389/fcell.2014.00001
Scambler PJ. The 22q11 deletion syndromes. Hum Mol Genet. 2000;9:2421–6.
pubmed: 11005797
doi: 10.1093/hmg/9.16.2421
Lindsay EA, Vitelli F, Su H, Morishima M, Huynh T, Pramparo T, et al. Tbx1 haploinsufficieny in the DiGeorge syndrome region causes aortic arch defects in mice. Nature. 2001;410:97–101.
pubmed: 11242049
doi: 10.1038/35065105
Yagi H, Furutani Y, Hamada H, Sasaki T, Asakawa S, Minoshima S, et al. Role of TBX1 in human del22q11.2 syndrome. Lancet. 2003;362:1366–73.
pubmed: 14585638
doi: 10.1016/S0140-6736(03)14632-6
Chieffo C, Garvey N, Gong W, Roe B, Zhang G, Silver L, et al. Isolation and characterization of a gene from the DiGeorge chromosomal region homologous to the mouse Tbx1 gene. Genomics. 1997;43:267–77.
pubmed: 9268629
doi: 10.1006/geno.1997.4829
de Wilde J, Hulshof MF, Boekschoten MV, de Groot P, Smit E, Mariman EC. The embryonic genes Dkk3, Hoxd8, Hoxd9 and Tbx1 identify muscle types in a diet-independent and fiber-type unrelated way. BMC Genomics. 2010;11:176.
pubmed: 20230627
pmcid: 2847971
doi: 10.1186/1471-2164-11-176
Chemello F, Bean C, Cancellara P, Laveder P, Reggiani C, Lanfranchi G. Microgenomic analysis in skeletal muscle: expression signatures of individual fast and slow myofibers. PLoS ONE. 2011;6:e16807.
pubmed: 21364935
pmcid: 3043066
doi: 10.1371/journal.pone.0016807
Wu J, Bostrom P, Sparks LM, Ye L, Choi JH, Giang AH, et al. Beige adipocytes are a distinct type of thermogenic fat cell in mouse and human. Cell. 2012;150:366–76.
pubmed: 22796012
pmcid: 3402601
doi: 10.1016/j.cell.2012.05.016
Lee KY, Singh MK, Ussar S, Wetzel P, Hirshman MF, Goodyear LJ, et al. Tbx15 controls skeletal muscle fibre-type determination and muscle metabolism. Nat Commun. 2015;6:8054.
pubmed: 26299309
doi: 10.1038/ncomms9054
Scarpulla RC. Transcriptional paradigms in mammalian mitochondrial biogenesis and function. Physiol Rev. 2008;88:611–38.
pubmed: 18391175
doi: 10.1152/physrev.00025.2007
Kim HS, Xiao C, Wang RH, Lahusen T, Xu X, Vassilopoulos A, et al. Hepatic-specific disruption of SIRT6 in mice results in fatty liver formation due to enhanced glycolysis and triglyceride synthesis. Cell Metab. 2010;12:224–36.
pubmed: 20816089
pmcid: 2935915
doi: 10.1016/j.cmet.2010.06.009
Baar K, Song Z, Semenkovich CF, Jones TE, Han DH, Nolte LA, et al. Skeletal muscle overexpression of nuclear respiratory factor 1 increases glucose transport capacity. FASEB J. 2003;17:1666–73.
pubmed: 12958173
doi: 10.1096/fj.03-0049com
Kelly RG, Jerome-Majewska LA, Papaioannou VE. The del22q11.2 candidate gene Tbx1 regulates branchiomeric myogenesis. Hum Mol Genet. 2004;13:2829–40.
pubmed: 15385444
doi: 10.1093/hmg/ddh304
Jerome LA, Papaioannou VE. DiGeorge syndrome phenotype in mice mutant for the T-box gene, Tbx1. Nat Genet. 2001;27:286–91.
pubmed: 11242110
doi: 10.1038/85845
Sambasivan R, Gayraud-Morel B, Dumas G, Cimper C, Paisant S, Kelly RG, et al. Distinct regulatory cascades govern extraocular and pharyngeal arch muscle progenitor cell fates. Dev Cell. 2009;16:810–21.
pubmed: 19531352
doi: 10.1016/j.devcel.2009.05.008
Oustanina S, Hause G, Braun T. Pax7 directs postnatal renewal and propagation of myogenic satellite cells but not their specification. EMBO J. 2004;23:3430–9.
pubmed: 15282552
pmcid: 514519
doi: 10.1038/sj.emboj.7600346
Kuang S, Charge SB, Seale P, Huh M, Rudnicki MA. Distinct roles for Pax7 and Pax3 in adult regenerative myogenesis. J Cell Biol. 2006;172:103–13.
pubmed: 16391000
pmcid: 2063538
doi: 10.1083/jcb.200508001
Rocheteau P, Gayraud-Morel B, Siegl-Cachedenier I, Blasco MA, Tajbakhsh S. A subpopulation of adult skeletal muscle stem cells retains all template DNA strands after cell division. Cell. 2012;148:112–25.
pubmed: 22265406
doi: 10.1016/j.cell.2011.11.049
Yamamoto M, Legendre NP, Biswas AA, Lawton A, Yamamoto S, Tajbakhsh S, et al. Loss of MyoD and Myf5 in skeletal muscle stem cells results in altered myogenic programming and failed regeneration. Stem Cell Rep. 2018;10:956–69.
doi: 10.1016/j.stemcr.2018.01.027
Fulcoli FG, Huynh T, Scambler PJ, Baldini A. Tbx1 regulates the BMP-Smad1 pathway in a transcription independent manner. PLoS ONE. 2009;4:e6049.
pubmed: 19557177
pmcid: 2698216
doi: 10.1371/journal.pone.0006049
Chen L, Fulcoli FG, Tang S, Baldini A. Tbx1 regulates proliferation and differentiation of multipotent heart progenitors. Circ Res. 2009;105:842–51.
pubmed: 19745164
pmcid: 2796444
doi: 10.1161/CIRCRESAHA.109.200295
van Bueren KL, Papangeli I, Rochais F, Pearce K, Roberts C, Calmont A, et al. Hes1 expression is reduced in Tbx1 null cells and is required for the development of structures affected in 22q11 deletion syndrome. Dev Biol. 2010;340:369–80.
pubmed: 20122914
pmcid: 2877781
doi: 10.1016/j.ydbio.2010.01.020
Pane LS, Zhang Z, Ferrentino R, Huynh T, Cutillo L, Baldini A. Tbx1 is a negative modulator of Mef2c. Hum Mol Genet. 2012;21:2485–96.
pubmed: 22367967
pmcid: 3349424
doi: 10.1093/hmg/dds063
Nowotschin S, Liao J, Gage PJ, Epstein JA, Campione M, Morrow BE. Tbx1 affects asymmetric cardiac morphogenesis by regulating Pitx2 in the secondary heart field. Development. 2006;133:1565–73.
pubmed: 16556915
doi: 10.1242/dev.02309
Okabe M, Ikawa M, Kominami K, Nakanishi T, Nishimune Y. ‘Green mice’ as a source of ubiquitous green cells. FEBS Lett. 1997;407:313–9.
pubmed: 9175875
doi: 10.1016/S0014-5793(97)00313-X
Motohashi N, Asakura Y, Asakura A. Isolation, culture, and transplantation of muscle satellite cells. J Vis Exp. 2014. https://doi.org/10.3791/50846.
Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc. 2008;3:1101–8.
pubmed: 18546601
doi: 10.1038/nprot.2008.73