Transcriptome and epigenome diversity and plasticity of muscle stem cells following transplantation

Autoři: Brendan Evano aff001;  Diljeet Gill aff003;  Irene Hernando-Herraez aff003;  Glenda Comai aff001;  Thomas M. Stubbs aff003;  Pierre-Henri Commere aff004;  Wolf Reik aff003;  Shahragim Tajbakhsh aff001
Působiště autorů: Stem Cells & Development, Department of Developmental & Stem Cell Biology, Institut Pasteur, 25 rue du Dr. Roux, Paris, France aff001;  CNRS UMR 3738, Institut Pasteur, Paris, France aff002;  Epigenetics Programme, Babraham Institute, Cambridge, United Kingdom aff003;  Cytometry and Biomarkers, Center for Technological Resources and Research, Institut Pasteur, 28 rue du Dr. Roux, Paris, France aff004
Vyšlo v časopise: Transcriptome and epigenome diversity and plasticity of muscle stem cells following transplantation. PLoS Genet 16(10): e32767. doi:10.1371/journal.pgen.1009022
Kategorie: Research Article


Adult skeletal muscles are maintained during homeostasis and regenerated upon injury by muscle stem cells (MuSCs). A heterogeneity in self-renewal, differentiation and regeneration properties has been reported for MuSCs based on their anatomical location. Although MuSCs derived from extraocular muscles (EOM) have a higher regenerative capacity than those derived from limb muscles, the molecular determinants that govern these differences remain undefined. Here we show that EOM and limb MuSCs have distinct DNA methylation signatures associated with enhancers of location-specific genes, and that the EOM transcriptome is reprogrammed following transplantation into a limb muscle environment. Notably, EOM MuSCs expressed host-site specific positional Hox codes after engraftment and self-renewal within the host muscle. However, about 10% of EOM-specific genes showed engraftment-resistant expression, pointing to cell-intrinsic molecular determinants of the higher engraftment potential of EOM MuSCs. Our results underscore the molecular diversity of distinct MuSC populations and molecularly define their plasticity in response to microenvironmental cues. These findings provide insights into strategies designed to improve the functional capacity of MuSCs in the context of regenerative medicine.

Klíčová slova:

Body limbs – DNA methylation – Gene expression – Muscle biochemistry – Muscle differentiation – Muscle regeneration – principal component analysis – Transcriptome analysis


1. von Maltzahn J, Jones AE, Parks RJ, Rudnicki MA. Pax7 is critical for the normal function of satellite cells in adult skeletal muscle. Proc Natl Acad Sci. 2013;110:16474–16479. doi: 10.1073/pnas.1307680110 24065826

2. Sambasivan R, Yao R, Kissenpfennig A, Van Wittenberghe L, Paldi A, Gayraud-Morel B et al. Pax7-expressing satellite cells are indispensable for adult skeletal muscle regeneration. Development. 2011;138:3647–3656. doi: 10.1242/dev.067587 21828093

3. Lepper C, Partridge TA, Fan C-M. An absolute requirement for Pax7-positive satellite cells in acute injury-induced skeletal muscle regeneration. Development. 2011;138:3639–3646. doi: 10.1242/dev.067595 21828092

4. 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;16:557–565. doi: 10.1007/BF01233096 2267630

5. Blau HM, Webster C, Pavlath GK. Defective myoblasts identified in Duchenne muscular dystrophy. Proc Natl Acad Sci U S A. 1983;80:4856–4860. doi: 10.1073/pnas.80.15.4856 6576361

6. Chakkalakal JV, Jones KM, Basson MA, Brack AS. The aged niche disrupts muscle stem cell quiescence. Nature. 2012;490:355–360. doi: 10.1038/nature11438 23023126

7. Bernet JD, Olwin BB. P38 MAPK signaling underlies a cell autonomous loss of stem cell self-renewal in aged skeletal muscle. Nat Med. 2015;2:265–271. doi: 10.1038/nm.3465 24531379

8. Sousa-Victor P, Gutarra S, García-Prat L, Rodriguez-Ubreva J, Ortet L, Ruiz-Bonilla V et al. Geriatric muscle stem cells switch reversible quiescence into senescence. Nature. 2014;506:316–321. doi: 10.1038/nature13013 24522534

9. Cosgrove BD, Gilbert PM, Porpiglia E, Mourkioti F, Lee SP, Corbel SY et al. Rejuvenation of the aged muscle stem cell population restores strength to injured aged muscles. Nat Med. 2014;20:255–264. doi: 10.1038/nm.3464 24531378

10. Price FD, Von Maltzahn J, Bentzinger CF, Nicolas A, Yin H, Chang NC et al. Inhibition of JAK/STAT signaling stimulates adult satellite cell function. Nat Med. 2015;20:1174–1181. doi: 10.1038/nm.3655 25194569

11. Tierney MT, Sacco A. STAT3 signaling controls satellite cell expansion and skeletal muscle repair. Nat Med. 2012;76:211–220. doi: 10.1038/nm.3656 25194572

12. Evans WJ, Campbell WW. Sarcopenia and age-related changes in body composition and functional capacity. J Nutr. 1993;123:465–468. doi: 10.1093/jn/123.suppl_2.465 8429405

13. Brack AS, Muñoz-Cánoves P. The ins and outs of muscle stem cell aging. Skelet Muscle. 2016;6:1–9. doi: 10.1186/s13395-016-0072-z 26783424

14. Jang YC, Sinha M, Cerletti M, Dall’Osso C, Wagers AJ. Skeletal Muscle Stem Cells: Effects of Aging and Metabolism on Muscle Regenerative Function. Cold Spring Harb Symp Quant Biol. 2011;76:101–111. doi: 10.1101/sqb.2011.76.010652 21960527

15. Renault V, Thornell L-E, Eriksson P-O, Butler-Browne G, Mouly V, Thorne L-E. Regenerative potential of human skeletal muscle during aging. Aging Cell. 2002;1:132–139. doi: 10.1046/j.1474-9728.2002.00017.x 12882343

16. Montarras D, Morgan J, Collins C, Relaix F, Zaffran S, Cumano A et al. Direct Isolation of Satellite Cells for Skeletal Muscle Regeneration. Science. 2005;309:2064–2067. doi: 10.1126/science.1114758 16141372

17. 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;16:810–821. doi: 10.1016/j.devcel.2009.05.008 19531352

18. Tajbakhsh S, Rocancourt D, Cossu G, Buckingham M. Redefining the genetic hierarchies controlling skeletal myogenesis: Pax-3 and Myf-5 act upstream of MyoD. Cell. 1997;89:127–138. doi: 10.1016/s0092-8674(00)80189-0 9094721

19. Relaix F, Rocancourt D, Mansouri A, Buckingham M. A Pax3/Pax7-dependent population of skeletal muscle progenitor cells. Nature. 2005;435:948–953. doi: 10.1038/nature03594 15843801

20. Kassar-Duchossoy L, Giacone E, Gayraud-Morel B, Jory A, Gomès D, Tajbakhsh S. Pax3/Pax7 mark a novel population of primitive myogenic cells during development. Genes Dev. 2005;19:1426–1431. doi: 10.1101/gad.345505 15964993

21. Noden DM, Francis-West P. The differentiation and morphogenesis of craniofacial muscles. Dev Dyn. 2006;235:1194–1218. doi: 10.1002/dvdy.20697 16502415

22. Couly GF, Coltey PM, Le Douarin NM. The developmental fate of the cephalic mesoderm in quail-chick chimeras. Development. 1992;114:1–15. 1576952

23. Diogo R, Kelly RG, Christiaen L, Levine M, Ziermann JM, Molnar JL et al. A new heart for a new head in vertebrate cardiopharyngeal evolution. Nature. 2015;520:466–473. doi: 10.1038/nature14435 25903628

24. Kelly RG, Jerome-Majewska LA, Papaioannou VE. The del22q11.2 candidate gene Tbx1 regulates branchiomeric myogenesis. Hum Mol Genet. 2004;13:2829–2840. doi: 10.1093/hmg/ddh304 15385444

25. Nathan E, Monovich A, Tirosh-Finkel L, Harrelson Z, Rousso T, Rinon A et al. The contribution of Islet1-expressing splanchnic mesoderm cells to distinct branchiomeric muscles reveals significant heterogeneity in head muscle development. Development. 2008;135:647–657. doi: 10.1242/dev.007989 18184728

26. Saga Y, Hata N, Kobayashi S, Magnuson T, Seldin MF, Taketo MM. MesP1: a novel basic helix-loop-helix protein expressed in the nascent mesodermal cells during mouse gastrulation. Development. 1996;122:2769–78. 8787751

27. Gage PJ, Suh H, Camper SA. Dosage requirement of Pitx2 for development of multiple organs. Development. 1999;126:4643–4651. 10498698

28. Harel I, Nathan E, Tirosh-Finkel L, Zigdon H, Guimarães-Camboa N, Evans SM et al. Distinct Origins and Genetic Programs of Head Muscle Satellite Cells. Dev Cell. 2009;16:822–832. doi: 10.1016/j.devcel.2009.05.007 19531353

29. Gage PJ, Rhoades W, Prucka SK, Hjalt T. Fate maps of neural crest and mesoderm in the mammalian eye. Investig Ophthalmol Vis Sci. 2005;46:4200–4208. doi: 10.1167/iovs.05-0691 16249499

30. Comai G, Tajbakhsh S. Molecular and Cellular Regulation of Skeletal Myogenesis. Current topics in developmental biology. 2014. p. 1–73. doi: 10.1016/B978-0-12-405943-6.00001-4 25248473

31. Zammit PS, Golding JP, Nagata Y, Hudon V, Partridge TA, Beauchamp JR. Muscle satellite cells adopt divergent fates. J Cell Biol. 2004;166:347–357. doi: 10.1083/jcb.200312007 15277541

32. Olguin HC, Olwin BB. Pax-7 up-regulation inhibits myogenesis and cell cycle progression in satellite cells: a potential mechanism for self-renewal. Dev Biol. 2004;275:375–388. doi: 10.1016/j.ydbio.2004.08.015 15501225

33. Conboy IM, Rando TA. The regulation of Notch signaling controls satellite cell activation and cell fate determination in postnatal myogenesis. Dev Cell. 2002;3:397–409. doi: 10.1016/s1534-5807(02)00254-x 12361602

34. Brack AS, Rando TA. Tissue-specific stem cells: lessons from the skeletal muscle satellite cell. Cell Stem Cell. 2012;10:504–514. doi: 10.1016/j.stem.2012.04.001 22560074

35. Kaminski HJ, Al-Hakim M, Leigh RJ, Bashar MK, Ruff RL. Extraocular muscles are spared in advanced duchenne dystrophy. Ann Neurol. 1992;32:586–588. doi: 10.1002/ana.410320418 1456746

36. Schoser BGH, Pongratz D. Extraocular Mitochondrial Myopathies and their Differential Diagnoses. Strabismus. 2006;14:107–113. doi: 10.1080/09273970600701218 16760117

37. Porter JD, Rafael JA, Ragusa RJ, Brueckner JK, Trickett JI, Davies KE. The sparing of extraocular muscle in dystrophinopathy is lost in mice lacking utrophin and dystrophin. J Cell Sci 1998;111(Pt 1): 1801–11. 9625743

38. Emery AE. The muscular dystrophies. Lancet. 2002;359:687–695. doi: 10.1016/S0140-6736(02)07815-7 11879882

39. Stuelsatz P, Shearer A, Li Y, Muir LA, Ieronimakis N, Shen QW et al. Extraocular muscle satellite cells are high performance myo-engines retaining efficient regenerative capacity in dystrophin deficiency. Dev Biol. 2015;397:31–44. doi: 10.1016/j.ydbio.2014.08.035 25236433

40. Ryall JG, Dell’Orso S, Derfoul A, Juan A, Zare H, Feng X et al. The NAD+-dependent sirt1 deacetylase translates a metabolic switch into regulatory epigenetics in skeletal muscle stem cells. Cell Stem Cell. 2015;16:171–183. doi: 10.1016/j.stem.2014.12.004 25600643

41. Pallafacchina G, François S, Regnault B, Czarny B, Dive V, Cumano A et al. An adult tissue-specific stem cell in its niche: A gene profiling analysis of in vivo quiescent and activated muscle satellite cells. Stem Cell Res. 2010;4:77–91. doi: 10.1016/j.scr.2009.10.003 19962952

42. Liu L, Cheung TH, Charville GW, Hurgo BMC, Leavitt T, Shih J et al. Chromatin modifications as determinants of muscle stem cell quiescence and chronological aging. Cell Rep. 2013;4:189–204. doi: 10.1016/j.celrep.2013.05.043 23810552

43. Tsumagari K, Baribault C, Terragni J, Varley KE, Gertz J, Pradhan S et al. Early de novo DNA methylation and prolonged demethylation in the muscle lineage. Epigenetics. 2013;8:317–332. doi: 10.4161/epi.23989 23417056

44. Carrió E, Díez-Villanueva A, Lois S, Mallona I, Cases I, Forn M et al. Deconstruction of DNA methylation patterns during myogenesis reveals specific epigenetic events in the establishment of the skeletal muscle lineage. Stem Cells. 2015;33:2025–2036. doi: 10.1002/stem.1998 25801824

45. Miyata K, Miyata T, Nakabayashi K, Okamura K, Naito M, Kawai T et al. DNA methylation analysis of human myoblasts during in vitro myogenic differentiation: De novo methylation of promoters of muscle-related genes and its involvement in transcriptional down-regulation. Hum Mol Genet. 2015;24:410–423. doi: 10.1093/hmg/ddu457 25190712

46. Hernando-Herraez I, Evano B, Stubbs T, Commere PH, Jan Bonder M, Clark S et al. Ageing affects DNA methylation drift and transcriptional cell-to-cell variability in mouse muscle stem cells. Nat Commun. 2019;10:1–11. doi: 10.1038/s41467-018-07882-8 30602773

47. Macaulay IC, Teng MJ, Haerty W, Kumar P, Ponting CP, Voet T. Separation and parallel sequencing of the genomes and transcriptomes of single cells using G&T-seq. Nat Protoc. 2016;11:2081–2103. doi: 10.1038/nprot.2016.138 27685099

48. Clark SJ, Smallwood SA, Lee HJ, Krueger F, Reik W, Kelsey G. Genome-wide base-resolution mapping of DNA methylation in single cells using single-cell bisulfite sequencing (scBS-seq). Nat Protoc. 2017;12:534–547. doi: 10.1038/nprot.2016.187 28182018

49. Relaix F, Montarras D, Zaffran S, Gayraud-Morel B, Rocancourt D, Tajbakhsh S et al. Pax3 and Pax7 have distinct and overlapping functions in adult muscle progenitor cells. J Cell Biol. 2006;172:91–102. doi: 10.1083/jcb.200508044 16380438

50. Gross MK, Moran-Rivard L, Velasquez T, Nakatsu MN, Jagla K, Goulding M. Lbx1 is required for muscle precursor migration along a lateral pathway into the limb. Development. 2000;127:413–424. 10603357

51. Brohmann H, Jagla K, Birchmeier C. The role of Lbx1 in migration of muscle precursor cells. Development. 2000;127:437–445. 10603359

52. Kelly RG, Jerome-Majewska LA, Papaioannou VE. The del22q11.2 candidate gene Tbx1 regulates branchiometric myogenesis. Hum Mol Genet. 2004;13:2829–2840. doi: 10.1093/hmg/ddh304 15385444

53. Biressi S, Rando TA. Heterogeneity in the muscle satellite cell population. Seminars in Cell and Developmental Biology. Elsevier Ltd; 2010. p. 845–854. doi: 10.1016/j.semcdb.2010.09.003 20849971

54. Doucet-Beaupré H, Ang SL, Lévesque M. Cell fate determination, neuronal maintenance and disease state: The emerging role of transcription factors Lmx1a and Lmx1b. FEBS Letters. Elsevier; 2015. p. 3727–3738. doi: 10.1016/j.febslet.2015.10.020 26526610

55. Montague P, McCallion AS, Davies RW, Griffiths IR. Myelin-associated oligodendrocytic basic protein: A family of abundant CNS myelin proteins in search of a function. Developmental Neuroscience. 2006. p. 479–487. doi: 10.1159/000095110 17028425

56. Mallo M, Wellik DM, Deschamps J. Hox genes and regional patterning of the vertebrate body plan. Developmental Biology. Academic Press Inc.; 2010. p. 7–15. doi: 10.1016/j.ydbio.2010.04.024 20435029

57. Pearson JC, Lemons D, McGinnis W. Modulating Hox gene functions during animal body patterning. Nature Reviews Genetics. 2005. p. 893–904. doi: 10.1038/nrg1726 16341070

58. Machado L. Esteves de Lima J, Fabre O, Proux C, Legendre R, Szegedi A, et al. In situ fixation redefines quiescence and early activation of skeletal muscle stem cells. Cell Rep. 2017;21:1982–1993. doi: 10.1016/j.celrep.2017.10.080 29141227

59. Mazurier F, Fontanellas A, Salesse S, Taine L, Landriau S, Moreau-Gaudry F et al. A Novel Immunodeficient Mouse Model-RAG2 gamma Cytokine Receptor Chain Double Mutants-Requiring Exogenous Cytokine Administration for Human Hematopoietic Stem Cell Engraftment Common. J Interf Cytokine Res. 1999;19:533–541. doi: 10.1089/107999099313983 10386866

60. Hardy D, Besnard A, Latil M, Jouvion G, Briand D, Thépenier C et al. Comparative Study of Injury Models for Studying Muscle Regeneration in Mice. PLoS One. 2016;11:e0147198. doi: 10.1371/journal.pone.0147198 26807982

61. De Micheli AJ, Laurilliard EJ, Heinke CL, Ravichandran H, Fraczek P, Soueid-Baumgarten S et al. Single-Cell Analysis of the Muscle Stem Cell Hierarchy Identifies Heterotypic Communication Signals Involved in Skeletal Muscle Regeneration. Cell Rep. 2020;30:3583 –3595.e5. doi: 10.1016/j.celrep.2020.02.067 32160558

62. Itasaki N, Sharpe J, Morrison A, Krumlauf R. Reprogramming Hox expression in the vertebrate hindbrain: influence of paraxial mesoderm and rhombomere transposition. Neuron. 1996;16:487–500. doi: 10.1016/s0896-6273(00)80069-0 8785047

63. Leucht P, Kim JB, Amasha R, James AW, Girod S, Helms JA. Embryonic origin and Hox status determine progenitor cell fate during adult bone regeneration. Development. 2008;135:2845–2854. doi: 10.1242/dev.023788 18653558

64. Zakany J, Duboule D. The role of Hox genes during vertebrate limb development. Current Opinion in Genetics and Development. 2007. p. 359–366. doi: 10.1016/j.gde.2007.05.011 17644373

65. Motohashi N, Uezumi A, Asakura A, Ikemoto-Uezumi M, Mori S, Mizunoe Y et al. Tbx1 regulates inherited metabolic and myogenic abilities of progenitor cells derived from slow- and fast-type muscle. Cell Death Differ. 2019;26:1024–1036. doi: 10.1038/s41418-018-0186-4 30154444

66. Brunk BP, Goldhamer DJ, Emerson CP. Regulated Demethylation of the myoD Distal Enhancer during Skeletal Myogenesis. 1996;503:490–503. doi: 10.1006/dbio.1996.0180 8806826

67. Lucarelli M, Fuso A, Strom R, Scarpa S. The dynamics of myogenin site-specific demethylation is strongly correlated with its expression and with muscle differentiation. J Biol Chem. 2001;276:7500–7506. doi: 10.1074/jbc.M008234200 11096088

68. Allen M, Koch CM, Clelland GK, Dunham I, Antoniou M. DNA methylation-histone modification relationships across the desmin locus in human primary cells. BMC Mol Biol. 2009;10. doi: 10.1186/1471-2199-10-10 19224648

69. Wu W, Ren Z, Liu H, Wang L, Huang R, Chen J et al. Core promoter analysis of porcine Six1 gene and its regulation of the promoter activity by CpG methylation. Gene. 2013;529:238–244. doi: 10.1016/j.gene.2013.07.102 23954877

70. Hu B, Gharaee-Kermani M, Wu Z, Phan SH. Epigenetic regulation of myofibroblast differentiation by DNA methylation. Am J Pathol. 2010;177:21–28. doi: 10.2353/ajpath.2010.090999 20489138

71. Illingworth R, Kerr A, Desousa D, Jørgensen H, Ellis P, Stalker J, et al. A novel CpG island set identifies tissue-specific methylation at developmental gene loci. Liu ET, editor. PLoS Biol. 2008;6:e22. doi: 10.1371/journal.pbio.0060022 18232738

72. Sørensen AL, Timoskainen S, West FD, Vekterud K, Boquest AC, Ährlund-richter L et al. Lineage-specific promoter DNA methylation patterns segregate adult progenitor cell types. Stem Cells Dev. 2010;19:1257–1266. doi: 10.1089/scd.2009.0309 19886822

73. Fernandez AF, Assenov Y, Martin-Subero JI, Balint B, Siebert R, Taniguchi H et al. A DNA methylation fingerprint of 1628 human samples. Genome Res. 2012;22:407–419. doi: 10.1101/gr.119867.110 21613409

74. Calvanese V, Fernández AF, Urdinguio RG, Suárez-Alvarez B, Mangas C, Pérez-García V et al. A promoter DNA demethylation landscape of human hematopoietic differentiation. Nucleic Acids Res. 2012;40:116–131. doi: 10.1093/nar/gkr685 21911366

75. Nazor KL, Altun G, Lynch C, Tran H, Harness JV, Slavin I et al. Recurrent Variations in DNA Methylation in Human Pluripotent Stem Cells and Their Differentiated Derivatives. Cell Stem Cell. 2012;10:620–634. doi: 10.1016/j.stem.2012.02.013 22560082

76. Carrió E, Magli A, Muñoz M, Peinado MA, Perlingeiro R, Suelves M. Muscle cell identity requires Pax7-mediated lineage-specific DNA demethylation. BMC Biol. 2016;14:30. doi: 10.1186/s12915-016-0250-9 27075038

77. Bigot A, Duddy WJ, Ouandaogo ZG, Negroni E, Mariot V, Ghimbovschi S et al. Age-associated methylation suppresses SPRY1, leading to a failure of re-quiescence and loss of the reserve stem cell pool in elderly muscle. Cell Rep. 2015;13:1172–1182. doi: 10.1016/j.celrep.2015.09.067 26526994

78. Lister R, Pelizzola M, Dowen RH, Hawkins RD, Hon G, Tonti-Filippini J et al. Human DNA methylomes at base resolution show widespread epigenomic differences. Nature. 2009;462:315–322. doi: 10.1038/nature08514 19829295

79. Begue G, Raue U, Jemiolo B, Trappe S. DNA methylation assessment from human slow- and fast-twitch skeletal muscle fibers. J Appl Physiol. 2017;122:952–967. doi: 10.1152/japplphysiol.00867.2016 28057818

80. Kaaij LTJ, van de Wetering M, Fang F, Decato B, Molaro A, van de Werken HJG et al. DNA methylation dynamics during intestinal stem cell differentiation reveals enhancers driving gene expression in the villus. Genome Biol. 2013;14. doi: 10.1186/gb-2013-14-5-r50 23714178

81. Challen GA, Sun D, Mayle A, Jeong M, Luo M, Rodriguez B et al. Dnmt3a and Dnmt3b have overlapping and distinct functions in hematopoietic stem cells. Cell Stem Cell. 2014;15:350–364. doi: 10.1016/j.stem.2014.06.018 25130491

82. Kaz AM, Wong CJ, Dzieciatkowski S, Luo Y, Schoen RE, Grady WM. Patterns of DNA methylation in the normal colon vary by anatomical location, gender, and age. Epigenetics. 2014;9:492–502. doi: 10.4161/epi.27650 24413027

83. Wu M, Li X, Zhang C, Zhang C, Qian D, Ma J et al. DNA methylation profile of psoriatic skins from different body locations. Epigenomics. 2019;11:1613–1625. doi: 10.2217/epi-2018-0225 31701765

84. Formicola L, Marazzi G, Sassoon DA. The extraocular muscle stem cell niche is resistant to ageing and disease. Front Aging Neurosci. 2014;6:328. doi: 10.3389/fnagi.2014.00328 25520657

85. Kusner LL, Young A, Tjoe S, Leahy P, Kaminski HJ. Perimysial fibroblasts of Extraocular muscle, as unique as the muscle fibers. Investig Ophthalmol Vis Sci. 2010;51:192–200. doi: 10.1167/iovs.08-2857 19661226

86. Incitti T, Magli A, Darabi R, Yuan C, Lin K, Arpke RW et al. Pluripotent stem cell-derived myogenic progenitors remodel their molecular signature upon in vivo engraftment. Proc Natl Acad Sci U S A. 2019;116:4346–4351. doi: 10.1073/pnas.1808303116 30760602

87. Grapin-Botton A, Bonnin MA, McNaughton LA, Krumlauf R, Le Douarin NM. Plasticity of transposed rhombomeres: Hox gene induction is correlated with phenotypic modifications. Development. 1995;121:2707–21. 7555700

88. Grieshammer U, Sassoon D, Rosenthal N. A transgene target for positional regulators marks early rostrocaudal specification of myogenic lineages. Cell. 1992;69:79–93. doi: 10.1016/0092-8674(92)90120-2 1313337

89. Yoshioka K, Nagahisa H, Miura F, Araki H, Kamei Y, Kitajima Y et al. Hoxa10 mediates positional memory to govern stem cell function in adult skeletal muscle. bioRxiv. 2020. doi: 10.1101/2020.07.16.207654

90. Wang KC, Helms JA, Chang HY. Regeneration, repair and remembering identity: the three Rs of Hox gene expression. Trends in Cell Biology. 2009. p. 268–275. doi: 10.1016/j.tcb.2009.03.007 19428253

91. Vallejo D, Hernández-Torres F, Lozano-Velasco E, Rodriguez-Outeiriño L, Carvajal A, Creus C et al. PITX2 Enhances the Regenerative Potential of Dystrophic Skeletal Muscle Stem Cells. Stem Cell Reports. 2018;10:1398–1411. doi: 10.1016/j.stemcr.2018.03.009 29641992

92. L’Honoré A, Commère PH, Negroni E, Pallafacchina G, Friguet B, Drouin J et al. The role of Pitx2 and Pitx3 in muscle 1 stem cells gives new insights into P38α MAP kinase and redox regulation of muscle regeneration. elife. 2018;7. doi: 10.7554/eLife.32991 30106373

93. Dentice M, Marsili A, Ambrosio R, Guardiola O, Sibilio A, Paik JH et al. The FoxO3/type 2 deiodinase pathway is required for normal mouse myogenesis and muscle regeneration. J Clin Invest. 2010;120:4021–4030. doi: 10.1172/JCI43670 20978344

94. Dentice M, Ambrosio R, Damiano V, Sibilio A, Luongo C, Guardiola O et al. Intracellular inactivation of thyroid hormone is a survival mechanism for muscle stem cell proliferation and lineage progression. Cell Metab. 2014;20:1038–1048. doi: 10.1016/j.cmet.2014.10.009 25456740

95. McLoon L, Thorstenson K, Solomon A, Lewis M. Myogenic precursor cells in craniofacial muscles. Oral Dis. 2007;13:134–140. doi: 10.1111/j.1601-0825.2006.01353.x 17305613

96. Kallestad KM, Hebert SL, McDonald AA, Daniel ML, Cu SR, McLoon LK. Sparing of extraocular muscle in aging and muscular dystrophies: A myogenic precursor cell hypothesis. Exp Cell Res. 2011;317:873–885. doi: 10.1016/j.yexcr.2011.01.018 21277300

97. Gayraud-Morel B, Chrétien F, Flamant P, Gomès D, Zammit PS, Tajbakhsh S. A role for the myogenic determination gene Myf5 in adult regenerative myogenesis. Dev Biol. 2007;312:13–28. doi: 10.1016/j.ydbio.2007.08.059 17961534

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