Gene expression profiling of skeletal myogenesis in human embryonic stem cells reveals a potential cascade of transcription factors regulating stages of myogenesis, including quiescent/activated satellite cell-like gene expression
Autoři:
Michael Shelton aff001; Morten Ritso aff002; Jun Liu aff001; Daniel O’Neil aff001; Avetik Kocharyan aff001; Michael A. Rudnicki aff002; William L. Stanford aff001; Ilona S. Skerjanc aff001; Alexandre Blais aff001
Působiště autorů:
Department of Biochemistry, Microbiology, and Immunology, Faculty of Medicine, University of Ottawa, Ottawa, Ontario, Canada
aff001; Sprott Center for Stem Cell Research, Ottawa Hospital Research Institute, Regenerative Medicine Program, Ottawa, Ontario, Canada
aff002; Department of Cellular and Molecular Medicine, Faculty of Medicine, University of Ottawa, Ottawa, Ontario, Canada
aff003; Ottawa Institute of Systems Biology, University of Ottawa, Ottawa, Ontario, Canada
aff004; Department of Medicine, Faculty of Medicine, University of Ottawa, Ottawa, Ontario, Canada
aff005
Vyšlo v časopise:
PLoS ONE 14(9)
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pone.0222946
Souhrn
Human embryonic stem cell (hESC)-derived skeletal muscle progenitors (SMP)—defined as PAX7-expressing cells with myogenic potential—can provide an abundant source of donor material for muscle stem cell therapy. As in vitro myogenesis is decoupled from in vivo timing and 3D-embryo structure, it is important to characterize what stage or type of muscle is modeled in culture. Here, gene expression profiling is analyzed in hESCs over a 50 day skeletal myogenesis protocol and compared to datasets of other hESC-derived skeletal muscle and adult murine satellite cells. Furthermore, day 2 cultures differentiated with high or lower concentrations of CHIR99021, a GSK3A/GSK3B inhibitor, were contrasted. Expression profiling of the 50 day time course identified successively expressed gene subsets involved in mesoderm/paraxial mesoderm induction, somitogenesis, and skeletal muscle commitment/formation which could be regulated by a putative cascade of transcription factors. Initiating differentiation with higher CHIR99021 concentrations significantly increased expression of MSGN1 and TGFB-superfamily genes, notably NODAL, resulting in enhanced paraxial mesoderm and reduced ectoderm/neuronal gene expression. Comparison to adult satellite cells revealed that genes expressed in 50-day cultures correlated better with those expressed by quiescent or early activated satellite cells, which have the greatest therapeutic potential. Day 50 cultures were similar to other hESC-derived skeletal muscle and both expressed known and novel SMP surface proteins. Overall, a putative cascade of transcription factors has been identified which regulates four stages of myogenesis. Subsets of these factors were upregulated by high CHIR99021 or their binding sites were significantly over-represented during SMP activation, ranging from quiescent to late-activated stages. This analysis serves as a resource to further study the progression of in vitro skeletal myogenesis and could be mined to identify novel markers of pluripotent-derived SMPs or regulatory transcription/growth factors. Finally, 50-day hESC-derived SMPs appear similar to quiescent/early activated satellite cells, suggesting they possess therapeutic potential.
Klíčová slova:
Gene expression – Cell differentiation – Transcription factors – Skeletal muscles – TGF-beta signaling cascade – Muscle differentiation – Mesoderm – Pluripotency
Zdroje
1. Seale P, Sabourin LA, Girgis-Gabardo A, Mansouri A, Gruss P, Rudnicki MA. Pax7 Is Required for the Specification of Myogenic Satellite Cells. Cell. 2000;102: 777–786. doi: 10.1016/s0092-8674(00)00066-0 11030621
2. Kuang S, Kuroda K, Le Grand F, Rudnicki MA. Asymmetric Self-Renewal and Commitment of Satellite Stem Cells in Muscle. Cell. 2007;129: 999–1010. doi: 10.1016/j.cell.2007.03.044 17540178
3. Rosen GD, Sanes JR, LaChance R, Cunningham JM, Roman J, Dean DC. Roles for the integrin VLA-4 and its counter receptor VCAM-1 in myogenesis. Cell. 1992;69: 1107–19. doi: 10.1016/0092-8674(92)90633-n 1377605
4. Jesse TL, LaChance R, Iademarco MF, Dean DC. Interferon regulatory factor-2 is a transcriptional activator in muscle where it regulates expression of vascular cell adhesion molecule-1. J Cell Biol. 1998;140: 1265–76. doi: 10.1083/jcb.140.5.1265 9490737
5. Castiglioni A, Hettmer S, Lynes MD, Rao TN, Tchessalova D, Sinha I, et al. Isolation of progenitors that exhibit myogenic/osteogenic bipotency in vitro by fluorescence-activated cell sorting from human fetal muscle. Stem Cell Reports. 2014;2: 92–106. doi: 10.1016/j.stemcr.2013.12.006 24678452
6. Gnocchi VF, White RB, Ono Y, Ellis JA, Zammit PS. Further characterisation of the molecular signature of quiescent and activated mouse muscle satellite cells. PLoS One. 2009;4: e5205. doi: 10.1371/journal.pone.0005205 19370151
7. Shea KL, Xiang W, LaPorta VS, Licht JD, Keller C, Basson MA, et al. Sprouty1 regulates reversible quiescence of a self-renewing adult muscle stem cell pool during regeneration. Cell Stem Cell. 2010;6: 117–29. doi: 10.1016/j.stem.2009.12.015 20144785
8. 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
9. Chargé SBP, Rudnicki MA. Cellular and molecular regulation of muscle regeneration. Physiol Rev. 2004;84: 209–38. doi: 10.1152/physrev.00019.2003 14715915
10. Wang YX, Rudnicki MA. Satellite cells, the engines of muscle repair. Nat Rev Mol Cell Biol. 2011;13: 127–133. doi: 10.1038/nrm3265 22186952
11. 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: 2064–7. doi: 10.1126/science.1114758 16141372
12. Shelton M, Metz J, Liu J, Carpenedo RL, Demers SP, Stanford WL, et al. Derivation and expansion of PAX7-positive muscle progenitors from human and mouse embryonic stem cells. Stem Cell Reports. 2014;3: 516–529. doi: 10.1016/j.stemcr.2014.07.001 25241748
13. Shelton M, Kocharyan A, Liu J, Skerjanc IS, Stanford WL. Robust generation and expansion of skeletal muscle progenitors and myocytes from human pluripotent stem cells. Methods. 2016;101: 73–84. doi: 10.1016/j.ymeth.2015.09.019 26404920
14. Alexander MS, Rozkalne A, Colletta A, Spinazzola JM, Johnson S, Rahimov F, et al. CD82 Is a Marker for Prospective Isolation of Human Muscle Satellite Cells and Is Linked to Muscular Dystrophies. Cell Stem Cell. 2016;19: 800–807. doi: 10.1016/j.stem.2016.08.006 27641304
15. Cerletti M, Molloy MJ, Tomczak KK, Yoon S, Ramoni MF, Kho AT, et al. Melanoma cell adhesion molecule is a novel marker for human fetal myogenic cells and affects myoblast fusion. J Cell Sci. 2006;119: 3117–27. doi: 10.1242/jcs.03056 16835268
16. Lagha M, Sato T, Regnault B, Cumano A, Zuniga A, Licht J, et al. Transcriptome analyses based on genetic screens for Pax3 myogenic targets in the mouse embryo. BMC Genomics. 2010;11. doi: 10.1186/1471-2164-11-696 21143873
17. Lapan AD, Rozkalne A, Gussoni E. Human fetal skeletal muscle contains a myogenic side population that expresses the melanoma cell-adhesion molecule. Hum Mol Genet. 2012;21: 3668–3680. doi: 10.1093/hmg/dds196 22634225
18. Hicks MR, Hiserodt J, Paras K, Fujiwara W, Eskin A, Jan M, et al. ERBB3 and NGFR mark a distinct skeletal muscle progenitor cell in human development and hPSCs. Nat Cell Biol. 2018;20: 46–57. doi: 10.1038/s41556-017-0010-2 29255171
19. Xu C, Tabebordbar M, Iovino S, Ciarlo C, Liu J, Castiglioni A, et al. A zebrafish embryo culture system defines factors that promote vertebrate myogenesis across species. Cell. 2013;155: 909–921. doi: 10.1016/j.cell.2013.10.023 24209627
20. Borchin B, Chen J, Barberi T. Derivation and FACS-mediated purification of PAX3+/PAX7+ skeletal muscle precursors from human pluripotent stem cells. Stem Cell Reports. 2013;1: 620–631. doi: 10.1016/j.stemcr.2013.10.007 24371814
21. Hosoyama T, McGivern JV, Van Dyke JM, Ebert AD, Suzuki M. Derivation of myogenic progenitors directly from human pluripotent stem cells using a sphere-based culture. Stem Cells Transl Med. 2014;3: 564–74. doi: 10.5966/sctm.2013-0143 24657962
22. Chal J, Oginuma M, Al Tanoury Z, Gobert B, Sumara O, Hick A, et al. Differentiation of pluripotent stem cells to muscle fiber to model Duchenne muscular dystrophy. Nat Biotechnol. 2015;33: 962–969. doi: 10.1038/nbt.3297 26237517
23. Caron L, Kher D, Lee KL, McKernan R, Dumevska B, Hidalgo A, et al. A Human Pluripotent Stem Cell Model of Facioscapulohumeral Muscular Dystrophy-Affected Skeletal Muscles. Stem Cells Transl Med. 2016;5: 1145–61. doi: 10.5966/sctm.2015-0224 27217344
24. Choi IY, Lim HT, Estrellas K, Mula J, Cohen TV., Zhang Y, et al. Concordant but Varied Phenotypes among Duchenne Muscular Dystrophy Patient-Specific Myoblasts Derived using a Human iPSC-Based Model. Cell Rep. 2016;15: 2301–2312. doi: 10.1016/j.celrep.2016.05.016 27239027
25. Xi H, Fujiwara W, Gonzalez K, Jan M, Liebscher S, Van Handel B, et al. In Vivo Human Somitogenesis Guides Somite Development from hPSCs. Cell Rep. 2017;18: 1573–1585. doi: 10.1016/j.celrep.2017.01.040 28178531
26. Rao L, Tang W, Wei Y, Bao L, Chen J, Chen H, et al. Highly Efficient Derivation of Skeletal Myotubes from Human Embryonic Stem Cells. Stem Cell Rev Reports. 2012;8: 1109–1119. doi: 10.1007/s12015-012-9413-4 23104134
27. Albini S, Coutinho P, Malecova B, Giordani L, Savchenko A, Forcales SV, et al. Epigenetic Reprogramming of Human Embryonic Stem Cells into Skeletal Muscle Cells and Generation of Contractile Myospheres. Cell Rep. 2013;3: 661–670. doi: 10.1016/j.celrep.2013.02.012 23478022
28. Edom-Vovard F, Mouly V, Barbet JP, Butler-Browne GS. The four populations of myoblasts involved in human limb muscle formation are present from the onset of primary myotube formation. J Cell Sci. 1999;112: 191–9. Available: http://www.ncbi.nlm.nih.gov/pubmed/9858472 9858472
29. 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
30. Ulitsky I, Maron-Katz A, Shavit S, Sagir D, Linhart C, Elkon R, et al. Expander: from expression microarrays to networks and functions. Nat Protoc. 2010;5: 303–322. doi: 10.1038/nprot.2009.230 20134430
31. Chen J, Bardes EE, Aronow BJ, Jegga AG. ToppGene Suite for gene list enrichment analysis and candidate gene prioritization. Nucleic Acids Res. 2009;37: 305–311. doi: 10.1093/nar/gkp427 19465376
32. Daily K, Ho Sui SJ, Schriml LM, Dexheimer PJ, Salomonis N, Schroll R, et al. Molecular, phenotypic, and sample-associated data to describe pluripotent stem cell lines and derivatives. Sci Data. 2017;4: 170030. doi: 10.1038/sdata.2017.30 28350385
33. Soleimani VD, Punch VG, Kawabe Y ichi, Jones AE, Palidwor GA, Porter CJ, et al. Transcriptional Dominance of Pax7 in Adult Myogenesis Is Due to High-Affinity Recognition of Homeodomain Motifs. Dev Cell. 2012;22: 1208–1220. doi: 10.1016/j.devcel.2012.03.014 22609161
34. Lilja KC, Zhang N, Magli A, Gunduz V, Bowman CJ, Arpke RW, et al. Pax7 remodels the chromatin landscape in skeletal muscle stem cells. PLoS One. 2017;12: 1–24. doi: 10.1371/journal.pone.0176190 28441415
35. Yamaguchi TP, Takada S, Yoshikawa Y, Wu N, McMahon AP. T (Brachyury) is a direct target of Wnt3a during paraxial mesoderm specification. Genes Dev. 1999;13: 3185–3190. doi: 10.1101/gad.13.24.3185 10617567
36. Yoon JK, Moon RT, Wold B. The bHLH Class Protein pMesogenin1 Can Specify Paraxial Mesoderm Phenotypes. Dev Biol. 2000;222: 376–391. doi: 10.1006/dbio.2000.9717 10837126
37. Chapman DL, Agulnik I, Hancock S, Silver LM, Papaioannou VE. Tbx6, a mouse T-Box gene implicated in paraxial mesoderm formation at gastrulation. Dev Biol. 1996;180: 534–542. doi: 10.1006/dbio.1996.0326 8954725
38. Loh KMM, Chen A, Koh PWW, Deng TZZ, Sinha R, Tsai JMM, et al. Mapping the Pairwise Choices Leading from Pluripotency to Human Bone, Heart, and Other Mesoderm Cell Types. Cell. 2016;166: 451–468. doi: 10.1016/j.cell.2016.06.011 27419872
39. Chalamalasetty RB, Garriock RJ, Dunty WC, Kennedy MW, Jailwala P, Si H, et al. Mesogenin 1 is a master regulator of paraxial presomitic mesoderm differentiation. Development. 2014;141: 4285–4297. doi: 10.1242/dev.110908 25371364
40. Zeineddine D, Papadimou E, Chebli K, Gineste M, Liu J, Grey C, et al. Oct-3/4 Dose Dependently Regulates Specification of Embryonic Stem Cells toward a Cardiac Lineage and Early Heart Development. Dev Cell. 2006;11: 535–546. doi: 10.1016/j.devcel.2006.07.013 17011492
41. Thomson M, Liu SJ, Zou LN, Smith Z, Meissner A, Ramanathan S. Pluripotency factors in embryonic stem cells regulate differentiation into germ layers. Cell. 2011;145: 875–889. doi: 10.1016/j.cell.2011.05.017 21663792
42. DeVeale B, Brokhman I, Mohseni P, Babak T, Yoon C, Lin A, et al. Oct4 is required ~E7.5 for proliferation in the primitive streak. PLoS Genet. 2013;9: e1003957. doi: 10.1371/journal.pgen.1003957 24244203
43. Liu N, Nelson BR, Bezprozvannaya S, Shelton JM, Richardson JA, Bassel-Duby R, et al. Requirement of MEF2A, C, and D for skeletal muscle regeneration. Proc Natl Acad Sci. 2014;111: 4109–4114. doi: 10.1073/pnas.1401732111 24591619
44. Dumont NA, Wang YX, von Maltzahn J, Pasut A, Bentzinger CF, Brun CE, et al. Dystrophin expression in muscle stem cells regulates their polarity and asymmetric division. Nat Med. 2015;21: 1455–1463. doi: 10.1038/nm.3990 26569381
45. Hwang PM, Sykes BD. Targeting the sarcomere to correct muscle function. Nat Rev Drug Discov. 2015;14: 313–328. doi: 10.1038/nrd4554 25881969
46. Shih HP, Gross MK, Kioussi C. Expression pattern of the homeodomain transcription factor Pitx2 during muscle development. Gene Expr Patterns. 2007;7: 441–51. doi: 10.1016/j.modgep.2006.11.004 17166778
47. 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. doi: 10.1016/j.ydbio.2009.10.005 19835858
48. Leroy MC, Perroud J, Darbellay B, Bernheim L, Konig S. Epidermal growth factor receptor down-regulation triggers human myoblast differentiation. PLoS One. 2013;8: e71770. doi: 10.1371/journal.pone.0071770 23967242
49. Wang YX, Feige P, Brun CE, Hekmatnejad B, Dumont NA, Renaud J-M, et al. EGFR-Aurka Signaling Rescues Polarity and Regeneration Defects in Dystrophin-Deficient Muscle Stem Cells by Increasing Asymmetric Divisions. Cell Stem Cell. 2019;24: 419–432.e6. doi: 10.1016/j.stem.2019.01.002 30713094
50. Peng M, Palin MF, Véronneau S, LeBel D, Pelletier G. Ontogeny of epidermal growth factor (EGF), EGF receptor (EGFR) and basic fibroblast growth factor (bFGF) mRNA levels in pancreas, liver, kidney, and skeletal muscle of pig. Domest Anim Endocrinol. 1997;14: 286–294. doi: 10.1016/S0739-7240(97)00025-8 9347249
51. Grzywacz B, Kataria N, Kataria N, Blazar BR, Miller JS, Verneris MR. Natural killer-cell differentiation by myeloid progenitors. Blood. 2011;117: 3548–58. doi: 10.1182/blood-2010-04-281394 21173117
52. Turner DA, Rué P, Mackenzie JP, Davies E, Martinez Arias A. Brachyury cooperates with Wnt/β-catenin signalling to elicit primitive-streak-like behaviour in differentiating mouse embryonic stem cells. BMC Biol. 2014;12: 63. doi: 10.1186/s12915-014-0063-7 25115237
53. Blauwkamp TA, Nigam S, Ardehali R, Weissman IL, Nusse R. Endogenous Wnt signalling in human embryonic stem cells generates an equilibrium of distinct lineage-specified progenitors. Nat Commun. 2012;3: 1070. doi: 10.1038/ncomms2064 22990866
54. Cao N, Liang H, Huang J, Wang J, Chen Y, Chen Z, et al. Highly efficient induction and long-term maintenance of multipotent cardiovascular progenitors from human pluripotent stem cells under defined conditions. Cell Res. 2013;23: 1119–1132. doi: 10.1038/cr.2013.102 23896987
55. Nazareth EJP, Ostblom JEE, Lücker PB, Shukla S, Alvarez MM, Oh SKW, et al. High-throughput fingerprinting of human pluripotent stem cell fate responses and lineage bias. Nat Methods. 2013;10: 1225–1231. doi: 10.1038/nmeth.2684 24141495
56. Loh KM, Ang LT, Zhang J, Kumar V, Ang J, Auyeong JQ, et al. Efficient endoderm induction from human pluripotent stem cells by logically directing signals controlling lineage bifurcations. Cell Stem Cell. 2014;14: 237–252. doi: 10.1016/j.stem.2013.12.007 24412311
57. Naujok O, Diekmann U, Lenzen S. The generation of definitive endoderm from human embryonic stem cells is initially independent from activin A but requires canonical Wnt-signaling. Stem Cell Rev. 2014;10: 480–93. doi: 10.1007/s12015-014-9509-0 24913278
58. Hu J, Wang Y, Jiao J, Liu Z, Zhao C, Zhou Z, et al. Patient-specific cardiovascular progenitor cells derived from integration-free induced pluripotent stem cells for vascular tissue regeneration. Biomaterials. 2015;73: 51–59. doi: 10.1016/j.biomaterials.2015.09.008 26398309
59. Barberi T, Bradbury M, Dincer Z, Panagiotakos G, Socci ND, Studer L. Derivation of engraftable skeletal myoblasts from human embryonic stem cells. Nat Med. 2007;13: 642–648. doi: 10.1038/nm1533 17417652
60. Tan JY, Sriram G, Rufaihah AJ, Neoh KG, Cao T. Efficient Derivation of Lateral Plate and Paraxial Mesoderm Subtypes from Human Embryonic Stem Cells Through GSKi-Mediated Differentiation. Stem Cells Dev. 2013;22: 1893–1906. doi: 10.1089/scd.2012.0590 23413973
61. Mendjan S, Mascetti VL, Ortmann D, Ortiz M, Karjosukarso DW, Ng Y, et al. NANOG and CDX2 pattern distinct subtypes of human mesoderm during exit from pluripotency. Cell Stem Cell. 2014;15: 310–325. doi: 10.1016/j.stem.2014.06.006 25042702
62. Gadue P, Huber TL, Paddison PJ, Keller GM. Wnt and TGF-beta signaling are required for the induction of an in vitro model of primitive streak formation using embryonic stem cells. Proc Natl Acad Sci. 2006;103: 16806–16811. doi: 10.1073/pnas.0603916103 17077151
63. Rodríguez-Esteban C, Capdevila J, Kawakami Y, Belmonte JCI. Wnt signaling and PKA control Nodal expression and left-right determination in the chick embryo. Development. 2001;128: 3189–3195. Available: http://dev.biologists.org/content/128/16/3189.abstract 11688567
64. Sumi T, Tsuneyoshi N, Nakatsuji N, Suemori H. Defining early lineage specification of human embryonic stem cells by the orchestrated balance of canonical Wnt/ -catenin, Activin/Nodal and BMP signaling. Development. 2008;135: 2969–2979. doi: 10.1242/dev.021121 18667462
65. Toyama R, O’Connell ML, Wright CV, Kuehn MR, Dawid IB. Nodal induces ectopic goosecoid and lim1 expression and axis duplication in zebrafish. Development. 1995;121: 383–91. Available: http://www.ncbi.nlm.nih.gov/pubmed/7768180 7768180
66. Katoh M, Katoh M. CER1 is a common target of WNT and NODAL signaling pathways in human embryonic stem cells. Int J Mol Med. 2006;17: 795–799. doi: 10.3892/ijmm.17.5.795 16596263
67. Guo X, Wang X-F. Signaling cross-talk between TGF-β/BMP and other pathways. Cell Res. 2009;19: 71–88. doi: 10.1038/cr.2008.302 19002158
68. Belo JA, Bachiller D, Agius E, Kemp C, Borges AC, Marques S, et al. Cerberus-like is a secreted BMP and nodal antagonist not essential for mouse development. Genesis. 2000;26: 265–70. doi: 10.1002/(SICI)1526-968X(200004)26:4<265::AID-GENE80>3.0.CO;2-4 10748465
69. Kempf H, Olmer R, Haase A, Franke A, Bolesani E, Schwanke K, et al. Bulk cell density and Wnt/TGFbeta signalling regulate mesendodermal patterning of human pluripotent stem cells. Nat Commun. 2016;7: 13602. doi: 10.1038/ncomms13602 27934856
70. 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
71. 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
72. van Velthoven CTJ, de Morree A, Egner IM, Brett JO, Rando TA. Transcriptional Profiling of Quiescent Muscle Stem Cells In Vivo. Cell Rep. 2017;21: 1994–2004. doi: 10.1016/j.celrep.2017.10.037 29141228
73. Marchildon F, Lala N, Li G, St.-Louis C, Lamothe D, Keller C, et al. CCAAT/enhancer binding protein beta is expressed in satellite cells and controls myogenesis. Stem Cells. 2012;30: 2619–2630. doi: 10.1002/stem.1248 23034923
74. Magli A, Incitti T, Kiley J, Swanson SA, Darabi R, Rinaldi F, et al. PAX7 Targets, CD54, Integrin α9β1, and SDC2, Allow Isolation of Human ESC/iPSC-Derived Myogenic Progenitors. Cell Rep. 2017;19: 2867–2877. doi: 10.1016/j.celrep.2017.06.005 28658631
75. Fukada S, Yamaguchi M, Kokubo H, Ogawa R, Uezumi A, Yoneda T, et al. Hesr1 and Hesr3 are essential to generate undifferentiated quiescent satellite cells and to maintain satellite cell numbers. Development. 2011;138: 4609–19. doi: 10.1242/dev.067165 21989910
76. Bjornson CRRR, Cheung TH, Liu L, Tripathi PV., Steeper KM, Rando TA. Notch signaling is necessary to maintain quiescence in adult muscle stem cells. Stem Cells. 2012;30: 232–242. doi: 10.1002/stem.773 22045613
77. Philippos M, Sambasivan R, Castel D, Rocheteau P, Bizzarro V, Tajbakhsh S. A critical requirement for notch signaling in maintenance of the quiescent skeletal muscle stem cell state. Stem Cells. 2012;30: 243–252. doi: 10.1002/stem.775 22069237
78. Fujimaki S, Seko D, Kitajima Y, Yoshioka K, Tsuchiya Y, Masuda S, et al. Notch1 and Notch2 Coordinately Regulate Stem Cell Function in the Quiescent and Activated States of Muscle Satellite Cells. Stem Cells. 2018;36: 278–285. doi: 10.1002/stem.2743 29139178
79. Ge X, McFarlane C, Vajjala A, Lokireddy S, Ng ZH, Tan CK, et al. Smad3 signaling is required for satellite cell function and myogenic differentiation of myoblasts. Cell Res. 2011;21: 1591–604. doi: 10.1038/cr.2011.72 21502976
80. Bengal E, Ransone L, Scharfmann R, Dwarki VJ, Tapscott SJ, Weintraub H, et al. Functional antagonism between c-Jun and MyoD proteins: A direct physical association. Cell. 1992;68: 507–519. doi: 10.1016/0092-8674(92)90187-h 1310896
81. Andreucci JJ, Grant D, Cox DM, Tomc LK, Prywes R, Goldhamer DJ, et al. Composition and function of AP-1 transcription complexes during muscle cell differentiation. J Biol Chem. 2002;277: 16426–16432. doi: 10.1074/jbc.M110891200 11877423
82. Alli NS, Yang EC, Miyake T, Aziz A, Collins-Hooper H, Patel K, et al. Signal-dependent fra-2 regulation in skeletal muscle reserve and satellite cells. Cell Death Dis. 2013;4: e692. doi: 10.1038/cddis.2013.221 23807221
83. Zalc A, Hayashi S, Auradé F, Bröhl D, Chang T, Mademtzoglou D, et al. Antagonistic regulation of p57kip2 by Hes/Hey downstream of Notch signaling and muscle regulatory factors regulates skeletal muscle growth arrest. Development. 2014;141: 2780–90. doi: 10.1242/dev.110155 25005473
84. Lee KS, Kim HJ, Li QL, Chi XZ, Ueta C, Komori T, et al. Runx2 is a common target of transforming growth factor beta1 and bone morphogenetic protein 2, and cooperation between Runx2 and Smad5 induces osteoblast-specific gene expression in the pluripotent mesenchymal precursor cell line C2C12. Mol Cell Biol. 2000;20: 8783–92. doi: 10.1128/mcb.20.23.8783-8792.2000 Updated 11073979
85. Asakura A, Komaki M, Rudnicki M. Muscle satellite cells are multipotential stem cells that exhibit myogenic, osteogenic, and adipogenic differentiation. Differentiation. 2001;68: 245–53. doi: 10.1046/j.1432-0436.2001.680412.x 11776477
86. Komori T, Yagi H, Nomura S, Yamaguchi A, Sasaki K, Deguchi K, et al. Targeted disruption of Cbfa1 results in a complete lack of bone formation owing to maturational arrest of osteoblasts. Cell. 1997;89: 755–64. doi: 10.1016/s0092-8674(00)80258-5 9182763
87. Lu M-F, Cheng H-T, Lacy AR, Kern MJ, Argao EA, Potter SS, et al. Paired-Related Homeobox Genes Cooperate in Handplate and Hindlimb Zeugopod Morphogenesis. Dev Biol. 1999;205: 145–157. doi: 10.1006/dbio.1998.9116 9882503
88. Wißmüller S, Kosian T, Wolf M, Finzsch M, Wegner M. The high-mobility-group domain of Sox proteins interacts with DNA-binding domains of many transcription factors. Nucleic Acids Res. 2006;34: 1735–1744. doi: 10.1093/nar/gkl105 16582099
89. Schmidt K, Glaser G, Wernig A, Wegner M, Rosorius O. Sox8 is a specific marker for muscle satellite cells and inhibits myogenesis. J Biol Chem. 2003;278: 29769–29775. doi: 10.1074/jbc.M301539200 12782625
90. Brzóska E, Bello V, Darribère T, Moraczewski J. Integrin α3 subunit participates in myoblast adhesion and fusion in vitro. Differentiation. 2006;74: 105–118. doi: 10.1111/j.1432-0436.2005.00059.x 16533309
91. Seale P, Ishibashi J, Holterman C, Rudnicki MA. Muscle satellite cell-specific genes identified by genetic profiling of MyoD-deficient myogenic cell. Dev Biol. 2004;275: 287–300. doi: 10.1016/j.ydbio.2004.07.034 15501219
92. Ducceschi M, Clifton LG, Stimpson SA, Billin AN. Post-transcriptional regulation of ITGB6 protein levels in damaged skeletal muscle. J Mol Histol. 2014;45: 329–336. doi: 10.1007/s10735-014-9567-2 24488487
93. Gopinath SD, Webb AE, Brunet A, Rando TA. FOXO3 promotes quiescence in adult muscle stem cells during the process of self-renewal. Stem Cell Reports. 2014;2: 414–426. doi: 10.1016/j.stemcr.2014.02.002 24749067
94. Hagiwara N, Klewer SE, Samson RA, Erickson DT, Lyon MF, Brilliant MH. Sox6 is a candidate gene for p100H myopathy, heart block, and sudden neonatal death. Proc Natl Acad Sci. 2000;97: 4180–5. doi: 10.1073/pnas.97.8.4180 10760285
95. An C- I, Dong Y, Hagiwara N. Genome-wide mapping of Sox6 binding sites in skeletal muscle reveals both direct and indirect regulation of muscle terminal differentiation by Sox6. BMC Dev Biol. 2011;11: 59. doi: 10.1186/1471-213X-11-59 21985497
96. Rescan PY, Ralliere C. A Sox5 gene is expressed in the myogenic lineage during trout embryonic development. Int J Dev Biol. 2010;54: 913–918. doi: 10.1387/ijdb.092893pr 20336612
97. Berger MF, Badis G, Gehrke AR, Talukder S, Philippakis AA, Peña-Castillo L, et al. Variation in Homeodomain DNA Binding Revealed by High-Resolution Analysis of Sequence Preferences. Cell. 2008;133: 1266–1276. doi: 10.1016/j.cell.2008.05.024 18585359
98. Piao Y, Ko MSH, Nedorezov T, Shaik N, Sharov AA, Sharova LV. Database for mRNA Half-Life of 19 977 Genes Obtained by DNA Microarray Analysis of Pluripotent and Differentiating Mouse Embryonic Stem Cells. DNA Res. 2008;16: 45–58. doi: 10.1093/dnares/dsn030 19001483
99. Zetser A, Gredinger E, Bengal E. p38 mitogen-activated protein kinase pathway promotes skeletal muscle differentiation. Participation of the Mef2c transcription factor. J Biol Chem. 1999;274: 5193–5200. doi: 10.1074/jbc.274.8.5193 9988769
100. Wu Z, Woodring PJ, Bhakta KS, Tamura K, Wen F, Feramisco JR, et al. P38 and Extracellular Signal-Regulated Kinases Regulate the Myogenic Program At Multiple Steps. Mol Cell Biol. 2000;20: 3951–64. doi: 10.1128/mcb.20.11.3951-3964.2000 10805738
101. De Angelis L, Zhao J, Andreucci JJ, Olson EN, Cossu G, McDermott JC. Regulation of vertebrate myotome development by the p38 MAP kinase-MEF2 signaling pathway. Dev Biol. 2005;283: 171–179. doi: 10.1016/j.ydbio.2005.04.009 15890335
102. Shamblott MJ, Bugg EM, Lawler AM, Gearhart JD. Craniofacial abnormalities resulting from targeted disruption of the murine Sim2 gene. Dev Dyn. 2002;224: 373–380. doi: 10.1002/dvdy.10116 12203729
103. Bothe I, Dietrich S. The molecular setup of the avian head mesoderm and its implication for craniofacial myogenesis. Dev Dyn. 2006;235: 2845–2860. doi: 10.1002/dvdy.20903 16894604
104. Pedrosa-Domellöf F, Eriksson PO, Butler-Browne GS, Thornell LE. Expression of alpha-cardiac myosin heavy chain in mammalian skeletal muscle. Experientia. 1992;48: 491–4. doi: 10.1007/bf01928171 1601115
105. Cachaço AS, Pereira CS, Pardal RG, Bajanca F, Thorsteinsdóttir S. Integrin repertoire on myogenic cells changes during the course of primary myogenesis in the mouse. Dev Dyn. 2005;232: 1069–1078. doi: 10.1002/dvdy.20280 15739233
106. Vasyutina E, Stebler J, Brand-Saberi B, Schulz S, Raz E, Birchmeier C. CXCR4 and Gab1 cooperate to control the development of migrating muscle progenitor cells. Genes Dev. 2005;19: 2187–98. doi: 10.1101/gad.346205 16166380
107. Chang H, Yoshimoto M, Umeda K, Iwasa T, Mizuno Y, Fukada S, et al. Generation of transplantable, functional satellite-like cells from mouse embryonic stem cells. FASEB J. 2009;23: 1907–19. doi: 10.1096/fj.08-123661 19168704
108. Song WK, Wang W, Foster RF, Bielser DA, Kaufman SJ. H36-alpha 7 is a novel integrin alpha chain that is developmentally regulated during skeletal myogenesis. J Cell Biol. 1992;117: 643–57. doi: 10.1083/jcb.117.3.643 1315319
109. Uezumi A, Nakatani M, Ikemoto-Uezumi M, Yamamoto N, Morita M, Yamaguchi A, et al. Cell-Surface Protein Profiling Identifies Distinctive Markers of Progenitor Cells in Human Skeletal Muscle. Stem Cell Reports. 2016;7: 263–278. doi: 10.1016/j.stemcr.2016.07.004 27509136
110. Fukada S, Uezumi A, Ikemoto M, Masuda S, Segawa M, Tanimura N, et al. Molecular Signature of Quiescent Satellite Cells in Adult Skeletal Muscle. Stem Cells. 2007;25: 2448–2459. doi: 10.1634/stemcells.2007-0019 17600112
111. Dearth CL, Goh Q, Marino JS, Cicinelli PA, Torres-Palsa MJ, Pierre P, et al. Skeletal muscle cells express ICAM-1 after muscle overload and ICAM-1 contributes to the ensuing hypertrophic response. PLoS One. 2013;8: e58486. doi: 10.1371/journal.pone.0058486 23505517
112. Moriguchi T, Haraguchi K, Ueda N, Okada M, Furuya T, Akiyama T. DREG, a developmentally regulated G protein-coupled receptor containing two conserved proteolytic cleavage sites. Genes to Cells. 2004;9: 549–560. doi: 10.1111/j.1356-9597.2004.00743.x 15189448
113. Waller-Evans H, Prömel S, Langenhan T, Dixon J, Zahn D, Colledge WH, et al. The orphan adhesion-GPCR GPR126 is required for embryonic development in the mouse. PLoS One. 2010;5: e14047. doi: 10.1371/journal.pone.0014047 21124978
114. Andrechek ER, Hardy WR, Girgis-Gabardo AA, Perry RLS, Butler R, Graham FL, et al. ErbB2 is required for muscle spindle and myoblast cell survival. Mol Cell Biol. 2002;22: 4714–22. doi: 10.1128/MCB.22.13.4714-4722.2002 12052879
115. Golding JP, Calderbank E, Partridge TA, Beauchamp JR. Skeletal muscle stem cells express anti-apoptotic ErbB receptors during activation from quiescence. Exp Cell Res. 2007;313: 341–356. doi: 10.1016/j.yexcr.2006.10.019 17123512
116. Dollé P, Izpisúa-Belmonte JC, Falkenstein H, Renucci A, Duboule D. Coordinate expression of the murine Hox-5 complex homoeobox-containing genes during limb pattern formation. Nature. 1989;342: 767–72. doi: 10.1038/342767a0 2574828
117. Sandelin A. JASPAR: an open-access database for eukaryotic transcription factor binding profiles. Nucleic Acids Res. 2004;32: 91D–94. doi: 10.1093/nar/gkh012 14681366
118. Mammucari C, Milan G, Romanello V, Masiero E, Rudolf R, Del Piccolo P, et al. FoxO3 Controls Autophagy in Skeletal Muscle In Vivo. Cell Metab. 2007;6: 458–471. doi: 10.1016/j.cmet.2007.11.001 18054315
119. Zhao J, Brault JJ, Schild A, Cao P, Sandri M, Schiaffino S, et al. FoxO3 Coordinately Activates Protein Degradation by the Autophagic/Lysosomal and Proteasomal Pathways in Atrophying Muscle Cells. Cell Metab. 2007;6: 472–483. doi: 10.1016/j.cmet.2007.11.004 18054316
120. Shi X, Wallis AM, Gerard RD, Voelker KA, Grange RW, DePinho RA, et al. Foxk1 promotes cell proliferation and represses myogenic differentiation by regulating Foxo4 and Mef2. J Cell Sci. 2012;125: 5329–5337. doi: 10.1242/jcs.105239 22956541
121. Peserico A, Chiacchiera F, Grossi V, Matrone A, Latorre D, Simonatto M, et al. A novel AMPK-dependent FoxO3A-SIRT3 intramitochondrial complex sensing glucose levels. Cell Mol Life Sci. 2013;70: 2015–2029. doi: 10.1007/s00018-012-1244-6 23283301
122. Bowman CJ, Ayer DE, Dynlacht BD. Foxk proteins repress the initiation of starvation-induced atrophy and autophagy programs. Nat Cell Biol. 2014;16: 1202–1214. doi: 10.1038/ncb3062 25402684
123. Wu J, Matthias N, Lo J, Ortiz-Vitali JL, Shieh AW, Wang SH, et al. A Myogenic Double-Reporter Human Pluripotent Stem Cell Line Allows Prospective Isolation of Skeletal Muscle Progenitors. Cell Rep. 2018;25: 1966–1981.e4. doi: 10.1016/j.celrep.2018.10.067 30428361
124. Webster C, Pavlath GK, Parks DR, Walsh FS, Blau HM. Isolation of human myoblasts with the fluorescence-activated cell sorter. Exp Cell Res. 1988;174: 252–265. doi: 10.1016/0014-4827(88)90159-0 3335226
125. Borue X. Normal and aberrant craniofacial myogenesis by grafted trunk somitic and segmental plate mesoderm. Development. 2004;131: 3967–3980. doi: 10.1242/dev.01276 15269174
126. Fomenou MD, Scaal M, Stockdale FE, Christ B, Huang R. Cells of all somitic compartments are determined with respect to segmental identity. Dev Dyn. 2005;233: 1386–1393. doi: 10.1002/dvdy.20464 15973735
127. Dias AS, de Almeida I, Belmonte JM, Glazier JA, Stern CD. Somites without a clock. Science (80-). 2014;343: 791–795. doi: 10.1126/science.1247575 24407478
128. Darabi R, Arpke RW, Irion S, Dimos JT, Grskovic M, Kyba M, et al. Human ES- and iPS-derived myogenic progenitors restore DYSTROPHIN and improve contractility upon transplantation in dystrophic mice. Cell Stem Cell. 2012;10: 610–619. doi: 10.1016/j.stem.2012.02.015 22560081
129. Zakariyah A, Rajgara R, Shelton M, Blais A, Skerjanc IS, Burgon PG. Combinatorial Utilization of Murine Embryonic Stem Cells and In Vivo Models to Study Human Congenital Heart Disease. Curr Protoc Stem Cell Biol. 2019;48: e75. doi: 10.1002/cpsc.75 30548532
130. Sharan R, Shamir R. CLICK: a clustering algorithm with applications to gene expression analysis. Proceedings Int Conf Intell Syst Mol Biol. 2000;8: 307–16. Available: http://www.ncbi.nlm.nih.gov/pubmed/10977092
131. Mi H, Huang X, Muruganujan A, Tang H, Mills C, Kang D, et al. PANTHER version 11: Expanded annotation data from Gene Ontology and Reactome pathways, and data analysis tool enhancements. Nucleic Acids Res. 2017;45: D183–D189. doi: 10.1093/nar/gkw1138 27899595
132. Kwon AT, Arenillas DJ, Worsley Hunt R, Wasserman WW. oPOSSUM-3: advanced analysis of regulatory motif over-representation across genes or ChIP-Seq datasets. G3. 2012;2: 987–1002. doi: 10.1534/g3.112.003202 22973536
133. Keil C, Leach R, Faizaan S, Bezawada S, Parsons L, Baryshnikova A. Treeview 3.0 (beta 1)—Visualization and analysis of large data matrices. In: Zenodo [Internet]. 2016 p. http://doi.org/10.5281/zenodo.1303402
134. McQuin C, Goodman A, Chernyshev V, Kamentsky L, Cimini BA, Karhohs KW, et al. CellProfiler 3.0: Next-generation image processing for biology. PLoS Biol. 2018;16: e2005970. doi: 10.1371/journal.pbio.2005970 29969450
Článok vyšiel v časopise
PLOS One
2019 Číslo 9
- Metamizol jako analgetikum první volby: kdy, pro koho, jak a proč?
- Nejasný stín na plicích – kazuistika
- Masturbační chování žen v ČR − dotazníková studie
- Je Fuchsova endotelová dystrofie rohovky neurodegenerativní onemocnění?
- Fixní kombinace paracetamol/kodein nabízí synergické analgetické účinky
Najčítanejšie v tomto čísle
- Graviola (Annona muricata) attenuates behavioural alterations and testicular oxidative stress induced by streptozotocin in diabetic rats
- CH(II), a cerebroprotein hydrolysate, exhibits potential neuro-protective effect on Alzheimer’s disease
- Comparison between Aptima Assays (Hologic) and the Allplex STI Essential Assay (Seegene) for the diagnosis of Sexually transmitted infections
- Assessment of glucose-6-phosphate dehydrogenase activity using CareStart G6PD rapid diagnostic test and associated genetic variants in Plasmodium vivax malaria endemic setting in Mauritania