Abstract
The vertebrate body axis elongates by extending the posterior end and generating a variety of somatic cells of the trunk (posterior) tissues. Recent studies have demonstrated that the posterior neural plate and posterior paraxial mesoderm are generated from bipotential stem cells, the axial stem cells, which reside in the caudal lateral epiblast of gastrulating embryos. The fate of axial stem cells, neural or mesodermal lineages, depends on the counteracting transcription factors for respective tissues, Sox2 and Tbx6. Tbx6 represses the Sox2 expression in the axial stem cell-derived mesodermal precursors. In the absence of the Tbx6 gene, Sox2 is ectopically expressed in the mesodermal precursors, causing ectopic neural tube development at the expense of paraxial mesoderm. While producing two somatic lineages, axial stem cells are proliferatively maintained by a process that depends on the Wnt-Brachyury regulatory loop; mutant embryos lacking Wnt3a or Brachyury activity prematurely terminate axis elongation as the result of stem cell exhaustion. Although the axial stem cells serve as a cellular source for the neural and paraxial mesoderm tissues of the trunk, at the craniocervical level these tissues are presumably produced via completely different mechanisms. In this chapter, experimental evidence for axial stem cells and their regulation is summarized.
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References
Anderson MJ, Naiche LA, Wilson CP, Elder C, Swing DA, Lewandoski M (2013) TCreERT2, a transgenic mouse line for temporal control of Cre-mediated recombination in lineages emerging from the primitive streak or tail bud. PLoS ONE 8(4):e62479. doi:10.1371/journal.pone.0062479
Brons IG, Smithers LE, Trotter MW, Rugg-Gunn P, Sun B, de Sousa C, Lopes SM, Howlett SK, Clarkson A, Ahrlund-Richter L, Pedersen RA, Vallier L (2007) Derivation of pluripotent epiblast stem cells from mammalian embryos. Nature (Lond) 448(7150):191–195. doi:10.1038/nature05950
Brown J, Storey K (2000) A region of the vertebrate neural plate in which neighbouring cells can adopt neural or epidermal fates. Curr Biol 10(14):869–872
Cambray N, Wilson V (2007) Two distinct sources for a population of maturing axial progenitors. Development (Camb) 134(15):2829–2840
Chapman D, Papaioannou V (1998) Three neural tubes in mouse embryos with mutations in the T-box gene Tbx6. Nature (Lond) 391(6668):695–697
Chapman D, Agulnik I, Hancock S, Silver L, Papaioannou V (1996) Tbx6, a mouse T-box gene implicated in paraxial mesoderm formation at gastrulation. Dev Biol 180(2):534–542
Chesley P (1935) Development of the short-tailed mutant in the house mouse. J Exp Zool 70(3):429–459
Delfino-MachÃn M, Lunn J, Breitkreuz D, Akai J, Storey K (2005) Specification and maintenance of the spinal cord stem zone. Development (Camb) 132(19):4273–4283
Greco TL, Takada S, Newhouse MM, McMahon JA, McMahon AP, Camper SA (1996) Analysis of the vestigial tail mutation demonstrates that Wnt-3a gene dosage regulates mouse axial development. Genes Dev 10(3):313–324
Huang Y, Osorno R, Tsakiridis A, Wilson V (2012) In vivo differentiation potential of epiblast stem cells revealed by chimeric embryo formation. Cell Rep 2(6):1571–1578. doi:10.1016/j.celrep.2012.10.022
Iwafuchi-Doi M, Yoshida Y, Onichtchouk D, Leichsenring M, Driever W, Takemoto T, Uchikawa M, Kamachi Y, Kondoh H (2011) The Pou5f1/Pou3f-dependent but SoxB-independent regulation of conserved enhancer N2 initiates Sox2 expression during epiblast to neural plate stages in vertebrates. Dev Biol 352(2):354–366. doi:10.1016/j.ydbio.2010.12.027, pii: S0012-1606(10)01268-6
Kamachi Y, Iwafuchi M, Okuda Y, Takemoto T, Uchikawa M, Kondoh H (2009) Evolution of non-coding regulatory sequences involved in the developmental process: reflection of differential employment of paralogous genes as highlighted by Sox2 and group B1 Sox genes. Proc Jpn Acad Ser B Phys Biol Sci 85(2):55–68
Kondoh H, Takemoto T (2012) Axial stem cells deriving both posterior neural and mesodermal tissues during gastrulation. Curr Opin Genet Dev 22(4):374–380. doi:10.1016/j.gde.2012.03.006, pii: S0959-437X(12)00044-5
Martin BL, Kimelman D (2012) Canonical Wnt signaling dynamically controls multiple stem cell fate decisions during vertebrate body formation. Dev Cell 22(1):223–232. doi:10.1016/j.devcel.2011.11.001
Olivera-Martinez I, Harada H, Halley PA, Storey KG (2012) Loss of FGF-dependent mesoderm identity and rise of endogenous retinoid signalling determine cessation of body axis elongation. PLoS Biol 10(10):e1001415. doi:10.1371/journal.pbio.1001415
Osorno R, Tsakiridis A, Wong F, Cambray N, Economou C, Wilkie R, Blin G, Scotting PJ, Chambers I, Wilson V (2012) The developmental dismantling of pluripotency is reversed by ectopic Oct4 expression. Development (Camb) 139(13):2288–2298. doi:10.1242/dev.078071
Perantoni AO, Timofeeva O, Naillat F, Richman C, Pajni-Underwood S, Wilson C, Vainio S, Dove LF, Lewandoski M (2005) Inactivation of FGF8 in early mesoderm reveals an essential role in kidney development. Development (Camb) 132(17):3859–3871. doi:10.1242/dev.01945
Takada S, Stark K, Shea M, Vassileva G, McMahon J, McMahon A (1994) Wnt-3a regulates somite and tailbud formation in the mouse embryo. Genes Dev 8(2):174–189
Takemoto T, Uchikawa M, Kamachi Y, Kondoh H (2006) Convergence of Wnt and FGF signals in the genesis of posterior neural plate through activation of the Sox2 enhancer N-1. Development (Camb) 133(2):297–306
Takemoto T, Uchikawa M, Yoshida M, Bell DM, Lovell-Badge R, Papaioannou VE, Kondoh H (2011) Tbx6-dependent Sox2 regulation determines neural or mesodermal fate in axial stem cells. Nature (Lond) 470(7334):394–398. doi:10.1038/nature09729, pii: nature09729
Tesar PJ, Chenoweth JG, Brook FA, Davies TJ, Evans EP, Mack DL, Gardner RL, McKay RD (2007) New cell lines from mouse epiblast share defining features with human embryonic stem cells. Nature (Lond) 448(7150):196–199. doi:10.1038/nature05972
Tzouanacou E, Wegener A, Wymeersch F, Wilson V, Nicolas J (2009) Redefining the progression of lineage segregations during mammalian embryogenesis by clonal analysis. Dev Cell 17(3):365–376
Uchikawa M, Ishida Y, Takemoto T, Kamachi Y, Kondoh H (2003) Functional analysis of chicken Sox2 enhancers highlights an array of diverse regulatory elements that are conserved in mammals. Dev Cell 4(4):509–519
Uchikawa M, Yoshida M, Iwafuchi-Doi M, Matsuda K, Ishida Y, Takemoto T, Kondoh H (2011) B1 and B2 Sox gene expression during neural plate development in chicken and mouse embryos: universal versus species-dependent features. Dev Growth Differ 53(6):761–771. doi:10.1111/j.1440-169X.2011.01286.x
Wilson V, Olivera-Martinez I, Storey K (2009) Stem cells, signals and vertebrate body axis extension. Development (Camb) 136(10):1591–1604
Wood HB, Episkopou V (1999) Comparative expression of the mouse Sox1, Sox2 and Sox3 genes from pre-gastrulation to early somite stages. Mech Dev 86(1–2):197–201
Yamaguchi T, Takada S, Yoshikawa Y, Wu N, McMahon A (1999) T (Brachyury) is a direct target of Wnt3a during paraxial mesoderm specification. Genes Dev 13:3185–3190
Yoshikawa Y, Fujimori T, McMahon A, Takada S (1997) Evidence that absence of Wnt-3a signaling promotes neuralization instead of paraxial mesoderm development in the mouse. Dev Biol 183(2):234–242
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Takemoto, T. (2014). Regulation of Axial Stem Cells Deriving Neural and Mesodermal Tissues During Posterior Axial Elongation. In: Kondoh, H., Kuroiwa, A. (eds) New Principles in Developmental Processes. Springer, Tokyo. https://doi.org/10.1007/978-4-431-54634-4_7
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DOI: https://doi.org/10.1007/978-4-431-54634-4_7
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