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Embryonal Neuromesodermal Progenitors for Caudal Central Nervous System and Tissue Development

  • Shaker, Mohammed R. (Australian Institute for Bioengineering and Nanotechnology, The University of Queensland) ;
  • Lee, Ju-Hyun (Department of Anatomy, Brain Korea 21 Plus Program for Biomedical Science, Korea University College of Medicine) ;
  • Sun, Woong (Department of Anatomy, Brain Korea 21 Plus Program for Biomedical Science, Korea University College of Medicine)
  • Received : 2020.12.23
  • Accepted : 2021.01.28
  • Published : 2021.05.01

Abstract

Neuromesodermal progenitors (NMPs) constitute a bipotent cell population that generates a wide variety of trunk cell and tissue types during embryonic development. Derivatives of NMPs include both mesodermal lineage cells such as muscles and vertebral bones, and neural lineage cells such as neural crests and central nervous system neurons. Such diverse lineage potential combined with a limited capacity for self-renewal, which persists during axial elongation, demonstrates that NMPs are a major source of trunk tissues. This review describes the identification and characterization of NMPs across multiple species. We also discuss key cellular and molecular steps for generating neural and mesodermal cells for building up the elongating trunk tissue.

Keywords

References

  1. Aires R, Dias A, Mallo M : Deconstructing the molecular mechanisms shaping the vertebrate body plan. Curr Opin Cell Biol 55 : 81-86, 2018 https://doi.org/10.1016/j.ceb.2018.05.009
  2. Amin S, Neijts R, Simmini S, van Rooijen C, Tan SC, Kester L, et al. : Cdx and T brachyury co-activate growth signaling in the embryonic axial progenitor niche. Cell Rep 17 : 3165-3177, 2016 https://doi.org/10.1016/j.celrep.2016.11.069
  3. Attardi A, Fulton T, Florescu M, Shah G, Muresan L, Lenz MO, et al. : Neuromesodermal progenitors are a conserved source of spinal cord with divergent growth dynamics. Development 145 : dev166728, 2018 https://doi.org/10.1242/dev.166728
  4. Berenguer M, Lancman JJ, Cunningham TJ, Dong PDS, Duester G : Mouse but not zebrafish requires retinoic acid for control of neuromesodermal progenitors and body axis extension. Dev Biol 441 : 127-131, 2018 https://doi.org/10.1016/j.ydbio.2018.06.019
  5. Chalamalasetty RB, Garriock RJ, Dunty WC Jr, Kennedy MW, Jailwala P, Si H, et al. : Mesogenin 1 is a master regulator of paraxial presomitic mesoderm differentiation. Development 141 : 4285-4297, 2014 https://doi.org/10.1242/dev.110908
  6. Costanzo R, Watterson RL, Schoenwolf GC : Evidence that secondary neurulation occurs autonomously in the chick embryo. J Exp Zool 219 : 233-240, 1982 https://doi.org/10.1002/jez.1402190212
  7. Cunningham TJ, Colas A, Duester G : Early molecular events during retinoic acid induced differentiation of neuromesodermal progenitors. Biol Open 5 : 1821-1833, 2016 https://doi.org/10.1242/bio.020891
  8. Cunningham TJ, Kumar S, Yamaguchi TP, Duester G : Wnt8a and Wnt3a cooperate in the axial stem cell niche to promote mammalian body axis extension. Dev Dyn 244 : 797-807, 2015 https://doi.org/10.1002/dvdy.24275
  9. Dady A, Havis E, Escriou V, Catala M, Duband JL : Junctional neurulation: a unique developmental program shaping a discrete region of the spinal cord highly susceptible to neural tube defects. J Neurosci 34 : 13208-13221, 2014 https://doi.org/10.1523/JNEUROSCI.1850-14.2014
  10. Dessaud E, McMahon AP, Briscoe J : Pattern formation in the vertebrate neural tube: a sonic hedgehog morphogen-regulated transcriptional network. Development 135 : 2489-2503, 2008 https://doi.org/10.1242/dev.009324
  11. Diez del Corral R, Morales AV : The multiple roles of FGF signaling in the developing spinal cord. Front Cell Dev Biol 5 : 58, 2017 https://doi.org/10.3389/fcell.2017.00058
  12. Evans AL, Faial T, Gilchrist MJ, Down T, Vallier L, Pedersen RA, et al. : Genomic targets of Brachyury (T) in differentiating mouse embryonic stem cells. PLoS One 7 : e33346, 2012 https://doi.org/10.1371/journal.pone.0033346
  13. Fior R, Maxwell AA, Ma TP, Vezzaro A, Moens CB, Amacher SL, et al. : The differentiation and movement of presomitic mesoderm progenitor cells are controlled by Mesogenin 1. Development 139 : 4656-4665, 2012 https://doi.org/10.1242/dev.078923
  14. Garriock RJ, Chalamalasetty RB, Kennedy MW, Canizales LC, Lewandoski M, Yamaguchi TP : Lineage tracing of neuromesodermal progenitors reveals novel Wnt-dependent roles in trunk progenitor cell maintenance and differentiation. Development 142 : 1628-1638, 2015 https://doi.org/10.1242/dev.111922
  15. Gouti M, Delile J, Stamataki D, Wymeersch FJ, Huang Y, Kleinjung J, et al. : A gene regulatory network balances neural and mesoderm specification during vertebrate trunk development. Dev Cell 41 : 243-261.e7, 2017 https://doi.org/10.1016/j.devcel.2017.04.002
  16. Gouti M, Metzis V, Briscoe J : The route to spinal cord cell types: a tale of signals and switches. Trends Genet 31 : 282-289, 2015 https://doi.org/10.1016/j.tig.2015.03.001
  17. Gouti M, Tsakiridis A, Wymeersch FJ, Huang Y, Kleinjung J, Wilson V, et al. : In vitro generation of neuromesodermal progenitors reveals distinct roles for Wnt signalling in the specification of spinal cord and paraxial mesoderm identity. PLoS Biol 12 : e1001937, 2014 https://doi.org/10.1371/journal.pbio.1001937
  18. Halpern ME, Ho RK, Walker C, Kimmel CB : Induction of muscle pioneers and floor plate is distinguished by the zebrafish no tail mutation. Cell 75 : 99-111, 1993 https://doi.org/10.1016/S0092-8674(05)80087-X
  19. Hofmann M, Schuster-Gossler K, Watabe-Rudolph M, Aulehla A, Herrmann BG, Gossler A : Wnt signaling, in synergy with T/TBX6, controls Notch signaling by regulating Dll1 expression in the presomitic mesoderm of mouse embryos. Genes Dev 18 : 2712-2717, 2004 https://doi.org/10.1101/gad.1248604
  20. Hubaud A, Pourquie O : Signalling dynamics in vertebrate segmentation. Nat Rev Mol Cell Biol 15 : 709-721, 2014 https://doi.org/10.1038/nrm3891
  21. Ille F, Atanasoski S, Falk S, Ittner LM, Marki D, Buchmann-Moller S, et al. : Wnt/BMP signal integration regulates the balance between proliferation and differentiation of neuroepithelial cells in the dorsal spinal cord. Dev Biol 304 : 394-408, 2007 https://doi.org/10.1016/j.ydbio.2006.12.045
  22. Javali A, Misra A, Leonavicius K, Acharyya D, Vyas B, Sambasivan R : Co-expression of Tbx6 and Sox2 identifies a novel transient neuromesoderm progenitor cell state. Development 144 : 4522-4529, 2017 https://doi.org/10.1242/dev.153262
  23. Kawachi T, Shimokita E, Kudo R, Tadokoro R, Takahashi Y : Neural-fated self-renewing cells regulated by Sox2 during secondary neurulation in chicken tail bud. Dev Biol 461 : 160-171, 2020 https://doi.org/10.1016/j.ydbio.2020.02.007
  24. Koch F, Scholze M, Wittler L, Schifferl D, Sudheer S, Grote P, et al. : Antagonistic activities of Sox2 and brachyury control the fate choice of neuro-mesodermal progenitors. Dev Cell 42 : 514-526.e7, 2017 https://doi.org/10.1016/j.devcel.2017.07.021
  25. Lee JH, Shin H, Shaker MR, Kim HJ, Kim JH, Lee N, et al. : Human spinal cord organoids exhibiting neural tube morphogenesis for a quantifiable drug screening system of neural tube defects. bioRxiv, 2020 [Epub ahead of print]
  26. Lee JY, Lee ES, Kim SP, Lee MS, Phi JH, Kim SK, et al. : Neurosphere formation potential resides not in the caudal cell mass, but in the secondary neural tube. Int J Dev Biol 61 : 545-550, 2017 https://doi.org/10.1387/ijdb.160344kw
  27. Li W, Germain RN, Gerner MY : Multiplex, quantitative cellular analysis in large tissue volumes with clearing-enhanced 3D microscopy (Ce3D). Proc Natl Acad Sci U S A 114 : E7321-E7330, 2017 https://doi.org/10.1073/pnas.1708981114
  28. Lin JR, Izar B, Wang S, Yapp C, Mei S, Shah PM, et al. : Highly multiplexed immunofluorescence imaging of human tissues and tumors using t-CyCIF and conventional optical microscopes. Elife 7 : e31657, 2018 https://doi.org/10.7554/elife.31657
  29. Lippmann ES, Williams CE, Ruhl DA, Estevez-Silva MC, Chapman ER, Coon JJ, et al. : Deterministic HOX patterning in human pluripotent stem cell-derived neuroectoderm. Stem Cell Reports 4 : 632-644, 2015 https://doi.org/10.1016/j.stemcr.2015.02.018
  30. Martin BL : Factors that coordinate mesoderm specification from neuromesodermal progenitors with segmentation during vertebrate axial extension. Semin Cell Dev Biol 49 : 59-67, 2016 https://doi.org/10.1016/j.semcdb.2015.11.014
  31. Martin BL, Kimelman D : Brachyury establishes the embryonic mesodermal progenitor niche. Genes Dev 24 : 2778-2783, 2010 https://doi.org/10.1101/gad.1962910
  32. Martin BL, Kimelman D : Regulation of canonical Wnt signaling by Brachyury is essential for posterior mesoderm formation. Dev Cell 15 : 121-133, 2008 https://doi.org/10.1016/j.devcel.2008.04.013
  33. Martin BL, Kimelman D : Wnt signaling and the evolution of embryonic posterior development. Curr Biol 19 : R215-R219, 2009 https://doi.org/10.1016/j.cub.2009.01.052
  34. McGrew MJ, Sherman A, Lillico SG, Ellard FM, Radcliffe PA, Gilhooley HJ, et al. : Localised axial progenitor cell populations in the avian tail bud are not committed to a posterior Hox identity. Development 135 : 2289-2299, 2008 https://doi.org/10.1242/dev.022020
  35. Morley RH, Lachani K, Keefe D, Gilchrist MJ, Flicek P, Smith JC, et al. : A gene regulatory network directed by zebrafish No tail accounts for its roles in mesoderm formation. Proc Natl Acad Sci U S A 106 : 3829-3834, 2009 https://doi.org/10.1073/pnas.0808382106
  36. Mugele D, Moulding DA, Savery D, Mole MA, Greene ND, Martinez-Barbera JP, et al. : Genetic approaches in mice demonstrate that neuromesodermal progenitors express T/Brachyury but not Sox2. bioRxiv, 2018 [Epub ahead of print]
  37. Muller F, O'rahilly R : The primitive streak, the caudal eminence and related structures in staged human embryos. Cells Tissues Organs 177 : 2-20, 2004 https://doi.org/10.1159/000078423
  38. Mulvaney J, Dabdoub A : Atoh1, an essential transcription factor in neurogenesis and intestinal and inner ear development: function, regulation, and context dependency. J Assoc Res Otolaryngol 13 : 281-293, 2012 https://doi.org/10.1007/s10162-012-0317-4
  39. Olivera-Martinez I, Harada H, Halley PA, Storey KG : Loss of FGF-dependent mesoderm identity and rise of endogenous retinoid signalling determine cessation of body axis elongation. PLoS Biol 10 : e1001415, 2012 https://doi.org/10.1371/journal.pbio.1001415
  40. Pai YJ, Abdullah NL, Mohd-Zin SW, Mohammed RS, Rolo A, Greene ND, et al. : Epithelial fusion during neural tube morphogenesis. Birth Defects Res A Clin Mol Teratol 94 : 817-823, 2012 https://doi.org/10.1002/bdra.23072
  41. Rodrigo Albors A, Halley PA, Storey KG : Lineage tracing of axial progenitors using Nkx1-2CreERT2 mice defines their trunk and tail contributions. Development 145 : dev164319, 2018 https://doi.org/10.1242/dev.164319
  42. Sadahiro T, Isomi M, Muraoka N, Kojima H, Haginiwa S, Kurotsu S, et al. : Tbx6 induces nascent mesoderm from pluripotent stem cells and temporally controls cardiac versus somite lineage diversification. Cell Stem Cell 23 : 382-395.e5, 2018 https://doi.org/10.1016/j.stem.2018.07.001
  43. Shaker MR, Kim JY, Kim H, Sun W : Identification and characterization of secondary neural tube-derived embryonic neural stem cells in vitro. Stem Cells Dev 24 : 1171-1181, 2015 https://doi.org/10.1089/scd.2014.0506
  44. Shaker MR, Lee JH, Kim KH, Kim VJ, Kim JY, Lee JY, et al. : Spatiotemporal contribution of neuromesodermal progenitor-derived neural cells in the elongation of developing mouse spinal cord. bioRxiv, 2020 [Epub ahead of print]
  45. Shaker MR, Lee JH, Park SH, Kim JY, Son GH, Son JW, et al. : Anteroposterior Wnt-RA gradient defines adhesion and migration properties of neural progenitors in developing spinal cord. Stem Cell Reports 15 : 898-911, 2020 https://doi.org/10.1016/j.stemcr.2020.08.016
  46. Shimokita E, Takahashi Y : Secondary neurulation: fate-mapping and gene manipulation of the neural tube in tail bud. Dev Growth Differ 53 : 401-410, 2011 https://doi.org/10.1111/j.1440-169X.2011.01260.x
  47. Shum AS, Tang LS, Copp AJ, Roelink H : Lack of motor neuron differentiation is an intrinsic property of the mouse secondary neural tube. Dev Dyn 239 : 3192-3203, 2010 https://doi.org/10.1002/dvdy.22457
  48. Tahara N, Kawakami H, Chen KQ, Anderson A, Yamashita Peterson M, Gong W, et al. : Sall4 regulates neuromesodermal progenitors and their descendants during body elongation in mouse embryos. Development 146 : dev177659, 2019 https://doi.org/10.1242/dev.177659
  49. Tsakiridis A, Huang Y, Blin G, Skylaki S, Wymeersch F, Osorno R, et al. : Distinct Wnt-driven primitive streak-like populations reflect in vivo lineage precursors. Development 141 : 1209-1221, 2014 https://doi.org/10.1242/dev.101014
  50. Tzouanacou E, Wegener A, Wymeersch FJ, Wilson V, Nicolas JF : Redefining the progression of lineage segregations during mammalian embryogenesis by clonal analysis. Dev Cell 17 : 365-376, 2009 https://doi.org/10.1016/j.devcel.2009.08.002
  51. Verrier L, Davidson L, Gierlinski M, Dady A, Storey KG : Neural differentiation, selection and transcriptomic profiling of human neuromesodermal progenitor-like cells in vitro. Development 145 : dev166215, 2018 https://doi.org/10.1242/dev.166215
  52. Yang HJ, Lee DH, Lee YJ, Chi JG, Lee JY, Phi JH, et al. : Secondary neurulation of human embryos: morphological changes and the expression of neuronal antigens. Childs Nerv Syst 30 : 73-82, 2014 https://doi.org/10.1007/s00381-013-2192-7