Regulation of Nematostella neural progenitors by SoxB, Notch and bHLH genes

Development (Cambridge)

Volumn 142, Issue 19, 2015, Pages 3332-3342

  Richards, Gemma Sian ^a   Rentzsch, Fabian ^a  

^a UNIVERSITY OF BERGEN   (Norway)

Author keywords

Cnidaria; DAPT; Neurogenesis; Proneural genes

Indexed keywords

BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; GROUP A BASIC HELIX LOOP HELIX PROTEIN; MORPHOLINO OLIGONUCLEOTIDE; NOTCH RECEPTOR; NVASHA PROTEIN; NVATH LIKE PROTEIN; PROTEIN; TRANSCRIPTION FACTOR SOX; UNCLASSIFIED DRUG;

ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; EMBRYO; NEMATOCYST; NEMATOCYTE; NEMATOSTELLA VECTENSIS; NERVE CELL; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; SIGNAL TRANSDUCTION; ANIMAL; CELL CULTURE TECHNIQUE; CYTOLOGY; EMBRYOLOGY; FLUORESCENCE IN SITU HYBRIDIZATION; GENE SILENCING; GENETICS; IMMUNOHISTOCHEMISTRY; METABOLISM; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEA ANEMONE; TRANSGENIC ANIMAL;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL CULTURE TECHNIQUES; GENE KNOCKDOWN TECHNIQUES; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION, FLUORESCENCE; NEURAL STEM CELLS; NEUROGENESIS; RECEPTORS, NOTCH; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEA ANEMONES; SIGNAL TRANSDUCTION; SOXB2 TRANSCRIPTION FACTORS;

EID: 84943535134     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.123745     Document Type: Article

References (60)

1. Agathocleous, M., Iordanova, I., Willardsen, M. I., Xue, X. Y., Vetter, M. L., Harris, W. A. and Moore, K. B. (2009). A directional Wnt/beta-catenin-Sox2-proneural pathway regulates the transition from proliferation to differentiation in the Xenopus retina. Development 136, 3289-3299.
2. Bertrand, N., Castro, D. S. and Guillemot, F. (2002). Proneural genes and the specification of neural cell types. Nat. Rev. Neurosci. 3, 517-530.
3. Bosch, T. C. G. and David, C. N. (1987). Stem cells of Hydra magnipapillata can differentiate into somatic cells and germ line cells. Dev. Biol. 121, 182-191.
4. Buescher, M., Hing, F. and Chia, W. (2002). Formation of neuroblasts in the embryonic central nervous system of Drosophila melanogaster is controlled by SoxNeuro. Development 129, 4193-4203.
5. Bylund, M., Andersson, E., Novitch, B. G. and Muhr, J. (2003). Vertebrate neurogenesis is counteracted by Sox1-3 activity. Nat. Neurosci. 6, 1162-1168.
6. Cau, E., Gradwohl, G., Fode, C. and Guillemot, F. (1997). Mash1 activates a cascade of bHLH regulators in olfactory neuron progenitors. Development 124, 1611-1621.
7. Chao, A. T., Jones, W. M. and Bejsovec, A. (2007). The HMG-box transcription factor SoxNeuro acts with Tcf to control Wg/Wnt signaling activity. Development 134, 989-997.
8. Chapman, J. A., Kirkness, E. F., Simakov, O., Hampson, S. E., Mitros, T., Weinmaier, T., Rattei, T., Balasubramanian, P. G., Borman, J., Busam, D. et al. (2010). The dynamic genome of Hydra. Nature 464, 592-596.
9. Chitnis, A., Henrique, D., Lewis, J., Ish-Horowicz, D. and Kintner, C. (1995). Primary neurogenesis in Xenopus embryos regulated by a homologue of the Drosophila neurogenic gene Delta. Nature 375, 761-766.
10. Eisen, J. S. and Smith, J. C. (2008). Controlling morpholino experiments: don't stop making antisense. Development 135, 1735-1743.
11. Ernsberger, U. (2015). Can the 'neuron theory' be complemented by a universal mechanism for generic neuronal differentiation. Cell Tissue Res. 359, 343-384.
12. Fode, C., Ma, Q., Casarosa, S., Ang, S.-L., Anderson, D. J. and Guillemot, F. (2000). A role for neural determination genes in specifying the dorsoventral identity of telencephalic neurons. Genes Dev. 14, 67-80.
13. Fritzenwanker, J. H. and Technau, U. (2002). Induction of gametogenesis in the basal cnidarian Nematostella vectensis (Anthozoa). Dev. Genes Evol. 212, 99-103.
14. Fritzsch, B., Jahan, I., Pan, N. and Elliott, K. L. (2015). Evolving gene regulatory networks into cellular networks guiding adaptive behavior: an outline how single cells could have evolved into a centralized neurosensory system. Cell Tissue Res. 359, 295-313.
15. Galliot, B., Quiquand, M., Ghila, L., de Rosa, R., Miljkovic-Licina, M. and Chera, S. (2009). Origins of neurogenesis, a cnidarian view. Dev. Biol. 332, 2-24.
16. Guillemot, F. (2007). Spatial and temporal specification of neural fates by transcription factor codes. Development 134, 3771-3780.
17. Hartenstein, V. and Wodarz, A. (2013). Initial neurogenesis in Drosophila. Wiley Interdiscip. Rev. Dev. Biol. 2, 701-721.
18. Hejnol, A., Obst, M., Stamatakis, A., Ott, M., Rouse, G. W., Edgecombe, G. D., Martinez, P., Baguñà, J., Bailly, X., Jondelius, U. et al. (2009). Assessing the root of bilaterian animals with scalable phylogenomic methods. Proc. R. Soc. B Biol. Sci. 276, 4261-4270.
19. Holmberg, J., Hansson, E., Malewicz, M., Sandberg, M., Perlmann, T., Lendahl, U. and Muhr, J. (2008). SoxB1 transcription factors and Notch signaling use distinct mechanisms to regulate proneural gene function and neural progenitor differentiation. Development 135, 1843-1851.
20. Imayoshi, I. and Kageyama, R. (2014). bHLH factors in self-renewal, multipotency, and fate choice of neural progenitor cells. Neuron 82, 9-23.
21. Jager, M., Quéinnec, E., Le Guyader, H. and Manuel, M. (2011). Multiple Sox genes are expressed in stem cells or in differentiating neuro-sensory cells in the hydrozoan Clytia hemisphaerica. EvoDevo 2, 12.
22. Jarman, A. P., Grell, E. H., Ackerman, L., Jan, L. Y. and Jan, Y. N. (1994). Atonal is the proneural gene for Drosophila photoreceptors. Nature 369, 398-400.
23. Käsbauer, T., Towb, P., Alexandrova, O., David, C. N., Dall'Armi, E., Staudigl, A., Stiening, B. and Böttger, A. (2007). The Notch signaling pathway in the cnidarian Hydra. Dev. Biol. 303, 376-390.
24. Kerner, P., Simionato, E., Le Gouar, M. and Vervoort, M. (2009). Orthologs of key vertebrate neural genes are expressed during neurogenesis in the annelid Platynereis dumerilii. Evol. Dev. 11, 513-524.
25. Kiefer, J. C. (2007). Back to basics: Sox genes. Dev. Dyn. 236, 2356-2366.
26. Kusserow, A., Pang, K., Sturm, C., Hrouda, M., Lentfer, J., Schmidt, H.A., Technau, U., von Haeseler, A., Hobmayer, B., Martindale, M. Q. et al. (2005). Unexpected complexity of the Wnt gene family in a sea anemone. Nature 433, 156-160.
27. Layden, M. J. and Martindale, M.Q. (2014). Non-canonicalNotch signaling represents an ancestral mechanism to regulate neural differentiation. EvoDevo 5, 30.
28. Layden, M. J., Boekhout, M. and Martindale, M. Q. (2012). Nematostella vectensis achaete-scute homolog NvashA regulates embryonic ectodermal neurogenesis and represents an ancient component of the metazoan neural specification pathway. Development 139, 1013-1022.
29. Lee, J. E. (1997). Basic helix-loop-helix genes in neural development. Curr. Opin. Neurobiol. 7, 13-20.
30. Lehmann, R., Jiménez, F., Dietrich, U. and Campos-Ortega, J. A. (1983). On the phenotype and development of mutants of early neurogenesis in Drosophila melanogaster. Roux's Arch. Dev. Biol. 192, 62-74.
31. Louvi, A. and Artavanis-Tsakonas, S. (2006). Notch signalling in vertebrate neural development. Nat. Rev. Neurosci. 7, 93-102.
32. Lowe, C. J., Wu, M., Salic, A., Evans, L., Lander, E., Stange-Thomann, N., Gruber, C. E., Gerhart, J. and Kirschner, M. (2003). Anteroposterior patterning in hemichordates and the origins of the chordate nervous system. Cell 113, 853-865.
33. Magie, C. R., Pang, K. and Martindale, M. Q. (2005). Genomic inventory and expression of Sox and Fox genes in the cnidarian Nematostella vectensis. Dev. Genes Evol. 215, 618-630.
34. Marlow, H. Q., Srivastava, M., Matus, D. Q., Rokhsar, D. and Martindale, M. Q. (2009). Anatomy and development of the nervous system of Nematostella vectensis, an anthozoan cnidarian. Dev. Neurobiol. 69, 235-254.
35. Marlow, H., Roettinger, E., Boekhout, M. and Martindale, M. Q. (2012). Functional roles of Notch signaling in the cnidarian Nematostella vectensis. Dev. Biol. 362, 295-308.
36. Marlow, H., Matus, D. Q. and Martindale, M. Q. (2013). Ectopic activation of the canonical wnt signaling pathway affects ectodermal patterning along the primary axis during larval development in the anthozoan Nematostella vectensis. Dev. Biol. 380, 324-334.
37. Martinez-Morales, P. L., Quiroga, A. C., Barbas, J. A. and Morales, A. V. (2010). SOX5 controls cell cycle progression in neural progenitors by interfering with the WNT-beta-catenin pathway. EMBO Rep. 11, 466-472.
38. Micchelli, C., Esler, W., Kimberly, W., Jack, C., Berezovska, O., Kornilova, A., Hyman, B., Perrimon, N. and Wolfe, M. (2003). Gamma-secretase/presenilin inhibitors for Alzheimer's disease phenocopy Notch mutations in Drosophila. FASEB J. 17, 79-81.
39. Nakanishi, N., Renfer, E., Technau, U. and Rentzsch, F. (2012). Nervous systems of the sea anemone Nematostella vectensis are generated by ectoderm and endoderm and shaped by distinct mechanisms. Development 139, 347-357.
40. Ninkovic, J. and Gotz, M. (2014). A time and place for understanding neural stem cell specification. Dev. Cell 30, 114-115.
41. Overton, P., Meadows, L., Urban, J. and Russell, S. (2002). Evidence for differential and redundant function of the Sox genes Dichaete and SoxN during CNS development in Drosophila. Development 129, 4219-4228.
42. Overton, P. M., Chia, W. and Buescher, M. (2007). The Drosophila HMG-domain proteins SoxNeuro and Dichaete direct trichome formation via the activation of shavenbaby and the restriction of Wingless pathway activity. Development 134, 2807-2813.
43. Pick, K. S., Philippe, H., Schreiber, F., Erpenbeck, D., Jackson, D. J., Wrede, P., Wiens, M., Alie, A., Morgenstern, B., Manuel, M. et al. (2010). Improved phylogenomic taxon sampling noticeably affects nonbilaterian relationships. Mol. Biol. Evol. 27, 1983-1987.
44. Pierfelice, T., Alberi, L. and Gaiano, N. (2011). Notch in the vertebrate nervous system: an old dog with new tricks. Neuron 69, 840-855.
45. Pioro, H. L. and Stollewerk, A. (2006). The expression pattern of genes involved in early neurogenesis suggests distinct and conserved functions in the diplopod Glomeris marginata. Dev. Genes Evol. 216, 417-430.
46. Putnam, N. H., Srivastava, M., Hellsten, U., Dirks, B., Chapman, J., Salamov, A., Terry, A., Shapiro, H., Lindquist, E., Kapitonov, V. V. et al. (2007). Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization. Science 317, 86-94.
47. Reiprich, S. and Wegner, M. (2015). From CNS stem cells to neurons and glia: Sox for everyone. Cell Tissue Res. 359, 111-124.
48. Rentzsch, F., Fritzenwanker, J. H., Scholz, C. B. and Technau, U. (2008). FGF signalling controls formation of the apical sensory organ in the cnidarian Nematostella vectensis. Development 135, 1761-1769.
49. Richards, G. S. and Rentzsch, F. (2014). Transgenic analysis of a SoxB gene reveals neural progenitor cells in the cnidarian Nematostella vectensis. Development 141, 4681-4689.
50. Sandberg, M., Källström, M. and Muhr, J. (2005). Sox21 promotes the progression of vertebrate neurogenesis. Nat. Neurosci. 8, 995-1001.
51. Simionato, E., Ledent, V., Richards, G., Thomas-Chollier, M., Kerner, P., Coornaert, D., Degnan, B. M. and Vervoort, M. M. (2007). Origin and diversification of the basic helix-loop-helix gene family in metazoans: insights from comparative genomics. BMC Evol. Biol. 7, 33.
52. Sommer, L., Ma, Q. and Anderson, D. J. (1996). neurogenins, a novel family of atonal-related bHLH transcription factors, are putative mammalian neuronal determination genes that reveal progenitor cell heterogeneity in the developing CNS and PNS. Mol. Cell. Neurosci. 8, 221-241.
53. Szczepanek, S., Cikala, M. and David, C.N. (2002). Poly-gamma-glutamate synthesis during formation of nematocyst capsules in Hydra. J. Cell Sci. 115, 745-751.
54. Technau, U. and Steele, R. E. (2011). Evolutionary crossroads in developmental biology: Cnidaria. Development 138, 1447-1458.
55. Uy, B. R., Simoes-Costa, M., Sauka-Spengler, T. and Bronner, M. E. (2012). Expression of Sox family genes in early lamprey development. Int. J. Dev. Biol. 56, 377-383.
56. Watanabe, H., Fujisawa, T. and Holstein, T. (2009). Cnidarians and the evolutionary origin of the nervous system. Dev. Growth Differ. 51, 167-183.
57. Watanabe, H., Kuhn, A., Fushiki, M., Agata, K., Özbek, S., Fujisawa, T. and Holstein, T. W. (2014). Sequential actions of beta-catenin and Bmp pattern the oral nerve net in Nematostella vectensis. Nat. Commun. 5, 5536.
58. Whittington, N., Cunningham, D., Le, T.-K., De Maria, D. and Silva, E. M. (2015). Sox21 regulates the progression of neuronal differentiation in a dose-dependent manner. Dev. Biol. 397, 237-247.
59. Zenkert, C., Takahashi, T., Diesner, M.-O. and Özbek, S. (2011). Morphological and molecular analysis of the Nematostella vectensis cnidom. PLoS ONE 6, e22725.
60. Zhao, G. and Skeath, J. (2002). The Sox-domain containing gene Dichaete/fishhook acts in concert with vnd and ind to regulate cell fate in the Drosophila neuroectoderm. Development 129, 1165-1174.