C. Elegans SoxB genes are dispensable for embryonic neurogenesis but required for terminal differentiation of specific neuron types

Development (Cambridge)

Volumn 142, Issue 14, 2015, Pages 2464-2477

  Vidal, Berta ^a   Santella, Anthony ^b   Serrano Sai, Esther ^a   Bao, Zhirong ^b   Chuang, Chiou Fen ^c   Hobert, Oliver ^a  

^a Department of Medicine   (United States)

^b MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^c UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

Caenorhabditis elegans; Neurogenesis; Sox genes

Indexed keywords

TRANSCRIPTION FACTOR SOX; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; CAENORHABDITIS ELEGANS PROTEIN;

ALLELE; ARTICLE; BLAST CELL; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; GENE FUNCTION; LARVAL DEVELOPMENT; MOLECULAR PHYLOGENY; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; ANIMAL; CELL DIFFERENTIATION; CELL LINEAGE; CYTOLOGY; EMBRYOLOGY; GENE EXPRESSION REGULATION; MALE; METABOLISM; MOTONEURON; MUTATION; NERVE CELL; NERVOUS SYSTEM; PHYSIOLOGY; SIGNAL TRANSDUCTION; TRANSGENE;

CAENORHABDITIS ELEGANS;

ALLELES; ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CELL DIFFERENTIATION; CELL LINEAGE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MALE; MOTOR NEURONS; MUTATION; NERVOUS SYSTEM; NEUROGENESIS; NEURONS; SIGNAL TRANSDUCTION; SOXB1 TRANSCRIPTION FACTORS; SOXC TRANSCRIPTION FACTORS; TRANSGENES;

EID: 84937820338     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.125740     Document Type: Article

References (62)

1. Bao, Z., Murray, J. I., Boyle, T., Ooi, S. L., Sandel, M. J. and Waterston, R. H. (2006). Automated cell lineage tracing in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 103, 2707-2712.
2. Basson, M. and Horvitz, H. R. (1996). The Caenorhabditis elegans gene sem-4 controls neuronal and mesodermal cell development and encodes a zinc finger protein. Genes Dev. 10, 1953-1965.
3. Bergsland, M., Werme, M., Malewicz, M., Perlmann, T. and Muhr, J. (2006). The establishment of neuronal properties is controlled by Sox4 and Sox11. Genes Dev. 20, 3475-3486.
4. Bertrand, N., Castro, D. S. and Guillemot, F. (2002). Proneural genes and the specification of neural cell types. Nat. Rev. Neurosci. 3, 517-530.
5. Bowles, J., Schepers, G. and Koopman, P. (2000). Phylogeny of the SOX family of developmental transcription factors based on sequence and structural indicators. Dev. Biol. 227, 239-255.
6. Buescher, M., Hing, F. S. and Chia, W. (2002). Formation of neuroblasts in the embryonic central nervous system of Drosophila melanogaster is controlled by SoxNeuro. Development 129, 4193-4203.
7. Burglin, T. R. and Ruvkun, G. (2001).Regulation of ectodermal and excretory function by the C. elegans POU homeobox gene ceh-6. Development 128, 779-790.
8. Burke, R. D., Moller, D. J., Krupke, O. A. and Taylor, V. J. (2014). Sea urchin neural development and the metazoan paradigm of neurogenesis. Genesis 52, 208-221.
9. Bylund, M., Andersson, E., Novitch, B. G. and Muhr, J. (2003). Vertebrate neurogenesis is counteracted by Sox1–3 activity. Nat. Neurosci. 6, 1162-1168.
10. Cavallaro, M., Mariani, J., Lancini, C., Latorre, E., Caccia, R., Gullo, F., Valotta, M., DeBiasi, S., Spinardi, L., Ronchi, A. et al. (2008). Impaired generation of mature neurons by neural stem cells from hypomorphic Sox2 mutants. Development 135, 541-557.
11. Chamberlin, H. M., Brown, K. B., Sternberg, P. W. and Thomas, J. H. (1999). Characterization of seven genes affecting Caenorhabditis elegans hindgut development. Genetics 153, 731-742.
12. Chisholm, A. (1991). Control of cell fate in the tail region of C. elegans by the gene egl-5. Development 111, 921-932.
13. Chisholm, A. D. and Hodgkin, J. (1989). The mab-9 gene controls the fate of B, the major male-specific blast cell in the tail region of Caenorhabditis elegans. Genes Dev. 3, 1413-1423.
14. Ekonomou, A., Kazanis, I., Malas, S., Wood, H., Alifragis, P., Denaxa, M., Karagogeos, D., Constanti, A., Lovell-Badge, R. and Episkopou, V. (2005). Neuronal migration and ventral subtype identity in the telencephalon depend on SOX1. PLoS Biol. 3, e186.
15. Ferrero, E., Fischer, B. and Russell, S. (2014). SoxNeuro orchestrates central nervous system specification and differentiation in Drosophila and is only partially redundant with Dichaete. Genome Biol. 15, R74.
16. Frøkjaer-Jensen, C., Davis, M. W., Hollopeter, G., Taylor, J., Harris, T. W., Nix, P., Lofgren, R., Prestgard-Duke, M., Bastiani, M., Moerman, D. G. et al. (2010). Targeted gene deletions in C. elegans using transposon excision. Nat. Methods 7, 451-453.
17. 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.
18. Girard, F., Joly, W., Savare, J., Bonneaud, N., Ferraz, C. and Maschat, F. (2006). Chromatin immunoprecipitation reveals a novel role for the Drosophila SoxNeuro transcription factor in axonal patterning. Dev. Biol. 299, 530-542.
19. Guth, S. I. E. and Wegner, M. (2008). Having it both ways: Sox protein function between conservation and innovation. Cell. Mol. Life Sci. 65, 3000-3018.
20. Hobert, O. (2011). Regulation of terminal differentiation programs in the nervous system. Annu. Rev. Cell Dev. Biol. 27, 681-696.
21. Huang, X., Tian, E., Xu, Y. and Zhang, H. (2009). The C. elegans engrailed homolog ceh-16 regulates the self-renewal expansion division of stem cell-like seam cells. Dev. Biol. 333, 337-347.
22. 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.
23. Jarriault, S., Schwab, Y. and Greenwald, I. (2008). A Caenorhabditis elegans model for epithelial-neuronal transdifferentiation. Proc. Natl. Acad. Sci. USA 105, 3790-3795.
24. Johnson, A. D., Fitzsimmons, D., Hagman, J. and Chamberlin, H. M. (2001). EGL-38 Pax regulates the ovo-related gene lin-48 during Caenorhabditis elegans organ development. Development 128, 2857-2865.
25. Kagias, K., Ahier, A., Fischer, N. and Jarriault, S. (2012). Members of the NODE (Nanog and Oct4-associated deacetylase) complex and SOX-2 promote the initiation of a natural cellular reprogramming event in vivo. Proc. Natl. Acad. Sci. USA 109, 6596-6601.
26. 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.
27. Kirilly, D., Gu, Y., Huang, Y., Wu, Z., Bashirullah, A., Low, B. C., Kolodkin, A. L., Wang, H. and Yu, F. (2009). A genetic pathway composed of Sox14 and Mical governs severing of dendrites during pruning. Nat. Neurosci. 12, 1497-1505.
28. Kondoh, H. and Kamachi, Y. (2010). SOX–partner code for cell specification: Regulatory target selection and underlying molecular mechanisms. Int. J. Biochem. Cell Biol. 42, 391-399.
29. Kondoh, H., Uchikawa, M. and Kamachi, Y. (2004). Interplay of Pax6 and SOX2 in lens development as a paradigm of genetic switch mechanisms for cell differentiation. Int. J. Dev. Biol. 48, 819-827.
30. Köppen, M., Simske, J. S., Sims, P. A., Firestein, B. L., Hall, D. H., Radice, A. D., Rongo, C. and Hardin, J. D. (2001). Cooperative regulation of AJM-1 controls junctional integrity in Caenorhabditis elegans epithelia. Nat. Cell Biol. 3, 983-991.
31. Korzelius, J., The, I., Ruijtenberg, S., Portegijs, V., Xu, H., Horvitz, H. R. and van den Heuvel, S. (2011). C. elegans MCM-4 is a general DNA replication and checkpoint component with an epidermis-specific requirement for growth and viability. Dev. Biol. 350, 358-369.
32. Kratsios, P., Stolfi, A., Levine, M. and Hobert, O. (2012). Coordinated regulation of cholinergic motor neuron traits through a conserved terminal selector gene. Nat. Neurosci. 15, 205-214.
33. Mango, S. E. (2007). The C. elegans pharynx: a model for organogenesis. WormBook, 1-26.
34. Mu, L., Berti, L., Masserdotti, G., Covic, M., Michaelidis, T. M., Doberauer, K., Merz, K., Rehfeld, F., Haslinger, A., Wegner, M. et al. (2012). SoxC transcription factors are required for neuronal differentiation in adult hippocampal neurogenesis. J. Neurosci. 32, 3067-3080.
35. Murray, J. I., Bao, Z., Boyle, T. J., Boeck, M. E., Mericle, B. L., Nicholas, T. J., Zhao, Z., Sandel, M. J. and Waterston, R. H. (2008). Automated analysis of embryonic gene expression with cellular resolution in C. elegans. Nat. Methods 5, 703-709.
36. Okuda, Y., Ogura, E., Kondoh, H. and Kamachi, Y. (2010). B1 SOX coordinate cell specification with patterning and morphogenesis in the early zebrafish embryo. PLoS Genet. 6, e1000936.
37. Overton, P. M., Meadows, L. A., 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.
38. Panayi, H., Panayiotou, E., Orford, M., Genethliou, N., Mean, R., Lapathitis, G., Li, S., Xiang, M., Kessaris, N., Richardson, W. D. et al. (2010). Sox1 is required for the specification of a novel p2-derived interneuron subtype in the mouse ventral spinal cord. J. Neurosci. 30, 12274-12280.
39. Pevny, L. H. and Nicolis, S. K. (2010). Sox2 roles in neural stem cells. Int. J. Biochem. Cell Biol. 42, 421-424.
40. Pevny, L. and Placzek, M. (2005). SOX genes and neural progenitor identity. Curr. Opin. Neurobiol. 15, 7-13.
41. Phochanukul, N. and Russell, S. (2010). No backbone but lots of Sox: invertebrate Sox genes. Int. J. Biochem. Cell Biol. 42, 453-464.
42. Reiprich, S. and Wegner, M. (2014). From CNS stem cells to neurons and glia: sox for everyone. Cell Tissue Res. 359, 111-124.
43. 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.
44. Ritter, A. R. and Beckstead, R. B. (2010). Sox14 is required for transcriptional and developmental responses to 20-hydroxyecdysone at the onset of drosophila metamorphosis. Dev. Dyn. 239, 2685-2694.
45. Rizzoti, K., Brunelli, S., Carmignac, D., Thomas, P. Q., Robinson, I. C. and Lovell-Badge, R. (2004). SOX3 is required during the formation of the hypothalamo-pituitary axis. Nat. Genet. 36, 247-255.
46. Sandberg, M., Källström, M. and Muhr, J. (2005). Sox21 promotes the progression of vertebrate neurogenesis. Nat. Neurosci. 8, 995-1001.
47. Santella, A., Du, Z., Nowotschin, S., Hadjantonakis, A.-K. and Bao, Z. (2010). A hybrid blob-slice model for accurate and efficient detection of fluorescence labeled nuclei in 3D. BMC Bioinformatics 11, 580.
48. Sarkar, A. and Hochedlinger, K. (2013). The sox family of transcription factors: versatile regulators of stem and progenitor cell fate. Cell Stem Cell 12, 15-30.
49. Schnabel, R., Hutter, H., Moerman, D. and Schnabel, H. (1997). Assessing normal embryogenesis in Caenorhabditis elegans using a 4D microscope: variability of development and regional specification. Dev. Biol. 184, 234-265.
50. Schnitzler, C. E., Simmons, D. K., Pang, K., Martindale, M. Q. and Baxevanis, A. D. (2014). Expression of multiple Sox genes through embryonic development in the ctenophore Mnemiopsis leidyi is spatially restricted to zones of cell proliferation. EvoDevo 5, 15.
51. Serrano-Saiz, E., Poole, R. J., Felton, T., Zhang, F., De La Cruz, E. D. and Hobert, O. (2013). Modular control of glutamatergic neuronal identity in C. elegans by distinct homeodomain proteins. Cell 155, 659-673.
52. Shinzato, C., Iguchi, A., Hayward, D. C., Technau, U., Ball, E. E. and Miller, D. J. (2008). Sox genes in the coral Acropora millepora: divergent expression patterns reflect differences in developmental mechanisms within the Anthozoa. BMC Evol. Biol. 8, 311.
53. Sulston, J. E. and Horvitz, H. R. (1977). Post-embryonic cell lineages of the nematode, Caenorhabditis elegans. Dev. Biol. 56, 110-156.
54. Taguchi, S., Tagawa, K., Humphreys, T. and Satoh, N. (2002). Group B sox genes that contribute to specification of the vertebrate brain are expressed in the apical organ and ciliary bands of hemichordate larvae. Zoolog. Sci. 19, 57-66.
55. Takahashi, K. and Yamanaka, S. (2006). Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126, 663-676.
56. Taranova, O. V., Magness, S. T., Fagan, B. M., Wu, Y., Surzenko, N., Hutton, S. R. and Pevny, L. H. (2006). SOX2 is a dose-dependent regulator of retinal neural progenitor competence. Genes Dev. 20, 1187-1202.
57. Tian, C., Shi, H., Colledge, C., Stern, M., Waterston, R. and Liu, J. (2011). The C. elegans SoxC protein SEM-2 opposes differentiation factors to promote a proliferative blast cell fate in the postembryonic mesoderm. Development 138, 1033-1043.
58. Tursun, B., Cochella, L., Carrera, I. and Hobert, O. (2009).Atoolkit and robust pipeline for the generation of fosmid-based reporter genes in C. elegans. PLoSONE4, e4625.
59. Wang, B. B., Müller-Immergluck, M. M., Austin, J., Robinson, N. T., Chisholm, A. and Kenyon, C. (1993). A homeotic gene cluster patterns the anteroposterior body axis of C. elegans. Cell 74, 29-42.
60. Woollard, A. and Hodgkin, J. (2000). The caenorhabditis elegans fate-determining gene mab-9 encodes a T-box protein required to pattern the posterior hindgut. Genes Dev. 14, 596-603.
61. Wu, Y., Ghitani, A., Christensen, R., Santella, A., Du, Z., Rondeau, G., Bao, Z., Colon-Ramos, D. and Shroff, H. (2011). Inverted selective plane illumination microscopy (iSPIM) enables coupled cell identity lineaging and neurodevelopmental imaging in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 108, 17708-17713.
62. Zhang, F., Bhattacharya, A., Nelson, J. C., Abe, N., Gordon, P., Lloret- Fernandez, C., Maicas, M., Flames, N., Mann, R. S., Colon-Ramos, D. A. et al. (2014). The LIM and POU homeobox genes ttx-3 and unc-86 act as terminal selectors in distinct cholinergic and serotonergic neuron types. Development 141, 422-435.