Unc5C and DCC act downstream of Ctip2 and Satb2 and contribute to corpus callosum formation

Nature Communications

Volumn 5, Issue , 2014, Pages

  Srivatsa, Swathi ^a,b   Parthasarathy, Srinivas ^a,b   Britanova, Olga ^a,c   Bormuth, Ingo ^a   Donahoo, Amber Lee ^d   Ackerman, Susan L ^e   Richards, Linda J ^d   Tarabykin, Victor ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b MAX PLANCK INSTITUTE OF EXPERIMENTAL MEDICINE   (Germany)

^c SHEMYAKIN OVCHINNIKOV INSTITUTE OF BIOORGANIC CHEMISTRY   (Russian Federation)

^d UNIVERSITY OF QUEENSLAND   (Australia)

^e HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NETRIN 1; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR CTIP2; TRANSCRIPTION FACTOR DCC; TRANSCRIPTION FACTOR UNC5C; TRANSCRIPTION FACTORS SATB2; UNCLASSIFIED DRUG; CELL SURFACE RECEPTOR; DCC PROTEIN, MOUSE; LUCIFERASE; NERVE GROWTH FACTOR RECEPTOR; PRIMER DNA; TUMOR SUPPRESSOR PROTEIN; UNC5C PROTEIN, MOUSE;

BRAIN; GENE EXPRESSION; MAMMAL; MOLECULAR ANALYSIS; NEUROLOGY; SPHERE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL FATE; CONTROLLED STUDY; CORPUS CALLOSUM; EMBRYO; HUMAN; HUMAN CELL; MOLECULE; MOUSE; NERVE FIBER; NONHUMAN; PROTEIN EXPRESSION; PYRAMIDAL NERVE CELL; ANIMAL; CHROMATIN IMMUNOPRECIPITATION; ELECTROPORATION; EMBRYOLOGY; GENE EXPRESSION REGULATION; GENETICS; IN SITU HYBRIDIZATION; METABOLISM; MORPHOGENESIS; PHYSIOLOGY; PLASMID; PROCEDURES;

ANIMALS; CHROMATIN IMMUNOPRECIPITATION; CORPUS CALLOSUM; DNA PRIMERS; ELECTROPORATION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; IN SITU HYBRIDIZATION; LUCIFERASES; MICE; MORPHOGENESIS; PLASMIDS; RECEPTORS, CELL SURFACE; RECEPTORS, NERVE GROWTH FACTOR; TUMOR SUPPRESSOR PROTEINS;

EID: 84898811199     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms4708     Document Type: Article

References (42)

1. Richards, L. J., Koester, S. E., Tuttle, R. & O'Leary, D. D. Directed growth of early cortical axons is influenced by a chemoattractant released from an intermediate target. J. Neurosci. 17, 2445-2458 (1997). (Pubitemid 27137411)
2. Kriegstein, A., Noctor, S. & Martinez-Cerdeno, V. Patterns of neural stem and progenitor cell division may underlie evolutionary cortical expansion. Nat. Rev. Neurosci. 7, 883-890 (2006). (Pubitemid 44624180)
3. Marin-Padilla, M. Ontogenesis of the pyramidal cell of the mammalian neocortex and developmental cytoarchitectonics: a unifying theory. J. Comp. Neurol. 321, 223-240 (1992).
4. Hill, R. S. & Walsh, C. A. Molecular insights into human brain evolution. Nature 437, 64-67 (2005). (Pubitemid 41613427)
5. Richards, L. J., Plachez, C. & Ren, T. Mechanisms regulating the development of the corpus callosum and its agenesis in mouse and human. Clin. Genet. 66, 276-289 (2004). (Pubitemid 39317630)
6. Arlotta, P. et al. Neuronal subtype-specific genes that control corticospinal motor neuron development in vivo. Neuron 45, 207-221 (2005). (Pubitemid 40136579)
7. Alcamo, E. A. et al. Satb2 regulates callosal projection neuron identity in the developing cerebral cortex. Neuron 57, 364-377 (2008). (Pubitemid 351179160)
8. Britanova, O. et al. Satb2 is a postmitotic determinant for upper-layer neuron specification in the neocortex. Neuron 57, 378-392 (2008). (Pubitemid 351179166)
9. Szemes, M., Gyorgy, A., Paweletz, C., Dobi, A. & Agoston, D. V. Isolation and characterization of SATB2, a novel AT-rich DNA binding protein expressed in development-and cell-specific manner in the rat brain. Neurochem. Res. 31, 237-246 (2006).
10. Kennedy, T. E., Serafini, T., de la Torre, J. R. & Tessier-Lavigne, M. Netrins are diffusible chemotropic factors for commissural axons in the embryonic spinal cord. Cell 78, 425-435 (1994). (Pubitemid 24250807)
11. Keino-Masu, K. et al. Deleted in colorectal cancer (DCC) encodes a netrin receptor. Cell 87, 175-185 (1996). (Pubitemid 26358997)
12. Serafini, T. et al. Netrin-1 is required for commissural axon guidance in the developing vertebrate nervous system. Cell 87, 1001-1014 (1996). (Pubitemid 26427984)
13. Ackerman, S. L. et al. The mouse rostral cerebellar malformation gene encodes an UNC-5-like protein. Nature 386, 838-842 (1997). (Pubitemid 27181258)
14. Metin, C., Deleglise, D., Serafini, T., Kennedy, T. E. & Tessier-Lavigne, M. A role for netrin-1 in the guidance of cortical efferents. Development 124, 5063-5074 (1997). (Pubitemid 28025130)
15. Finger, J. H. et al. The netrin 1 receptors Unc5h3 and Dcc are necessary at multiple choice points for the guidance of corticospinal tract axons. J. Neurosci. 22, 10346-10356 (2002). (Pubitemid 35416872)
16. Hong, K. et al. A ligand-gated association between cytoplasmic domains of UNC5 and DCC family receptors converts netrin-induced growth cone attraction to repulsion. Cell 97, 927-941 (1999). (Pubitemid 29375051)
17. Su, M. et al. Regulation of the UNC-5 netrin receptor initiates the first reorientation of migrating distal tip cells in Caenorhabditis elegans. Development 127, 585-594 (2000). (Pubitemid 30093406)
18. Gitai, Z., Yu, T. W., Lundquist, E. A., Tessier-Lavigne, M. & Bargmann, C. I. The netrin receptor UNC-40/DCC stimulates axon attraction and outgrowth through enabled and, in parallel, Rac and UNC-115/AbLIM. Neuron 37, 53-65 (2003). (Pubitemid 36106433)
19. Srinivasan, K. et al. A network of genetic repression and derepression specifies projection fates in the developing neocortex. Proc. Natl Acad. Sci. USA 109, 19071-19078 (2012).
20. Baranek, C. et al. Protooncogene Ski cooperates with the chromatin-remodeling factor Satb2 in specifying callosal neurons. Proc. Natl Acad. Sci. USA 109, 3546-3551 (2012).
21. Barallobre, M. J. et al. Aberrant development of hippocampal circuits and altered neural activity in netrin 1-deficient mice. Development 127, 4797-4810 (2000).
22. Fazeli, A. et al. Phenotype of mice lacking functional Deleted in colorectal cancer (Dcc) gene. Nature 386, 796-804 (1997). (Pubitemid 27181247)
23. Molyneaux, B. J. et al. Novel subtype-specific genes identify distinct subpopulations of callosal projection neurons. J. Neurosci. 29, 12343-12354 (2009).
24. Lickiss, T., Cheung, A. F., Hutchinson, C. E., Taylor, J. S. & Molnar, Z. Examining the relationship between early axon growth and transcription factor expression in the developing cerebral cortex. J. Anat. 220, 201-211 (2012).
25. Hedgecock, E. M., Culotti, J. G. & Hall, D. H. The unc-5, unc-6, and unc-40 genes guide circumferential migrations of pioneer axons and mesodermal cells on the epidermis in C. elegans. Neuron 4, 61-85 (1990). (Pubitemid 20149756)
26. Hamelin, M., Zhou, Y., Su, M. W., Scott, I. M. & Culotti, J. G. Expression of the UNC-5 guidance receptor in the touch neurons of C. elegans steers their axons dorsally. Nature 364, 327-330 (1993).
27. Colamarino, S. A. & Tessier-Lavigne, M. The axonal chemoattractant netrin-1 is also a chemorepellent for trochlear motor axons. Cell 81, 621-629 (1995).
28. Kim, D. & Ackerman, S. L. The UNC5C netrin receptor regulates dorsal guidance of mouse hindbrain axons. J. Neurosci. 31, 2167-2179 (2011).
29. Islam, S. M. et al. Draxin, a repulsive guidance protein for spinal cord and forebrain commissures. Science 323, 388-393 (2009).
30. Ahmed, G. et al. Draxin inhibits axonal outgrowth through the netrin receptor DCC. J. Neurosci. 31, 14018-14023 (2011).
31. Ren, T., Zhang, J., Plachez, C., Mori, S. & Richards, L. J. Diffusion tensor magnetic resonance imaging and tract-tracing analysis of Probst bundle structure in Netrin1-and DCC-deficient mice. J. Neurosci. 27, 10345-10349 (2007). (Pubitemid 47501989)
32. Fothergill, T. et al. Netrin-DCC signaling regulates corpus callosum formation through attraction of pioneering axons and by modulating Slit2-mediated repulsion. Cereb. Cortex. doi:10.1093/cercor/bhs395 (2013).
33. Muramatsu, R. et al. The ratio of 'deleted in colorectal cancer' to 'uncoordinated-5A' netrin-1 receptors on the growth cone regulates mossy fibre directionality. Brain 133, 60-75 (2010).
34. Garcez, P. P. et al. Axons of callosal neurons bifurcate transiently at the white matter before consolidating an interhemispheric projection. Eur. J. Neurosci. 25, 1384-1394 (2007). (Pubitemid 46568759)
35. Wakabayashi, Y. et al. Bcl11b is required for differentiation and survival of alphabeta T lymphocytes. Nat. Immunol. 4, 533-539 (2003). (Pubitemid 36701335)
36. Britanova, O. et al. Satb2 haploinsufficiency phenocopies 2q32-q33 deletions, whereas loss suggests a fundamental role in the coordination of jaw development. Am. J. Hum. Genet. 79, 668-678 (2006). (Pubitemid 44452744)
37. Rosoff, W. J., McAllister, R, Esrick, M. A., Goodhill, G. J. & Urbach, J. S. Generating controlled molecular gradients in 3D gels. Biotechnol. Bioeng. 91, 754-759 (2005). (Pubitemid 41283868)
38. Mortimer, D. et al. Bayesian model predicts the response of axons to molecular gradients. Proc. Natl Acad. Sci. USA 106, 10296-10301 (2009).
39. Saito, T. In vivo electroporation in the embryonic mouse central nervous system. Nat. Protoc. 1, 1552-1558 (2006).
40. Nehme, B., Henry, M. & Mouginot, D. Combined fluorescent in situ hybridization and immunofluorescence: limiting factors and a substitution strategy for slide-mounted tissue sections. J. Neurosci. Methods. 196, 281-288 (2011).
41. Polleux, F. & Ghosh, A. The slice overlay assay: a versatile tool to study the influence of extracellular signals on neuronal development. Sci. STKE. 2002, pl9 (2002).
42. Seuntjens, E. et al. Sip1 regulates sequential fate decisions by feedback signaling from postmitotic neurons to progenitors. Nat. Neurosci. 12, 1373-1380 (2009).