Dbx1 triggers crucial molecular programs required for midline crossing by midbrain commissural axons

Development (Cambridge)

Volumn 141, Issue 6, 2014, Pages 1260-1271

  Inamata, Yasuyuki ^a   Shirasaki, Ryuichi ^a  

^a OSAKA UNIVERSITY   (Japan)

Author keywords

Axon guidance; Commissural neurons; Dbx1; Midline crossing; Mouse; Robo3; Transcriptional program

Indexed keywords

ARTICLE; HUMAN; MESENCEPHALON; PRIORITY JOURNAL;

AXON GUIDANCE; COMMISSURAL NEURONS; DBX1; MIDLINE CROSSING; MOUSE; ROBO3; TRANSCRIPTIONAL PROGRAM;

ANIMALS; AXONS; BODY PATTERNING; ENHANCER ELEMENTS, GENETIC; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE KNOCKDOWN TECHNIQUES; HOMEODOMAIN PROTEINS; MEMBRANE PROTEINS; MESENCEPHALON; MICE; MICE, INBRED ICR; MICE, TRANSGENIC; NERVE TISSUE PROTEINS; NEURAL STEM CELLS; NEUROGENESIS; PREGNANCY; SIGNAL TRANSDUCTION;

EID: 84896823524     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.102327     Document Type: Article

References (50)

1. Abe, K., Noguchi, H., Tagawa, K., Yuzuriha, M., Toyoda, A., Kojima, T., Ezawa, K., Saitou, N., Hattori, M., Sakaki, Y. et al. (2004). Contribution of Asian mouse subspecies Mus musculus molossinus to genomic constitution of strain C57BL/6J, as defined by BAC-end sequence-SNP analysis. Genome Res. 14, 2439-2447.
2. Alcamo, E. A., Chirivella, L., Dautzenberg, M., Dobreva, G., Fariñas, I., Grosschedl, R. and McConnell, S. K. (2008). Satb2 regulates callosal projection neuron identity in the developing cerebral cortex. Neuron 57, 364-377.
3. Arber, S., Han, B., Mendelsohn, M., Smith, M., Jessell, T. M. and Sockanathan, S. (1999). Requirement for the homeobox gene Hb9 in the consolidation of motor neuron identity. Neuron 23, 659-674.
4. Bermingham, N. A., Hassan, B. A., Wang, V. Y., Fernandez, M., Banfi, S., Bellen, H. J., Fritzsch, B. and Zoghbi, H. Y. (2001). Proprioceptor pathway development is dependent on Math1. Neuron 30, 411-422.
5. Britanova, O., de Juan Romero, C., Cheung, A., Kwan, K. Y., Schwark, M., Gyorgy, A., Vogel, T., Akopov, S., Mitkovski, M., Agoston, D. et al. (2008). Satb2 is a postmitotic determinant for upper-layer neuron specification in the neocortex. Neuron 57, 378-392.
6. Chen, Z., Gore, B. B., Long, H., Ma, L. and Tessier-Lavigne, M. (2008). Alternative splicing of the Robo3 axon guidance receptor governs the midline switch from attraction to repulsion. Neuron 58, 325-332.
7. Dickson, B. J. and Gilestro, G. F. (2006). Regulation of commissural axon pathfinding by slit and its Robo receptors. Annu. Rev. Cell Dev. Biol. 22, 651-675.
8. Ding, Q., Joshi, P. S., Xie, Z. H., Xiang, M. and Gan, L. (2012). BARHL2 transcription factor regulates the ipsilateral/contralateral subtype divergence in postmitotic dI1 neurons of the developing spinal cord. Proc. Natl. Acad. Sci. USA 109, 1566-1571.
9. Dollé, P., Fraulob, V. and Duboule, D. (1994). Developmental expression of the mouse Evx-2 gene: relationship with the evolution of the HOM/Hox complex. Development Suppl. 1994, 143-153.
10. Evans, T. A. and Bashaw, G. J. (2010). Axon guidance at the midline: of mice and flies. Curr. Opin. Neurobiol. 20, 79-85.
11. Fedtsova, N. G. and Turner, E. E. (1995). Brn-3.0 expression identifies early postmitotic CNS neurons and sensory neural precursors. Mech. Dev. 53, 291-304.
12. Fedtsova, N., Quina, L. A., Wang, S. and Turner, E. E. (2008). Regulation of the development of tectal neurons and their projections by transcription factors Brn3a and Pax7. Dev. Biol. 316, 6-20.
13. García-Frigola, C., Carreres, M. I., Vegar, C., Mason, C. and Herrera, E. (2008). Zic2 promotes axonal divergence at the optic chiasm midline by EphB1-dependent and-independent mechanisms. Development 135, 1833-1841.
14. Gowan, K., Helms, A. W., Hunsaker, T. L., Collisson, T., Ebert, P. J., Odom, R. and Johnson, J. E. (2001). Crossinhibitory activities of Ngn1 and Math1 allow specification of distinct dorsal interneurons. Neuron 31, 219-232.
15. Helms, A. W. and Johnson, J. E. (1998). Progenitors of dorsal commissural interneurons are defined by MATH1 expression. Development 125, 919-928.
16. Herrera, E., Brown, L., Aruga, J., Rachel, R. A., Dolen, G., Mikoshiba, K., Brown, S. and Mason, C. A. (2003). Zic2 patterns binocular vision by specifying the uncrossed retinal projection. Cell 114, 545-557.
17. Kmita, M., Tarchini, B., Duboule, D. and Hérault, Y. (2002). Evolutionary conserved sequences are required for the insulation of the vertebrate Hoxd complex in neural cells. Development 129, 5521-5528.
18. Kröger, S. and Schwarz, U. (1990). The avian tectobulbar tract: development, explant culture, and effects of antibodies on the pattern of neurite outgrowth. J. Neurosci. 10, 3118-3134.
19. Lee, R., Petros, T. J. and Mason, C. A. (2008). Zic2 regulates retinal ganglion cell axon avoidance of ephrinB2 through inducing expression of the guidance receptor EphB1. J. Neurosci. 28, 5910-5919.
20. Liem, K. F., Jr, Tremml, G. and Jessell, T. M. (1997). A role for the roof plate and its resident TGFbeta-related proteins in neuronal patterning in the dorsal spinal cord. Cell 91, 127-138.
21. Lu, S., Shashikant, C. S. and Ruddle, F. H. (1996). Separate cis-acting elements determine the expression of mouse Dbx gene in multiple spatial domains of the central nervous system. Mech. Dev. 58, 193-202.
22. Marillat, V., Sabatier, C., Failli, V., Matsunaga, E., Sotelo, C., Tessier-Lavigne, M. and Chédotal, A. (2004). The slit receptor Rig-1/Robo3 controls midline crossing by hindbrain precerebellar neurons and axons. Neuron 43, 69-79.
23. Mastick, G. S. and Easter, S. S., Jr (1996). Initial organization of neurons and tracts in the embryonic mouse fore-and midbrain. Dev. Biol. 173, 79-94.
24. Mastick, G. S., Davis, N. M., Andrew, G. L. and Easter, S. S., Jr (1997). Pax-6 functions in boundary formation and axon guidance in the embryonic mouse forebrain. Development 124, 1985-1997.
25. Moran-Rivard, L., Kagawa, T., Saueressig, H., Gross, M. K., Burrill, J. and Goulding, M. (2001). Evx1 is a postmitotic determinant of v0 interneuron identity in the spinal cord. Neuron 29, 385-399.
26. Murray, E. A. and Coulter, J. D. (1982). Organization of tectospinal neurons in the cat and rat superior colliculus. Brain Res. 243, 201-214.
27. Nawabi, H. and Castellani, V. (2011). Axonal commissures in the central nervous system: how to cross the midline? Cell. Mol. Life Sci. 68, 2539-2553.
28. Niwa, H., Yamamura, K. and Miyazaki, J. (1991). Efficient selection for highexpression transfectants with a novel eukaryotic vector. Gene 108, 193-199.
29. Pak, W., Hindges, R., Lim, Y. S., Pfaff, S. L. and O'Leary, D. D. (2004). Magnitude of binocular vision controlled by islet-2 repression of a genetic program that specifies laterality of retinal axon pathfinding. Cell 119, 567-578.
30. Pierani, A., Brenner-Morton, S., Chiang, C. and Jessell, T. M. (1999). A sonic hedgehog-independent, retinoid-activated pathway of neurogenesis in the ventral spinal cord. Cell 97, 903-915.
31. Pierani, A., Moran-Rivard, L., Sunshine, M. J., Littman, D. R., Goulding, M. and Jessell, T. M. (2001). Control of interneuron fate in the developing spinal cord by the progenitor homeodomain protein Dbx1. Neuron 29, 367-384.
32. Polleux, F., Ince-Dunn, G. and Ghosh, A. (2007). Transcriptional regulation of vertebrate axon guidance and synapse formation. Nat. Rev. Neurosci. 8, 331-340.
33. Prakash, N., Puelles, E., Freude, K., Trümbach, D., Omodei, D., Di Salvio, M., Sussel, L., Ericson, J., Sander, M., Simeone, A. et al. (2009). Nkx6-1 controls the identity and fate of red nucleus and oculomotor neurons in the mouse midbrain. Development 136, 2545-2555.
34. Saba, R., Nakatsuji, N. and Saito, T. (2003). Mammalian BarH1 confers commissural neuron identity on dorsal cells in the spinal cord. J. Neurosci. 23, 1987-1991.
35. Sabatier, C., Plump, A. S., Le Ma, Brose, K., Tamada, A., Murakami, F., Lee, E. Y. and Tessier-Lavigne, M. (2004). The divergent Robo family protein rig-1/Robo3 is a negative regulator of slit responsiveness required for midline crossing by commissural axons. Cell 117, 157-169.
36. Saito, T. (2006). In vivo electroporation in the embryonic mouse central nervous system. Nat. Protoc. 1, 1552-1558.
37. Schneider, C. A., Rasband, W. S. and Eliceiri, K. W. (2012). NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671-675.
38. Shepherd, I. T. and Taylor, J. S. (1995). Early development of efferent projections from the chick tectum. J. Comp. Neurol. 354, 501-510.
39. Shimogori, T. and Ogawa, M. (2008). Gene application with in utero electroporation in mouse embryonic brain. Dev. Growth Differ. 50, 499-506.
40. Shirasaki, R. and Pfaff, S. L. (2002). Transcriptional codes and the control of neuronal identity. Annu. Rev. Neurosci. 25, 251-281.
41. Shirasaki, R., Tamada, A., Katsumata, R. and Murakami, F. (1995). Guidance of cerebellofugal axons in the rat embryo: directed growth toward the floor plate and subsequent elongation along the longitudinal axis. Neuron 14, 961-972.
42. Shirasaki, R., Mirzayan, C., Tessier-Lavigne, M. and Murakami, F. (1996). Guidance of circumferentially growing axons by netrin-dependent and-independent floor plate chemotropism in the vertebrate brain. Neuron 17, 1079-1088.
43. Shirasaki, R., Lewcock, J. W., Lettieri, K. and Pfaff, S. L. (2006). FGF as a targetderived chemoattractant for developing motor axons genetically programmed by the LIM code. Neuron 50, 841-853.
44. Tabata, H. and Nakajima, K. (2001). Efficient in utero gene transfer system to the developing mouse brain using electroporation: visualization of neuronal migration in the developing cortex. Neuroscience 103, 865-872.
45. Tamada, A., Kumada, T., Zhu, Y., Matsumoto, T., Hatanaka, Y., Muguruma, K., Chen, Z., Tanabe, Y., Torigoe, M., Yamauchi, K. et al. (2008). Crucial roles of Robo proteins in midline crossing of cerebellofugal axons and lack of their up-regulation after midline crossing. Neural Dev. 3, 29.
46. Tessier-Lavigne, M. and Goodman, C. S. (1996). The molecular biology of axon guidance. Science 274, 1123-1133.
47. Thaler, J., Harrison, K., Sharma, K., Lettieri, K., Kehrl, J. and Pfaff, S. L. (1999). Active suppression of interneuron programs within developing motor neurons revealed by analysis of homeodomain factor HB9. Neuron 23, 675-687.
48. Vue, T. Y., Aaker, J., Taniguchi, A., Kazemzadeh, C., Skidmore, J. M., Martin, D. M., Martin, J. F., Treier, M. and Nakagawa, Y. (2007). Characterization of progenitor domains in the developing mouse thalamus. J. Comp. Neurol. 505, 73-91.
49. Weiner, J. A., Koo, S. J., Nicolas, S., Fraboulet, S., Pfaff, S. L., Pourquié, O. and Sanes, J. R. (2004). Axon fasciculation defects and retinal dysplasias in mice lacking the immunoglobulin superfamily adhesion molecule BEN/ALCAM/SC1. Mol. Cell. Neurosci. 27, 59-69.
50. Wilson, S. I., Shafer, B., Lee, K. J. and Dodd, J. (2008). A molecular program for contralateral trajectory: Rig-1 control by LIM homeodomain transcription factors. Neuron 59, 413-424.