Nkx6.1 controls migration and axon pathfinding of cranial branchio-motoneurons

Development

Volumn 130, Issue 23, 2003, Pages 5815-5826

  Müller, Myriam ^a   Jabs, Normund ^a   Lorke, Dietrich E ^c   Fritzsch, Bernd ^b   Sander, Maike ^a,d  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^b CREIGHTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF HAMBURG   (Germany)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Facial nucleus; Hindbrain; Motoneuron; Mouse; Neuronal differentation; Neuronal migration; Nkx6.1 Nkx6.2

Indexed keywords

CELL SURFACE RECEPTOR; TRANSCRIPTION FACTOR;

CELL MIGRATION; CONTROLLED STUDY; EMBRYO; MITOSIS; MOTONEURON; MOUSE; MUTANT; NERVE FIBER; NERVOUS SYSTEM DEVELOPMENT; NEUROMERE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; RHOMBENCEPHALON; SPINAL CORD; STEM CELL;

ANIMALS; BODY PATTERNING; BRAIN; CELL DIFFERENTIATION; CELL LINEAGE; CELL MOVEMENT; EMBRYO; HOMEODOMAIN PROTEINS; IN SITU HYBRIDIZATION; MICE; MICE, KNOCKOUT; MOTOR NEURONS; RECEPTOR, EPHA4; RECEPTORS, CELL SURFACE;

EID: 0348013148     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.00815     Document Type: Review

References (60)

1. Ackerman, S. L., Kozak, L. P., Przyborski, S. A., Rund, L. A., Boyer, B. B. and Knowles, B. B. (1997). The mouse rostral cerebellar malformation gene encodes an UNC-5-like protein. Nature 386, 838-842.
2. Alcantara, S., Ruiz, M., de Castro, F., Soriano, E. and Sotelo, C. (2000). Netrin 1 acts as an attractive or as a repulsive cue for distinct migrating neurons during the development of the cerebellar system. Development 127, 1359-1372.
3. Altman, J. and Bayer, S. A. (1982). Development of the cranial nerve ganglia and related nuclei in the rat. Adv. Anat. Embryol. Cell Biol. 74, 1-90.
4. Ashwell, K. W. and Watson, C. R. (1983). The development of facial motoneurones in the mouse-neuronal death and the innervation of the facial muscles. J. Embryol. Exp. Morphol. 77, 117-141.
5. Auclair, F., Valdes, N. and Marchand, R. (1996). Rhombomere-specific origin of branchial and visceral motoneurons of the facial nerve in the rat embryo. J. Comp. Neurol. 369, 451-461.
6. Bloch-Gallego, E., Ezan, F., Tessier-Lavigne, M. and Sotelo, C. (1999). Floor plate and netrin-1 are involved in the migration and survival of inferior olivary neurons. J. Neurosci. 19, 4407-4420.
7. Briscoe, J., Sussel, L., Serup, P., Hartigan-O'Connor, D., Jessell, T. M., Rubenstein, J. L. and Ericson, J. (1999). Homeobox gene Nkx2.2 and specification of neuronal identity by graded Sonic hedgehog signalling. Nature 398, 622-627.
8. Briscoe, J., Pierani, A., Jessell, T. M. and Ericson, J. (2000). A homeodomain protein code specifies progenitor cell identity and neuronal fate in the ventral neural tube. Cell 101, 435-445.
9. Brunet, J. F. and Pattyn, A. (2002). Phox2 genes - from patterning to connectivity. Curr. Opin. Genet. Dev. 12, 435-440.
10. Causeret, F., Danne, F., Ezan, F., Sotelo, C. and Bloch-Gallego, E. (2002). Slit antagonizes netrin-1 attractive effects during the migration of inferior olivary neurons. Dev. Biol. 246, 429-440.
11. Cooper, K. L., Leisenring, W. M. and Moens, C. B. (2003). Autonomous and nonautonomous functions for Hox/Pbx in branchiomotor neuron development. Dev. Biol. 253, 200-213.
12. Enomoto, H., Heuckeroth, R. O., Golden, J. P., Johnson, E. M. and Milbrandt, J. (2000). Development of cranial parasympathetic ganglia requires sequential actions of GDNF and neurturin. Development 127, 4877-4889.
13. Enomoto, H., Crawford, P. A., Gorodinsky, A., Heuckeroth, R. O., Johnson, E. M., Jr and Milbrandt, J. (2001). RET signaling is essential for migration, axonal growth and axon guidance of developing sympathetic neurons. Development 128, 3963-3974.
14. Ericson, J., Rashbass, P., Schedl, A., Brenner-Morton, S., Kawakami, A., van Heyningen, V., Jessell, T. M. and Briscoe, J. (1997). Pax6 controls progenitor cell identity and neuronal fate in response to graded Shh signaling. Cell 90, 169-180.
15. Escurat, M., Djabali, K., Gumpel, M., Gros, F. and Portier, M. M. (1990). Differential expression of two neuronal intermediate- filament proteins, peripherin and the low-molecular-mass neurofilament protein (NF-L), during the development of the rat. J. Neurosci. 10, 764-784.
16. Finger, J. H., Bronson, R. T., Harris, B., Johnson, K., Przyborski, S. A. and Ackerman, S. L. (2002). 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.
17. Fritzsch, B. (1998). Of mice and genes: evolution of vertebrate brain development. Brain Behav. Evol. 52, 207-217.
18. Fritzsch, B. and Nichols, D. H. (1993). DiI reveals a prenatal arrival of efferents at the differentiating otocyst of mice. Hear Res. 65, 51-60.
19. Garel, S., Garcia-Dominguez, M. and Charnay, P. (2000). Control of the migratory pathway of facial branchiomotor neurones. Development 127, 529-307.
20. Gilardi-Hebenstreit, P., Nieto, M. A., Frain, M., Mattei, M. G., Chestier, A., Wilkinson, D. G. and Charnay, P. (1992). An Eph-related receptor protein tyrosine kinase gene segmentally expressed in the developing mouse hindbrain. Oncogene 7, 2499-2506.
21. Goddard, J. M., Rossel, M., Manley, N. R. and Capecchi, M. R. (1996). Mice with targeted disruption of Hoxb-1 fail to form the motor nucleus of the VIIth nerve. Development 122, 3217-3228.
22. Gradwohl, G., Fode, C. and Guillemot, F. (1996). Restricted expression of a novel murine atonal-related bHLH protein in undifferentiated neural precursors. Dev. Biol. 180, 227-241.
23. Hatten, M. E. (2002). New directions in neuronal migration. Science 297, 1660-1663.
24. Hong, K., Hinck, L., Nishiyama, M., Poo, M. M., Tessier-Lavigne, M. and Stein, E. (1999). 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.
25. Jensen, J., Serup, P., Karlsen, C., Nielsen, T. F. and Madsen, O. D. (1996). mRNA profiling of rat islet tumors reveals nkx 6.1 as a beta-cell-specific homeodomain transcription factor. J. Biol. Chem. 271, 18749-18758.
26. Jessell, T. M. (2000). Neuronal specification in the spinal cord: inductive signals and transcriptional codes. Nat. Rev. Genet. 1, 20-29.
27. Keleman, K. and Dickson, B. J. (2001). Short- and long-range repulsion by the Drosophila Unc5 netrin receptor. Neuron 32, 605-617.
28. Kyriakopoulou, K., de Diego, I, Wassef, M. and Karagogeos, D. (2002). A combination of chain and neurophilic migration involving the adhesion molecule TAG-1 in the caudal medulla. Development 129, 287-296.
29. Leonardo, E. D., Hinck, L., Masu, M., Keino-Masu, K., Ackerman, S. L. and Tessier-Lavigne, M. (1997). Vertebrate homologues of C. elegans UNC-5 are candidate netrin receptors. Nature 386, 833-838.
30. Lu, Q. R., Sun, T., Zhu, Z., Ma, N., Garcia, M., Stiles, C. D. and Rowitch, D. H. (2002). Common developmental requirement for Olig function indicates a motor neuron/oligodendrocyte connection. Cell 109, 75-86.
31. Lumsden, A. and Krumlauf, R. (1996). Patterning the vertebrate neuraxis. Science 274, 1109-1115.
32. Manzanares, M., Trainor, P. A., Nonchev, S., Ariza-McNaughton, L., Brodie, J., Gould, A., Marshall, H., Morrison, A., Kwan, C. T., Sham, M. H. et al. (1999). The role of kreisler in segmentation during hindbrain development. Dev. Biol. 211, 220-237.
33. McKay, I. J., Lewis, J. and Lumsden, A. (1997). Organization and development of facial motor neurons in the kreisler mutant mouse. Eur. J. Neurosci. 9, 1499-1506.
34. Meyerhardt, J. A., Look, A. T., Bigner, S. H. and Fearon, E. R. (1997). Identification and characterization of neogenin, a DCC-related gene. Oncogene 14, 1129-1136.
35. Murphy, P., Davidson, D. R. and Hill, R. E. (1989). Segment-specific expression of a homoeobox-containing gene in the mouse hindbrain. Nature 341, 156-159.
36. Nadarajah, B. and Parnavelas, J. G. (2002). Modes of neuronal migration in the developing cerebral cortex. Nat. Rev. Neurosci. 3, 423-432.
37. Nardelli, J., Thiesson, D., Fujiwara, Y., Tsai, F. Y. and Orkin, S. H. (1999). Expression and genetic interaction of transcription factors GATA-2 and GATA-3 during development of the mouse central nervous system. Dev. Biol. 210, 305-321.
38. Novitch, B. G., Chen, A. I. and Jessell, T. M. (2001). Coordinate regulation of motor neuron subtype identity and pan-neuronal properties by the bHLH repressor Olig2. Neuron 31, 773-789.
39. Osumi, N., Hirota, A., Ohuchi, H., Nakafuku, M., Iimura, T., Kuratani, S., Fujiwara, M., Noji, S. and Eto, K. (1997). Pax-6 is involved in the specification of hindbrain motor neuron subtype. Development 124, 2961-2972.
40. Pabst, O., Rummelies, J., Winter, B. and Arnold, H. H. (2003). Targeted disruption of the homeobox gene Nkx2.9 reveals a role in development of the spinal accessory nerve. Development 130, 1193-1202.
41. Pachnis, V., Mankoo, B. and Costantini, F. (1993). Expression of the c-ret proto-oncogene during mouse embryogenesis. Development 119, 1005-1017.
42. Pata, I., Studer, M., van Doorninck, J. H., Briscoe, J., Kuuse, S., Engel, J. D., Grosveld, F. and Karis, A. (1999). The transcription factor GATA3 is a downstream effector of Hoxb1 specification in rhombomere 4. Development 126, 5523-5531.
43. Pattyn, A., Morin, X., Cremer, H., Goridis, C. and Brunet, J. F. (1997). Expression and interactions of the two closely related homeobox genes Phox2a and Phox2b during neurogenesis. Development 124, 4065-4075.
44. Pattyn, A., Hirsch, M., Goridis, C. and Brunet, J. F., (2000). Control of hindbrain motor neuron differentiation by the homeobox gene Phox2b. Development 127, 1349-1358.
45. Pattyn, A., Vallstedt, A., Dias, J. M., Sander, M. and Ericson, J. (2003). Complementary roles for Nkx6 and Nkx2 class proteins in the establishment of motoneuron identity in the hindbrain. Development 130, 4149-4159.
46. Przyborski, S. A., Knowles, B. B. and Ackerman, S. L. (1998). Embryonic phenotype of Unc5h3 mutant mice suggests chemorepulsion during the formation of the rostral cerebellar boundary. Development 125, 41-50.
47. Rijli, F. M., Gavalas, A. and Chambon, P. (1998). Segmentation and specification in the branchial region of the head: the role of the Hox selector genes. Int. J. Dev. Biol. 42, 393-401.
48. Sander, M., Paydar, S., Ericson, J., Briscoe, J., Berber, E., German, M., Jessell, T. M. and Rubenstein, J. L. (2000a). Ventral neural patterning by Nkx homeobox genes: Nkx6.1 controls somatic motor neuron and ventral interneuron fates. Genes Dev. 14, 2134-2139.
49. Sander, M., Sussel, L., Conners, J., Scheel, D., Kalamaras, J., Dela Cruz, F., Schwitzgebel, V., Hayes-Jordan, A. and German, M. (2000b). Homeobox gene Nkx6.1 lies downstream of Nkx2.2 in the major pathway of beta-cell formation in the pancreas. Development 127, 5533-5540.
50. Schneider-Maunoury, S., Seitanidou, T., Charnay, P. and Lumsden, A. (1997). Segmental and neuronal architecture of the hindbrain of Krox-20 Mouse mutants. Development 124, 1215-1226.
51. Seitanidou, T., Schneider-Maunoury, S., Desmarquet, C., Wilkinson, D. G. and Charnay, P. (1997). Krox-20 is a key regulator of rhombomere-specific gene expression in the developing hindbrain. Mech. Dev. 65, 31-42.
52. Stolt, C. C., Lommes, P., Sock, E., Chaboissier, M.-C., Schedl, A. and Wegner, M. (2003). The Sox9 transcription factor determines glial fate choice in the developing spinal cord. Genes Dev. 17, 1677-1689.
53. Studer, M. (2001). Initiation of facial motoneurone migration is dependent on rhombomeres 5 and 6. Development 128, 3707-3716.
54. Studer, M., Lumsden, A., Ariza-McNaughton, L., Bradley, A. and Krumlauf, R. (1996). Altered segmental identity and abnormal migration of motor neurons in mice lacking Hoxb-1. Nature 384, 630-634.
55. Swiatek, P. J. and Gridley, T. (1993). Perinatal lethality and defects in hindbrain development in mice homozygous for a targeted mutation of the zinc finger gene Krox20. Genes Dev 7, 2071-2084.
56. Vallstedt, A., Muhr, J., Pattyn, A., Pierani, A., Mendelsohn, M., Sander, M., Jessell, T. M. and Ericson, J. (2001). Different levels of repressor activity assign redundant and specific roles to Nkx6 genes in motor neuron and interneuron specification. Neuron 31, 743-755.
57. Varela-Echavarria, A., Tucker, A., Puschel, A. W. and Guthrie, S. (1997). Motor axon subpopulations respond differentially to the chemorepellents netrin-1 and semaphorin D. Neuron 18, 193-207.
58. Wilkinson, D. G. (1992). Whole mount in situ hybridisation of vertebrate embryos. In In situ hybridisation. A practical approach (ed. D. G. Wilkinson), pp. 75-83. Oxford: Oxford University Press.
59. Yee, K. T., Simon, H. H., Tessier-Lavigne, M. and O'Leary, D. M. (1999). Extension of long leading processes and neuronal migration in the mammalian brain directed by the chemoattractant netrin-1. Neuron 24, 607-622.
60. Zhou, Q. and Anderson, D. J. (2002). The bHLH transcription factors OLIG2 and OLIG1 couple neuronal and glial subtype specification. Cell 109, 61-73.