Motor neuron columnar fate imposed by sequential phases of Hox-c activity

Nature

Volumn 425, Issue 6961, 2003, Pages 926-933

  Dasen, Jeremy S ^a   Liu, Jeh Ping ^b   Jessell, Thomas M ^a  

^a Och Spine at New York Presbyterian Hospitals   (United States)

^b UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN; GENES; PROTEINS; TRAJECTORIES;

AXONAL TRAJECTORIES; NEURONS;

NEUROLOGY;

BASIC FIBROBLAST GROWTH FACTOR; HOX C PROTEIN; HOX PROTEIN; HOX6 PROTEIN; HOX9 PROTEIN; PROTEIN ACTIVATOR; REGULATOR PROTEIN; REPRESSOR PROTEIN; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CELL SUBPOPULATION; CENTRAL NERVOUS SYSTEM FUNCTION; CHICK EMBRYO; EMBRYO; GENE EXPRESSION REGULATION; MITOSIS; NERVE CELL DIFFERENTIATION; NERVE PROJECTION; NERVOUS SYSTEM DEVELOPMENT; NEUROANATOMY; NONHUMAN; PRECURSOR NERVE CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; SPINAL CORD MOTONEURON; STEM CELL; TOPOGRAPHY;

ANIMALS; BODY PATTERNING; CELL DIFFERENTIATION; CHICK EMBRYO; DNA-BINDING PROTEINS; FIBROBLAST GROWTH FACTOR 8; FIBROBLAST GROWTH FACTORS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HOMEODOMAIN PROTEINS; MICE; MITOSIS; MOTOR NEURONS; NEOPLASM PROTEINS; RNA, MESSENGER; SIGNAL TRANSDUCTION; SPINAL CORD; STEM CELLS;

ANIMALIA;

EID: 0242569162     PISSN: 00280836     EISSN: None     Source Type: Journal    
DOI: 10.1038/nature02051     Document Type: Article

References (49)

1. Mountcastle, V. B. The columnar organization of the neocortex. Brain 120, 701-722 (1997).
2. Sanders, T. A., Lumsden, A. & Ragsdale, C. W. Arcuate plan of chick midbrain development. J. Neurosci. 22, 10742-10750 (2002).
3. Jessell, T. M. Neuronal specification in the spinal cord: inductive signals and transcriptional codes. Nature Rev. Genet. 1, 20-29 (2000).
4. Briscoe, J. & Ericson, J. Specification of neuronal fates in the ventral neural tube. Curr. Opin. Neurobiol. 11, 43-49 (2001).
5. Landmesser, L. The distribution of motoneurons supplying chick hind limbs muscles. J. Physiol. (Lond.) 284, 371-389 (1978).
6. Hollyday, M. Organization of motor pools in the chick lumbar lateral motor column. J. Comp. Neurol. 194, 143-170 (1980).
7. Hollyday, M. Motoneuron histogenesis and the development of limb intervention. Curr. Top. Dev. Biol. 15, 181-215 (1980).
8. Gutmam, C. R., Ajmera, M. K. & Hollyday, M. Organization of motor pools supplying axial muscles in the chicken. Brain Res. 609, 129-136 (1993).
9. Shirasaki, R. & Pfaff S. L. Transcriptional codes and the control of neuronal identity. Annu. Rev. Neurosci. 25, 251-281 (2002).
10. Ensini, M., Tsuchida, T. N., Belting, H. G. & Jessell, T. M. The control of rostrocaudal pattern in the developing spinal cord: specification of motor neuron subtype identity is initiated by signals from paraxial mesoderm. Development 125, 969-982 (1998).
11. Liu, J. P., Laufer, E. & Jessell, T. M. Assigning the positional identity of spinal motor neurons: rostrocaudal patterning of Hox-c expression by FGFs, Gdf11, and retinoids. Neuron 32, 997-1012 (2001).
12. Bel-Vialar, S., Itasaki, N. & Krumlauf, R. Initiating Hox gene expression: in the early chick neural tube differential sensitivity to FGF and RA signaling subdivides the HoxB genes in two distinct groups. Development 129, 5103-5115 (2002).
13. Studer, M., Lumsden, A., Ariza-McNaughton, L., Bradley, A. & Krumlauf, R. Altered segmental identity and abnormal migration of motor neurons in mice lacking Hoxb-1. Nature 384, 630-634 (1996).
14. Bell, E., Wingate, R. J. & Lumsden, A. Homeotic transformation of rhombomere identity after localized Hoxb1 misexpression. Science 284, 2168-2171 (1999).
15. Rossel, M. & Capecchi, M. R. Mice mutant for both Hoxa1 and Hoxb1 show extensivo remodeling of the hindbrain and defects in craniofacial development. Development 126, 5027-5040 (1999).
16. Prasad, A. & Hollyday, M. Development and migration of avian sympathetic preganglionic neurons. J. Comp. Neurol. 307, 237-258 (1991).
17. Tsuchida, T. et al. Topographic organization of embryonic motor neurons defined by expression of LIM homeobox genes. Cell 79, 957-970 (1994).
18. William, C. M., Tananbe, Y. & Jessell, T. M. Regulation of motor neuron subtype identity by repressor activity of Mnx class homeodomain proteins. Development 130, 1523-1536 (2003).
19. Niederreither, K., McCaffery, P., Drager, U. C., Chambon, P. & Dolle, P. Restricted expression and retinoic acid-induced downregulation of the retinaldehyde dehydrogenase type 2 (RALDH-2) gene during mouse development. Mech. Dev. 62, 67-78 (1997).
20. Sockanathan, S. & Jessell, T. M. Motor neuron-derived retinoid signaling specifies the subtype identity of spinal motor neurons. Cell 94, 503-514 (1998).
21. Hart, K. C. et al. Transformation and Stat activation by derivatives of FGFR1, FGFR3, and FGFR4. Oncogene 19, 3309-3320 (2000).
22. Gabay, L., Seger, R. & Shilo, B. Z. MAP kinase in situ activation atlas during Drosophila embryogenesis. Development 124, 3535-3541 (1997).
23. Cai, J. et al. Evidence for the differential regulation of Nkx-6.1 expression in the ventral spinal cord and foregut by Shh-dependent and -independent mechanisms. Genesis 27, 6-11 (2000).
24. Arber, S. et al. Requirement for the homeobox gene Hb9 in the consolidation of motor neuron identity. Neuron 23, 659-674 (1999).
25. Jaynes, J. B. & O'Farrell, P. H. Active repression of transcription by the engrailed homeodomain protein. EMBO J. 10, 1427-1433 (1991).
26. Sockanathan, S., Perlmann, T. & Jessell, T. M. Retinoid receptor signaling in postmitotic motor neurons regulates rostrocaudal positional identity and axonal projection pattern. Neuron 40, 97-111 (2003).
27. Kostic, D. & Capecchi, M. R. Targeted disruptions of the murine Hoxa-4 and Hoxa-6 genes result in homeotic transformations of components of the vertebral column. Mech. Dev. 46, 231-247 (1994).
28. Garcia-Gasca, A. & Spyropoulos, D. D. Differential mammary morphogenesis along the anteroposterior axis in Hoxc6 gene targeted mice. Dev. Dyn. 219, 261-276 (2000).
29. Chen, F. & Capecchi, M. R. Hoxa9, Hoxb9, and Hoxd9, function together to control development of the mammary gland in response to pregnancy. Proc. Natl Acad. Sci. USA 96, 541-546 (1999).
30. Suemori, H. & Noguchi, S. Hox C cluster genes are dispensible for overall body plan of mouse embryonic development. Dev. Biol. 220, 333-342 (2000).
31. Lance-Jones, C., Omelchenko, N., Bailis, A., Lynch, S. & Sharma, K. Hoxd10 induction and regionalization in the developing lumbosacral spinal cord. Development 128, 2255-2268 (2001).
32. Carpenter, E. M. Hox genes and spinal cord development. Dev. Neurosci. 24, 24-34 (2002).
33. Briscoe, J., Pierani, A., Jessell, T. M. & Ericson, J. A homeodomain protein code specifies progenitor cell identity and neuronal fate in the ventral neural tube. Cell 101, 435-445 (2000).
34. Muhr, J., Andersson, E., Persson, M., Jessell, T. M. & Ericson, J. Groucho-mediated transcriptional repression establishes progenitor cell pattern and neuronal fate in the ventral neural tube. Cell 104, 861-873 (2001).
35. Goddard, J. M., Rossel, M., Manley, N. R. & Capecchi, M. R. Mice with targeted disruption of Hoxb-1 fail to form the motor nucleus of the VIIth nerve. Development 122, 3217-3228 (1996).
36. Cooper, K. L., Leisenring, W. M. & Moens, C. B. Autonomous and nonautonomous functions for Hox/Pbx in branchiomotor neuron development. Dev. Biol. 253, 200-213 (2003).
37. Duboule, D. & Morata, G. Colinearity and functional hierarchy among genes of the homeotic complexes. Trends Genet. 10, 358-364 (1994).
38. Kmita, M. & Duboule, D. Organizing axes in time and space; 25 years of colinear tinkering. Science 301, 331-333 (2003).
39. Jegalian, B. G. & De Robertis, E. M. Homeotic transformations in the mouse induced by overexpression of a human Hox3.3 transgene. Cell 71, 901-910 (1992).
40. Cohn, M. J., Izpisua-Belmonte, J. C., Abud, H., Heath, J. K. & Tickle, C. Fibrobtast growth factors induce additional limb development from the flank of chick embryos. Cell 80, 739-746 (1995).
41. Cohn, M. J. et al. Hox9 genes and vertebrate limb specification. Nature 387, 97-101 (1997).
42. Kania, A. & Jessell, T. M. Topographic motor projections in the limb imposed by LIM homeodomain protein regulation of ephrin-A:EphA interactions. Neuron 38, 581-596 (2003).
43. Hollyday, M. & Jacobson, R. D. Location of motor pools innervating chick wing. J. Comp. Neurol. 302, 575-588 (1990).
44. Wahba, G. M., Hostikka, S. L. & Carpenter, E. M. The paralogous Hox genes Hoxa10 and Hoxd10 interact to pattern the mouse hindlimb peripheral nervous system and skeleton. Dev. Biol. 231,87-102 (2001).
45. Tiret, L., Le Mouellic, H., Maury, M. & Brulet, P. Increased apoptosis of motoneurons and altered somatotopic maps in the brachial spinal cord of Hoxc-8-deficient mice. Development 125, 279-291 (1998).
46. Mann, R. S. & Affolter, M. Hox proteins meet more partners. Curr. Opin. Genet. Dev. 8, 423-429 (1998).
47. Nelson, C. E. et al. Analysis of Hox gene expression in the chick limb bud. Development 122, 1449-1466 (1996).
48. Brend, T., Gilthorpe, J., Summerbell, D. & Rigby, P. W. Multiple levels of transcriptional and post-transcriptional regulation are required to define the domain of Hoxb4 expression. Development 130, 2717-2728 (2003).
49. Li, X. & McGinnis, W. Activity regulation of Hox proteins, a mechanism for altering functional specificity in development and evolution. Proc. Natl Acad. Sci. USA 96, 6802-6807 (1999).