The control of rostrocaudal pattern in the developing spinal cord: Specification of motor neuron subtype identity is initiated by signals from paraxial mesoderm

Development

Volumn 125, Issue 6, 1998, Pages 969-982

  Ensini, Monica ^a,b,d   Tsuchida, Tammy N ^a,e   Belting, Heinz Georg ^c,f   Jessell, Thomas M ^a  

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

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c YALE UNIVERSITY   (United States)

^d CNR   (Italy)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f UNIVERSITY OF FREIBURG   (Germany)

Author keywords

Cell signalling; Chick; Mesoderm; Motor neurons; Neural tube; Positional identity; Quail

Indexed keywords

HOMEODOMAIN PROTEIN;

ARTICLE; CHICK EMBRYO; EMBRYO; EMBRYO PATTERN FORMATION; LOCOMOTION; MESODERM; MOTONEURON; NERVE CELL; NERVE CELL PLASTICITY; NERVE TRANSPLANTATION; NEURAL TUBE; NONHUMAN; PRIORITY JOURNAL; QUAIL; SPINAL CORD;

ANIMALS; BODY PATTERNING; CHICK EMBRYO; HOMEODOMAIN PROTEINS; IMMUNOHISTOCHEMISTRY; MESODERM; MICROSCOPY, CONFOCAL; MOTOR NEURONS; NERVE TISSUE; NERVE TISSUE PROTEINS; NEURONAL PLASTICITY; QUAIL; SIGNAL TRANSDUCTION; SPINAL CORD; TIME FACTORS; TRANSPLANTATION, HETEROLOGOUS;

AVES; PHASIANIDAE; VERTEBRATA;

EID: 0031894361     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (80)

1. Appel, B., Korzh, V., Glasgow, E., Thor, S., Edlund, T., Dawid, I. B., and Eisen, J. (1995). Motoneuron fate specification revealed by patterned LIM homeobox gene expression in embryonic zebratish. Development 121, 4117-4125.
2. Awgulewitsch, A. and Jacobs, D. (1990). Differential expression of Hox3.1 protein in subregions of the embryonic and adult spinal cord. Development 108, 411-420.
3. Bang, A. G., Papalopulu, N., Kintner, C., and Goulding, M. D. (1997). Expression of Pax-3 is initiated in the early neural plate by posteriorizing signals produced by the organizer and by posterior non-axial mesoderm. Development 124, 2075-2085.
4. Belting, H. G., Shashikant, C. S. and Ruddle, F. H. (1998). Multiple phases of expression and regulation of Hoxc8 in mouse embryonic development. J. Exp. Zool. In Press.
5. Burke, A. C., Nelson, C. E., Morgan, B. A. and Tabin, C. (1995). Hox genes and the evolution of vertebrate axial morphology. Development 121, 333-46.
6. Chaube, S. (1959). On axiation and symmetry in transplanted wing of the chick. J. Exp. Zool 140, 29-77.
7. Chawengsaksophak, K., James, R., Hammond, V. E., Köntgen, and Beck, F. (1997). Homeosis and intestinal tumours in Cdx2 mutant mice. Nature 386, 84-87.
8. Chevallier, A. (1979). Role of the somitic mesoderm in the development of the thorax in bird embryos. J. Embryol. Exp. Morph. 49, 73-88.
9. Chevallier, A, Kieny, M, and Mauger, A (1977). Limb-somite relationship: origin of the limb musculature.J. Embryol. Exp. Morph. 41, 245-258.
10. Chiang, C., Litingtung, Y., Lee, E., Young, K. E., Corden, J. L., Westphal, H., and Beachy, P. A. (1996). Cyclopia and defective axial patterning in mice lacking sonic hedgehog gene function. Nature 383, 407-413.
11. Cohn, M. J., Izpisúa-Belmonte, J. C., Abud, H., Heath, J. K. and Tickle, C. (1995). Fibroblast growth factors induce additional limb development from the flank of chick embryos. Cell 80, 739-746.
12. Crossley, P. H., Minowada, G., MacArthur, C. A. and Martin G. R. (1996) Roles for FGF8 in the induction, initiation and maintenance of chick limb development. Cell 84, 127-136.
13. Deschamps, J. and Wijgerde, M. (1993). Two phases in the establishment of Hox expression domains. Dev. Biol. 156, 473-480.
14. Donoghue, M. J., Morris-Valero, R., Johnson, Y. R., Merlie, J. P. and Sanes, J. R. (1992) Mammalian muscle cells bear a cell-autonomous, heritable memory of their rostrocaudal position. Cell 69, 61-11.
15. Eisen, J. S. (1991). Deterination of primary motoneuron identity in developing zebrafish embryos. Science 252, 569-572.
16. Eisen, J. S. and Pike, S. H. (1991). The spt-1 mutation alters the segmental arrangement and axonal development of identified neurons in the spinal cord of the embryonic zebrafish. Neuron 6, 767-776.
17. Ericson, J., Thor, S., Edlund, T., Jessell, T. M. and Yamada, T. (1992) Early stages of motor neuron differentiation revealed by expression of homeobox gene Islet-1. Science 256, 1555-60.
18. Ericson, J., Morton, S., Kawakami, A., Roelink, H.,and Jessell, T. M. (1996). Two critical periods of Sonic hedgehog signaling required for the specification of motor neuron identity. Cell 87, 661-673.
19. 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 the ventral spinal cord and hindbrain in response to graded Shh signaling. Cell 90, 169-180.
20. Fernandez-Teran, M., Piedra, M. E., Simandl, B. K., Villon, J. F. and Ros, M. A. (1997). Limb initiation and development is normal in the absence of the mesonephros. Dev. Biol. 189, 246-255.
21. Fukushima, M., Nakamura, M., Ohta, K., Okamura, R. and Negi, A. (1996). Regional specification of motoneurons along the anterior-posterior axis is independent of the notochord. Development 122, 905-914.
22. Gaunt, S. J. and Strachan, L. (1994). Forward spreading in the establishment of a vertebrate Hox expression boundary: The expression domain separates into anterior and posterior zones, and the spread occurs across implanted glass barriers. Dev. Dyn. 199, 229-240.
23. 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.
24. Grapin-Botton, A., Bonnin, M. and Le Douarin, M. (1997). Hox gene induction in the neural tube depends on three parameters: competence, signal supply and paralogue group. Development 124, 849-859.
25. Grieshammer, U., Sassoon, D. and Rosenthal, N. (1992). A transgene target for positional regulators marks early rostrocaudal specification of myogenic lineages. Cell 69, 79-63.
26. Gutman, C. R., Ajmera, M. K. and Hollyday, M. (1993). Organization of motor pools supplying axial muscles in the chicken. Brain Res. 609, 129-136.
27. Hamburger, V. and Hamilton, H. (1951) A series of normal stages in the development of chick embryo. J. Morph. 88, 49-92.
28. Hobert, O., Mori, I, Yamashita, Y., Honda, H., Ohshima, Y., Liu, Y. and Ruvkun, G. (1997). Regulation of interneuron function in the C. elegans thermoregulatory pathway by the ttx-3 LIM Homeobox gene. Neuron 19, 345-357.
29. Hollyday, M. (1980). Organization of motor pools in the chick lumbar lateral motor column. J. Comp. Neurol. 194, 143-170.
30. Hollyday, M. and Hamburger, V. (1977). An autoradiographic study of the formation of the lateral motor column in the chick embryo. Brain Res. 132, 197-208.
31. Hollyday, M. and Jacobson, R. D. (1990). Location of motor pools innervating chick wing. J. Comp. Neurol. 302, 575-588.
32. Hornbruch, A. and Wolpert L. (1991). The spatial and temporal distribution of polarizing activity in the flank of the pre-limb-bud stages in the chick embryo. Development 111, 725-731.
33. Itasaki, N., Sharpe, J., Morrison, A. and Krumlauf, R. (1996). Reprogramming Hox expression in the vertebrate hindbrain: influence of paraxial mesoderm and rhombomere transposition. Neuron 16, 487-500.
34. Kessel, M. and Gruss, P. (1991). Homeotic transformations of murine prevertebrae and concommitant alteration of Hox codes induced by retinoic acid. Cell 67, 89-104.
35. Kieny, M. (1971) Les phases d'activité morphogene du mesodermes somatopleural pendant le developpement precoce du membre chez l'embryon de poulet. Annales D'Embryologie et de Morphogenese 4, 281-298.
36. Kieny, M., Mauger, A. and Sengel, P. (1972). Early regionalization of the somitic mesoderm as studied by the development of the axial skeleton of the chick embryo. Dev. Biol. 28, 142-161.
37. Krumlauf, R. (1994). Hox genes in vertebrate development. Cell 78, 191-201.
38. Lance-Jones, C. and Dias, M. (1991). The influence of presumptive connective tissue on motoneuron axon guidance. Dev. Biol. 143, 78-92.
39. Lance-Jones, C. and Landmesser, L. (1980). Motoneuron projection patterns in the chick limb following early partial reversals of the spinal cord. J. Physiol. 302, 581-602.
40. Landmesser, L. (1978). The distribution of motor neurons supplying the chick hind limb muscles. J. Physiol 284, 371-389.
41. Landmesser, L. (1980). The generation of neuromuscular specificity, Ann. Rev. Neurosci. 3, 279-302.
42. Landmesser, L. T. (1992). Growth cone guidance in the avian limb: a search for cellular and molecular mechanisms. In: The Nerve Growth Cone. (ed. Letourneau. P.C., Kater. S.B. and Macagno. E.R), pp. 373-385. New York: Raven Press.
43. Le Mouellic, H., Condamine, H. and Brulet, P. (1988). Pattern of transcription of the homeo gene Hox-3. 1 in the mouse embryo. Genes Dev. 2, 125-135.
44. Levi-Montalcini, R. (1950). The origin and development of the visceral system in the spinal cord of the chick embryo. J. Morphol. 86, 253-283.
45. Lundgren, S. E., Callahan, C. A., Thor, S. and Thomas, J. B. (1995). Control of neuronal pathway selection by the Drosophila LIM homeodomain gene apterous. Development 121, 1769-1773.
46. Matise, M. P. and Lance-Jones, C. (1996). A critical period for the specification of motor pools in the chick lumbosacral spinal cord. Development 121, 659-669.
47. Marti, E., Bumcrot, D. A., Takada, R. and McMahon, A. P. (1995). Requirement of 19K form of Sonic hedgehog tor induction of distinct ventral cell types in CNS expiants. Nature 375, 322-325.
48. Michaud, J. L., Lapointe, F. and Le Douarin, N. M. (1997). The dorsoventral polarity of the presumptive limb is determined by signals produced by the somites and by the lateral somatopleure. Development 124, 1453-1463.
49. Muhr, J., Jessell, T. M. and Edlund, T. (1997). Assignment of early caudal identity to neural plate cells by a signal from caudal paraxial mesoderm. Neuron 19, 487-502.
50. Narayanan, C. H. and Hamburger, V. (1971). Motility in chick embryos with substitution of lumbosacral by brachial and brachial by lumbosacral spinal cord segments. J. Exp. Zool. 178, 415-432.
51. O'Brien, M. K. and Oppenheim, R. W. (1990) Development and survival of thoracic motoneurons and hindlimb musculature following transplantation of the thoracic neural tube to the lumbar region in the chick embryo: anatomical aspects. J. Neurobiol 21, 313-340.
52. O'Brien, M. K., Landmesser, L. and Oppenheim, R. W. (1990). Development and survival of thoracic motoneurons and hindlimb musculature following transplantation of the thoracic neural tube to the lumbar region in the chick embryo: functional aspects. J. Neurobiol, 21, 341-55.
53. Ohuchi, H., Nakagawa, T., Yamamoto, A., Araga, A., Ohata, T., Ishimaru, Y., Yoshioka, H., Kuwana, T., Nohno, T., Yamasaki, M., Itoh, N. and Noji, S. (1997). The mesenchymal factor, FGF10, initiates and maintains the outgrowth of the chick limb bud through interaction with FGF8, an apical ectodermal factor. Development 124, 2235-2244.
54. Pfaff, S. L., Mendelsohn, M., Stewart, C. L., Edlund, T. and Jessell, T. M. (1996). Requirement for LIM homeobox gene Isll in motor neuron generation reveals a motor neuron-dependent step in interneuron differentiation. Cell 84, 309-320.
55. Pourquie, O., Fan, C. M., Coltey, M., Hirsinger, E., Watanabe, Y., Breant, C., Francis-West, P., Brickell, P., Tessier-Lavigne, M. and Le Douarin N. M. (1996). Lateral and axial signals involved in avian somite patterning: a role for BMP4. Cell 84, 461-471.
56. Pownall, M. E., Tucker, A. S., Slack, J. M. W. and Isaacs, H. V. (1996). EFGF, Xcad3 and Hox genes form a molecular pathway that establishes the anteroposterior axis in Xenopus. Development 122, 3881-3892.
57. Prasad, A. and Hollyday, M. (199I). Development and migration of avian sympathetic preganglionic neurons. J. Comp. Neurol. 307, 237-258.
58. Roelink, H., Porter, J., Chiang, C., Tanabe, Y., Chang, D. T., Beachy, P. A. and Jessell, T. M. (1995). Floor plate and motor neuron induction by different concentration of the amino terminal cleavage product of Sonic hedgehog autoproteolysis. Cell 81, 445-455.
59. Shashikant, C. S., Bieberich, C. J., Belting, H. G., Wang, J. C., Borbely, M. A. and Ruddle, F. H. (1995). Regulation of Hoxc8 during mouse embryonic development: identification and characterization of critical elements involved in early neural tube expression. Development 121, 4339-4347.
60. Shieh, P. (1951) The neoformation of celts of preganglionic type in the cervical spinal cord of the chick embryo following its transplantation to the thoracic level. J. Exp. Zool 117, 359-395.
61. Simon, H., Hornbruch, A. and Lumsden, A. (1995). Independent assignment of antero-posterior and dorso-ventral positional values in the developing chick hindbrain. Current Biology 5, 205-214.
62. Stephens, T. D., Spall, R., Baker, W. C., Hiatt, S. R., Pugmire, D. E., Shaker, M. R., Willis, H. J. and Winger, K. P. (1991) Axial and paraxial influences on limb morphogenesis. J. Morphol. 208, 367-379.
63. Stern, C. D., Jaques, K. F., Lim, T., Fraser, S. E. and Keynes, R. J. (1991). Segmental lineage restrictions in the chick embryo spinal cord depend on the adjacent somites. Development 113, 239-244.
64. Stern, C. D. and Holland, W. H. (1993). Essential Developmental Biology: A Practical Approach. Oxford University Press.
65. Straznicky, C. and Tay, C. (1983) The localization of motoneuron pools innervating wing muscles in the chick. Anal. Embryol. 166, 209-218.
66. Studer, H., 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.
67. Subramanian, V., Meyer, B. I. and Gruss, P. (1995). Disruption of the murine homeobox gene Cdxl affects axial skeletal identitites by altering the mesodermal expression domains of Hox genes. Cell 83, 641-653.
68. Sundin, O. and Eichele, G. (1992). An early marker of axial pattern in the chick embryo and its respecification by retinoic acid. Development 114, 841-852.
69. Tanabe, Y., Roelink, H. and Jessell, T. M. (1995). Induction of motor neurons by Sonic hedgehog is independent of floor plate differentiation. Current Biol. 5, 651-658.
70. Tanabe, Y. and Jessell, T. M. (1996). Diversity and pattern in the developing spinal cord. Science 274, 1115-1123.
71. Thor, S. and Thomas, J. B. (1997). The Drosophila islet gene governs axon pathfinding and neurotransmitter identity. Neuron 18, 397-409.
72. Tokumoto, M., Gong, Z., Tsubokawa, T., Hew, C. L., Uyemura, K., Hotta, Y. and Okamoto, H. (1995). Molecular heterogeneity among primary motoneurons and within myotomes revealed by the differential mRNA expression of novel Islet-1 homologs in embryonic zebraflsh. Dev. Biol. 171, 578-589.
73. Tosney, K. W. (1991). Cells and cell-interactions that guide motor axons in the developing chick embryo. BioEssays 13, 17-23.
74. Tsuchida, T., Ensini, M., Morton, S. B., Baldassare, M., Edlund, T., Jessell, T. M. and Pfaff, S. L. (1994). Topographic organization of embryonic motor neurons defined by expression of LIM homeobox genes. Cell 79, 957-70.
75. Wenger, B. S. (1951). Determination of structural patterns in the spinal cord of the chick embryo studied by transplantations between brachial and adjacent levels. J. Exp. Zool. 116, 123-161.
76. Wilkinson, D. G., Bhatt, S., Cook, M., Boncinelli, E. and Krumlauf, R. (1989). Segmental expression of Hox2 homeobox-containing genes in the developing mouse hindbrain. Nature 341, 405-409.
77. Woo, K. and Fraser, S. E. (1997). Specification of the zebrafish nervous system by nonaxial signals. Science 277, 254-257.
78. Yaginuma, H., Tomita, M., Takashita, N., McKay, S. E., Cardwell, C., Yin, Q. W. and Oppenheim R. W. (1996). A novel type of programmed neuronal death in the cervical spinal cord of the chick embryo. J. Neurosci. 16, 3685-3703.
79. Yamada, T., Placzek, M., Tanaka, H., Dodd, J. and Jessell, T. M. (1991). Control of cell pattern in the developing nervous system: polarizing activity of the floor plate and notochord. Cell 64, 635-47.
80. Zhang, M., Kim, H. J., Marshall, H., Gendron-Maguire, M., Locas, D. A., Baron, A., Gudas, L. J., Gudas, L. J., Gridley, T., Krumlauf, R. and Grippo, J. F. (1994). Ectopic Hoxa-1 induces rhombomere transformation in mouse hindbrain. Development 120, 2431-2442.