Lmx1b controls the differentiation and migration of the superficial dorsal horn neurons of the spinal cord

Development

Volumn 131, Issue 15, 2004, Pages 3693-3703

  Ding, Yu Qiang ^a,d   Yin, Jun ^a   Kania, Artur ^b   Zhao, Zhong Qiu ^a   Johnson, Randy L ^c   Chen, Zhou Feng ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

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

^c UNIVERSITY OF TEXAS   (United States)

^d INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

Author keywords

Cutaneous afferents; Differentiation; Dorsal horn; Lmx1b; Migration; Mouse

Indexed keywords

HOMEODOMAIN PROTEIN; MUTANT PROTEIN; PROTEIN EBF; PROTEIN LMX1B; PROTEIN ZIC; REGULATOR PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR DRG11; TRANSCRIPTION FACTOR RNX; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CELL DISRUPTION; CELL MIGRATION; CONTROLLED STUDY; DORSAL ROOT; EMBRYO; GENE EXPRESSION; GENE REPRESSION; GENE TARGETING; MOUSE; MUTATIONAL ANALYSIS; NERVE CELL DIFFERENTIATION; NERVE CELL NETWORK; NERVE FIBER; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; REGULATORY MECHANISM; SENSORY NERVE CELL; SPINAL CORD DORSAL HORN; SPINAL CORD NERVE CELL;

ANIMALS; CELL DIFFERENTIATION; CELL MOVEMENT; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HOMEODOMAIN PROTEINS; IN SITU HYBRIDIZATION; MICE; MICE, KNOCKOUT; NERVE TISSUE PROTEINS; POSTERIOR HORN CELLS; PREGNANCY; RECEPTOR, TRKA; TRANSCRIPTION FACTORS;

ANIMALIA;

EID: 4444239058     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.01250     Document Type: Article

References (69)

1. Adams, K. A., Maida, J. M., Golden, J. A. and Riddle, R. D. (2000). The transcription factor Lmx1b maintains Wnt1 expression within the isthmic organizer. Development 127, 1857-1867.
2. Aruga, J., Yokota, N., Hashimoto, M., Furuichi, T., Fukuda, M. and Mikoshiba, K. (1994). A novel zinc finger protein, zic, is involved in neurogenesis, especially in the cell lineage of cerebellar granule cells. J. Neurochem. 63, 1880-1890.
3. Aruga, J., Nagai, T., Tokuyama, T., Hayashizaki, Y., Okazaki, Y., Chapman, V. M. and Mikoshiba, K. (1996a). The mouse zic gene family. Homologues of the Drosophila pair-rule gene odd-paired. J. Biol. Chem. 271, 1043-1047.
4. Aruga, J., Yozu, A., Hayashizaki, Y., Okazaki, Y., Chapman, V. M. and Mikoshiba, K. (1996b). Identification and characterization of Zic4, a new member of the mouse Zic gene family. Gene 172, 291-294.
5. Aruga, J., Minowa, O., Yaginuma, H., Kuno, J., Nagai, T., Noda, T. and Mikoshiba, K. (1998). Mouse Zic1 is involved in cerebellar development. J. Neurosci. 18, 284-293.
6. Aruga, J., Inoue, T., Hoshino, J. and Mikoshiba, K. (2002a). Zic2 controls cerebellar development in cooperation with Zic1. J. Neurosci. 22, 218-225.
7. Aruga, J., Tohmonda, T., Homma, S. and Mikoshiba, K. (2002b). Zic1 promotes the expansion of dorsal neural progenitors in spinal cord by inhibiting neuronal differentiation. Dev. Biol. 244, 329-341.
8. 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.
9. Brose, K. and Tessier-Lavigne, M. (2000). Slit proteins: key regulators of axon guidance, axonal branching, and cell migration. Curr. Opin. Neurobiol. 10, 95-102.
10. Brunet, J. F. and Pattyn, A. (2002). Phox2 genes - from patterning to connectivity. Curr. Opin. Genet. Dev. 12, 435-440.
11. Caspary, T. and Anderson, K. V. (2003). Patterning cell types in the dorsal spinal cord: what the mouse mutants say. Nat. Rev. Neurosci. 4, 289-297.
12. Chen, H., Lun, Y., Ovchinnikov, D., Kokubo, H., Oberg, K. C., Pepicelli, C. V., Gan, L., Lee, B. and Johnson, R. L. (1998a). Limb and kidney defects in Lmx1b mutant mice suggest an involvement of LMX1B in human nail patella syndrome. Nat. Genet. 19, 51-55.
13. Chen, Z. F., Paquette, A. J. and Anderson, D. J. (1998b). NRSF/REST is required in vivo for repression of multiple neuronal target genes during embryogenesis. Nat. Genet. 20, 136-142.
14. Chen, Z. F., Rebelo, S., White, F., Malmberg, A. B., Baba, H., Lima, D., Woolf, C. J., Basbaum, A. I. and Anderson, D. J. (2001). The paired homeodomain protein DRG11 is required for the projection of cutaneous sensory afferent fibers to the dorsal spinal cord. Neuron 31, 59-73.
15. Cheng, L., Chen, C. L., Luo, P., Tan, M., Qiu, M., Johnson, R. and Ma, Q. (2003). Lmx1b, Pet-1, and Nkx2.2 coordinately specify serotonergic neurotransmitter phenotype. J. Neurosci. 23, 9961-9967.
16. Christensen, B. N. and Perl, E. R. (1970). Spinal neurons specifically excited by noxious or thermal stimuli: marginal zone of the dorsal horn. J. Neurophysiol. 33, 293-307.
17. Ding, Y. Q., Marklund, U., Yuan, W., Yin, J., Wegman, L., Ericson, J., Deneris, E., Johnson, R. L. and Chen, Z. F. (2003). Lmx1b is essential for the development of serotonergic neurons. Nat. Neurosci. 6, 933-938.
18. Dreyer, S. D., Zhou, G., Baldini, A., Winterpacht, A., Zabel, B., Cole, W., Johnson, R. L. and Lee, B. (1998). Mutations in LMX1B cause abnormal skeletal patterning and renal dysplasia in nail patella syndrome. Nat. Genet. 19, 47-50.
19. Ebert, P. J., Timmer, J. R., Nakada, Y., Helms, A. W., Parab, P. B., Liu, Y., Hunsaker, T. L. and Johnson, J. E. (2003). Zic1 represses Math1 expression via interactions with the Math1 enhancer and modulation of Math1 autoregulation. Development 130, 1949-1959.
20. Fedtsova, N. G. and Turner, E. E. (1995). Brn-3.0 expression identifies early post-mitotic CNS neurons and sensory neural precursors. Mech. Dev. 53, 291-304.
21. Feiner, L., Webber, A. L., Brown, C. B., Lu, M. M., Jia, L., Feinstein, P., Mombaerts, P., Epstein, J. A. and Raper, J. A. (2001). Targeted disruption of semaphorin 3C leads to persistent truncus arteriosus and aortic arch interruption. Development 128, 3061-3070.
22. Garcia-Dominguez, M., Poquet, C., Garel, S. and Charnay, P. (2003). Ebf gene function is required for coupling neuronal differentiation and cell cycle exit. Development 130, 6013-6025.
23. Garel, S., Marin, F., Mattei, M. G., Vesque, C., Vincent, A. and Charnay, P. (1997). Family of Ebf/Olf-1-related genes potentially involved in neuronal differentiation and regional specification in the central nervous system. Dev. Dyn. 210, 191-205.
24. Garel, S., Garcia-Dominguez, M. and Charnay, P. (2000). Control of the migratory pathway of facial branchiomotor neurones. Development 127, 5297-5307.
25. Goldstein, M. E., House, S. B. and Gainer, H. (1991). NF-L and peripherin immunoreactivities define distinct classes of rat sensory ganglion cells. J. Neurosci. Res. 30, 92-104.
26. Graham, A., Maden, M. and Krumlauf, R. (1991). The murine Hox-2 genes display dynamic dorsoventral patterns of expression during central nervous system development. Development 112, 255-264.
27. Gross, M. K., Dottori, M. and Goulding, M. (2002). Lbx1 specifies somatosensory association interneurons in the dorsal spinal cord. Neuron 34, 535-549.
28. He, Z. and Tessier-Lavigne, M. (1997). Neuropilin is a receptor for the axonal chemorepellent Semaphorin III. Cell 90, 739-751.
29. Helms, A. W. and Johnson, J. E. (2003). Specification of dorsal spinal cord interneurons. Curr. Opin. Neurobiol. 13, 42-49.
30. Hobert, O., Tessmar, K. and Ruvkun, G. (1999). The Caenorhabditis elegans lim-6 LIM homeobox gene regulates neurite outgrowth and function of particular GABAergic neurons. Development 126, 1547-1562.
31. Huang, E. J. and Reichardt, L. F. (2001). Neurotrophins: roles in neuronal development and function. Annu. Rev. Neurosci. 24, 677-736.
32. Huang, E. J., Wilkinson, G. A., Farinas, I., Backus, C., Zang, K., Wong, S. L. and Reichardt, L. F. (1999). Expression of Trk receptors in the developing mouse trigeminal ganglion: in vivo evidence for NT-3 activation of TrkA and TrkB in addition to TrkC. Development 126, 2191-2203.
33. Kania, A. and Jessell, T. M. (2003). Topographic motor projections in the limb imposed by LIM homeodomain protein regulation of Ephrin-A:EphA interactions. Neuron 38, 581-596.
34. Kania, A., Johnson, R. L. and Jessell, T. M. (2000). Coordinate roles for LIM homeobox genes in directing the dorsoventral trajectory of motor axons in the vertebrate limb. Cell 102, 161-173.
35. Kaufman, M. H. (1998). The Atlas of Mouse Development. San Diego: Academic Press.
36. Kolodkin, A. L., Levengood, D. V., Rowe, E. G., Tai, Y. T., Giger, R. J. and Ginty, D. D. (1997). Neuropilin is a semaphorin III receptor. Cell 90, 753-762.
37. Lawson, S. N. and Biscoe, T. J. (1979). Development of mouse dorsal root ganglia: an autoradiographic and quantitative study. J. Neurocytol. 8, 265-274.
38. Lee, K. J. and Jessell, T. M. (1999). The specification of dorsal cell fates in the vertebrate central nervous system. Annu. Rev. Neurosci. 22, 261-294.
39. Lewis, S. A., Villasante, A., Sherline, P. and Cowan, N. J. (1986). Brain-specific expression of MAP2 detected using a cloned cDNA probe. J. Cell Biol. 102, 2098-2105.
40. 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.
41. Luo, Y., Raible, D. and Raper, J. A. (1993). Collapsin: a protein in brain that induces the collapse and paralysis of neuronal growth cones. Cell 75, 217-227.
42. Matsunaga, E., Katahira, T. and Nakamura, H. (2002). Role of Lmx1b and Wnt1 in mesencephalon and metencephalon development. Development 129, 5269-5277.
43. Messersmith, E. K., Leonardo, E. D., Shatz, C. J., Tessier-Lavigne, M., Goodman, C. S. and Kolodkin, A. L. (1995). Semaphorin III can function as a selective chemorepellent to pattern sensory projections in the spinal cord. Neuron 14, 949-959.
44. Molander, C. and Grant, G. (1995). Spinal cord cytoarchitecture. In The Rat Nervous System (ed. G. Paxinos). Sydney: Academic Press.
45. Muller, T., Brohmann, H., Pierani, A., Heppenstall, P. A., Lewin, G. R., Jessell, T. M. and Birchmeier, C. (2002). The homeodomain factor lbx1 distinguishes two major programs of neuronal differentiation in the dorsal spinal cord. Neuron 34, 551-562.
46. Niwa, H., Yamamura, K. and Miyazaki, J. (1991). Efficient selection for high-expression transfectants with a novel eukaryotic vector. Gene 108, 193-199.
47. Nornes, H. O. and Das, G. D. (1974). Temporal pattern of neurogenesis in spinal cord of rat. I. An autoradiographic study - time and sites of origin and migration and settling patterns of neuroblasts. Brain Res. 73, 121-138.
48. Nornes, H. O. and Carry, M. (1978). Neurogenesis in spinal cord of mouse: an autoradiographic analysis. Brain Res. 159, 1-6.
49. Ozaki, S. and Snider, W. D. (1997). Initial trajectories of sensory axons toward laminar targets in the developing mouse spinal cord. J. Comp. Neurol. 380, 215-229.
50. Pressman, C. L., Chen, H. and Johnson, R. L. (2000). LMX1B, a LIM homeodomain class transcription factor, is necessary for normal development of multiple tissues in the anterior segment of the murine eye. Genesis 26, 15-25.
51. Qian, Y., Shirasawa, S., Chen, C. L., Cheng, L. and Ma, Q. (2002). Proper development of relay somatic sensory neurons and D2/D4 interneurons requires homeobox genes Rnx/Tlx-3 and Tlx- 1. Genes Dev. 16, 1220-1233.
52. Rexed, B. (1952). The cytoarchitectonic organization of the spinal cord in the cat. J. Comp. Neurol. 96, 415-496.
53. Riddle, R. D., Ensini, M., Nelson, C., Tsuchida, T., Jessell, T. M. and Tabin, C. (1995). Induction of the LIM homeobox gene Lmx1 by WNT7a establishes dorsoventral pattern in the vertebrate limb. Cell 83, 631-640.
54. Roberts, C. W., Shutter, J. R. and Korsmeyer, S. J. (1994). Hox11 controls the genesis of the spleen. Nature 368, 747-749.
55. Saba, R., Nakatsuji, N. and Saito, T. (2003). Mammalian BarHI confers commissural neuron identity on dorsal cells in the spinal cord. J. Neurosci. 23, 1987-1991.
56. Saito, T. and Nakatsuji, N. (2001). Efficient gene transfer into the embryonic mouse brain using in vivo electroporation. Dev. Biol. 240, 237-246.
57. Scott, S. A. (1992). Sensory neurons: diversity, development, and plasticity. In The Development of Peripheral Sensory Innervation Patterns (ed. S. A. Scott), pp. 242-263. New York: Oxford Univeristy Press.
58. Serafini, T., Kennedy, T. E., Galko, M. J., Mirzayan, C., Jessell, T. M. and Tessier-Lavigne, M. (1994). The netrins define a family of axon outgrowth-promoting proteins homologous to C. elegans UNC-6. Cell 78, 409-424.
59. Sharma, K. and Frank, E. (1998). Sensory axons are guided by local cues in the developing dorsal spinal cord. Development 125, 635-643.
60. Smidt, M. P., Asbreuk, C. H., Cox, J. J., Chen, H., Johnson, R. L. and Burbach, J. P. (2000). A second independent pathway for development of mesencephalic dopaminergic neurons requires Lmx1b. Nat. Neurosci. 3, 337-341.
61. Snider, W. D. (1994). Functions of the neurotrophins during nervous system development: what the knockouts are teaching us. Cell 77, 627-638.
62. Takahashi, T., Fournier, A., Nakamura, F., Wang, L. H., Murakami, Y., Kalb, R. G., Fujisawa, H. and Strittmatter, S. M. (1999). Plexin-neuropilin-1 complexes form functional semaphorin-3A receptors. Cell 99, 59-69.
63. Tanabe, Y., William, C. and Jessell, T. M. (1998). Specification of motor neuron identity by the MNR2 homeodomain protein. Cell 95, 67-80.
64. Tessier-Lavigne, M. and Goodman, C. S. (1996). The molecular biology of axon guidance. Science 274, 1123-1133.
65. Tiveron, M. C., Hirsch, M. R. and Brunet, J. F. (1996). The expression pattern of the transcription factor Phox2 delineates synaptic pathways of the autonomic nervous system. J. Neurosci. 16, 7649-7660.
66. Vogel, A., Rodriguez, C., Warnken, W. and Izpisua Belmonte, J. C. (1995). Dorsal cell fate specified by chick Lmx during vertebrate limb development. Nature 378, 716-720.
67. Wang, S. S., Tsai, R. Y. L. and Reed, R. R. (1997). The characterization of the Olf-1/EBF-like HLH transcription factor family: implications in olfactory gene regulation and neuronal development. J. Neurosci. 17, 4149-4158.
68. Willis, W. D., Westlund, K. N. and Carlton, S. M. (1995). Pain. In The Rat Nervous System (ed. G. Paxinos). pp. 725-750. Sydney: Academic Press.
69. Wong, K., Park, H. T., Wu, J. Y. and Rao, Y. (2002). Slit proteins: molecular guidance cues for cells ranging from neurons to leukocytes. Curr. Opin. Genet. Dev. 12, 583-591.