Regulation of motor neuron subtype identity by repressor activity of Mnx class homeodomain proteins

Development

Volumn 130, Issue 8, 2003, Pages 1523-1536

  William, Christopher M ^a   Tanabe, Yasuto ^a,b   Jessell, Thomas M ^a  

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

^b MITSUBISHI KAGAKU INSTITUTE OF LIFE SCIENCES   (Japan)

Author keywords

Mnx class homeodomain proteins; Motor neuron; Motor neuron specification; Transcriptional repression

Indexed keywords

HB9 PROTEIN; HOMEODOMAIN PROTEIN; LIM3 PROTEIN; MNR2 PROTEIN; MNX PROTEIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; AUTONOMIC NERVOUS SYSTEM; CELL FATE; CELL SPECIFICITY; CHICK EMBRYO; CONTROLLED STUDY; EMBRYO; MITOSIS; MOTONEURON; NERVE CELL DIFFERENTIATION; NONHUMAN; PREGANGLIONIC NERVE CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SPINAL CORD; STEM CELL; TRANSCRIPTION REGULATION;

AMINO ACID SEQUENCE; ANIMALS; BIOLOGICAL MARKERS; BONE MORPHOGENETIC PROTEINS; CELL DIFFERENTIATION; CHICK EMBRYO; GENE EXPRESSION REGULATION; HOMEODOMAIN PROTEINS; IMMUNOHISTOCHEMISTRY; MITOSIS; MODELS, ANATOMIC; MOLECULAR SEQUENCE DATA; MOTOR NEURONS; NERVE TISSUE PROTEINS; REPRESSOR PROTEINS; SPINAL CORD; TRANSCRIPTION FACTORS;

ANIMALIA; VERTEBRATA;

EID: 0038076129     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.00358     Document Type: Review

References (66)

1. 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 motoneuron identity. Neuron 23, 659-674.
2. Barolo, S., Stone, T., Bang, A. G. and Posakony, J. W. (2002). Default repression and Notch signaling: Hairless acts as an adaptor to recruit the corepressors Groucho and dCtBP to Suppressor of Hairless. Genes Dev. 16, 1964-1976.
3. Bellomonte, D., di Bernardo, M., Russo, R., Caronia, G. and Spinelli, G. (1998). Highly restricted expression at the ectoderm-endoderm boundary of PIHbox 9, a sea urchin homeobox gene related to the human Hb9 gene. Mech. Dev. 74, 185-188.
4. Boyd, J. M., Subramanian, T., Schaeper, U., la Regina, M., Bayley, S. and Chinnadurai, G. (1993). A region in the C-terminus of adenovirus 2/5 E1a protein is required forassociation with a cellular phosphoprotein and important for the negative modulation of T24-ras mediated transformation, tumorigenesis and metastasis. EMBO J. 12, 469-478.
5. Briscoe, J. and Ericson, J. (2001). Specification of neuronal fates in the ventral neural tube. Curr. Opin. Neurobiol. 11, 43-49.
6. 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.
7. 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.
8. Broihier, H. T. and Skeath, J. B. (2002). Drosophila homeodomain protein dHb9 directs neuronal fate via crossrepressive and cell-nonautonomous mechanisms. Neuron 35, 39-50.
9. Cai, J., Xu, X., Yin, H., Wu, R., Modderman, G., Chen, Y., Jensent, J., Hui, C. C. and Qui, M. (2000). 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.
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. Chinnadurai, G. (2002). CtBP, an unconventional transcriptional corepressor in development and oncogenesis Mol. Cell. 9, 213-224.
12. Deltour, S., Pinte, S., Guerardel, C., Wasylyk, B. and Leprince, D. (2002). The human candidate tumor suppressor gene HIC1 recruits CtBP through a degenerate GLDLSKK motif. Mol. Cell. Biol. 22, 4890-4901.
13. Ensini, M., Tsuchida, T. N., Belting, H. G. and Jessell, T. M. (1998). The control of rostrocaudal pattern in the developing spinal cord: specification of motoneuron subtype identity is initiated by signals from paraxial mesoderm. Development 125, 969-982.
14. 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 motoneuron identity. Cell 87, 661-673.
15. 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.
16. Ferrier, D. E., Brooke, N. M., Panopoulou, G. and Holland, P. W. (2001). The Mnx homeobox gene class defined by Hb9, Mnr2 and amphioxus AmphiMnx. Dev. Genes Evol. 211, 103-107.
17. 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.
18. Goridis, C. and Brunet, J. F. (1999). Transcriptional control of neurotransmitter phenotype. Curr. Opin. Neurobiol. 9, 47-53.
19. Gross, M. K., Dottori, M. and Goulding, M. (2002). Lbx1 specifies somatosensory association interneurons in the dorsal spinal cord. Neuron 34, 535-549.
20. Hamburger, H. and Hamilton, H. (1951). A series of normal stages in the development of the chick embryo. J. Morphol. 88, 49-92.
21. Hasson, P., Muller, B., Basler, K. and Paroush, Z. (2001). Brinker requires two corepressors for maximal and versatile repression in Dpp signalling. EMBO J. 20, 5725-5736.
22. Hughes, S. H., Greenhouse, J. J., Petropoulos, C. J. and Sutrave, P. (1987). Adaptor plasmids simplify the insertion of foreign DNA into helper-independent retroviral vectors. J. Virol. 61, 3004-3012.
23. Jessell, T. M. (2000). Neuronal specification in the spinal cord: inductive signals and transcriptional codes. Nat. Rev. Genet. 1, 20-29.
24. Jessell, T. M. and Melton, D. A. (1992). Diffusible factors in vertebrate embryonic induction. Cell 68, 257-270.
25. 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.
26. Landmesser, L. (1978a). The distribution of motoneurones supplying chick hind limb muscles. J. Physiol. 284, 371-389.
27. Landmesser, L. (1978b). The development of motor projection patterns in the chick hind limb. J. Physiol. 284, 391-414.
28. Litingtung, Y. and Chiang, C. (2000). Control of Shh activity and signaling in the neural tube. Dev. Dyn. 219, 143-154.
29. Liu, J. P., Laufer, E. and Jessell, T. M. (2001). Assigning the Positional Identity of Spinal Motoneurons. Rostrocaudal Patterning of Hox-c Expression by FGFs, Gdfl1 and Retinoids. Neuron 32, 997-1012.
30. Lu, Q. R., Sun, T., Zhu, Z., Ma, N., Garcia, M. and Stiles, C. D. (2002). Common developmental requirement for Olig function indicates a motoneuron/oligodendrocyte connection. Cell 109, 75-86.
31. Mizuguchi, R., Sugimori, M., Takebayashi, H., Kosako, H., Nagao, M., Yoshida, S., Nabeshima, Y., Shimamura, K. and Nakafuku, M. (2001). Combinatorial roles of olig2 and neurogenin2 in the coordinated induction of pan-neuronal and subtype-specific properties of motoneurons. Neuron 31, 757-771.
32. Molloy, D. P., Barral, P. M., Bremner, K. H., Gallimore, P. H. and Grand, R. J. (2001). Structural determinants outside the PXDLS sequence affect the interaction of adenovirus E1A, C-terminal interacting protein and Drosophila repressors with C-terminal binding protein. Biochim. Biophys. Acta 1546, 55-70.
33. Moran-Rivard, L., Kagawa, T., Saueressig, H., Groww, 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.
34. Morgan, B. A. and Fekete, D. M. (1996). Manipulating gene expression with replication competent retroviruses. Methods Cell Biol. 51, 185-218.
35. Muhr, J., Andersson, E., Persson, M., Jessell, T. M. and Ericson, J. (2001). Groucho-mediated transcriptional repression establishes progenitor cell pattern and neuronal fate in the ventral neural tube. Cell 104, 861-873.
36. 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.
37. Novitch, B. G., Chen, A. I. and Jessell, T. M. (2001). Coordinate regulation of motoneuron subtype identity and pan-neuronal properties by the bHLH repressor Olig2. Neuron 31, 773-789.
38. Patten, I. and Placzek, M. (2000). The role of Sonic hedgehog in neural tube patterning. Cell. Mol. Life Sci. 57, 1695-1708.
39. Perlmann, T. and Jansson, L. (1995). A novel pathway for vitamin A signaling mediated by RXR heterodimerization with NGFI-B and Nurrl. Genes Dev. 9, 769-782.
40. Pfaff, S. L., Mendelsohn, M., Stewart, C. L., Edlund, T. and Jessell, T. M. (1996). Requirement for LIM homeobox gene Isl1 in motoneuron generation reveals a motoneuron-dependent step in interneuron differentiation. Cell 84, 309-320.
41. 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.
42. Prasad, A. and Hollyday, M. (1991). Development and migration of avian sympathetic preganglionic neurons. J. Comp. Neurol. 307, 237-258.
43. Ross, A. J., Ruiz-Perez, V., Wang, Y., Hagan, D. M., Scherer, S., Lynch, S. A., Lindsay, S., Custard, E., Belloni, E., Wilson, D. I., et al. (1998). A homeobox gene, HLXB9, is the major locus for dominantly inherited sacral agenesis. Nat. Genet. 20, 358-361.
44. Sadowski, I. and Ptashne, M. (1989). A vector for expressing GAL4(1-147) fusions in mammalian cells. Nucl. Acids Res. 17, 7539.
45. Saha, M. S., Miles, R. R. and Grainger, R. M. (1997). Dorsal-ventral patterning during neural induction in Xenopus: assessment of spinal cord regionalization with xHb9, a marker for the motoneuron region. Dev. Biol. 15, 209-223.
46. Sander, M., Paydar, S., Ericson, J., Briscoe, J., Berber, E., German, M., Jessell, T. M. and Rubenstein, J. L. (2000). Ventral neural patterning by Nkx homeobox genes: Nkx6.1 controls somatic motoneuron and ventral interneuron fates. Genes Dev. 14, 2134-2139.
47. Schaeren-Wiemers, N. and Gerfin-Moser, A. (1993). A single protocol to detect transcripts of various types and expression levels in neural tissue and cultured cells: in situ hybridization using digoxigenin-labelled cRNA probes. Histochemistry 100, 431-440.
48. Sharma, K., Sheng, H. Z., Lettieri, K., Li, H., Karavanov, A., Potter, S., Westphal, H. and Pfaff, S. L. (1998). LIM homeodomain factors Lhx3 and Lhx4 assign subtype identities for motoneurons. Cell 95, 817-828.
49. Sharma, K., Leonard, A. E., Lettieri, K. and Pfaff, S. L. (2000). Genetic and epigenetic mechanisms contribute to motoneuron pathfinding. Nature 406, 515-519.
50. Shirasaki, R. and Pfaff, S. L. (2002). Transcriptional codes and the control of neuronal identity. Annu. Rev. Neurosci. 25, 251-281.
51. Smith, S. T. and Jaynes, J. B. (1996). A conserved region of engrailed, shared among all en-, gsc-, Nk1-, Nk2- and msh-class homeoproteins, mediates active transcriptional repression in vivo. Development 122, 3141-3150.
52. Sockanathan, S. and Jessell, T. M. (1998). Motoneuron-derived retinoid signaling specifies the subtype identity of spinal motoneurons. Cell 94, 503-514.
53. Takebayashi, H., Nabeshima, Y., Yoshida, S., Chisaka, O., Ikenaka, K. and Nabeshima, Y. (2002). The basic helix-loop-helix factor olig2 is essential for the development of motoneuron and oligodendrocyte lineages. Curr. Biol. 12, 1157-1163.
54. Tanabe, Y. and Jessell, T. M. (1996). Diversity and pattern in the developing spinal cord. Science 274, 1115-1123.
55. Tanabe, Y., William, C. and Jessell, T. M. (1998). Specification of motoneuron identity by the Mnr2 homeodomain protein. Cell 95, 67-80.
56. Thaler, J., Harrison, K., Sharma, K., Lettieri, K., Kehrl, J. and Pfaff, S. L. (1999). Active suppression of interneuron programs within developing motoneurons revealed by analysis of homeodomain factor Hb9. Neuron 23, 675-687.
57. Thaler, J. P., Lee, S. K., Jurata, L. W., Gill, G. N. and Pfaff, S. L. (2002). LIM factor Lhx3 contributes to the specification of motoneuron and interneuron identity through cell-type-specific protein-protein interactions. Cell 110, 237-249.
58. Tosney, K. W., Hotary, K. B. and Lance-Jones, C. (1995). Specifying the target identity of motoneurons. BioEssays 17, 379-382.
59. Triezenberg, S. J., Kingsbury, R. C. and McKnight, S. L. (1988). Functional dissection of VP16, the trans-activator of herpes simplex virus immediate early gene expression. Genes Dev. 2, 718-729.
60. Tsuchida, T., Ensini, M., Morton, S. B., Baldassare, M., Edlund, T., Jessell, T. M. and Pfaff, S. L. (1994). Topographic organization of embryonic motoneurons defined by expression of LIM homeobox genes. Cell 79. 957-970.
61. Turner, D. L. and Weintraub, H. (1994). Expression of achaete-scute homolog 3 in Xenopus embryos converts ectodermal cells to a neural fate. Genes Dev. 8, 1434-1447.
62. Turner, J. and Crossley, M. (2001). The CtBP family: enigmatic and enzymatic transcriptional co-repressors. BioEssays 23, 683-690.
63. 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 motoneuron and interneuron specification. Neuron 31, 743-970.
64. Weintraub, H., Dwarki, V. J., Verma, I., Davis, R., Hollenberg, S., Snider, L., Lassar, A. and Tapscott, S. J. (1991). Muscle-specific transcriptional activation by MyoD. Genes Dev. 5, 1377-1386.
65. Zhou, Q. and Anderson, D. J. (2002). The bHLH transcription factors OLIG2 and OLIG1 couple neuronal and glial subtype specification. Cell 109, 61-73.
66. Zhou, Q., Wang, S. and Anderson, D. J. (2000). Identification of a novel family of oligodendrocyte lineage-specific basic helix-loop-helix transcription factors. Neuron 25, 331-343.