LIM homeodomain factors Lhx3 and Lhx4 assign subtype identities for motor neurons

Cell

Volumn 95, Issue 6, 1998, Pages 817-828

  Sharma, Kamal ^a   Sheng, Hui Z ^b   Lettieri, Karen ^a   Li, Hung ^c   Karavanov, Alexander ^b   Potter, Steven ^d   Westphal, Heiner ^b   Pfaff, Samuel L ^a  

^a SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^b EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^c INSTITUTE OF MOLECULAR BIOLOGY   (Taiwan)

^d CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HOMEODOMAIN PROTEIN; TRANSCRIPTION FACTOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CHICKEN; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; GENE EXPRESSION; GENE SWITCHING; MOTONEURON; MOUSE; NERVE CELL DIFFERENTIATION; NERVE FIBER GROWTH; NERVE PROJECTION; NEURAL TUBE; NONHUMAN; PRIORITY JOURNAL;

ANIMALIA; GALLUS GALLUS;

EID: 0032425468     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0092-8674(00)81704-3     Document Type: Article

References (55)

1. Agulnick, A.D., Taira, M., Breen, J.J., Tanaka, T., Dawid, I.B., and Westphal, H. (1996). Interactions of the LIM-domain binding factor Ldb1 with LIM homeodomain proteins. Nature 384, 270-272.
2. Appel, B., Korzh, V., Glasgow, E., Thor, S., Edlund, T., Dawid, I.B., and Eisen, J.S. (1995). Motoneuron fate specification revealed by patterned LIM homeobox gene expression in embryonic zebrafish. Development 121, 4117-4125.
3. Bach, I., Rhodes, S.J., Pearse, R.V., 2nd, Heinzel, T., Gloss, B., Scully, K.M., Sawchenko, P.E., and Rosenfeld, M.G. (1995). P-Lim, a LIM homeodomain factor, is expressed during pituitary organ and cell commitment and synergizes with Pit-1. Proc. Natl. Acad. Sci. USA 92, 2720-2724.
4. Bach, I., Carriere, C., Ostendorff, H.P., Andersen, B., and Rosenfeld, M.G. (1997). A family of LIM domain-associated cofactors confer transcriptional synergism between LIM and Otx homeodomain proteins. Genes Dev. 11, 1370-1380.
5. Brichta, A.M., Callister, R.J., and Peterson, E.H. (1987). Quantitative analysis of cervical musculature in rats: histochemical composition and motor pool organization. I. Muscles of the spinal accessory complex. J. Comp. Neurol. 255, 351-368.
6. 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.
7. Colamarino, S.A., and Tessier-Lavigne, M. (1995). The axonal chemoattractant netrin-1 is also a chemorepellent for trochlear motor axons. Cell 81, 621-629.
8. Eisen, J.S. (1991). Determination of primary motoneuron identity in developing zebrafish embryos. Science 252, 569-572.
9. 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 motor neuron subtype identity is initiated by signals from paraxial mesoderm. Development 725, 969-982.
10. 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, 1555-1560.
11. 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.
12. 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, 169-80.
13. Fedtsova, N., and Turner, E.E. (1997). Inhibitory effects of ventral signals on the development of Brn-3.0-expressing neurons in the dorsal spinal cord. Dev. Biol. 190, 18-31.
14. Fritzsch, B., and Northcutt, R.G. (1993). Cranial and spinal nerve organization in amphioxus and lampreys: evidence for an ancestral craniate pattern. Acta Anat. 148, 96-109.
15. Guthrie, S., and Pini, A. (1995). Chemorepulsion of developing motor axons by the floor plate. Neuron 14, 1117-1130.
16. Hobert, O., D'Alberti, T., Liu, Y., and Ruvkun, G. (1998). Control of neural development and function in a thermoregulatory network by the LIM homeobox gene lin-11. J. Neurosci. 18, 2084-2096.
17. Hogan, B., Beddington, R., Costantini, F., and Lacy, E. (1994). Manipulating the Mouse Embryo, Second Edition (Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press).
18. Jurata, L.W., Kenny, D.A., and Gill, G.N. (1996). Nuclear LIM interactor, a rhombotin and LIM homeodomain interacting protein, is expressed early in neuronal development. Proc. Natl. Acad. Sci. USA 93, 11693-11698.
19. Karlsson, O., Thor, S., Norberg, T., Ohlsson, H., and Edlund, T. (1990). Insulin gene enhancer binding protein lsl-1 is a member of a novel class of proteins containing both a homeo- and a Cys-His domain. Nature 344, 879-882.
20. Lance-Jones, C., and Landmesser, L. (1980). Motoneurone projection patterns in the chick hind limb following partial reversals of the spinal cord. J. Physiol. 302, 581-602.
21. Landmesser, L. (1978). The development of motor projection patterns in the chick hind limb. J. Physiol. 284, 391-414.
22. Landmesser, L.T. (1992). Growth cone guidance in the avian limb: a search for cellular and molecular mechanisms. In The Nerve Growth Cone, P.C. Letourneau, S.B. Kater, and E.R. Macagno, eds. (New York: Raven Press), pp. 373-385.
23. Leber, S.M., and Sanes, J.R. (1995). Migratory paths of neurons and glia in the embryonic chick spinal cord. J. Neurosci. 15, 1236-1248.
24. Leber, S.M., Breedlove, S.M., and Sanes, J.R. (1990). Lineage, arrangement, and death of clonally related motoneurons in chick spinal cord. J. Neurosci. 10, 2451-2462.
25. Li, H., Witte, O.P., Branford, W.W., Aronow, B.J., Weinstein, M., Kaur, S., Wert, S., Singh, G., Schreiner, C.M., Whitsett, J.A., et al. (1994). Gsh-4 encodes a LIM-type homeodomain, is expressed in the developing central nervous system and is required for early postnatal survival. EMBO J. 13, 2876-2885.
26. Lumsden, A., and Krumlauf, R. (1996). Patterning the vertebrate neuraxis. Science 274, 1109-1115.
27. 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.
28. Marti, E., Bumcrot, D.A., Takada, R., and McMahon, A.P. (1995). Requirement of 19K form of Sonic hedgehog for induction of distinct ventral cell types in CNS explants. Nature 375, 322-325.
29. Matise, M.P., and Lance-Jones, C. (1996). A critical period for the specification of motor pools in the chick lumbosacral spinal cord. Development 122, 659-669.
30. Nornes, W.O., and Carry, M. (1978). Neurogenesis in spinal cord of mouse: an autoradiographic analysis. Brain Res. 159, 1-6.
31. O'Gorman, S., Dagenais, N.A., Qian, M., and Marchuk, Y. (1997). Protamine-Cre recombinase transgenes efficiently recombine target sequences in the male germ line of mice, but not in embryonic stem cells. Proc. Natl. Acad. Sci. USA 94, 14602-14607.
32. Pfaff, S., and Kintner, C. (1998). Neuronal diversification: development of motor neuron subtypes. Curr. Opin. Neurobiol. 8, 27-36.
33. Pfaff, S.L., Mendelsohn, M., Stewart, C.L., Edlund, T., and Jessell, T.M. (1996). Requirement for LIM homeobox gene lsl1 in motor neuron generation reveals a motor neuron-dependent step in interneuron differentiation. Cell 84, 309-320.
34. Roelink, H., Augsberger, A., Heemskerk, J., Korzh, V., Norlin, S., Ruiz i Altaba, A., Tanabe, Y., Placzek, M., Edlund, T., Jessell, T.M., and Dodd, J. (1994). Floor plate and motor neuron induction by vhh-1, a vertebrate homolog of hedgehog expressed by the notochord. Cell 76, 761-775.
35. Sauer, B. (1993). Manipulation of transgenes by site-specific recombination: use of Cre recombinase. In Guide to Techniques in Mouse Development, P.M. Wassarman and M.L. DePamphilis, eds. (San Diego: Academic Press, Inc.), pp. 890-899.
36. Schaeren-Wiemars, 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-labeled cRNA probes. Histochemistry 100, 431-440.
37. Seidah, N.G., Barale, J.C., Marcinkiewicz, M., Mattel, M.G., Day, R., and Chrétien, M. (1994). The mouse homeoprotein mLIM-3 is expressed early in cells derived from the neuroepithelium and persists in adult pituitary. DNA Cell Biol. 13, 1163-1180.
38. Sharma, K., Korade, Z., and Frank, E. (1994). Development of specific muscle and cutaneous sensory projections in cultured segments of spinal cord. Development 120, 1315-1323.
39. Sheng, H., Zhadanov, B.M., Fujii, T., Bertuzzi, S., Grinberg, A., Lee, E.J., Huang, S.-P., Mahon, K.A., and Westphal, H. (1996). The LIM homeobox gene Lhx-3 is essential for the specification and proliferation of pituitary cell lineages. Science 272, 1004-1007.
40. Sheng, H.Z., Moriyama, K., Yamashita, T., Li, H., Potter, S.S., Mahon, K.A., and Westphal, H. (1997). Multistep control of pituitary organogenesis. Science 278, 1809-1812.
41. Singh, G., Kaur, S., Stock, J.L., Jenkins, N.A., Gilbert, D.J., Copeland, N.G., and Potter, S.S. (1991). Identification of 10 murine homeobox genes. Proc. Natl. Acad. Sci. USA 88, 10706-10710.
42. Sockanathan, S., and Jessell, T.M. (1998). Motor neuron-derived retinoid signaling specifies the subtype identity of spinal motor neurons. Cell 94, 503-514.
43. Taira, M., Hayes, W.P., Otani, H., and Dawid, I.B. (1993). Expression of LIM class homeobox gene Xlim-3 in Xenopus development is limited to neural and neuroendocrine tissues. Dev. Biol. 159, 245-256.
44. Tanabe, Y., and Jessell, T.M. (1996). Diversity and pattern in the developing spinal cord. Science 274, 1115-1122.
45. Tanabe, Y., William, C., and Jessell, T.M. (1998). Specification of motor neuron identity by the MNR2 homeodomain protein. Cell 95, 67-80.
46. Thor, S., and Thomas, J.B. (1997). The Drosophila islet gene governs axon pathfinding and neurotransmitter identity. Neuron 18, 397-409.
47. Tsien, J.Z., Chen, D.F., Gerber, D., Tom, C., Mercer, E.H., Anderson, D.J., Mayford, M., Kandel, E.R., and Tonegawa, S. (1996). Subregion- and cell type-restricted gene knockout in mouse brain. Cell 87, 1317-1326.
48. 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, 957-970.
49. Varela-Echavarria, A., Pfaff, S.L., and Guthrie, S. (1996). Differential expression of LIM homeobox genes among motor neuron subpopulations in the developing chick brain stem. Mol. Cell. Neurosci. 8, 242-257.
50. 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.
51. Westendorf, J.M., Rao, P.N., and Gerace, L. (1994). Cloning of cDNAs for M-phase phosphoproteins recognized by the MPM2 monoclonal antibody and determination of the phosphorylated epitope. Proc. Natl. Acad. Sci. USA 91, 714-718.
52. Wetts, R., and Vaughn, J.E. (1994). Choline acetyltransferase and NADPH diaphorase are co-expressed in rat spinal cord neurons. Neuroscience 63, 1117-1124.
53. Yamashita, T., Moriyama, K., Sheng, H.Z., and Westphal, H. (1997). Lhx4, a LIM homeobox gene. Genomics 44, 144-146.
54. Zhadanov, A.B., Bertuzzi, S., Taira, M., Dawid, I.B., and Westphal, H. (1995). Expression pattern of the murine LIM class homeobox gene Lhx3 in subsets of neural and neuroendocrine tissues. Dev. Dyn. 202, 354-364.
55. Zinyk, D.L., Mercer, E.H., Harris, E., Anderson, D.J., and Joyner, A.L. (1998). Fate mapping of the mouse midbrain-hindbrain constriction using a site-specific recombination system. Curr. Biol. 8, 665-668.