Neuronal diversification: Development of motor neuron subtypes

Current Opinion in Neurobiology

Volumn 8, Issue 1, 1998, Pages 27-36

  Pfaff, Sam ^a   Kintner, Chris ^a  

^a SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR;

CELL TYPE; GENE EXPRESSION; MOTONEURON; NERVE CELL; NERVE CELL DIFFERENTIATION; PRIORITY JOURNAL; REVIEW; STEM CELL; SYNAPSE;

EID: 0031900077     PISSN: 09594388     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0959-4388(98)80005-6     Document Type: Article

References (62)

1. Cheng HJ, Flanagan JG. Identification and cloning of ELF-1, a developmentally expressed ligand for the Mek4 and Sek receptor tyrosine kinases. Cell. 79:1994;157-168.
2. Vassar R, Ngai J, Axel R. Spatial segregation of odorant receptor expression in the mammalian olfactory epithelium. Cell. 74:1993;309-318.
3. Landmesser LT. Growth cone guidance in the avian limb: a search for cellular and molecular mechanisms. Letourneau PC, Kater SB, Macagno ER. The Nerve Growth Cone. 1992;373-385 Raven Press, New York.
4. Colamarino SA, Tessier-Lavigne M. The axonal chemoattractant netrin-1 is also a chemorepellent for trochlear motor axons. Cell. 81:1995;621-629.
5. Varela-Echavarria A, Tucker A, Puschel AW, Guthrie S. Motor axon subpopulations respond differentially to the chemorepellents netrin-1 and semaphorin D. Neuron. 18:1997;193-207.
6. Eisen JS, Myers PZ, Westerfield M. Pathway selection by growth cones of identified motoneurones in live zebra fish embryos. Nature. 320:1986;269-271.
7. Jurata LW, Gill GN. Structure and function of LIM domains. Pawson AJ. Protein Modules in Signal Transduction. Topics in Microbiology and Immunology. 228:1998;75-113 Springer-Verlag, Berlin.
8. Appel B, Korzh V, Glasgow E, Thor S, Edlund T, Dawid IB, Eisen JS. Motoneuron fate specification revealed by patterned LIM homeobox gene expression in embryonic zebrafish. Development. 121:1995;4117-4125.
9. Tsuchida T, Ensini M, Morton SB, Baldassare M, Edlund T, Jessell TM, Pfaff SL. Topographic organization of embryonic motor neurons defined by expression of LIM homeobox genes. Cell. 79:1994;957-970.
10. Varela-Echavarria A, Pfaff SL, Guthrie S. Differential expression of LIM homeobox genes among motor neuron subpopulations in the developing brain stem. of special interest Mol Cell Neurosci. 8:1996;242-257 This report describes the combinatorial expression of LIM homeobox genes in the developing chick hindbrain. The assignment of Isl-1, Isl-2, and Lim-3 expression to individual cranial motor neuron subtypes is made by combining immunofluorescence and neuronal backlabeling.
11. Agulnick AD, Taira M, Breen JJ, Tanaka T, Dawid IB, Westphal H. Interactions of the LIM-domain binding factor Ldb1 with LIM homeodomain proteins. Nature. 384:1996;270-272.
12. Jurata LW, Kenny DA, Gill GN. Nuclear LIM interactor, a rhombotin and LIM homeodomain interacting protein, is expressed early in neuronal development. Proc Natl Acad Sci USA. 93:1996;11693-11698.
13. Jurata LW, Pfaff SL, Gill GN. The nuclear LIM domain interactor NLI mediates homo- and heterodimerization of LIM domain transcription factors. of special interest J Biol Chem. 273:1998;3152-3157 Epitope-tagged LIM proteins were used in double immunoprecipitations to examine protein - protein interactions. NLI is shown to mediate the formation of homo- and heteromeric complexes between LIM factors. While most LIM factors cannot bind to each other without NLI, Isl-1 and Lim-3 are unusual in their ability to form heteromeric complexes directly.
14. Bach I, Carriere C, Ostendorff HP, Andersen B, Rosenfeld MG. A family of LIM domain-associated co-factors confer transcriptional synergism between LIM and Otx homeodomain proteins. Genes Dev. 11:1997;1370-1380.
15. Sheng HZ, Moriyama K, Yamashita T, Li H, Potter SS, Mahan KA, Westphal H. Multistep control of pituitary organogenesis. Science. 278:1997;1809-1812.
16. Ericson J, Thor S, Edlund T, Jessell TM, Yamada T. Early stages of motor neuron differentiation revealed by expression of homeobox gene Islet-1. Science. 256:1992;1555-1560.
17. Pfaff SL, Mendelsohn M, Stewart CL, Edlund T, Jessell TM. Requirement for LIM homeobox gene Isl1 in motor neuron generation reveals a motor neuron-dependent step in interneuron differentiation. of outstanding interest Cell. 84:1996;309-320 In this report, evidence is shown that motor neurons fail to differentiate if Isl-1 function is eliminated by a targeted mutation. The consequence of this mutation is the appearance of apoptotic cells at the stage Isl-1 is first expressed. The loss of motor neurons appears to have indirect effects on the differentiation of other cell types in the ventral neural tube.
18. Tokumoto M, Gong Z, Tsubokawa T, Hew CL, Uyemura K, Hotta Y, Okamoto H. Molecular heterogeneity among primary motoneurons and within myotomes revealed by the differential mRNA expression of novel islet-1 homologs in embryonic zebrafish. Dev Biol. 171:1995;578-589.
19. Eisen JS. Determination of primary motoneuron identity in developing zebrafish embryos. Science. 252:1991;569-572.
20. Itasaki N, Sharpe J, Morrison A, Krumlauf R. Reprogramming Hox expression in the vertebrate hindbrain: influence of paraxial mesoderm and rhombomere transposition. of outstanding interest Neuron. 16:1996;487-500 This study demonstrates that the caudal hindbrain exhibits plasticity at neural tube stages. Mouse - chick and chick - chick tissue grafts are used to show that nonaxial mesoderm expresses a graded signal capable of influencing the anterior - posterior identity of the neuroepithelium, as assayed by Hox gene marker expression.
21. Grapin-Botton A, Bonnin MA, McNaughton L, Krumlauf R, Le Douarin N. Plasticity of transposed rhombomeres: Hox gene induction is correlated with phenotypic modifications. Development. 121:1995;2707-2721.
22. 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. of special interest Development. 125:1998;279-291 Mutation of the Hoxc-8 gene results in the ectopic projection of inappropriate motor neurons to forelimb muscle in the paw. The ectopic innervation of these muscles by inappropriate motor neurons leads to the eventual death of cervical motor neurons.
23. Zhang M, Kim HJ, Marshall H, Gendron-Maguire M, Lucas DA, Baron A, Gudas LJ, Grindley T, Krumlauf R, Grippo JF. Ectopic Hoxa-1 induces rhombomere transformation in mouse hindbrain. Development. 120:1994;2431-2442.
24. Alexandre D, Clarke J, Oxtoby E, Yan YL, Jowett T, Holder N. Ectopic expression of Hoxa-1 in the zebrafish alters the fate of the mandibular arch neural crest and phenocopies a retinoic acid-induced phenotype. Development. 122:1996;735-746.
25. Carpenter EM, Goddard JM, Chisaka O, Manley NR, Capecchi MR. Loss of Hox-A1 (Hox-1.6) function results in the reorganization of the murine hindbrain. Development. 118:1993;1063-1075.
26. Barrow JR, Capecchi MR. Targeted disruption of the Hoxb-2 locus in mice interferes with expression of Hoxb-1 and Hoxb-4. Development. 122:1996;3817-3828.
27. Goddard JM, Rossel M, Manley NR, Capecchi MR. Mice with targeted disruption of Hoxb-1 fail to form the motor nucleus of the VIIth nerve. of outstanding interest Development. 122:1996;3217-3228 See annotation [28].
28. 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. of outstanding interest Nature. 384:1996;630-634 These reports [27,28] show that Hoxb-1 expression in rhombomere (4) (r4) is an important determinant for the normal development of facial (VII) and vestibuloacoustic (VIII) motor neurons. The initial patterning of r4 appears normal in mice lacking Hoxb-1. However, the axonal projections and cell-body migrations for VII and VIII occur inappropriately in the mutant mice.
29. Fredette BJ, Ranscht B. T-cadherin expression delineates specific regions of the developing motor axon-hindlimb projection pathway. J Neurosci. 14:1994;7331-7346.
30. Ohta K, Nakamura M, Hirokawa K, Tanaka S, Iwama A, Suda T, Ando M, Tanaka H. The receptor tyrosine kinase, Cek8, is transiently expressed on subtypes of motoneurons in the spinal cord during development. Mech Dev. 54:1996;59-69.
31. Kilpatrick TJ, Brown A, Lai C, Gassmann M, Goulding M, Lemke G. Expression of the Tyro4/Mek4/Cek4 gene specifically marks a subset of embryonic motor neurons and their muscle targets. Mol Cell Neurosci. 7:1996;62-74.
32. Ebens A, Brose K, Leonardo ED, Hanson MG Jr, Bladt F, Birchmeier C, Barres BA, Tessier-Lavigne M. Hepatocyte growth factor/scatter factor is an axonal chemoattractant and a neurotrophic factor for spinal motor neurons. Neuron. 17:1996;1157-1172.
33. Marti E, Bumcrot DA, Takada R, McMahon AP. Requirement of 19K form of Sonic hedgehog for induction of distinct ventral cell types in CNS explants. Nature. 375:1995;322-325.
34. Roelink H, Porter JA, Chiang C, Tanabe Y, Chang DT, Beachy PA, Jessell TM. Floor plate and motor neuron induction by different concentrations of the amino-terminal cleavage product of sonic hedgehog autoproteolysis. Cell. 81:1995;445-455.
35. Tanabe Y, Roelink H, Jessell TM. Induction of motor neurons by Sonic Hedgehog is independent of floor plate differentiation. Curr Biol. 5:1995;651-658.
36. Yamada T, Pfaff SL, Edlund T, Jessell TM. Control of cell pattern in the neural tube: motor neuron induction by diffusible factors from notochord and floor plate. Cell. 73:1993;673-686.
37. Ericson J, Morton S, Kawakami A, Roelink H, Jessell TM. Two critical periods of Sonic Hedgehog signaling required for the specification of motor neuron identity. of outstanding interest Cell. 87:1996;661-673 An in vitro assay is used to examine the early steps of motor neuron differentiation initiated by Shh on naive chick neuroepithelial explants. These explants quickly loose their competence to respond to Shh for motor neuron differentiation. By providing Shh at low levels this competence is maintained, but is not sufficient to trigger motor neuron differentiation without increasing the level of Shh. Blocking antibodies for Shh signaling are used to provide evidence that the fate of motor neuron progenitor cells is plastic until the end of S phase.
38. Tremblay P, Pituello F, Gruss P. Inhibition of floor plate differentiation by Pax3: evidence from ectopic expression in transgenic mice. Development. 122:1996;2555-2567.
39. Liem KF Jr, Tremml G, Roelink H, Jessell TM. Dorsal differentiation of neural plate cells induced by BMP-mediated signals from epidermal ectoderm. Cell. 82:1995;969-979.
40. of special interest Ericson J, Rashbass P, Schedl A, Brenner-Morton S, Kawakami A, van Heyningen V, Jessell TM, Briscoe J. Pax6 controls progenitor cell identity and neuronal fate in response to graded Shh signaling. of outstanding interest Cell. 90:1997;169-180 The expression of Pax6 and Nkx2.2 are shown to be regulated by the graded actions of Shh on neuroepithelial cells. At the hindbrain levels, motor neuron subtypes for the vagal and hypoglossal cranial nerves differentiate from different dorsal - ventral positions. The progenitors for hypoglossal motor neurons express Pax6; small eye mutant mice lacking Pax6 fail to generate this class of motor neurons [58].
41. Ericson J, Muhr J, Placzek M, Lints T, Jessell TM, Edlund T. Sonic hedgehog induces the differentiation of ventral forebrain neurons: a common signal for ventral patterning within the neural tube. Cell. 81:1995;747-756.
42. Leber SM, Breedlove SM, Sanes JR. Lineage, arrangement, and death of clonally related motoneurons in chick spinal cord. J Neurosci. 10:1990;2451-2462.
43. Hemond SG, Glover JC. Clonal patterns of cell proliferation, migration, and dispersal in the brainstem of the chicken embryo. J Neurosci. 13:1993;1387-1402.
44. Lumsden A, Clarke JD, Keynes R, Fraser S. Early phenotypic choices by neuronal precursors, revealed by clonal analysis of the chick embryo hindbrain. Development. 120:1994;1581-1589.
45. Tabin CJ, McMahon AP. Recent advances in hedgehog signaling. Trends Cell Biol. 7:1997;442-446.
46. Chiang C, Litingtung Y, Lee E, Young KE, Corden JL, Westphal H, Beachy PA. Cyclopia and defective axial patterning in mice lacking Sonic hedgehog gene function. of special interest Nature. 383:1996;407-413 The targeted mutation of Shh leads to defects in patterning of the ventral neural tube along the entire anterior - posterior neuraxis, demonstrating the critical role this factor plays in vivo.
47. Hynes M, Porter JA, Chiang C, Chang D, Tessier-Lavigne M, Beachy PA, Rosenthal A. Induction of midbrain dopaminergic neurons by Sonic hedgehog. Neuron. 15:1995;35-44.
48. Dale JK, Vesque C, Lints TJ, Sampath TK, Furley A, Dodd J, Placzek M. Cooperation of BMP7 and SHH in the induction of forebrain ventral midline cells by prechordal mesoderm. of outstanding interest Cell. 90:1997;257-269 Using in vitro explant assays, the authors find that BMP7 from prechordal mesoderm modifies the response of cells to Shh. These results demonstrate that axial mesoderm influences the anterior - posterior identity of the early ventral neuroepithelium.
49. Muhr J, Jessell TM, Edlund T. Assignment of early caudal identity to neural plate cells by a signal from caudal paraxial mesoderm. of special interest Neuron. 19:1997;487-502 Explants of the proencephalic region of the chick are used to show that nonaxial mesoderm is the source of a signal that can caudalize the identity of the neuroepithelium.
50. Grapin-Botton A, Bonnin MA, Le Douarin NM. Hox gene induction in the neural tube depends on three parameters: competence, signal supply and paralogue group. Development. 124:1997;849-859.
51. Matise MP, Lance-Jones C. A critical period for the specification of motor pools in the chick lumbosacral spinal cord. of special interest Development. 122:1996;659-669 See annotation [52].
52. Ensini M, Tsuchida TN, Belting H-G, Jessell TM. The control of rostrocaudal pattern in the developing spinal cord: specification of motor neuron subtype identity is initiated by signals from paraxial mesoderm. of special interest Development. 125:1998;969-982 These reports [51,52] combine tissue grafting and marker genes or back-labeling to show that signals from the nonaxial mesoderm can induce the differentiation of specific motor column and motor pool cell identities.
53. Eisen JS, Pike SH. The spt-1 mutation alters segmental arrangement and axonal development of identified neurons in the spinal cord of the embryonic zebrafish. Neuron. 6:1991;767-776.
54. Lance-Jones C, Landmesser L. Motoneurone projection patterns in the chick hind limb following early partial reversals of the spinal cord. J Physiol (Lond). 302:1980;581-602.
55. Guthrie S, Muchamore I, Kuroiwa A, Marshall H, Krumlauf R, Lumsden A. Neuroectodermal autonomy of Hox-2.9 expression revealed by rhombomere transpositions. Nature. 356:1992;157-159.
56. Simon H, Hornbruch A, Lumsden A. Independent assignment of antero-posterior and dorso-ventral positional values in the developing chick hindbrain. Curr Biol. 5:1995;205-214.
57. Pattyn A, Morin X, Cremer H, Goridis C, Brunet JF. Expression and interactions of the two closely related homeobox genes Phox2a and Phox2b during neurogenesis. Development. 124:1997;4065-4075.
58. of outstanding interest Osumi N, Hirota A, Ohuchi H, Nakafuku M, Iimura T, Kuratani S, Fujiwara M, Noji S, Eto K. Pax-6 is involved in the specification of hindbrain motor neuron subtype. of special interest Development. 124:1997;2961-2972 Cranial motor nuclei were examined by neuronal labeling and marker gene expression in small eye (Pax6 mutant) rat embryos. In small eye embryos, the ventral expression of Wnt-7b in the neural tube was not detected, and the abducens and hypoglossal motor nuclei failed to differentiate properly (see also [40]).
59. Henrique D, Adam J, Myat A, Chitnis A, Lewis J, Ish-Horowicz D. Expression of a Delta homologue in prospective neurons in the chick. Nature. 375:1995;787-790.
60. Chitnis A, Henrique D, Lewis J, Ish-Horowicz D, Kintner C. Primary neurogenesis in Xenopus embryos regulated by a homologue of the Drosophila neurogenic gene Delta. Nature. 375:1995;761-766.
61. Appel B, Eisen JS. Regulation of neuronal specification in the zebrafish spinal cord by Delta function. of outstanding interest Development. 125:1998;371-380 The expression of dominant-negative forms of Delta in zebrafish embryos results in the ectopic differentiation of primary motor neurons. The disruption of Notch signaling also leads to a reduction in secondary motor neuron and interneuron number.
62. Ma Q, Kintner C, Anderson DJ. Identification of neurogenin, a vertebrate neuronal determination gene. Cell. 87:1996;43-52.