Complementary expression of transmembrane ephrins and their receptors in the mouse spinal cord: A possible role in constraining the orientation of longitudinally projecting axons

Development

Volumn 127, Issue 7, 2000, Pages 1397-1410

  Imondi, Ralph ^a   Wideman, Christi ^a   Kaprielian, Zaven ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

B class Eph receptors; B class ephrins; Commissural axons; Floor plate; Midline repellent; Mouse; Ventral funiculus; Ventral midline

Indexed keywords

EPHRIN; MEMBRANE PROTEIN; MEMBRANE RECEPTOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN COMMISSURE; CONTROLLED STUDY; EMBRYO; GROWTH CONE; MOUSE; NERVE FIBER; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPINAL CORD; VENTRAL ROOT;

ANIMALS; AXONS; BODY PATTERNING; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GROWTH CONES; IN SITU HYBRIDIZATION; LIGANDS; MEMBRANE PROTEINS; MICE; PREGNANCY; RECEPTOR PROTEIN-TYROSINE KINASES; RECEPTOR, EPHB4; RECEPTORS, EPH FAMILY; RNA, MESSENGER; SPINAL CORD;

ANIMALIA;

EID: 0034009748     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (65)

1. Altman, J. and Bayer, S. (1984). The development of the rat spinal cord. Adv. Anat. Embryol. Cell Biol. 85, 1-165.
2. Ba-Charvet, K., Brose, K., Marillat, V., Kidd, T., Goodman, C., Tessier-Lavigne, M., Sotelo, C. and Chedotal, A. (1999). Slit2-mediated chemorepulsion and collapse of developing forebrain axons. Neuron 22, 463-473.
3. Bennett, B., Zeigler, K, Gu, Q., Fendly, B., Goddard, A., Gillett, N. and Matthews, W. (1995). Molecular cloning of a ligand for the EPH-related receptor protein-tyrosine kinase Htk. Proc. Natn. Acad. Sci. USA 92, 1866-1870.
4. Bergemann, A., Zhang, L., Chiang, M.-K., Brambilla, R., Klein, R. and Flanagan, J. (1998). Ephrin-B3, a ligand for the receptor EphB3, expressed at the midline of the developing neural tube. Oncogene 16, 471-480.
5. Bouillet, P., Oulad-Abdelghani, M., Vicaire, S., Garnier, J.-M., Schuhbaur, B., Dolle, P. and Chambon, P. (1495). Efficient cloning of cDNAs of retinoic acid-responsive genes in P19 embryonal carcinoma cells and characterization of a novel mouse gene. Stra1 (mouse LERK-2/EPIg2). Dev. Biol. 170, 420-433.
6. Buvolenta, P. and Dodd, J. (1990), Guidance of commissural growth cones at the floor plate in embryonic rat spinal cord. Development 109, 435-447.
7. Bovolenta, P. and Dodd, J. (1991). Perturbation of neuronal differentiation and axon guidance in the spinal cord of mouse embryos lacking a floor plate: analysis of Danforth's short tail mutation. Development 113, 625-639.
8. Brambilla, R., Bruckner, K., Orioli, D., Bergemann, A., Flanagan, J. and Klein, R. (1996). Similarities and differences in the way transmembrane-type ligands interact with the Elk subclass of Eph receptors. Mol. Cell Neurol. 8, 199-209.
9. Brose, K., Bland, K., Wang, K., Arnott, D., Henzel, W., Goodman, C., Tessier-Lavigne, M. and Kidd, T. (1999). Slit proteins bind Robo receptors and have an evolutionary conserved role in repulsive axon guidance. Cell 96, 795-806.
10. Callahan, C., Muralidhar, M., Lundgren, S., Scully, A. and Thomas, J. (1995). Control of neuronal pathway selection by a Drosophila receptor protein-tyrosine kinase family member. Nature 376, 171-174.
11. Chen, H., Chedotal, A., He, Z., Goodman, C. and Tessier-Lavigne, M. (1997). Neuropilin-2, a novel member of the neuropilin family, is a high affinity receptor for the semaphorins Sema E and Sema IV but not Sema III. Neuron 19, 547-559.
12. Ciossek, T., Lerch, M. and Ullrich, A. (1995). Cloning, characterization, and differential expression of MDK2 and MDK5, two novel receptor tyrosine kinases of the eck/eph family. Oncogene 11, 2085-2095.
13. Clarke, J., Holder, N., Soffe, S. and Storm-Mathisen, J. (1991). Neuroanatomical and functional analysis of neural tube formation in notochordless Xenopus embryos: laterality of the ventral spinal cord is lost. Development 112, 499-516.
14. Cohen, N., Taylor, J., Scott, L., Guillery, R., Soriano, P. and Furley, A. (1997). Errors in corticospinal axon guidance in mice lacking the neural cell adhesion molecule L1. Curr. Biol. 8, 26-33.
15. Colamarino, S. and Tessier-Lavigne, M. (1995). The role of the floor plate in axon guidance. Ann. Rev. Neurosci. 18, 497-529.
16. Cooper, H., Armes, P., Britto, J., Gad, J. and Wilks, A. (1995). Cloning of the mouse homologue of the deleted in colorectal cancer gene (mDCC) and its expression in the developing mouse embryo. Oncogene 11, 2243-2254.
17. Davis, S., Gale, N., Aldrich, T., Maisonpierre, P., Lhotak, V., Pawson, T., Goldfarb, M. and Yancopoulos, G. (1994). Ligands for the EPH-related receptor tyrosine kinases that require membrane attachment or clustering for activity. Science 266, 816-819.
18. Dodd, J., Morton, S., Karagogeos, D., Yamamoto, M. and Jessell, T. (1988). Spatial regulation of axonal glycoprotein expression on subsets of embryonic spinal neurons. Neuron 1, 105-116.
19. Fazeli, A., Dickinson, S., Hermiston, M., Tighe, R., Steen, R., Small, C., Stoeckli, E., Keino-Masu, K., Masu, M., Rayburn, H., Simons, J., Bronson, R., Gordon, J., Tessier-Lavigne, M. and Weinberg, R. (1997). Phenotype of mice lacking functional Deleted in Colorectal Carcinoma (DCC) gene. Nature 386, 796-804.
20. Flanagan, J. and Vactor, D. V. (1998). Through the looking glass: Axon guidance at the midline choice point. Cell 92, 429-432.
21. Flanagan, J. and Vanderhaeghen, P. (1998). The ephrins and Eph receptors in neural development. Ann. Rev. Neurosci. 21, 309-345.
22. Flenniken, A., Gale, N., Yancopoulos, G. and Wilkinson, D. (1996). Distinct and overlapping expression patterns of ligands for Eph-related tyrosine kinases during mouse emhryogenesis. Dev. Biol. 179, 382-401.
23. Gale, N., Flenniken, A., Compton, D., Jenkins, N., Copeland, N., Gilbert, D., Davis, S., Wilkinson, D. and Yancopoulos, G. (1996a). Elk-L3, a novel transmembrane ligand for the Eph family of receptor tyrosine kinases. expressed in embryonic floor plate, roof plate and hindbrain segments. Oncogene 13, 1343-1352.
24. Gale, N., Holland, S., Valenzuela, D., Flenniken, A., Pan, L., Ryan, T., Henkemeyer, M., Strebhardt, K., Hirai, H., Wilkinson, D., Pawson, T., Davis, S. and Yancopoulos, G. (1996b). Eph receptors and ligands comprise two major specificity subclasses and are reciprocally compartmentalized during embryogenesis. Neuron 17, 9-19.
25. Gale, N. and Yancopoulos, G. (1997). Ephrins and their receptors: a repulsive topic? Cell Tiss. Res. 290, 227-241.
26. Hatta, K. (1992). Role of the floor plate in axonal patterning in the zebrafish CNS. Neuron 9, 629-642.
27. Helms, A. and Johnson, J. (1998). Progenitors of dorsal commissural interneurons are defined by MATH1 expression. Development 125, 919-928.
28. Henkemeyer, M., Marengere, L., McLade, J., Olivier, J., Conlon, R., Holmyard, D., Letwin, K. and Pawson, T. (1994). Immunolocalization of the Nuk receptor tyrosine kinase suggests roles in segmental patterning of the brain and axogenesis. Oncogene 9, 1001-1014.
29. Henkemeyer, M., Orioli, D., Henderson, J., Saxton, T., Roder, J., Pawson, T. and Klein, R. (1996). Nuk controls pathfinding of commissural axons in the mammalian central nervous system. Cell 86, 35-46.
30. Holder, N. and Klein, R. (1999). Eph receptors and ephrins: effectors of morphogenesis. Development 126, 2033-2044.
31. Itoh, A., Miyabayashi, T., Ohno, M. and Sakano, S. (1998). Cloning and expression of three mammalian homologs of Drosophila Slit suggest possible roles for Slit in the formation and maintenance of the nervous system. Mol. Brain Res. 62, 175-186.
32. Kaprielian, Z., Cho, K.-O., Hadjiargyrou, M. and Patterson, P. H. (1995). CD9, a major platelet cell surface glycoprotein, is a ROCA antigen and is expressed in the nervous system. J. Neurosci. 15, 562-573.
33. Karagogeos, D., Morton, S., Casano, F., Dodd, J. and Jessell, T. (1991). Developmental expression of the axonal glycoprotein TAG-1: differential regulation by central and peripheral neurons in vitro. Development 112, 51-67.
34. Kennedy, T., Serafini, T., delaTorre, J. and Tessier-Lavigne, M. (1994). Netrins are diffusible chemotropic factors for commissural axons in the embryonic spinal cord. Cell 78, 425-435.
35. Kidd, T., Bland, K. and Goodman, C. (1999). Slit is the midline repellent for the Robo receptor in Drosophila. Cell 96, 785-794.
36. Kidd, T., Brose, K., Mitchell, K., Fetter, R., Tessier-Lavigne, M., Goodman, C. and Tear, G. (1998a). Roundabout controls axon crossing of the CNS midline and defines a novel subfamily of evolutionarily conserved guidance receptors. Cell 92, 205-215.
37. Kidd, T., Russell, C., Goodman, C. and Tear, G. (1998b). Dosage-sensitive and complementary functions of roundabout and commissureless control axon crossing of the CNS midline. Neuron 20, 25-33.
38. Krull, C., Iansford, R., Gale, N., Collazo, A., Marcelle, C., Yancopoulos, G., Fraser, S. and Bronner-Fraser, M. (1997). Interactions of Eph-related receptors and ligands confer rostrocaudal pattern to trunk neural crest migration. Curr. Biol. 7, 571-580.
39. Leonardo, K., Hinck, L., Masu, M., Keino-Masu, K., Ackerman, S, and Tessier-Lavigne, M. (1947). Vertebrate, homologues of C. elegans UNC-5 are candidate netrin receptors. Nature 386, 833-838.
40. Li, H.-s., Chen, J.-h., Wu, W., Fagaly, T., Zhou, L., Yuan, W., Dupuis, S., Jiang, Z.-h., Nash, W., Gick, C., Ornitz, D., Wu, J. and Rao, Y. (1999). Vertebrate Slit, a secreted ligand for the transmembrane protein roundabout is a repellent for olfactory bulb axons. Cell 96, 807-818.
41. Matise, M., Lustig, M., Sakurai, T., Grumet, M. and Joyner, A. (1999). Ventral midline cells are required for the local control of commissural axon guidance in the mouse spinal cord. Developmental 126, 3649-1659.
42. Moscoso, I., and Sanes, J. (1995). Expression of four immunoglobulin superfamily adhesion molecules (L1, Nr-CAM/Bravo, Neurofascin/ABGP, and N-CAM) in the developing mouse spinal cord. J. Comp. Neurol. 352, 321-334.
43. Myers, P. and Bastiani, M. (1993). Cell-cell interactions during the migration of an identified commissural growth cone in the embryonic grasshopper. J. Neurosci. 13, 115-126.
44. Ohta, K., Nakamura, M., Hirokawa, K., Tanaka, S., Iwama, A., Suda, T., Ando, M. and Tanaka, H. (1996). The receptor tyrosine kinase. Cek8,is transiently expressed on subtypes of notorneurons in the spinal cord during development. Mech. Dev. 54, 59-69.
45. Orioli, D., Henkemeyer, M., Lemke, G., Klein, R. and Pawson, T. (1996). Sek4 and Nuk receptors cooperate in guidance of commissural axons and in palate formation. EMBO J. 15, 6035-6049.
46. Orioli, D. and Klein, R. (1997). The Eph receptor family: axon guidance by contact repulsion. Trends Genet. 13, 354-359.
47. Sakano, S., Serizawa, R., Inada, T., Iwama, A., Itoh, A., Kato, C., Shimizu, Y., Shinkai, K. Shimizu, R., Kondo, S., Ohna, M. and Suda, T. (1996). Characterization of a ligand for receptor protein-tyrosine kinase HTK expressed in immature hematopoietic cells. Oncogene 13, 813-822.
48. Saueressig, H., Burrill, J. and Goulding, M. (1999). Engrailed-1 and netrin-1 regulate axon pathfinding by association interneurons that project to motor neurons. Development 126, 4201-4212.
49. Scully, A., McKeown, M. and Thomas, J. (1999). Isolation and characterization of Dek, a Drosophila Eph receptor protein tyrosine kinase. Mol. Cell Neurosci. 13, 337-347.
50. Seeger, M., Tear, G., Ferres-Marco, D. and Goodman, C. (1993). Mutations affecting growth cone guidance in Drosophila: Genes necessary for guidance toward or away from the midline. Neuron 10, 409-426.
51. Serafini, T., Colamarino, S., Leonardo, K., Wang, H., Beddington, R., Skarnes, W. and Tessier-Lavigne, M. (1996). Netrin-1 is required for commissural axon guidance in the developing vertebrate nervous system. Cell 87, 1001-1014.
52. Serafini, T., Kennedy, T., Galko, M., Mirzayan, C., Jessell, T. 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.
53. Shirasaki, R., Mirzayan, C., Tessier-Lavigne, M. and Murakami, F. (1996). Guidance of circumferentially growing axons by netrin-dependent and -independent floor plate chemotropism in the vertebrate brain. Neuron 17, 1079-1088.
54. Silos-Santiago, I. and Snider, W. (1992). Development of commissural neurons in the embryonic rat spinal cord. J. Comp. Neurol. 325, 514-526.
55. Silos-Santiago, I. and Snider, W. (1994). Development of interneurons with ipsilateral projections in embryonic rat spinal cord. J. Comp. Neurol. 342, 221-231.
56. Stoeckli, K. and Landmesser, L. (1995). Axonin-1, Nr-CAM, and Ng-CAM play different roles in the in vivo guidance of chick commissural neurons. Neuron 14, 1165-1179.
57. Stoeckli, K. and Landmesser, L. (1998). Axon guidance at choice points. Curr: Opin. Neurobiol. 8, 73-79.
58. Stoeckli, E., Sondregger, P., Pollerberg, G. and Landmesser, L. (1997). Interference with Axonin-1 and NrCAM interactions unmasks a floor-plate activity inhibitory for commissural axons. Neuron 18, 209-221.
59. Takahashi, T., Nakamura, F. and Strittmatter, S. (1997). Neuronal and non-neuronal collapsin-1 binding sites in the developing chick are distinct from other semaphorin binding sites. J. Neurosci. 17, 9183-9193.
60. Tear, G., Harris, R., Sutaria, S., Kilomanski, K., Goodman, C. and Seeger, M. (1996). commissureless controls growth cone guidance across the CNS midline in Drosophila and encodes a novel membrane protein. Neuron 16, 501-514.
61. Thomas, J. (1998). Axon guidance: crossing the midline. Curr. Biol. 8, R102-R104.
62. Wang, H. and Anderson, D. (1997). Eph family transmembrane ligands can mediate repulsive guidance of trunk neural crest migration and motor axon outgrowth. Neuron 18, 383-396.
63. Wang, K., Brose, K., Arnott, D., Kidd, T., Goodman, C., Henzel, W. and Tessier-Lavigne, M. (1999). Biochemical purification of a mammalian Slit protein as positive regulator of sensory axon elongation and branching. Cell 96, 771-784.
64. Yue, Y., Widmer, D. A. J., Halladay, A. K., Ceretti, D. P., Wagner, G. C., Dreyer, J.-L. and Zhou, R. (1999). Specification of distinct dopaminergic neural pathways: roles of the Eph family receptor EphB1 and ligand ephrinB2. J. Neurosci. 19, 2090-2101.
65. Zhu, Q., Runko, E., Imondi, R., Milligan, T., Kapitula, D. and Kaprielian, Z. (1998). New cell surface marker of the rat floor plate and notochord. Dev. Dynam. 211, 314-326.