The Eph kinase ligand AL-1 is expressed by rostral muscles and inhibits outgrowth from caudal neurons

Molecular and Cellular Neurosciences

Volumn 8, Issue 2-3, 1996, Pages 185-198

  Donoghue, Maria J ^a,b   Lewis, Renate M ^a   Merlie, John P ^a   Sanes, Joshua R ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE PROTEIN;

ARTICLE; CELL CULTURE; HYBRIDIZATION; NERVE FIBER GROWTH; NERVE PROJECTION; PRIORITY JOURNAL; SENSORY GANGLION; SPINAL CORD;

EID: 0030221910     PISSN: 10447431     EISSN: None     Source Type: Journal    
DOI: 10.1006/mcne.1996.0056     Document Type: Article

References (58)

1. Altschul, S. F., Gish, W., Miller, W., Myers, E. W., and Lipman, D. J. (1990). Basic local alignment search tool. J. Mol. Biol 215: 403-410.
2. Aviv, H., and Leder, P. (1972). Purification of biologically active globin messenger RNA by chromatography on oligothymidylic acid-cellulose. Proc. Natl. Acad. Sci. USA 69: 1408-1412.
3. Becker, N., Seitanidou, T., Murphy, P., Mattei, M. G., Topilko, P., Nieto, M. A., Wilkinson, D. G., Charnay, P., and Gilardi-Hebenstreit, P. (1994). Several receptor tyrosine kinase genes of the Eph family are segmentally expressed in the developing hindbrain. Mech. Dev. 47: 3-17.
4. Bergemann, A. D., Cheng, H. J., Brambilla, R., Klein, R., and Flanagan, J. G. (1995). Elf-2, a new member of the Eph ligand family, is segmentally expressed in mouse embryos in the region of the hindbrain and newly forming somites. Mol. Cell. Biol. 15: 4921-4929.
5. Brambilla, R., and Klein, R. (1995). Telling axons where to grow: A role for Eph receptor tyrosine kinases in guidance. Mol. Cell. Neurosci. 6: 487-495.
6. Brambilla, R., Schnapp, A., Casagranda, F., Labrador, J. P., Bergemann, A. D., Flanagan, J. G., Pasquale, E. B., and Klein, R. (1995). Membrane-bound LERK2 ligand can signal through three different Eph-related receptor tyrosine kinases. EMBO J. 14: 3116-3126.
7. Brennan, T. J., and Olson, E. N. (1990). Myogenin resides in the nucleus and acquires high affinity for a conserved enhancer element on heterodimerization. Genes Dev. 4: 582-595.
8. Chen, C., and Okayama, H. (1987). High-efficiency transformation of mammalian cells by plasmid DNA. Mol. Cell. Biol. 7: 2745-2752.
9. Cheng, H.-J., and Flanagan, J. G. (1994). Identification and cloning of ELF-1, a developmentally expressed ligand for the Mek-4 and Sek receptor tyrosine kinases. Cell 79: 157-168.
10. Cheng, H.-J., Nakamoto, M., Bergemann, A. D., and Flanagan, J. G. (1995). Complementary gradients in expression and binding of ELF-1 and Mek-4 in development of the topographic retinotectal projection map. Cell 82: 371-381.
11. Chomczynski, P., and Sacchi, N. (1987). Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162: 156-159.
12. Covault, J., and Sanes, J. R. (1986). Distribution of N-CAM in synaptic and extrasynaptic portions of developing and adult skeletal muscle. J. Cell Biol. 102: 716-730.
13. Davis, C. A., Holmyard, D. P., Millen, K. J., and Joyner, A. L. (1991). Examining pattern formation in mouse, chicken and frog embryos with an En-specific antiserum. Development 111: 287-298.
14. Donoghue, M. J., and Sanes, J. R. (1994). All muscles are not created equal. Trends Genet. 10: 395-401.
15. Donoghue, M. J., Merlie, J. P., Rosenthal, N., and Sanes, J. R. (1991a). A rostrocaudal gradient of transgene expression in adult skeletal muscle. Proc. Natl. Acad. Sci. USA 88: 5847-5851.
16. Donoghue, M. J., Alvarez, J. D., Merlie, J. P., and Sanes, J. R. (1991b). Fiber type and position-dependent expression of a myosin light chain chloramphenicol acetyltransferase (CAT) transgene detected with a novel histochemical stain for CAT. J. Cell Biol. 115: 423-434.
17. Donoghue, M. J., Morris-Valero, R., Johnson, Y. R., Merlie, J. P., and Sanes, J. R. (1992a). Mammalian muscle cells bear a cell-autonomous, heritable memory of their rostrocaudal position. Cell 69: 67-77.
18. Donoghue, M. J., Patton, B. L., Sanes, J. R., and Merlie, J. P. (1992b). An axial gradient of transgene methylation in murine skeletal muscle: Genomic imprint of rostrocaudal position. Development 116: 1101-1112.
19. Drescher, U., Kremoser, C., Handwerker, C., Loschinger, J., Noda, M., and Bonhoeffer, F. (1995). In vitro guidance of retinal ganglion cell axons by RAGS, a 25 kDa tectal protein related to ligands for Eph receptor tyrosine kinases. Cell 82: 359-370.
20. Fukushima, M., Nakamura, M., Ohta, K., Okamura, R., Negi, A., and Tanaka, H. (1996). Regional specification of motor neurons along the anterior-posterior axis is independent of the notocord. Development 122: 905-914.
21. Gale, N. W., Holland, S. J., Valenzuela, D. W., Flenniken, A., Pan, L., Ryan, T. E., Henkemeyer, M., Strebhardt, K., Hirai, H., Wilkinson, D. G., Pawson, T., Davis, S., and Yancopoulos, G. D. (1996). Eph receptors and ligands comprise two major specificity subclasses, and are reciprocally compartmentalized during embryogenesis. Neuron 17: 9-19.
22. Ganju, P., Shigemoto, K., Brennan, J., Entwistle, A., and Reith, A. D. (1994). The Eck receptor tyrosine kinase is implicated in pattern formation during gastrulation, hindbrain segmentation and limb development. Oncogene 9: 1613-1624.
23. Girard, L. R., Castle, A. M., Hand, A. R., Castle, J. D., and Mirels, L. (1993). Characterization of common salivary protein I, a product of rat submandibular, sublingual and parotid glands. J. Biol. Chem. 268: 26592-26601.
24. Goodman, C. S. (1996). Mechanisms and molecules that control growth cone guidance. Annu. Rev. Neurosci. 59: 341-377.
25. Henkemeyer, M., Orioli, D., Henderson, J. T., Saxton, T. M., Roder, J., Pawson, T., and Klein, R. (1996). Nuk controls pathfinding of commissural axons in the mammalian central nervous system. Cell 86: 35-46.
26. Holash, J. A., and Pasquale, E. B. (1995). Polarized expression of the receptor protein tyrosine kinase Cek5 in the developing avian visual system. Dev. Biol. 172: 683-693.
27. Kaprielian, Z., and Patterson, P. H. (1994). The molecular basis of retinotectal topography. Bioessays 16: 1-11.
28. Kenny, D., Bronner-Fraser, M., and Marcelle, C. (1995). The receptor tyrosine kinase QEK-5 mRNA is expressed in a gradient within the neural retina and the tectum. Dev. Biol. 172: 708-716.
29. Kilpatrick, T. J., Brown, A., Lai, C., Gassmann, M., Goulding, M., and Lemke, G. (1996). Expression of the Tyro4/Mek4/Cek4 gene specifically marks a subset of embryonic motor neurons and their muscle targets. Mol. Cell. Neurosci. 7: 62-74.
30. Langley, J. N. (1897). On the regeneration of pre-ganglionic and of post-ganglionic visceral nerve fibres. J. Physiol. (London) 22: 215-230.
31. Laskowski, M. B., and Owens, J. L. (1994). Embryonic expression of motoneuron topography in the rat diaphragm muscle. Dev. Biol. 166: 502-508.
32. Laskowski, M. B., and Sanes, J. R. (1987). Topographic mapping of motor pools onto skeletal muscles. J. Neurosci. 7: 252-260.
33. Laskowski, M. B., and Sanes, J. R. (1988). Topographically selective reinnervation of adult mammalian skeletal muscles. J. Neurosci. 8: 3094-3099.
34. Logan, C., Khoo, W. K., Cado, D., and Joyner, A. L. (1993). Two enhancer regions in the mouse En-2 locus direct expression to the mid/hindbrain region and mandibular myoblasts. Development 117: 905-916.
35. Melton, D. A., Krieg, P. A., Rebagliati, M. R., Maniatis, T., Zinn, K., and Green, M. R. (1984). Efficient in vitro synthesis of biologically active RNA and RNA hybridization probes from plasmids containing a bacteriophage SP6 promoter. Nucleic Acids Res. 12: 7035-7056.
36. Moscoso, L. M., Merlie, J. P., and Sanes, J. R. (1995). N-CAM, 43K-rapsyn, and s-laminin mRNAs are concentrated at synaptic sites in muscle fibers. Mol. Cell. Neurosci. 6: 80-89.
37. Moscovici, C., Moscovici, M. G., Jimenez, H., Lai, M. M., Hayman, M. J., and Vogt, P. K. (1977). Continuous tissue culture cell lines derived from chemically induced tumors of Japanese quail. Cell 11: 95-103.
38. Mulle, C., Benoit, P., Pinset, C., Roa, M., and Changeux, J.-P. (1988). Calcitonin gene related peptide enhances the rate of desensitization of the nicotinic acetylcholine receptor in cultured mouse muscle cells. Proc. Natl. Acad. Sci. USA 85: 5728-5732.
39. Ohta, K., Nakamura, M., Hirokawa, K., Tanaka, S., Iwana, A., Suda, T., Ando, M., and Tanaka, H. (1996). The receptor tyrosine kinase, Cek8, is transiently expressed on subtypes of motor neurons in the spinal cord during development. Mech. Dev. 54: 59-69.
40. Porteus, M. H., Brice, A. E., Bulfone, A., Usdin, T. B., Ciaranello, R. D., and Rubenstein, J. L. (1992). Isolation and characterization of a library of cDNA clones that are preferentially expressed in the embryonic telencephelon. Mol. Brain Res. 12: 7-22.
41. Purves, D., Thompson, W., and Yip, J. W. (1981). Re-innervation of ganglia transplanted to the neck from different levels of the guinea-pig sympathetic chain. J. Physiol. 313: 49-63.
42. Rao, M. V., Donoghue, M. J., Merlie, J. P., and Sanes, J. R. (1996). Distinct regulatory elements control muscle-specific, fiber type-selective, and axially graded expression of a myosin light-chain gene in transgenic mice. Mol. Cell. Biol. 16: 3909-3922.
43. Rubenstein, J. L. R., Brice, A. E., Ciaranello, R. D., Denney, D., Porteus, M. H., and Usdin, T. B. (1990). Subtractive hybridization system using single-stranded phagemids with directional inserts. Nucleic Acids Res. 18: 4833-4842.
44. Rutishauser, U., and Edelman, G. M. (1980). Effects of fasciculation on the outgrowth of neurites from spinal ganglia in culture. J. Cell Biol. 87: 370-378.
45. Sambrook, J., Fritsch, E. F., and Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
46. Sanes, J. R. (1993). Topographic maps and molecular gradients. Curr. Opin. Neurobiol. 3: 67-74.
47. Sperry, R. W. (1963). Chemoaffinity in the orderly growth of nerve fiber patterns and connections. Proc. Natl. Acad. Sci. USA 50: 703-710.
48. Spiegelman, B. M., Frank, M., and Green, H. (1983). Molecular cloning of mRNA from 3T3 adipocytes: Developmental regulation of glyceriphosphate dehydrogenase and other differentiation-dependent proteins during adipocyte development. J. Biol. Chem. 258: 10083-10089.
49. Tuzi, N. L., and Gullick, W. J. (1994). Eph, the largest known family of putative growth factor receptors. Br. J. Cancer Res. 69: 417-421.
50. Udin, S. B., and Fawcett, J. W. (1988). Formation of topographic maps. Annu. Rev. Neurosci. 11: 289-327.
51. Velleca, M. A., Wallace, M. C., and Merlie, J. P. (1994). A novel synapse-associated noncoding RNA. Mol. Cell. Biol. 14: 7095-7104.
52. Wigston, D. J., and Sanes, J. R. (1982). Selective reinnervation of adult mammalian muscle by axons from different segmental levels. Nature 299: 464-467.
53. Wigston, D. J., and Sanes, J. R. (1985). Selective reinnervation of intercostal muscles transplanted from different segmental levels to a common site. J. Neurosci. 5: 1208-1221.
54. Winslow, J. W., Moran, P., Valverde, J., Shih, A., Yuan, J. Q., Wong, S. C., Tsai, S. P., Goddard, A., Henzel, W. J., Hefti, F., Beck, K. D., and Caras, I. W (1995). Cloning of AL-1, a ligand for an Eph-related tyrosine kinase receptor involved in axon bundle formation. Neuron 14: 973-981.
55. 2--dependent synaptic release delays motor neuron differentiation in the rat spinal cord. J. Neurosci. 15: 5900-5911.
56. Xu, Q., Alldus, G., Holder, N., and Wilkinson, D. G. (1995). Expression of truncated Sek-1 receptor tyrosine kinase disrupts the segmental restriction of gene expression in the Xenopus and zebrafish hindbrain. Development 121: 4005-4016.
57. Xu, Q., Alldus, G., MacDonald, R., Wilkinson, D. G., and Holder, N. (1996). Function of the Eph-related kinase RTK1 in patterning of the zebrafish forebrain. Nature 381: 319-322.
58. Yaffe, D. (1968). Retention of differentiation potentialities during prolonged cultivation of myogenic cells. Proc. Natl. Acad. Sci. USA 61: 477-483.