Expression patterns of transmembrane and released forms of neuregulin during spinal cord and neuromuscular synapse development

Development

Volumn 126, Issue 4, 1999, Pages 781-791

  Loeb, Jeffrey A ^a   Khurana, Tejvir S ^a   Robbins, Janet T ^a   Yee, Ann G ^a   Fischbach, Gerald D ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

ARIA; Chick; Heparan sulfate; Motor neuron; Neuregulin; Neuromuscular junction; Proteoglycan; Spinal cord; Synapse

Indexed keywords

MESSENGER RNA; NEU DIFFERENTIATION FACTOR; PROTEOHEPARAN SULFATE;

ANIMAL CELL; ARTICLE; BASEMENT MEMBRANE; CHICKEN; EMBRYO; EXTRACELLULAR MATRIX; GENE EXPRESSION; GLIA; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MOTONEURON; MOUSE; MUSCLE; NERVE FIBER; NERVOUS SYSTEM DEVELOPMENT; NEUROEPITHELIUM; NEUROMUSCULAR SYNAPSE; NONHUMAN; PRIORITY JOURNAL; SENSORY NERVE CELL; SPINAL CORD;

AMINO ACID SEQUENCE; ANIMALS; CHICK EMBRYO; EMBRYONIC DEVELOPMENT; EXTRACELLULAR MATRIX; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLYCOPROTEINS; HEPARAN SULFATE PROTEOGLYCANS; IMMUNOCHEMISTRY; IN SITU HYBRIDIZATION; MICROSCOPY, ELECTRON; MOLECULAR SEQUENCE DATA; MUSCLE DEVELOPMENT; NEUREGULINS; RNA SPLICING; RNA, MESSENGER; SPINAL CORD;

ANIMALIA; EUKARYOTA; GALLUS GALLUS; MAMMALIA;

EID: 0033046811     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (60)

1. Altiok, N., Bessereau, J. L. and Changeux, J. P. (1995) ErbB3 and ErbB2/neu mediate the effect of heregulin on acetylcholine receptor gene expression in muscle: differential expression at the endplate. EMBO J. 14, 4258-4266.
2. Anderson, M. J. and Fambrough, D. M. (1983) Aggregates of acetylcholine receptors are associated with plaques of a basal lamina heparan sulfate proteoglycan on the surface of skeletal muscle libers. J. Cell Biol. 97, 1396-1411.
3. Anderson, M. J., Klier, F. G. and Tanguay, K. E. (1984) Acetylcholine receptor aggregation parallels the deposition of a basal lamina proteoglycan during development of the neuromuscular junction. J. Cell Biol. 99, 1769-1784.
4. Anton, E. S., Marchionni, M. A., Lee, K. F. and Rakic, P. (1997) Role of GGF/neuregulin signaling in interactions between migrating neurons and radial glia in the developing cerebral cortex. Development 124, 3501-3510.
5. Bayne, E. K., Anderson, M. J. and Fambrough D. M. (1984) Extracellular matrix organization in developing muscle: correlation with acetylcholine receptor aggregates. J. Cell Biol. 99, 1486-1501.
6. Bobrow, M. N., Harris, T. D., Shaughnessy, K. J. and Litt, G. J. (1989) Catalyzed reporter deposition, a novel method of signal amplification. Application to immunoassays. J. Immunol. Meth. 125, 279-285.
7. Bowe, M. A. and J. R. Fallon (1995) The role of agrin in synapse formation. Annu. Rev. Neurosci. 18, 443-462.
8. Burden, S. (1977) Development of the neuromuscular junction in the chick embryo: the number, distribution, and stability of acetylcholine receptors. Dev. Biol. 57, 317-329.
9. Burden, S. and Yarden, Y. (1997) Neuregulins and lheir receptors: A versatile signaling module in organogenesis and oncogenesis. Neuron 18, 847-855.
10. Burgess, T. L., Ross, S. L., Qian, Y., Brankow, D. and Hu, S. (1995). Biosynthetic processing of neu differentiation factor: glycosylation, trafficking, and regulated cleavage from the cell surface. J. Biol. Chem. 270,19188-19196.
11. Busfield, S. J., Michnick, D. A., Chickering, T. W., Revett, T. L., Ma, J., Woolf, E. A., Comrack, C. A., Dussault, B. J., Woolf, J., Goodearl, A. D. and Gearing, D. P. (1997) Characterization of a neuregulin-related gene, Don-1, that is highly expressed in restricted regions of the cerebellum and hippocampus. Mol. Cell. Biol. 17, 4007-4014.
12. Carraway, K. L. 3rd., Weber, J. L., Unger, M. J., Ledesma, J., Yu, N., Gassmann, M. and Lai, C. (1997) Neuregulin-2, a new ligand of ErbB3/ErbB4-receptor tyrosine kinases. Nature 387, 512-516.
13. Chang, H., Riese, D. J. 2nd., Gilbert, W., Stern, D. F. and McMahan, U. J. (1997) Ligands for ErbB-family receptors encoded by a neuregulin-like gene. Nature 387, 509-512.
14. Chiu, A. Y. and Sanes, J. R. (1984). Development of basal lamina in synaptic and extrasynaptic portions of embryonic rat muscle. Dev. Biol. 103, 456-467.
15. + channels in cultured chick muscle is increased by ARIA, an acetylcholine receptor-inducing activity. J. Neurosci. 13, 2118-2125.
16. Corfas, G., Rosen, K. M., Aratake, H., Krauss, R. and Fischbach, G. D. (1995) Differential expression of NRG isoforms in the rat brain. Neuron 14, 103-115.
17. Dieckmann, C. L. and Tzagoloff, A. (1985). Assembly of the mitochondrial membrane system: CBP6, a yeast nuclear gene necessary for synthesis of cytochrome b. J. Biol. Chem. 260, 1513-1520.
18. 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.
19. Fallon, J. R. and Gelfman, C. E. (1989) Agrin-related molecules are concentrated at acetylcholine receptor clusters in normal and aneural developing muscle. J. Cell Biol. 108, 1527-1535.
20. Falls, D. L., Rosen, K. M., Corfas, G., Lane, W. and Fischbach, G. D. (1993). NRG, a protein that stimulates acetylcholine receptor synthesis is a member of the neu ligand family. Cell 72, 801-815.
21. Fischbach, G. D. and Rosen, K. M. (1997) NRG: a neuromuscular junction neuregulin. Annu. Rev. Neurosci. 20, 429-458.
22. Gassmann, M. and Lemke, G. (1997) Neuregulins and neuregulin receptors in neural development. Curr. Opin. Neurobiol. 7, 87-92.
23. Goodearl, A. D., Yee, A. G., Sandrock, A. W. Jr., Corfas, G. and Fischbach, G. D. (1995) ARIA is concentrated in the synaptic basal lamina of the developing chick neuromuscular junction. J. Cell Biol. 130, 1423-1434.
24. Halfter, W., Schurer, B., Yip, J., Yip, L., Tsen, G., Lee, J. A. and Cole, G. J. (1997) Distribution and substrate properties of agrin, a heparan sulfate proteoglycan of developing axonal pathways. J. Comp. Neurol. 383, 1-17.
25. Hamburger, V. (1948) The mitotic patterns in the spinal cord of the chick embryo and their relation to histogenetic processes. J. Comp. Neuro. 88, 221-284.
26. Hamburger, V. and Hamilton, H. (1951) A series of normal stages in the development of the chick embryo. J. Morph. 88, 49-92.
27. Harlow, K. and Lane, D. (1988) Antibodies. A Laboratory Manual. Cold Spring Harbor, New York: Cold Spring Harbor Press.
28. Ho, W. H., Armanini, M. P., Nuijens, A., Phillips, H. S. and Osheroff, P. L. (1995) Sensory and motor neuron-derived factor. A novel heregulin variant highly expressed in sensory and motor neurons. J. Biol. Chem. 270, 14523-14532.
29. Ivins, J. K., Litwack, E. D., Kumbasar, A., Stipp, C. S. and Lander, A. D. (1997) Cerebroglycan, a developmentally regulated cell-surface heparan sulfate proteoglycan, is expressed on developing axons and growth cones. Dev. Biol. 184, 320-332.
30. Jo, S. A., Zhu, X., Marchionni, M. A. and Burden, S. J. (1995) Neuregulins are concentrated at nerve-muscle synapses and activate ACh-receptor gene expression. Nature 373, 158-161.
31. Koenig, M. and Kunkel, L. M. (1990) Detailed analysis of the repeat domain of dystrophin reveals four potential hinge segments that may confer flexibility. J. Biol. Chem. 265, 4560-4566.
32. Kogaya, Y., Kim, S., Haruna, S. and Akisaka, T. (1990). Heterogeneity of distribution pattern at the electron microscopic level of heparan sulfate in various basement membranes. J. Histochem. Cytochem. 38, 1459-1467.
33. Kramer, R., Bucay, N., Kane, D. J., Martin, L. K., Tarpley, J. E. and Theill, L. E. (1996) Neuregulins with an Ig-like domain are essential for mouse myocardial and neuronal development. Proc. Natl. Acad. Sci. USA 93, 4833-4838.
34. Lemke, G. (1996) Neuregulins in development. Mol. Cell. Neurosci. 7, 247-262.
35. Liou, W., Geuze, H. J. and Slot J. W. (1996) Improving structural integrity of cryosections for immunogold labeling. Histochem. Cell Biol. 106, 41-58.
36. Loeb, J. A. and Fischbach, G. D. (1995) NRG can be released from extracellular matrix through cleavage of a heparin-binding domain. J. Cell Biol. 130, 127-135.
37. Loeb, J. A. and Fischbach, G. D. (1997) Neurotrophic factors increase neuregulin expression in embryonic ventral spinal cord neurons. J. Neurosci. 17, 1416-1424.
38. Loeb, J. A., Susanto, F. and Fischbach, G. D. (1998). The neuregulin precursor proARIA is processed to ARIA after expression on the cell surface by a protein kinase C-enhanced mechanism. Mol. Cell. Neurosci. 11, 77-91.
39. Marchionni, M. A., et al. (1993). Glial growth factors are alternatively spliced erbB2 ligands expressed in the nervous system. Nature 362, 312-318.
40. Martinou, J.-C., Falls, D. L., Fischbach, G. D. and Merlie, J. P. (1991) Acetylcholine receptor-inducing activity stimulates expression of the ε-subunit of the muscle acetylcholine receptor. Proc. Natl. Acad. Sci. USA 88, 7669-7673.
41. Massague, J. and Pandiella, A. (1993) Membrane-anchored growth factors. Ann. Rev. Biochem. 62, 515-541.
42. Meyer, D. and Birchmeier, C. (1995) Multiple essential functions of neuregulin in development. Nature. 378, 386-390.
43. Meyer, D., Yamaai, T., Garratt, A., Riethmacher-Sonnenberg, E., Kane, D., Theill, L. E. and Birchmeier, C. (1997) Isotbrm-specific expression and function of neuregulin. Development 124, 3575-3586.
44. Moscoso, L. M., Chu, G. C., Gautam, M., Noakes, P. G., Merlie, J. P. and Sanes, J. R. (1945) Synapse-associated expression of an acetylcholine receptor-inducing protein. NRG/heregulin, its putative receptors, ErbB2 and ErbB3, in developing mammalian muscle. Dev. Biol. 172, 158-169.
45. Orr-Urtreger, A., Trakhtenbrot, L., Ben-Levy, R., Wen, D., Rechavi, G., Lonai, P. and Yarden, Y. (1993). Neural expression and chromosomal mapping of Neu differentiation factor to 8p12-p21. Proc. Natl. Acad. Sci. USA 90, 1867-1871.
46. Peles, E. and Yarden, Y. (1993) Neu and its ligands: From an oncogene to neural factors. BioEssays 15, 815-824.
47. Plaff, S. L., Mendelsohn, M., Stewart, C. L., Edlund, T. and Jessell, T. M. (1996) Requirement for LIM homeobox gene IsI1 in motor neuron generation reveals a motor neuron-dependent step in interneuron differentiation. Cell 84, 309-320.
48. Rio, C., Rief, H. I., Qi, P., Khurana, T. S. and Corfas, G. (1997) Neuregulin and erbB receptors play a critical role in neuronal migration. Neuron 19, 39-50.
49. Sandrock, A. W. Jr., Dryer, S. E., Rosen, K. M., Gozani, S. N., Kramer, R., Theill, L. E. and Fischbach, G. D. (1997). Maintenance of acetylcholine receptor number by neuregulins at the neuromuscular junction in vivo. Science 276, 599-603.
50. Sandrack, A. W. Jr., Goodearl, A. D., Yin, Q. W., Chang, D. and Fischbach, G. D. (1995) NRG is concentrated in nerve terminals at neuromuscular junctions and at other synapses. J. Neurosci. 15, 6124-6136.
51. Shah, N. M., Marchionni, M. A., Isaacs, I., Stroobant, P. and Anderson, D. J. (1994). Glial growth factor restricts mammalian neural crest stem cells to a glial line. Cell 77, 349-360.
52. Slot, J. W. and Geuze H. J. (1985) A new method of preparing gold probes for multiple- labeling cytochemistry. Eur. J. Cell Biol. 38, 87-93.
53. Swenarchuk, L. E., Shashikant, C. and Anderson, M. J. (1990) Induction of a specialized muscle basal lamina at chimaeric synapses in culture. Development 111, 51-61.
54. Tokuyasu, K. T. (1989) Use of poly(vinylpyrrolidone) and polyl(vinyl alcohol) for cryoultramicrotomy. Histochemical J. 21, 163-171.
55. Tsen, G., Halfter, W., Kroger, S. and Cole, G. J. (1995) Agrin is a heparan sulfate proteoglycan. J. Biol. Chem. 270, 3392-3399.
56. Tsuchida, T., Ensini, M., Morton, S. B., Baldassare, M., Edlund, T., Jessell, T. M. and Plaff, S. L. (1994). Topographic organization of embryonic motor neurons defined by expression of LIM homeobox genes. Cell 79, 957-970.
57. Trachtenberg, J. T. and Thompson, W. J. (1996) Schwann cell apoptosis at developing neuromuscular junctions is regulated by glial growth factor. Nature 379, 174-177.
58. Yang, X., Kuo, Y., Devay, P., Yu, C. and Role, L. (1998) A cysleine-rich isoform of neuregulin controls the level of expression of neuronal nicotinic receptor channels during synaptogenesis. Neuron 20, 255-270.
59. Zhang, D., Sliwkowski, M. X., Mark, M., Frantz, G., Akita, R., Sun, Y., Hillan, K., Crowley, C., Brush, J. and Godowski, P. J. (1997) Neuregulin-3 (NRG3): a novel neural tissue-enriched protein that binds and activates ErbB4. Proc. Natl. Acad. Sci. USA 94, 9562-9567.
60. Zhu X., Lai, C., Thomas, S. and Burden, S. J. (1995) Neuregulin receptors, erbB3 and erbB4, are localized at neuromuscular junctions. EMBO J. 14, 5842-5848.