Neuregulin expression in PNS neurons: Isoforms and regulation by target interactions

Molecular and Cellular Neurosciences

Volumn 10, Issue 3-4, 1997, Pages 184-195

  Bermingham Mcdonogh, Olivia ^a   Xu, Yi Tian ^b   Marchionni, Mark A ^a   Scherer, Steven S ^b  

^a CeNeS Pharmaceuticals plc   (United States)

^b HOSPITAL OF THE UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Axon Schwann cell interactions; Axotomy; Motor neurons; Sensory neurons; Trophic factors

Indexed keywords

ISOPROTEIN; NEU DIFFERENTIATION FACTOR;

ADOLESCENT; ANIMAL TISSUE; ARTICLE; CELL INTERACTION; IN SITU HYBRIDIZATION; MOTONEURON; NERVE FIBER TRANSECTION; NERVE REGENERATION; NONHUMAN; NORTHERN BLOTTING; PERIPHERAL NERVOUS SYSTEM; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REINNERVATION; SCHWANN CELL; SENSORY NERVE CELL;

ANIMALIA;

EID: 0031410876     PISSN: 10447431     EISSN: None     Source Type: Journal    
DOI: 10.1006/mcne.1997.0654     Document Type: Article

References (67)

1. Bargman C. I., Hung M. C., Weinberg R. A. The New oncogene encodes an epidermal growth factor related receptor. Nature. 319:1986;226-230.
2. Bermingham-McDonogh O., McCabe K. L., Reh T. A. Effects of GGF/neuregulins on neuronal survival and neurite outgrowth correlate with erbB2/neu expression in developing rat retina. Development. 122:1996;1427-1438.
3. Bisby M. A. Regeneration of peripheral system axons. The Axon. 1995;Oxford Univ. Press. p. 553-578.
4. Brockes J. P. Assay and isolation of glial growth factor from the bovine pituitary. Methods Enzymol. 147:1987;217-225.
5. Burden S., Yarden Y. Neuregulins and their receptors: A versatile signaling module in organogenesis and oncogenesis. Neuron. 18:1997;847-855.
6. Busfield S. J., Michnick D. A., Chickering T. W., Revett T. L., Ma J. Y., Woolf E. A., Comrack C. A., Dussault B. J., Woolf J., Goodearl A. D. J., Gearing D. P. Characterization of a neuregulin-related gene, Don-1 that is highly expressed in restricted regions of the cerebellum and hippocampus. Mol. Cell. Biol. 17:1997;4007-4014.
7. Canoll P. D., Musacchio J. M., Hardy R., Reynolds R., Marchionni M. A., Salzer J. L. GGF/neuregulin is a neuronal signal that promotes the proliferation and survival and inhibits the differentiation of oligodendrocyte progenitors. Neuron. 17:1996;229-243.
8. Carraway K. L., Cantley L. C. A neu acquaintance for erbB3 and erbB4: A role for receptor heterodimerization in growth signaling. Cell. 78:1994;5-8.
9. Carraway K. L., Weber J. L., Unger M. J., Ledesma J., Yu N., Gassman M., Lai C. Neuregulin-2, a new ligand of ErbB3/ErbB4-receptor tyrosine kinases. Nature. 387:1997;512-516.
10. Carroll S. L., Miller M. L., Frohert P. W., Kim S. S., Corbett J. A. Expression of neuregulins and their putative receptors, ErbB2 and ErbB3, is induced during Wallerian degeneration. J. Neurosci. 17:1997;1642-1659.
11. Chang H., Riese D. J., Gilbert W., Stern D. F., McMahan U. J. Ligands for ErbB-family receptors encoded by a neuregulin-like gene. Nature. 387:1997;509-512.
12. Chen M. S., Bermingham-McDonogh O., Danehy F. T. Jr., Nolan C., Scherer S. S., Lucas J., Gwynne D., Marchionni M. A. Expression of multiple neuregulin transcripts in postnatal rat brains. J. Comp. Neurol. 349:1994;389-400.
13. Chirgwin J. M., Przbyla A. E., MacDonald R. J., Rutter R. J. Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry. 18:1979;5294-5299.
14. Chong M. S., Reynolds M. L., Irwin N., Coggeshall R. E., Emson P. C., Benowitz L. I., Woolf C. J. GAP-43 expression in primary sensory neurons following central axotomy. J. Neurosci. 14:1994;4375-4384.
15. Chu G. C., Moscoso L. M., Sliwkowski M. X., Merlie J. P. Regulation of the acetylcholine receptor epsilon subunit gene by recombinant ARIA: Anin vitro. Neuron. 14:1995;329-339.
16. Corfas G., Rosen K. M., Aratake H., Krauss R., Fischbach G. D. Differential expression of ARIA isoforms in the rat brain. Neuron. 14:1995;103-115.
17. Dong Z., Brennan A., Liu N., Yarden Y., Lefkowitz G., Mirsky R., Jessen K. R. Neu differentiation factor acts as a neuron-glia signal and regulates the survival, proliferation and maturation of the rat Schwann cell precursor. Neuron. 15:1995;585-596.
18. English K. B., Kavka-Van Norman D., Horch K. Effects of chronic denervation in type I cutaneous mechanoreceptors (Haarscheiber). Anat. Rec. 207:1983;79-88.
19. Falls D. L., Harris D. A., Johnson F. A., Morgan M. M., Corfas G., Fischbach G. D. Mr 42,000 ARIA: A protein that may regulate the accumulation of acetylcholine receptors at developing chick neuromuscular junctions. Cold Spring Harb. Symp. Quant. Biol. 55:1990;397-406.
20. Falls D. L., Rosen K. M., Corfas G., Lane W. S., Fischbach G. D. ARIA, a protein that stimulates acetylcholine receptor synthesis, is a member of the neu ligand family. Cell. 72:1993;801-815.
21. Fort P., Marty L., Piechaczyk M., Sabrouty S. E., Dani C., Jeanteur P., Blanchard J. M. Various rat adult tissues express only one major mRNA species from the glyceraldehyde-3-phosphate-dehydrogenase multigenic family. Nucleic Acids Res. 13:1985;1431-1442.
22. Goodearl A. D., Davis J. B., Mistry K., Minghetti L., Otsu M., Waterfield M. D., Stroobant P. Purification of multiple forms of glial growth factor. J Biol Chem. 268:1993;18095-18102.
23. Grabczyk E., Zuber M. X., Federoff H. J., Ny S.-C., Pack A., Fishman M. C. Cloning and characterization of the rat gene encoding GAP-43. Eur. J. Neurosci. 2:1990;822-827.
24. Griffin J. W., Hoffman P. N. Degeneration and regeneration in the peripheral nervous system. Dyck P. J., Thomas P. K., Low P. A., Poduslo J. F. Peripheral Neuropathy. 1993;361-376 Saunders, Philadelphia.
25. Grinspan J. B., Marchionni M., Reeves M., Coulaloglou M., Scherer S. S. Axonal interactions regulate Schwann cell apoptosis in developing peripheral nerve: Neuregulin receptors and the role of neuregulins. J. Neurosci. 16:1996;6107-6118.
26. Ho W.-H., Armanini M. P., Nuijens A., Phillips H. S., Osheroff P. L. Sensory and motor neuron-derived factor - A novel heregulin variant highly expressed in sensory and motor neurons. J. Biol. Chem. 270:1995;14523-14532.
27. Hoffman P. N. Expression of GAP-43, a rapidly transported growth-associated protein and class II beta tubulin, a slowly transported cytoskeletal protein, are co-ordinated in regenerating neurons. J. Neurosci. 9:1989;893-897.
28. Holmes W. E., Sliwkowski M. X., Akita R. W., Henzel W. J., Lee J., Park J. W., Yansura D., Abadi N., Raab H., Lewis G. D. Identification of heregulin, a specific activator of p185erbB2. Science. 256:1992;1205-1210.
29. Jo S. A., Zhu X., Marchionni M. A., Burden S. J. Neuregulins are concentrated at nerve-muscle synapses and activate ACh-receptor gene expression. Nature. 373:1995;158-161.
30. Kelly B. M., Gillespie C. S., Sherman D. L., Brophy P. J. Schwann cells of the myelin-forming phenotype express neurofilament protein NF-M. J. Cell Biol. 118:1992;397-410.
31. Kopp D. M., Trachtenberg J. T., Thompson W. J. Glial growth factor rescues Schwann cells of mechanoreceptors from denervation-induced apoptosis. J. Neurosci. 17:1997;6697-6706.
32. Kreutzberg G. W. Reaction of the neuronal cell body to axonal damage. Waxman S. G., Kocsis J. D., Stys P. K. The Axon. 1995;355-374 Oxford Univ. Press.
33. Land H., Parada L. F., Weinberg R. A. Tumorigenic conversion of primary embryo fibroblasts requires at least two cooperating oncogenes. Nature. 304:1983;596-602.
34. Lee K. F., Simon H., Chen H., Bates B., Hung M.-C., Hauser C. Requirement for neuregulin receptor erbB2 in neural and cardiac development. Nature. 378:1995;394-398.
35. Lemke G. Neuregulins in development. Mol. Cell. Neurosci. 7:1996;247-262.
36. Loeb J. A., Fischbach G. D. Neurotrophic factors increase neuregulin expression in embryonic ventral spinal cord neurons. J Neurosci. 17:1997;1416-1424.
37. Mahanthappa N. K., Anton E. S., Matthew W. D. Glial growth factor 2, a soluble neuregulin, directly increases Schwann cell motility and indirectly promotes neurite outgrowth. J. Neurosci. 16:1996;4673-4683.
38. Marchionni M. A., Goodearl A. D., Chen M. S., Bermingham-McDonogh O., Kirk C., Hendricks M., Danehy F., Misumi D., Sudhalter J., Kobayashi K. Glial growth factors are alternatively spliced erbB2 ligands expressed in the nervous system [see Comments]. Nature. 362:1993;312-318.
39. Martinou J. C., Falls D. L., Fischbach G. D., Merlie J. P. Acetylcholine receptor-inducing activity stimulates expression of the epsilon-subunit gene of the muscle acetylcholine receptor. Proc. Natl. Acad. Sci. USA. 88:1991;7669-7673.
40. Meyer D., Birchmeier C. Distinct isoforms of neuregulin are expressed in mesenchymal and neuronal cells during mouse development. Proc. Natl. Acad. Sci. USA. 91:1994;1064-1068.
41. Meyer D., Birchmeier C. Multiple essential functions of neurogulin in development. Nature. 378:1995;386-390.
42. Meyer D., Yamaai T., Garratt A., Riethmacher-Sonnenberg E., Kane D., Theill L. E., Birchmeier C. Isoform-specific expression and function of neuregulin. Development. 124:1997;3575-3586.
43. Nurse C. A., Macintyre L., Diamond J. Reinnervation of the rat touch dome restores the Merkel cell population reduced after deneration. Neuroscience. 13:1984;563-571.
44. Peles E., Yarden Y. Neu and its ligands: From an oncogene to neural factors. Bioessays. 15:1993;815-824.
45. Pinkas-Kramarski R., Eilam R., Spiegler O., Lavi S., Liu N., Chang D., Wen D., Schwartz M., Yarden Y. Brain neurons and glial cells express Neu differentiation factor/heregulin: A survival factor for astrocytes. Proc. Natl. Acad. Sci. USA. 91:1994;9387-9391.
46. Raabe T. D., Clive D. R., Neuberger T. J., Wen D., DeVries G. H. Cultured neonatal Schwann cells contain and secrete neuregulins. J. Neurosci. Res. 46:1996;263-270.
47. Ramon y Cajal S. May R. M. Degeneration and Regeneration of the Nervous System. 1928;769 Oxford Univ. Press, Oxford.
48. Sambrook J., Fritsch E. F., Maniatis T. Molecular Cloning. 1989;Cold Spring Harbor Press, Cold Spring Harbor.
49. Scherer S. S., Salzer J. L. Axon-Schwann cell interactions in peripheral nerve regeneration. Jessen K. R., Richardson W. D. Glial Cell Development. 1996;165-196 Bios Scientific, Oxford.
50. Schmalbruch H. Fiber composition of the rat sciatic nerve. Anat. Rec. 215:1986;71-81.
51. Scott S. A. Sensory Neurons. 1992;Oxford Univ. Press. p. 441-.
52. Shah N. M., Marchionni M. A., Isaacs I., Stroobant P., Anderson D. J. Glial growth factor restricts mammalian neural crest stem cells to a glial fate. Cell. 77:1994;349-360.
53. Snider W. D. Functions of the neurotrophins during nervous sytem development: What the knockouts are teaching us. Cell. 77:1994;627-638.
54. Sommervaille T., Reynolds M. L., Woolf C. J. Time-dependent differences in the increase in GAP-43 expression in dorsal root ganglion cells after peripheral axotomy. Neuroscience. 45:1991;213-220.
55. Son Y.-J., Thompson W. J. Nerve sprouting in muscle is induced and guided by processes extended by Schwann cells. Neuron. 14:1995;133-141.
56. Son Y.-J., Thompson W. J. Schwann cell processes guide regeneration of peripheral axons. Neuron. 14:1995;125-132.
57. Syroid D. E., Maycox P. R., Burrola P. G., Liu N., Wen d., Lee K.-F., Lemke G., Kilpatrick T. J. Cell death in the Schwann cell lineage and its regulation by neuregulin. Proc. Natl. Acad. Sci. USA. 93:1996;9229-9234.
58. Tansey M. G., Chu G. C., Merlie J. P. ARIA/HRG regulates AChR epsilon subunit gene expression at the neuromuscular synapse via activation of phosphatidylinositol 3-kinase and Ras/MAPK pathway. J. Cell Biol. 134:1996;465-476.
59. Tetzlaff W., Alexander S. W., Miller F. D., Bisby M. A. Response of facial and rubrospinal neurons to axotomy - Changes in messenger RNA expression for cytoskeletal proteins and GAP-43. J. Neurosci. 11:1991;2528-2544.
60. Trachtenberg J. T., Thompson W. J. Schwann cell apoptosis and its regulation at the developing neuromuscular junction. Nature. 379:1996;174-177.
61. Verdi J. M., Groves A. K., Farinas I., Jones K., Marchionni M. A., Reichardt L. F., Anderson D. J. A reciprocal cell-cell interaction mediated by NT-3 and neuregulins controls the early survival and development of sympathetic neuroblasts. Neuron. 16:1996;515-527.
62. Wen D., Peles E., Cupples R., Suggs S. V., Bacus S. S., Lou Y., Trail G., Hu S., Silbiger S. M., Ben Levy R., Koski R. A., Lu H. S., Yarden Y. Neu differentiation factor: A transmenbrane glycoprotein containing an EGF domain and an immunoglobulin homology unit. Cell. 69:1992;559-572.
63. Wen D., Suggs S. V., Karunagaran D., Liu N., Cupples R. L., Luo Y., Janssen A. M., Ben-Baruch N., Trollinger D. B., Jacobsen V. L., Meng S.-Y., Lu H. S., Hu S., Chang D., Yang W., Yanigahara D., Koski R. A., Yarden Y. Structural and functional aspects of the multiplicity of neu differentiation factors. Mol. Cell. Biol. 14:1994;1909-1919.
64. Woolf C. J., Reynolds M. L., Molander C., O'Brein C., Lindsay R. M., Benowitz L. I. The growth-associated protein GAP-43 appears in dorsal root ganglion cells and in the dorsal horn of the rat spinal cord following peripheral nerve injury. Neuroscience. 34:1990;465-478.
65. Zelena J. The morphogenetic influence of innervation on the ontogenetic development of muscle spindles. J. Embryol. Exp. Morphol. 5:1957;283-292.
66. Zelena J. Development, degeneration and regeneration of receptor organs. Prog. Brain Res. 13:1964;175-213.
67. Zheng D. X., Sliwkowski M. X., Mark M., Frantz G., Akita R., Sun Y., Hillan K., Crowley C., Brush J., Godowski P. J. Neuregulin-3 (NRG3): A novel neural tissue-enriched protein that binds and activates ErbB4. Proc. Nat. Acad. Sci. USA. 94:1997;9562-9567.