Postsynaptic expression of an epidermal growth factor receptor regulates cholinergic synapse formation between identified molluscan neurons

European Journal of Neuroscience

Volumn 27, Issue 8, 2008, Pages 2043-2056

  Van Kesteren, Ronald E ^a   Gagatek, Jessica S ^b   Hagendorf, Antje ^a   Gouwenberg, Yvonne ^a   Smit, August B ^a   Syed, Naweed I ^b  

^a VU UNIVERSITY AMSTERDAM   (Netherlands)

^b UNIVERSITY OF CALGARY   (Canada)

Author keywords

Epidermal growth factor (EGF); ErbB receptor; Lymnaea stagnalis; Neuregulin; Synaptogenesis

Indexed keywords

EPIDERMAL GROWTH FACTOR; EPIDERMAL GROWTH FACTOR RECEPTOR;

ANIMAL CELL; ARTICLE; CHOLINERGIC NERVE CELL; CONTROLLED STUDY; IN SITU HYBRIDIZATION; LYMNAEA; NERVE CELL CULTURE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SYNAPTIC MEMBRANE; SYNAPTOGENESIS;

ACETYLCHOLINE; ANIMALS; CELLS, CULTURED; CLONING, MOLECULAR; EPIDERMAL GROWTH FACTOR; EXCITATORY POSTSYNAPTIC POTENTIALS; HUMANS; IN SITU HYBRIDIZATION; LYMNAEA; NERVE GROWTH FACTORS; NEURONS; PATCH-CLAMP TECHNIQUES; PHYLOGENY; POLYMERASE CHAIN REACTION; RECEPTOR, EPIDERMAL GROWTH FACTOR; SYNAPSES;

EID: 42049121187     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2008.06189.x     Document Type: Article

References (58)

1. Altschul, S.F., Madden, T.L., Schaffer, A.A., Zhang, J., Zhang, Z., Miller, W. Lipman, D.J. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res., 25, 3389 3402.
2. Arevalo, J.C. Wu, S.H. (2006) Neurotrophin signaling: many exciting surprises! Cell Mol. Life Sci., 63, 1523 1537.
3. Aroian, R.V., Koga, M., Mendel, J.E., Ohshima, Y. Sternberg, P.W. (1990) The let-23 gene necessary for Caenorhabditis elegans vulval induction encodes a tyrosine kinase of the EGF receptor subfamily. Nature, 348, 693 699.
4. Bothwell, M. (2006) Evolution of the neurotrophin signaling system in invertebrates. Brain Behav. Evol., 68, 124 132.
5. Britsch, S., Goerich, D.E., Riethmacher, D., Peirano, R.I., Rossner, M., Nave, K.A., Birchmeier, C. Wegner, M. (2001) The transcription factor Sox10 is a key regulator of peripheral glial development. Genes Dev., 15, 66 78.
6. Buonanno, A. Fischbach, G.D. (2001) Neuregulin and ErbB receptor signaling pathways in the nervous system. Curr. Opin. Neurobiol., 11, 287 296.
7. Burke, R.D., Angerer, L.M., Elphick, M.R., Humphrey, G.W., Yaguchi, S., Kiyama, T., Liang, S., Mu, X., Agca, C., Klein, W.H., Brandhorst, B.P., Rowe, M., Wilson, K., Churcher, A.M., Taylor, J.S., Chen, N., Murray, G., Wang, D., Mellott, D., Olinski, R., Hallbook, F. Thorndyke, M.C. (2006) A genomic view of the sea urchin nervous system. Dev. Biol., 300, 434 460.
8. Chao, M.V. (2000) Trophic factors: an evolutionary cul-de-sac or door into higher neuronal function? J. Neurosci. Res., 59, 353 355.
9. Chao, M.V. (2003) Neurotrophins and their receptors: a convergence point for many signalling pathways. Nat. Rev. Neurosci., 4, 299 309.
10. Escher, P., Lacazette, E., Courtet, M., Blindenbacher, A., Landmann, L., Bezakova, G., Lloyd, K.C., Mueller, U. Brenner, H.R. (2005) Synapses form in skeletal muscles lacking neuregulin receptors. Science, 308, 1920 1923.
11. Fainzilber, M., Smit, A.B., Syed, N.I., Wildering, W.C., Hermann, P.M., Van der Schors, R.C., Jimenez, C., Li, K.W., Van Minnen, J., Bulloch, A.G., Ibanez, C.F. Geraerts, W.P. (1996) CRNF, a molluscan neurotrophic factor that interacts with the p75 neurotrophin receptor. Science, 274, 1540 1543.
12. Feng, Z.P., Klumperman, J., Lukowiak, K. Syed, N.I. (1997) In vitro synaptogenesis between the somata of identified Lymnaea neurons requires protein synthesis but not extrinsic growth factors or substrate adhesion molecules. J. Neurosci., 17, 7839 7849.
13. Fiumara, F., Leitinger, G., Milanese, C., Montarolo, P.G. Ghirardi, M. (2005) In vitro formation and activity-dependent plasticity of synapses between Helix neurons involved in the neural control of feeding and withdrawal behaviors. Neuroscience, 134, 1133 1151.
14. Fry, D.W., Kraker, A.J., McMichael, A., Ambroso, L.A., Nelson, J.M., Leopold, W.R., Connors, R.W. Bridges, A.J. (1994) A specific inhibitor of the epidermal growth factor receptor tyrosine kinase. Science, 265, 1093 1095.
15. Garrett, T.P., McKern, N.M., Lou, M., Elleman, T.C., Adams, T.E., Lovrecz, G.O., Zhu, H.J., Walker, F., Frenkel, M.J., Hoyne, P.A., Jorissen, R.N., Nice, E.C., Burgess, A.W. Ward, C.W. (2002) Crystal structure of a truncated epidermal growth factor receptor extracellular domain bound to transforming growth factor alpha. Cell, 110, 763 773.
16. Hamakawa, T., Woodin, M.A., Bjorgum, M.C., Painter, S.D., Takasaki, M., Lukowiak, K., Nagle, G. Syed, N.I. (1999) Excitatory synaptogenesis between identified Lymnaea neurons requires extrinsic trophic factors and is mediated by receptor tyrosine kinases. J. Neurosci., 19, 9306 9312.
17. Hermann, P.M., van Kesteren, R.E., Wildering, W.C., Painter, S.D., Reno, J.M., Smith, J.S., Kumar, S.B., Geraerts, W.P., Ericsson, L.H., Smit, A.B., Bulloch, A.G. Nagle, G.T. (2000) Neurotrophic actions of a novel molluscan epidermal growth factor. J. Neurosci., 20, 6355 6364.
18. Hidalgo, A., Kinrade, E.F. Georgiou, M. (2001) The Drosophila neuregulin vein maintains glial survival during axon guidance in the CNS. Dev. Cell, 1, 679 690.
19. Hill, R.J. Sternberg, P.W. (1992) The gene lin-3 encodes an inductive signal for vulval development in C. elegans. Nature, 358, 470 476.
20. Huang, E.J. Reichardt, L.F. (2001) Neurotrophins: roles in neuronal development and function. Annu. Rev. Neurosci., 24, 677 736.
21. Huang, Y.Z., Won, S., Ali, D.W., Wang, Q., Du Tanowitz, M.Q.S., Pelkey, K.A., Yang, D.J., Xiong, W.C., Salter, M.W. Mei, L. (2000) Regulation of neuregulin signaling by PSD-95 interacting with ErbB4 at CNS synapses. Neuron, 26, 443 455.
22. Jaaro, H., Beck, G., Conticello, S.G. Fainzilber, M. (2001) Evolving better brains: a need for neurotrophins? Trends Neurosci., 24, 79 85.
23. Jaaro, H. Fainzilber, M. (2006) Building complex brains - missing pieces in an evolutionary puzzle. Brain Behav. Evol., 68, 191 195.
24. Jo, S.A., Zhu, X., Marchionni, M.A. Burden, S.J. (1995) Neuregulins are concentrated at nerve-muscle synapses and activate ACh-receptor gene expression. Nature, 373, 158 161.
25. Kassabov, S.R., Monje, F.J., Fiumara, F. Kandel, E.R. (2007) Identification of ApTrk, a Trk receptor homolog expressed in aplysia sensory and motor neurons critical for the induction and maintenance of secretion dependent long term facilitation. Soc. Neurosci. Abstr., 473.6.
26. Korneev, S.A., Park, J.H. O'Shea, M. (1999) Neuronal expression of neural nitric oxide synthase (nNOS) protein is suppressed by an antisense RNA transcribed from an NOS pseudogene. J. Neurosci., 19, 7711 7720.
27. Li, B., Woo, R.S., Mei, L. Malinow, R. (2007) The neuregulin-1 receptor erbB4 controls glutamatergic synapse maturation and plasticity. Neuron, 54, 583 597.
28. Lim, I.A., Hall, D.D. Hell, J.W. (2002) Selectivity and promiscuity of the first and second PDZ domains of PSD-95 and synapse-associated protein 102. J. Biol. Chem., 277, 21697 21711.
29. Mehlen, P., Mille, F. Thibert, C. (2005) Morphogens and cell survival during development. J. Neurobiol., 64, 357 366.
30. Munno, D.W., Woodin, M.A., Lukowiak, K., Syed, N.I. Dickinson, P.S. (2000) Different extrinsic trophic factors regulate neurite outgrowth and synapse formation between identified Lymnaea neurons. J. Neurobiol., 44, 20 30.
31. Nishida, E. Gotoh, Y. (1993) The MAP kinase cascade is essential for diverse signal transduction pathways. Trends Biochem. Sci., 18, 128 131.
32. Ogiso, H., Ishitani, R., Nureki, O., Fukai, S., Yamanaka, M., Kim, J.H., Saito, K., Sakamoto, A., Inoue, M., Shirouzu, M. Yokoyama, S. (2002) Crystal structure of the complex of human epidermal growth factor and receptor extracellular domains. Cell, 110, 775 787.
33. Okabayashi, Y., Kido, Y., Okutani, T., Sugimoto, Y., Sakaguchi, K. Kasuga, M. (1994) Tyrosines 1148 and 1173 of activated human epidermal growth factor receptors are binding sites of Shc in intact cells. J. Biol. Chem., 269, 18674 18678.
34. Ormond, J., Hislop, J., Zhao, Y., Webb, N., Vaillaincourt, F., Dyer, J.R., Ferraro, G., Barker, P., Martin, K.C. Sossin, W.S. (2004) ApTrkl, a Trk-like receptor, mediates serotonin-dependent ERK activation and long-term facilitation in Aplysia sensory neurons. Neuron, 44, 715 728.
35. Ozaki, M., Tohyama, K., Kishida, H., Buonanno, A., Yano, R. Hashikawa, T. (2000) Roles of neuregulin in synaptogenesis between mossy fibers and cerebellar granule cells. J. Neurosci. Res., 59, 612 623.
36. Ridgway, R.L., Syed, N.I., Lukowiak, K. Bulloch, A.G.M. (1991) Nerve growth factor (NGF) induces sprouting of specific neurons of the snail, Lymnaea stagnalis. J. Neurobiol., 22, 377 390.
37. Riese, D.J. 2nd Stern, D.F. (1998) Specificity within the EGF family/ErbB receptor family signaling network. Bioessays, 20, 41 48.
38. Rubin, G.M., Yandell, M.D., Wortman, J.R., Gabor Miklos, G.L., Nelson, C.R., Hariharan, I.K., Fortini, M.E., Li, P.W., Apweiler, R., Fleischmann, W., Cherry, J.M., Henikoff, S., Skupski, M.P., Misra, S., Ashburner, M., Birney, E., Boguski, M.S., Brody, T., Brokstein, P., Celniker, S.E., Chervitz, S.A., Coates, D., Cravchik, A., Gabrielian, A., Galle, R.F., Gelbart, W.M., George, R.A., Goldstein, L.S., Gong, F., Guan, P., Harris, N.L., Hay, B.A., Hoskins, R.A., Li, J., Li, Z., Hynes, R.O., Jones, S.J., Kuehl, P.M., Lemaitre, B., Littleton, J.T., Morrison, D.K., Mungall, C., O'Farrell, P.H., Pickeral, O.K., Shue, C., Vosshall, L.B., Zhang, J., Zhao, Q., Zheng, X.H. Lewis, S. (2000) Comparative genomics of the eukaryotes. Science, 287, 2204 2215.
39. Sandrock, A.W. Jr., Dryer, S.E., Rosen, K.M., Gozani, S.N., Kramer, R., Theill, L.E. Fischbach, G.D. (1997) Maintenance of acetylcholine receptor number by neuregulins at the neuromuscular junction in vivo. Science, 276, 599 603.
40. Segal, R.A. (2003) Selectivity in neurotrophin signaling: theme and variations. Annu. Rev. Neurosci., 26, 299 330.
41. Smit, A.B., Spijker, S., Van Minnen, J., Burke, J.F., De Winter, F., Van Elk, R. Geraerts, W.P. (1996) Expression and characterization of molluscan insulin-related peptide VII from the mollusc Lymnaea stagnalis. Neuroscience, 70, 589 596.
42. Smit, A.B., Syed, N.I., Schaap, D., van Minnen, J., Klumperman, J., Kits, K.S., Lodder, H., van der Schors, R.C., van Elk, R., Sorgedrager, B., Brejc, K., Sixma, T.K. Geraerts, W.P. (2001) A glia-derived acetylcholine-binding protein that modulates synaptic transmission. Nature, 411, 261 268.
43. Spafford, J.D., Munno, D.W., Van Nierop, P., Feng, Z.P., Jarvis, S.E., Gallin, W.J., Smit, A.B., Zamponi, G.W. Syed, N.I. (2003) Calcium channel structural determinants of synaptic transmission between identified invertebrate neurons. J. Biol. Chem., 278, 4258 4267.
44. Spijker, S., Houtzager, S.W., De Gunst, M.C., De Boer, W.P., Schoffelmeer, A.N. Smit, A.B. (2004) Morphine exposure and abstinence define specific stages of gene expression in the rat nucleus accumbens. FASEB J., 18, 848 850.
45. Stemerdink, C. Jacobs, J.R. (1997) Argos and SpitZ group genes function to regulate midline glial cell number in Drosophila embryos. Development, 124, 3787 3796.
46. Syed, N., Richardson, P. Bulloch, A. (1996) Ciliary neurotrophic factor, unlike nerve growth factor, supports neurite outgrowth but not synapse formation by adult Lymnaea neurons. J. Neurobiol., 29, 293 303.
47. Syed, N.I. Winlow, W. (1991) Coordination of locomotor and cardiorespiratory networks of Lymnaea stagnalis by a pair of identified interneurones. J. Exp. Biol., 158, 37 62.
48. Truman, J.W., Thorn, R.S. Robinow, S. (1992) Programmed neuronal death in insect development. J. Neurobiol., 23, 1295 1311.
49. Van der Steen, W.J. (1969) A method for breeding and studying freshwater snails under continous water change, with some remarks on growth and reproduction in Lymnaea stagnalis. Neth. J. Zool., 19, 131 139.
50. van Diepen, M.T., Spencer, G.E., van Minnen, J., Gouwenberg, Y., Bouwman, J., Smit, A.B. van Kesteren, R.E. (2005) The molluscan RING-finger protein L-TRIM is essential for neuronal outgrowth. Mol. Cell Neurosci., 29, 74 81.
51. van Kesteren, R.E., Fainzilber, M., Hauser, G., van Minnen, J., Vreugdenhil, E., Smit, A.B., Ibanez, C.F., Geraerts, W.P. Bulloch, A.G. (1998) Early evolutionary origin of the neurotrophin receptor family. EMBO J., 17, 2534 2542.
52. van Kesteren, R.E., Carter, C., Dissel, H.M., van Minnen, J., Gouwenberg, Y., Syed, N.I., Spencer, G.E. Smit, A.B. (2006) Local synthesis of actin-binding protein beta-thymosin regulates neurite outgrowth. J. Neurosci., 26, 152 157.
53. Wolpowitz, D., Mason, T.B., Dietrich, P., Mendelsohn, M., Talmage, D.A. Role, L.W. (2000) Cysteine-rich domain isoforms of the neuregulin-1 gene are required for maintenance of peripheral synapses. Neuron, 25, 79 91.
54. Won, S., Si, J., Colledge, M., Ravichandran, K.S., Froehner, S.C. Mei, L. (1999) Neuregulin-increased expression of acetylcholine receptor epsilon-subunit gene requires ErbB interaction with Shc. J. Neurochem., 73, 2358 2368.
55. Wong, R.G., Hadley, R.D., Kater, S.B. Hauser, G.C. (1981) Neurite outgrowth in molluscan organ and cell cultures: the role of conditioning factor (s). J. Neurosci., 1, 1008 1021.
56. Wong, R.W. Guillaud, L. (2004) The role of epidermal growth factor and its receptors in mammalian CNS. Cytokine Growth Factor Rev., 15, 147 156.
57. Woodin, M.A., Hamakawa, T., Takasaki, M., Lukowiak, K. Syed, N.I. (1999) Trophic factor-induced plasticity of synaptic connections between identified Lymnaea neurons. Learn. Mem., 6, 307 316.
58. Woodin, M.A., Munno, D.W. Syed, N.I. (2002) Trophic factor-induced excitatory synaptogenesis involves postsynaptic modulation of nicotinic acetylcholine receptors. J. Neurosci., 22, 505 514.