Axonal wrapping in the Drosophila PNS is controlled by glia-derived neuregulin homolog Vein

Development (Cambridge)

Volumn 142, Issue 7, 2015, Pages 1336-1345

  Matzat, Till ^a   Sieglitz, Florian ^a   Kottmeier, Rita ^a   Babatz, Felix ^a   Engelen, Daniel ^a   Klämbt, Christian ^a  

^a UNIVERSITY OF MÜNSTER   (Germany)

Author keywords

Drosophila; Neuregulin; Neuron glia interaction; Septate junction; Subperineurial glia; Wrapping glia

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; NEU DIFFERENTIATION FACTOR; DROSOPHILA PROTEIN; VEIN PROTEIN, DROSOPHILA;

ANIMAL CELL; ANTERIOR POSTERIOR AXIS; ARTICLE; BLOOD BRAIN BARRIER; CELL COUNT; CELL DIFFERENTIATION; CELL MATURATION; CELL ULTRASTRUCTURE; CONTINUOUS PROCESS; CONTROLLED STUDY; DROSOPHILA; ELECTRON MICROSCOPY; EMBRYO; EMBRYO DEVELOPMENT; EXTRACELLULAR SPACE; GENE FUNCTION; GENE SILENCING; GLIA CELL; LARVAL STAGE; MOTONEURON; NERVE FIBER; NONHUMAN; PERIPHERAL NERVOUS SYSTEM; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RNA INTERFERENCE; SCHWANN CELL; ANIMAL; CYTOLOGY; DROSOPHILA MELANOGASTER; GLIA; LARVA; METABOLISM; PERIPHERAL NERVE; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; ULTRASTRUCTURE;

INVERTEBRATA; MAMMALIA;

ANIMALS; AXONS; BLOOD-BRAIN BARRIER; CELL DIFFERENTIATION; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; LARVA; NEUREGULINS; NEUROGLIA; PERIPHERAL NERVES; PERIPHERAL NERVOUS SYSTEM; RECEPTOR, EPIDERMAL GROWTH FACTOR; SEQUENCE HOMOLOGY, AMINO ACID; SIGNAL TRANSDUCTION;

EID: 84930715621     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.116616     Document Type: Article

References (78)

1. Auld, V. J., Fetter, R. D., Broadie, K. and Goodman, C. S. (1995). Gliotactin, a novel transmembrane protein on peripheral glia, is required to form the bloodnerve barrier in Drosophila. Cell 81, 757-767.
2. Awasaki, T., Lai, S.-L., Ito, K. and Lee, T. (2008). Organization and postembryonic development of glial cells in the adult central brain of Drosophila. J. Neurosci. 28, 13742-13753.
3. Banerjee, S. and Bhat, M. A. (2007). Neuron-glial interactions in blood-brain barrier formation. Annu. Rev. Neurosci. 30, 235-258.
4. Banerjee, S., Pillai, A. M., Paik, R., Li, J. and Bhat, M. A. (2006). Axonal ensheathment and septate junction formation in the peripheral nervous system of Drosophila. J. Neurosci. 26, 3319-3329.
5. Baumgartner, S., Littleton, J. T., Broadie, K., Bhat, M. A., Harbecke, R., Lengyel, J. A., Chiquet-Ehrismann, R., Prokop, A. and Bellen, H. J. (1996). A Drosophila neurexin is required for septate junction and blood-nerve barrier formation and function. Cell 87, 1059-1068.
6. Bodmer, R. and Jan, Y. N. (1987). Morphological differentiation of the embryonic peripheral neurons in Drosophila. Dev. Genes Evol. 196, 69-77.
7. Bodmer, R., Carretto, R. and Jan, Y. N. (1989). Neurogenesis of the peripheral nervous system in Drosophila embryos: DNA replication patterns and cell lineages. Neuron 3, 21-32.
8. Brown, K. E., Kerr, M. and Freeman, M. (2007). The EGFR ligands Spitz and Keren act cooperatively in the Drosophila eye. Dev. Biol. 307, 105-113.
9. Doherty, P. and Walsh, F. S. (1996). CAM-FGF receptor interactions: a model for axonal growth. Mol. Cell. Neurosci. 8, 99-111.
10. Donaldson, T., Wang, S.-H., Jacobsen, T. L., Schnepp, B., Price, J. and Simcox, A. (2004). Regulation of the Drosophila epidermal growth factor-ligand vein is mediated by multiple domains. Genetics 167, 687-698.
11. Donier, E., Gomez-Sanchez, J. A., Grijota-Martinez, C., Lakomá, J., Baars, S., Garcia-Alonso, L. and Cabedo, H. (2012). L1CAM binds ErbB receptors through Ig-like domains coupling cell adhesion and neuregulin signalling. PLoS ONE 7, e40674.
12. Dubois, L., Lecourtois, M., Alexandre, C., Hirst, E. and Vincent, J.-P. (2001). Regulated endocytic routing modulates wingless signaling in Drosophila embryos. Cell 105, 613-624.
13. Ebersole, T. A., Chen, Q., Justice, M. J. and Artzt, K. (1996). The quaking gene product necessary in embryogenesis and myelination combines features of RNA binding and signal transduction proteins. Nat. Genet. 12, 260-265.
14. Edenfeld, G., Volohonsky, G., Krukkert, K., Naffin, E., Lammel, U., Grimm, A., Engelen, D., Reuveny, A., Volk, T. and Klämbt, C. (2006). The splicing factor crooked neck associates with the RNA-binding protein HOW to control glial cell maturation in Drosophila. Neuron 52, 969-980.
15. Edenfeld, G., Altenhein, B., Zierau, A., Cleppien, D., Krukkert, K., Technau, G. and Klämbt, C. (2007). Notch and Numb are required for normal migration of peripheral glia in Drosophila. Dev. Biol. 301, 27-37.
16. Eulenberg, K.G. and Schuh, R. (1997). The tracheae defective gene encodes a bZIP protein that controls tracheal cell movement during Drosophila embryogenesis. EMBO J. 16, 7156-7165.
17. Faivre-Sarrailh, C., Banerjee, S., Li, J., Hortsch, M., Laval, M. and Bhat, M. A. (2004). Drosophila contactin, a homolog of vertebrate contactin, is required for septate junction organization and paracellular barrier function. Development 131, 4931-4942.
18. Franzdóttir, S. R., Engelen, D., Yuva-Aydemir, Y., Schmidt, I., Aho, A. and Klämbt, C. (2009). Switch in FGF signalling initiates glial differentiation in the Drosophila eye. Nature 460, 758-761.
19. Fünfschilling, U., Supplie, L. M., Mahad, D., Boretius, S., Saab, A. S., Edgar, J., Brinkmann, B. G., Kassmann, C. M., Tzvetanova, I. D., Möbius, W. et al. (2012). Glycolytic oligodendrocytes maintain myelin and long-term axonal integrity. Nature 485, 517-521.
20. García-Alonso, L., Romani, S. and Jiménez, F. (2000). The EGF and FGF receptors mediate neuroglian function to control growth cone decisions during sensory axon guidance in Drosophila. Neuron 28, 741-752.
21. Genova, J. L. and Fehon, R. G. (2003). Neuroglian, Gliotactin, and the Na+/K+ ATPase are essential for septate junction function in Drosophila. J. Cell Biol. 161, 979-989.
22. Gibson, N. J. and Tolbert, L. P. (2006). Activation of epidermal growth factor receptor mediates receptor axon sorting and extension in the developing olfactory system of the moth Manduca sexta. J. Comp. Neurol. 495, 554-572.
23. Gibson, N. J., Tolbert, L. P. and Oland, L. A. (2012). Activation of glial FGFRs is essential in glial migration, proliferation, and survival and in glia-neuron signaling during olfactory system development. PLoS ONE 7, e33828.
24. Goldstein, L. S. B., Fyrberg, E. A., Wilson, L. and Matsudaira, P. T. (eds) (1994) Drosophila melanogaster: Practical Uses in Cell and Molecular Biology (Methods in Cell Biology), 44. San Diego: Academic Press.
25. Halter, D. A., Urban, J., Rickert, C., Ner, S. S., Ito, K., Travers, A. A. and Technau, G. M. (1995). The homeobox gene repo is required for the differentiation and maintenance of glia function in the embryonic nervous system of Drosophila melanogaster. Development 121, 317-332.
26. Hummel, T., Attix, S., Gunning, D. and Zipursky, S. L. (2002). Temporal control of glial cell migration in the Drosophila eye requires gilgamesh, hedgehog, and eye specification genes. Neuron 33, 193-203.
27. Islam, R., Kristiansen, L. V., Romani, S., Garcia-Alonso, L. and Hortsch, M. (2004). Activation of EGF receptor kinase by L1-mediated homophilic cell interactions. Mol. Biol. Cell 15, 2003-2012.
28. Kristiansen, L. V., Velasquez, E., Romani, S., Baars, S., Berezin, V., Bock, E., Hortsch, M. and Garcia-Alonso, L. (2005). Genetic analysis of an overlapping functional requirement for L1- and NCAM-type proteins during sensory axon guidance in Drosophila. Mol. Cell. Neurosci. 28, 141-152.
29. Kumar, J. P., Tio, M., Hsiung, F., Akopyan, S., Gabay, L., Seger, R., Shilo, B. Z. and Moses, K. (1998). Dissecting the roles of the Drosophila EGF receptor in eye development and MAP kinase activation. Development 125, 3875-3885.
30. Landgraf, M. and Thor, S. (2006). Development of Drosophila motoneurons: specification and morphology. Semin. Cell Dev. Biol. 17, 3-11.
31. Lee, B. P. and Jones, B.W. (2005). Transcriptional regulation of the Drosophila glial gene repo. Mech. Dev. 122, 849-862.
32. Leiserson, W. M., Harkins, E. W. and Keshishian, H. (2000). Fray, a Drosophila serine/threonine kinase homologous to mammalian PASK, is required for axonal ensheathment. Neuron 28, 793-806.
33. Leiserson, W. M., Forbush, B. and Keshishian, H. (2011). Drosophila glia use a conserved cotransporter mechanism to regulate extracellular volume. Glia 59, 320-332.
34. Mahr, A. and Aberle, H. (2006). The expression pattern of the Drosophila vesicular glutamate transporter: a marker protein for motoneurons and glutamatergic centers in the brain. Gene Expr. Patterns 6, 299-309.
35. McGuire, S. E., Le, P. T., Osborn, A. J., Matsumoto, K. and Davis, R. L. (2003). Spatiotemporal rescue of memory dysfunction in Drosophila. Science 302, 1765-1768.
36. Merritt, D. J. and Whitington, P. M. (1995). Central projections of sensory neurons in the Drosophila embryo correlate with sensory modality, soma position, and proneural gene function. J. Neurosci. 15, 1755-1767.
37. Michailov, G. V., Sereda, M. W., Brinkmann, B. G., Fischer, T. M., Haug, B., Birchmeier, C., Role, L., Lai, C., Schwab, M. H. and Nave, K.-A. (2004). Axonal neuregulin-1 regulates myelin sheath thickness. Science 304, 700-703.
38. Nagaraj, K., Kristiansen, L. V., Skrzynski, A., Castiella, C., Garcia-Alonso, L. and Hortsch, M. (2009). Pathogenic human L1-CAM mutations reduce the adhesion-dependent activation of EGFR. Hum. Mol. Genet. 18, 3822-3831.
39. Nave, K.-A. (2010). Myelination and support of axonal integrity by glia. Nature 468, 244-252.
40. Nave, K.-A. and Salzer, J. L. (2006). Axonal regulation of myelination by neuregulin 1. Curr. Opin. Neurobiol. 16, 492-500.
41. Nave, K.-A. and Trapp, B. D. (2008). Axon-glial signaling and the glial support of axon function. Annu. Rev. Neurosci. 31, 535-561.
42. Nir, R., Grossman, R., Paroush, Z. and Volk, T. (2012). Phosphorylation of the Drosophila melanogaster RNA-binding protein HOWby MAPK/ERK enhances its dimerization and activity. PLoS Genet. 8, e1002632.
43. Oshima, K. and Fehon, R. G. (2011). Analysis of protein dynamics within the septate junction reveals a highly stable core protein complex that does not include the basolateral polarity protein Discs large. J. Cell Sci. 124, 2861-2871.
44. Peles, E., Joho, K., Plowman, G. D. and Schlessinger, J. (1997). Close similarity between Drosophila neurexin IV and mammalian Caspr protein suggests a conserved mechanism for cellular interactions. Cell 88, 745-746.
45. Poliak, S. and Peles, E. (2003). The local differentiation of myelinated axons at nodes of Ranvier. Nat. Rev. Neurosci. 4, 968-980.
46. Queenan, A. M., Ghabrial, A. and Schüpbach, T. (1997). Ectopic activation of torpedo/Egfr, a Drosophila receptor tyrosine kinase, dorsalizes both the eggshell and the embryo. Development 124, 3871-3880.
47. Ragone, G., Van de Bor, V., Sorrentino, S., Kammerer, M., Galy, A., Schenck, A., Bernardoni, R., Miller, A. A., Roy, N. and Giangrande, A. (2003). Transcriptional regulation of glial cell specification. Dev. Biol. 255, 138-150.
48. Read, R. D., Cavenee, W. K., Furnari, F. B. and Thomas, J. B. (2009). A Drosophila model for EGFR-Ras and PI3K-dependent human glioma. PLoS Genet. 5, e1000374.
49. Reich, A. and Shilo, B.-Z. (2002). Keren, a new ligand of the Drosophila epidermal growth factor receptor, undergoes two modes of cleavage. EMBO J. 21, 4287-4296.
50. Rodrigues, F., Schmidt, I. and Klämbt, C. (2011). Comparing peripheral glial cell differentiation in Drosophila and vertebrates. Cell. Mol. Life Sci. 68, 55-69.
51. Rodrigues, F., Thuma, L. and Klämbt, C. (2012). The regulation of glial-specific splicing of Neurexin IV requires HOW and Cdk12 activity. Development 139, 1765-1776.
52. Schnepp, B., Grumbling, G., Donaldson, T. and Simcox, A. (1996). Vein is a novel component in the Drosophila epidermal growth factor receptor pathway with similarity to the neuregulins. Genes Dev. 10, 2302-2313.
53. Schulte, J., Tepass, U. and Auld, V. J. (2003). Gliotactin, a novel marker of tricellular junctions, is necessary for septate junction development in Drosophila. J. Cell Biol. 161, 991-1000.
54. Schüpbach, T. (1987). Germ line and soma cooperate during oogenesis to establish the dorsoventral pattern of egg shell and embryo in Drosophila melanogaster. Cell 49, 699-707.
55. Schwabe, T., Bainton, R. J., Fetter, R. D., Heberlein, U. and Gaul, U. (2005). GPCR signaling is required for blood-brain barrier formation in Drosophila. Cell 123, 133-144.
56. Sepp, K. J. and Auld, V. J. (1999). Conversion of lacZ enhancer trap lines to Gal4 lines using targeted transposition in Drosophila melanogaster. Genetics 151, 1093-1101.
57. Sepp, K. J. and Auld, V. J. (2003a). RhoA and Rac1 GTPases mediate the dynamic rearrangement of actin in peripheral glia. Development 130, 1825-1835.
58. Sepp, K. J. and Auld, V. J. (2003b). Reciprocal interactions between neurons and glia are required for Drosophila peripheral nervous system development. J. Neurosci. 23, 8221-8230.
59. Sherman, D. L. and Brophy, P. J. (2005). Mechanisms of axon ensheathment and myelin growth. Nat. Rev. Neurosci. 6, 683-690.
60. Shilo, B.-Z. (2005). Regulating the dynamics of EGF receptor signaling in space and time. Development 132, 4017-4027.
61. Sidman, R. L., Dickie, M. M. and Appel, S. H. (1964). Mutant mice (Quaking and Jimpy) with deficient myelination in the central nervous system. Science 144, 309-311.
62. Silies, M. and Klämbt, C. (2010). APC/C(Fzr/Cdh1)-dependent regulation of cell adhesion controls glial migration in the Drosophila PNS. Nat. Neurosci. 13, 1357-1364.
63. Silies, M., Yuva, Y., Engelen, D., Aho, A., Stork, T. and Klämbt, C. (2007). Glial cell migration in the eye disc. J. Neurosci. 27, 13130-13139.
64. Sink, H. and Whitington, P. M. (1991). Location and connectivity of abdominal motoneurons in the embryo and larva of Drosophila melanogaster. J. Neurobiol. 22, 298-311.
65. Stassart, R. M., Fledrich, R., Velanac, V., Brinkmann, B. G., Schwab, M. H., Meijer, D., Sereda, M.W. and Nave, K.-A. (2013). A role for Schwann cell-derived neuregulin-1 in remyelination. Nat. Neurosci. 16, 48-54.
66. Stork, T., Engelen, D., Krudewig, A., Silies, M., Bainton, R. J. and Klämbt, C. (2008). Organization and function of the blood brain barrier in Drosophila. J. Neurosci. 28, 587-597.
67. Stork, T., Bernardos, R. and Freeman, M. R. (2012). Analysis of glial cell development and function in Drosophila. Cold Spring Harb. Protoc. 2012, 1-17.
68. Taveggia, C., Zanazzi, G., Petrylak, A., Yano, H., Rosenbluth, J., Einheber, S., Xu, X., Esper, R. M., Loeb, J. A., Shrager, P. et al. (2005). Neuregulin-1 type III determines the ensheathment fate of axons. Neuron 47, 681-694.
69. Unhavaithaya, Y. and Orr-Weaver, T. L. (2012). Polyploidization of glia in neural development links tissue growth to blood-brain barrier integrity. Genes Dev. 26, 31-36.
70. Venken, K. J. T., Schulze, K. L., Haelterman, N. A., Pan, H., He, Y., Evans-Holm, M., Carlson, J. W., Levis, R. W., Spradling, A. C., Hoskins, R. A. et al. (2011). MiMIC: a highly versatile transposon insertion resource for engineering Drosophila melanogaster genes. Nat. Methods 8, 737-743.
71. von Hilchen, C. M., Beckervordersandforth, R. M., Rickert, C., Technau, G. M. and Altenhein, B. (2008). Identity, origin, and migration of peripheral glial cells in the Drosophila embryo. Mech. Dev. 125, 337-352.
72. von Hilchen, C. M., Hein, I., Technau, G. M. and Altenhein, B. (2010). Netrins guide migration of distinct glial cells in the Drosophila embryo. Development 137, 1251-1262.
73. von Hilchen, C. M., Bustos, Á. E., Giangrande, A., Technau, G. M. and Altenhein, B. (2013). Predetermined embryonic glial cells form the distinct glial sheaths of the Drosophila peripheral nervous system. Development 140, 3657-3668.
74. Watts, R. J., Schuldiner, O., Perrino, J., Larsen, C. and Luo, L. (2004). Glia engulf degenerating axons during developmental axon pruning. Curr. Biol. 14, 678-684.
75. Witte, H. T., Jeibmann, A., Klämbt, C. and Paulus, W. (2009). Modeling glioma growth and invasion in Drosophila melanogaster. Neoplasia 11, 882-888.
76. Wong, A. M., Wang, J. W. and Axel, R. (2002). Spatial representation of the glomerular map in the Drosophila protocerebrum. Cell 109, 229-241.
77. Yarnitzky, T., Min, L. and Volk, T. (1997). The Drosophila neuregulin homolog Vein mediates inductive interactions between myotubes and their epidermal attachment cells. Genes Dev. 11, 2691-2700.
78. Yuva-Aydemir, Y., Bauke, A.-C. and Klämbt, C. (2011). Spinster controls Dpp signaling during glial migration in the Drosophila eye. J. Neurosci. 31, 7005-7015.