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Comparing peripheral glial cell differentiation in Drosophila and vertebrates

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Abstract

In all complex organisms, the peripheral nerves ensure the portage of information from the periphery to central computing and back again. Axons are in part amazingly long and are accompanied by several different glial cell types. These peripheral glial cells ensure electrical conductance, most likely nuture the long axon, and establish and maintain a barrier towards extracellular body fluids. Recent work has revealed a surprisingly similar organization of peripheral nerves of vertebrates and Drosophila. Thus, the genetic dissection of glial differentiation in Drosophila may also advance our understanding of basic principles underlying the development of peripheral nerves in vertebrates.

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References

  1. Nave KA (2010) Myelination and the trophic support of long axons. Nat Rev Neurosci 11:275–283

    Article  CAS  PubMed  Google Scholar 

  2. Woodhoo A, Sommer L (2008) Development of the Schwann cell lineage: from the neural crest to the myelinated nerve. Glia 56:1481–1490

    Article  PubMed  Google Scholar 

  3. Le Douarin NM, Dupin E (2003) Multipotentiality of the neural crest. Curr Opin Genet Dev 13:529–536

    Article  CAS  PubMed  Google Scholar 

  4. Le Douarin NM, Creuzet S, Couly G, Dupin E (2004) Neural crest cell plasticity and its limits. Development 131:4637–4650

    Article  CAS  PubMed  Google Scholar 

  5. Nave KA, Trapp BD (2008) Axon-glial signaling and the glial support of axon function. Annu Rev Neurosci 31:535–561

    Article  CAS  PubMed  Google Scholar 

  6. Haller FR, Low FN (1971) The fine structure of the peripheral nerve root sheath in the subarachnoid space in the rat and other laboratory animals. Am J Anat 131:1–19

    Article  CAS  PubMed  Google Scholar 

  7. Kristensson K, Olsson Y (1971) The perineurium as a diffusion barrier to protein tracers. Differences between mature and immature animals. Acta Neuropathol 17:127–138

    CAS  Google Scholar 

  8. Allt G (1969) Ultrastructural features of the immature peripheral nerve. J Anat 105:283–293

    CAS  PubMed  Google Scholar 

  9. Jessen KR, Mirsky R, Salzer J (2008) Introduction. Schwann cell biology. Glia 56:1479–1480

    Article  PubMed  Google Scholar 

  10. Grim M, Halata Z, Franz T (1992) Schwann cells are not required for guidance of motor nerves in the hindlimb in Splotch mutant mouse embryos. Anat Embryol (Berl) 186:311–318

    CAS  Google Scholar 

  11. Jessen KR, Mirsky R (2005) The origin and development of glial cells in peripheral nerves. Nat Rev Neurosci 6:671–682

    Article  CAS  PubMed  Google Scholar 

  12. Takahashi M, Osumi N (2005) Identification of a novel type II classical cadherin: rat cadherin19 is expressed in the cranial ganglia and Schwann cell precursors during development. Dev Dyn 232:200–208

    Article  CAS  PubMed  Google Scholar 

  13. Taveggia C, Zanazzi G, Petrylak A, Yano H, Rosenbluth J, Einheber S, Xu X, Esper RM, Loeb JA, Shrager P, Chao MV, Falls DL, Role L, Salzer JL (2005) Neuregulin-1 type III determines the ensheathment fate of axons. Neuron 47:681–694

    Article  CAS  PubMed  Google Scholar 

  14. Michailov GV, Sereda MW, Brinkmann BG, Fischer TM, Haug B, Birchmeier C, Role L, Lai C, Schwab MH, Nave KA (2004) Axonal neuregulin-1 regulates myelin sheath thickness. Science 304:700–703

    Article  CAS  PubMed  Google Scholar 

  15. Chen S, Velardez MO, Warot X, Yu ZX, Miller SJ, Cros D, Corfas G (2006) Neuregulin 1-erbB signaling is necessary for normal myelination and sensory function. J Neurosci 26:3079–3086

    Article  CAS  PubMed  Google Scholar 

  16. Du Plessis DG, Mouton YM, Muller CJ, Geiger DH (1996) An ultrastructural study of the development of the chicken perineurial sheath. J Anat 189(Pt 3):631–641

    PubMed  Google Scholar 

  17. Kucenas S, Takada N, Park HC, Woodruff E, Broadie K, Appel B (2008) CNS-derived glia ensheath peripheral nerves and mediate motor root development. Nat Neurosci 11:143–151

    Article  CAS  PubMed  Google Scholar 

  18. von Hilchen CM, Beckervordersandforth RM, Rickert C, Technau GM, Altenhein B (2008) Identity, origin, and migration of peripheral glial cells in the Drosophila embryo. Mech Dev 125:337–352

    Article  CAS  Google Scholar 

  19. Sepp KJ, Schulte J, Auld VJ (2000) Developmental dynamics of peripheral glia in Drosophila melanogaster. Glia 30:122–133

    Article  CAS  PubMed  Google Scholar 

  20. Sink H, Whitington PM (1991) Location and connectivity of abdominal motoneurons in the embryo and larva of Drosophila melanogaster. J Neurobiol 22:298–311

    Article  CAS  PubMed  Google Scholar 

  21. Mahr A, 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

    Article  CAS  PubMed  Google Scholar 

  22. Ghysen A, Dambly-Chaudiere C, Aeeves E, Jan LY, Jan YN (1986) Sensory neurons and peripheral pathways in Drosophila embryos. Roux’s Arch Dev Biol 195:281–289

    Article  Google Scholar 

  23. Bodmer R, Carretto R, Jan YN (1989) Neurogenesis of the peripheral nervous system in Drosophila embryos: DNA replication patterns and cell lineages. Neuron 3:21–32

    Article  CAS  PubMed  Google Scholar 

  24. Stork T, Engelen D, Krudewig A, Silies M, Bainton RJ, Klambt C (2008) Organization and function of the blood-brain barrier in Drosophila. J Neurosci 28:587–597

    Article  CAS  PubMed  Google Scholar 

  25. Olofsson B, Page DT (2005) Condensation of the central nervous system in embryonic Drosophila is inhibited by blocking hemocyte migration or neural activity. Dev Biol 279:233–243

    Article  CAS  PubMed  Google Scholar 

  26. Sun B, Xu P, Salvaterra PM (1999) Dynamic visualization of nervous system in live Drosophila. Proc Natl Acad Sci USA 96:10438–10443

    Article  CAS  PubMed  Google Scholar 

  27. Sun B, Salvaterra PM (1995) Two Drosophila nervous system antigens, Nervana 1 and 2, are homologous to the beta subunit of Na+, K(+)-ATPase. Proc Natl Acad Sci USA 92:5396–5400

    Article  CAS  PubMed  Google Scholar 

  28. Sun B, Wang W, Salvaterra PM (1998) Functional analysis and tissue-specific expression of Drosophila Na+, K+-ATPase subunits. J Neurochem 71:142–151

    Article  CAS  PubMed  Google Scholar 

  29. Sun B, Xu P, Wang W, Salvaterra PM (2001) In vivo modification of Na(+), K(+)-ATPase activity in Drosophila. Comp Biochem Physiol B Biochem Mol Biol 130:521–536

    Article  CAS  PubMed  Google Scholar 

  30. Pereanu W, Shy D, Hartenstein V (2005) Morphogenesis and proliferation of the larval brain glia in Drosophila. Dev Biol 283:191–203

    Article  CAS  PubMed  Google Scholar 

  31. Morin X, Daneman R, Zavortink M, Chia W (2001) A protein trap strategy to detect GFP-tagged proteins expressed from their endogenous loci in Drosophila. Proc Natl Acad Sci USA 98:15050–15055

    Article  CAS  PubMed  Google Scholar 

  32. Jia XX, Gorczyca M, Budnik V (1993) Ultrastructure of neuromuscular junctions in Drosophila: comparison of wild type and mutants with increased excitability. J Neurobiol 24:1025–1044

    Article  CAS  PubMed  Google Scholar 

  33. Schwabe T, Bainton RJ, Fetter RD, Heberlein U, Gaul U (2005) GPCR signaling is required for blood-brain barrier formation in Drosophila. Cell 123:133–144

    Article  CAS  PubMed  Google Scholar 

  34. Tepass U, Hartenstein V (1994) The development of cellular junctions in the Drosophila embryo. Dev Biol 161:563–596

    Article  CAS  PubMed  Google Scholar 

  35. Mayer F, Mayer N, Chinn L, Pinsonneault RL, Kroetz D, Bainton RJ (2009) Evolutionary conservation of vertebrate blood-brain barrier chemoprotective mechanisms in Drosophila. J Neurosci 29:3538–3550

    Article  CAS  PubMed  Google Scholar 

  36. Bainton RJ, Tsai LT, Schwabe T, DeSalvo M, Gaul U, Heberlein U (2005) Moody encodes two GPCRs that regulate cocaine behaviors and blood-brain barrier permeability in Drosophila. Cell 123:145–156

    Article  CAS  PubMed  Google Scholar 

  37. Sepp KJ, Auld VJ (1999) Conversion of lacZ enhancer trap lines to GAL4 lines using targeted transposition in Drosophila melanogaster. Genetics 151:1093–1101

    CAS  PubMed  Google Scholar 

  38. Schulte J, Tepass U, Auld VJ (2003) Gliotactin, a novel marker of tricellular junctions, is necessary for septate junction development in Drosophila. J Cell Biol 161:991–1000

    Article  CAS  PubMed  Google Scholar 

  39. Laprise P, Beronja S, Silva-Gagliardi NF, Pellikka M, Jensen AM, McGlade CJ, Tepass U (2006) The FERM protein Yurt is a negative regulatory component of the Crumbs complex that controls epithelial polarity and apical membrane size. Dev Cell 11:363–374

    Article  CAS  PubMed  Google Scholar 

  40. Laprise P, Lau KM, Harris KP, Silva-Gagliardi NF, Paul SM, Beronja S, Beitel GJ, McGlade CJ, Tepass U (2009) Yurt, Coracle, Neurexin IV and the Na(+), K(+)-ATPase form a novel group of epithelial polarity proteins. Nature 459:1141–1145

    Article  CAS  PubMed  Google Scholar 

  41. Laprise P, Paul SM, Boulanger J, Robbins RM, Beitel GJ, Tepass U (2010) Epithelial polarity proteins regulate Drosophila tracheal tube size in parallel to the luminal matrix pathway. Curr Biol 20:55–61

    Article  CAS  PubMed  Google Scholar 

  42. Leiserson WM, Harkins EW, Keshishian H (2000) Fray, a Drosophila serine/threonine kinase homologous to mammalian PASK, is required for axonal ensheathment. Neuron 28:793–806

    Article  CAS  PubMed  Google Scholar 

  43. Gagnon KB, England R, Delpire E (2006) Characterization of SPAK and OSR1, regulatory kinases of the Na-K-2Cl cotransporter. Mol Cell Biol 26:689–698

    Article  CAS  PubMed  Google Scholar 

  44. Lavery W, Hall V, Yager JC, Rottgers A, Wells MC, Stern M (2007) Phosphatidylinositol 3-kinase and Akt nonautonomously promote perineurial glial growth in Drosophila peripheral nerves. J Neurosci 27:279–288

    Article  CAS  PubMed  Google Scholar 

  45. Awasaki T, Lai SL, Ito K, Lee T (2008) Organization and postembryonic development of glial cells in the adult central brain of Drosophila. J Neurosci 28:13742–13753

    Article  CAS  PubMed  Google Scholar 

  46. Curtin KD, Wyman RJ, Meinertzhagen IA (2007) Basigin/EMMPRIN/CD147 mediates neuron-glia interactions in the optic lamina of Drosophila. Glia 55:1542–1553

    Article  PubMed  Google Scholar 

  47. Curtin KD, Meinertzhagen IA, Wyman RJ (2005) Basigin (EMMPRIN/CD147) interacts with integrin to affect cellular architecture. J Cell Sci 118:2649–2660

    Article  CAS  PubMed  Google Scholar 

  48. Lemmon MA, Schlessinger J (2010) Cell signaling by receptor tyrosine kinases. Cell 141:1117–1134

    Article  CAS  PubMed  Google Scholar 

  49. Maurel P, Salzer JL (2000) Axonal regulation of Schwann cell proliferation and survival and the initial events of myelination requires PI 3-kinase activity. J Neurosci 20:4635–4645

    CAS  PubMed  Google Scholar 

  50. Monk KR, Naylor SG, Glenn TD, Mercurio S, Perlin JR, Dominguez C, Moens CB, Talbot WS (2009) A G protein-coupled receptor is essential for Schwann cells to initiate myelination. Science 325:1402–1405

    Article  CAS  PubMed  Google Scholar 

  51. Monk KR, Talbot WS (2009) Genetic dissection of myelinated axons in zebrafish. Curr Opin Neurobiol 19:486–490

    Article  CAS  PubMed  Google Scholar 

  52. Franzdottir SR, Engelen D, Yuva-Aydemir Y, Schmidt I, Aho A, Klambt C (2009) Switch in FGF signalling initiates glial differentiation in the Drosophila eye. Nature 460:758–761

    CAS  PubMed  Google Scholar 

  53. Silies M, Yuva-Aydemir Y, Franzdottir SR, Klämbt C (2010) The eye imaginal disc as a model to study the coordination of neuronal and glial development. Fly (Austin) 4:71–79

    CAS  Google Scholar 

  54. Wolff T, Ready DF (1993) Pattern formation in the Drosophila retina. In: Bate M, Martinez Arias A (eds) The development of Drosophila. Cold Spring Harbor Press, Cold Spring Harbor, pp 1277–1325

    Google Scholar 

  55. Rangarajan R, Courvoisier H, Gaul U (2001) Dpp and Hedgehog mediate neuron-glia interactions in Drosophila eye development by promoting the proliferation and motility of subretinal glia. Mech Dev 108:93–103

    Article  CAS  PubMed  Google Scholar 

  56. Silies M, Yuva Y, Engelen D, Aho A, Stork T, Klambt C (2007) Glial cell migration in the eye disc. J Neurosci 27:13130–13139

    Article  CAS  PubMed  Google Scholar 

  57. Rangarajan R, Gong Q, Gaul U (1999) Migration and function of glia in the developing Drosophila eye. Development 126:3285–3292

    CAS  PubMed  Google Scholar 

  58. Hummel T, Attix S, Gunning D, Zipursky SL (2002) Temporal control of glial cell migration in the Drosophila eye requires gilgamesh, hedgehog, and eye specification genes. Neuron 33:193–203

    Article  CAS  PubMed  Google Scholar 

  59. Choi KW, Benzer S (1994) Migration of glia along photoreceptor axons in the developing Drosophila eye. Neuron 12:423–431

    Article  CAS  PubMed  Google Scholar 

  60. Roots BI, Lane NJ (1983) Myelinating glia of earthworm giant axons: thermally induced intramembranous changes. Tissue Cell 15:695–709

    Article  CAS  PubMed  Google Scholar 

  61. Gunther J (1976) Impulse conduction in the myelinated giant fibers of the earthworm. Structure and function of the dorsal nodes in the median giant fiber. J Comp Neurol 168:505–531

    Article  CAS  PubMed  Google Scholar 

  62. Weatherby TM, Davis AD, Hartline DK, Lenz PH (2000) The need for speed. II. Myelin in calanoid copepods. J Comp Physiol [A] 186:347–357

    Article  CAS  Google Scholar 

  63. Lenz PH, Hartline DK, Davis AD (2000) The need for speed. I. Fast reactions and myelinated axons in copepods. J Comp Physiol [A] 186:337–345

    Article  CAS  Google Scholar 

  64. Davis AD, Weatherby TM, Hartline DK, Lenz PH (1999) Myelin-like sheaths in copepod axons. Nature 398:571

    Article  CAS  PubMed  Google Scholar 

  65. Govind CK, Pearce J (1988) Remodeling of nerves during claw reversal in adult snapping shrimps. J Comp Neurol 268:121–130

    Article  CAS  PubMed  Google Scholar 

  66. Heuser JE, Doggenweiler CF (1966) The fine structural organization of nerve fibers, sheaths, and glial cells in the prawn, Palaemonetes vulgaris. J Cell Biol 30:381–403

    Article  CAS  PubMed  Google Scholar 

  67. Xu K, Terakawa S (1999) Fenestration nodes and the wide submyelinic space form the basis for the unusually fast impulse conduction of shrimp myelinated axons. J Exp Biol 202:1979–1989

    CAS  PubMed  Google Scholar 

  68. Hama K (1966) The fine structure of the Schwann cell sheath of the nerve fiber in the shrimp (Penaeus japonicus). J Cell Biol 31:624–632

    Article  CAS  PubMed  Google Scholar 

  69. Johnston WL, Dyer JR, Castellucci VF, Dunn RJ (1996) Clustered voltage-gated Na + channels in Aplysia axons. J Neurosci 16:1730–1739

    CAS  PubMed  Google Scholar 

  70. Borner J, Puschmann T, Duch C (2006) A steroid hormone affects sodium channel expression in Manduca central neurons. Cell Tissue Res 325:175–187

    Article  CAS  PubMed  Google Scholar 

  71. Poliak S, Peles E (2003) The local differentiation of myelinated axons at nodes of Ranvier. Nat Rev Neurosci 4:968–980

    Article  CAS  PubMed  Google Scholar 

  72. Salzer JL, Brophy PJ, Peles E (2008) Molecular domains of myelinated axons in the peripheral nervous system. Glia 56:1532–1540

    Article  PubMed  Google Scholar 

  73. Schafer DP, Rasband MN (2006) Glial regulation of the axonal membrane at nodes of Ranvier. Curr Opin Neurobiol 16:508–514

    Article  CAS  PubMed  Google Scholar 

  74. Susuki K, Rasband MN (2008) Molecular mechanisms of node of Ranvier formation. Curr Opin Cell Biol 20:616–623

    Article  CAS  PubMed  Google Scholar 

  75. MacKenzie ML, Ghabriel MN, Allt G (1984) Nodes of Ranvier and Schmidt-Lanterman incisures: an in vivo lanthanum tracer study. J Neurocytol 13:1043–1055

    Article  CAS  PubMed  Google Scholar 

  76. Hirano A, Becker NH, Zimmerman HM (1969) Isolation of the periaxonal space of the central myelinated nerve fiber with regard to the diffusion of peroxidase. J Histochem Cytochem 17:512–516

    CAS  PubMed  Google Scholar 

  77. Banerjee S, Bhat MA (2007) Neuron-glial interactions in blood–brain barrier formation. Annu Rev Neurosci 30:235–258

    Article  CAS  PubMed  Google Scholar 

  78. Bhat MA (2003) Molecular organization of axo-glial junctions. Curr Opin Neurobiol 13:552–559

    Article  CAS  PubMed  Google Scholar 

  79. Einheber S, Zanazzi G, Ching W, Scherer S, Milner TA, Peles E, Salzer JL (1997) The axonal membrane protein Caspr, a homologue of neurexin IV, is a component of the septate-like paranodal junctions that assemble during myelination. J Cell Biol 139:1495–1506

    Article  CAS  PubMed  Google Scholar 

  80. Bhat MA, Rios JC, Lu Y, Garcia-Fresco GP, Ching W, St Martin M, Li J, Einheber S, Chesler M, Rosenbluth J, Salzer JL, Bellen HJ (2001) Axon-glia interactions and the domain organization of myelinated axons requires neurexin IV/Caspr/Paranodin. Neuron 30:369–383

    Article  CAS  PubMed  Google Scholar 

  81. Bo L, Quarles RH, Fujita N, Bartoszewicz Z, Sato S, Trapp BD (1995) Endocytic depletion of L-MAG from CNS myelin in quaking mice. J Cell Biol 131:1811–1820

    Article  CAS  PubMed  Google Scholar 

  82. Peles E, Nativ M, Lustig M, Grumet M, Schilling J, Martinez R, Plowman GD, Schlessinger J (1997) Identification of a novel contactin-associated transmembrane receptor with multiple domains implicated in protein–protein interactions. EMBO J 16:978–988

    Article  CAS  PubMed  Google Scholar 

  83. Faivre-Sarrailh C, Banerjee S, Li J, Hortsch M, Laval M, Bhat MA (2004) Drosophila contactin, a homolog of vertebrate contactin, is required for septate junction organization and paracellular barrier function. Development 131:4931–4942

    Article  CAS  PubMed  Google Scholar 

  84. Boyle ME, Berglund EO, Murai KK, Weber L, Peles E, Ranscht B (2001) Contactin orchestrates assembly of the septate-like junctions at the paranode in myelinated peripheral nerve. Neuron 30:385–397

    Article  CAS  PubMed  Google Scholar 

  85. Bonnon C, Bel C, Goutebroze L, Maigret B, Girault JA, Faivre-Sarrailh C (2007) PGY repeats and N-glycans govern the trafficking of paranodin and its selective association with contactin and neurofascin-155. Mol Biol Cell 18:229–241

    Article  CAS  PubMed  Google Scholar 

  86. Rios JC, Melendez-Vasquez CV, Einheber S, Lustig M, Grumet M, Hemperly J, Peles E, Salzer JL (2000) Contactin-associated protein (Caspr) and contactin form a complex that is targeted to the paranodal junctions during myelination. J Neurosci 20:8354–8364

    CAS  PubMed  Google Scholar 

  87. Gollan L, Salomon D, Salzer JL, Peles E (2003) Caspr regulates the processing of contactin and inhibits its binding to neurofascin. J Cell Biol 163:1213–1218

    Article  CAS  PubMed  Google Scholar 

  88. Charles P, Tait S, Faivre-Sarrailh C, Barbin G, Gunn-Moore F, Denisenko-Nehrbass N, Guennoc AM, Girault JA, Brophy PJ, Lubetzki C (2002) Neurofascin is a glial receptor for the paranodin/Caspr-contactin axonal complex at the axoglial junction. Curr Biol 12:217–220

    Article  CAS  PubMed  Google Scholar 

  89. Zonta B, Tait S, Melrose S, Anderson H, Harroch S, Higginson J, Sherman DL, Brophy PJ (2008) Glial and neuronal isoforms of Neurofascin have distinct roles in the assembly of nodes of Ranvier in the central nervous system. J Cell Biol 181:1169–1177

    Article  CAS  PubMed  Google Scholar 

  90. Sherman DL, Brophy PJ (2005) Mechanisms of axon ensheathment and myelin growth. Nat Rev Neurosci 6:683–690

    Article  CAS  PubMed  Google Scholar 

  91. Pillai AM, Thaxton C, Pribisko AL, Cheng JG, Dupree JL, Bhat MA (2009) Spatiotemporal ablation of myelinating glia-specific neurofascin (Nfasc NF155) in mice reveals gradual loss of paranodal axoglial junctions and concomitant disorganization of axonal domains. J Neurosci Res 87:1773–1793

    Article  CAS  PubMed  Google Scholar 

  92. Sousa AD, Bhat MA (2007) Cytoskeletal transition at the paranodes: the Achilles’ heel of myelinated axons. Neuron Glia Biol 3:169–178

    Article  PubMed  Google Scholar 

  93. Jarjour AA, Bull SJ, Almasieh M, Rajasekharan S, Baker KA, Mui J, Antel JP, Di Polo A, Kennedy TE (2008) Maintenance of axo-oligodendroglial paranodal junctions requires DCC and netrin-1. J Neurosci 28:11003–11014

    Article  CAS  PubMed  Google Scholar 

  94. Ishibashi T, Ding L, Ikenaka K, Inoue Y, Miyado K, Mekada E, Baba H (2004) Tetraspanin protein CD9 is a novel paranodal component regulating paranodal junctional formation. J Neurosci 24:96–102

    Article  CAS  PubMed  Google Scholar 

  95. Dupree JL, Girault JA, Popko B (1999) Axo-glial interactions regulate the localization of axonal paranodal proteins. J Cell Biol 147:1145–1152

    Article  CAS  PubMed  Google Scholar 

  96. Honke K, Hirahara Y, Dupree J, Suzuki K, Popko B, Fukushima K, Fukushima J, Nagasawa T, Yoshida N, Wada Y, Taniguchi N (2002) Paranodal junction formation and spermatogenesis require sulfoglycolipids. Proc Natl Acad Sci USA 99:4227–4232

    Article  CAS  PubMed  Google Scholar 

  97. Poliak S, Gollan L, Martinez R, Custer A, Einheber S, Salzer JL, Trimmer JS, Shrager P, Peles E (1999) Caspr2, a new member of the neurexin superfamily, is localized at the juxtaparanodes of myelinated axons and associates with K + channels. Neuron 24:1037–1047

    Article  CAS  PubMed  Google Scholar 

  98. Baumgartner S, Littleton JT, Broadie K, Bhat MA, Harbecke R, Lengyel JA, Chiquet-Ehrismann R, Prokop A, Bellen HJ (1996) A Drosophila neurexin is required for septate junction and blood–nerve barrier formation and function. Cell 87:1059–1068

    Article  CAS  PubMed  Google Scholar 

  99. Wu VM, Beitel GJ (2004) A junctional problem of apical proportions: epithelial tube-size control by septate junctions in the Drosophila tracheal system. Curr Opin Cell Biol 16:493–499

    Article  CAS  PubMed  Google Scholar 

  100. Paul SM, Palladino MJ, Beitel GJ (2007) A pump-independent function of the Na, K-ATPase is required for epithelial junction function and tracheal tube-size control. Development 134:147–155

    Article  CAS  PubMed  Google Scholar 

  101. Paul SM, Ternet M, Salvaterra PM, Beitel GJ (2003) The Na+/K+ATPase is required for septate junction function and epithelial tube-size control in the Drosophila tracheal system. Development 130:4963–4974

    Article  CAS  PubMed  Google Scholar 

  102. Genova JL, Fehon RG (2003) Neuroglian, Gliotactin, and the Na +/K + ATPase are essential for septate junction function in Drosophila. J Cell Biol 161:979–989

    Article  CAS  PubMed  Google Scholar 

  103. Sepp KJ, Auld VJ (2003) RhoA and Rac1 GTPases mediate the dynamic rearrangement of actin in peripheral glia. Development 130:1825–1835

    Article  CAS  PubMed  Google Scholar 

  104. Pierce KL, Premont RT, Lefkowitz RJ (2002) Seven-transmembrane receptors. Nat Rev Mol Cell Biol 3:639–650

    Article  CAS  PubMed  Google Scholar 

  105. Granderath S, Stollewerk A, Greig S, Goodman CS, O’Kane CJ, Klambt C (1999) Loco encodes an RGS protein required for Drosophila glial differentiation. Development 126:1781–1791

    CAS  PubMed  Google Scholar 

  106. Edenfeld G, Volohonsky G, Krukkert K, Naffin E, Lammel U, Grimm A, Engelen D, Reuveny A, Volk T, Klambt 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

    Article  CAS  PubMed  Google Scholar 

  107. Chung S, McLean MR, Rymond BC (1999) Yeast ortholog of the Drosophila crooked neck protein promotes spliceosome assembly through stable U4/U6.U5 snRNP addition. RNA 5:1042–1054

    Article  CAS  PubMed  Google Scholar 

  108. Burnette JM, Hatton AR, Lopez AJ (1999) Trans-acting factors required for inclusion of regulated exons in the Ultrabithorax mRNAs of Drosophila melanogaster. Genetics 151:1517–1529

    CAS  PubMed  Google Scholar 

  109. Vernet C, Artzt K (1997) STAR, a gene family involved in signal transduction and activation of RNA. Trends Genet 13:479–484

    Article  CAS  PubMed  Google Scholar 

  110. Ebersole TA, Chen Q, Justice MJ, 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

    Article  CAS  PubMed  Google Scholar 

  111. Wang LL, Richard S, Shaw AS (1995) P62 association with RNA is regulated by tyrosine phosphorylation. J Biol Chem 270:2010–2013

    Article  CAS  PubMed  Google Scholar 

  112. Stork T, Thomas S, Rodrigues F, Silies M, Naffin E, Wenderdel S, Klambt C (2009) Drosophila Neurexin IV stabilizes neuron-glia interactions at the CNS midline by binding to Wrapper. Development 136:1251–1261

    Article  CAS  PubMed  Google Scholar 

  113. Wheeler SR, Banerjee S, Blauth K, Rogers SL, Bhat MA, Crews ST (2009) Neurexin IV and Wrapper interactions mediate Drosophila midline glial migration and axonal ensheathment. Development 136:1147–1157

    Article  CAS  PubMed  Google Scholar 

  114. Noordermeer JN, Kopczynski CC, Fetter RD, Bland KS, Chen WY, Goodman CS (1998) Wrapper, a novel member of the Ig superfamily, is expressed by midline glia and is required for them to ensheath commissural axons in Drosophila. Neuron 21:991–1001

    Article  CAS  PubMed  Google Scholar 

  115. Matter N, Herrlich P, Konig H (2002) Signal-dependent regulation of splicing via phosphorylation of Sam68. Nature 420:691–695

    Article  CAS  PubMed  Google Scholar 

  116. Najib S, Martin-Romero C, Gonzalez-Yanes C, Sanchez-Margalet V (2005) Role of Sam68 as an adaptor protein in signal transduction. Cell Mol Life Sci 62:36–43

    Article  CAS  PubMed  Google Scholar 

  117. Lu Z, Ku L, Chen Y, Feng Y (2005) Developmental abnormalities of myelin basic protein expression in fyn knock-out brain reveal a role of Fyn in posttranscriptional regulation. J Biol Chem 280:389–395

    CAS  PubMed  Google Scholar 

  118. Zhang Y, Lu Z, Ku L, Chen Y, Wang H, Feng Y (2003) Tyrosine phosphorylation of QKI mediates developmental signals to regulate mRNA metabolism. EMBO J 22:1801–1810

    Article  CAS  PubMed  Google Scholar 

  119. Ishii A, Dutta R, Wark GM, Hwang SI, Han DK, Trapp BD, Pfeiffer SE, Bansal R (2009) Human myelin proteome and comparative analysis with mouse myelin. Proc Natl Acad Sci USA 106:14605–14610

    Article  CAS  PubMed  Google Scholar 

  120. Jahn O, Tenzer S, Werner HB (2009) Myelin proteomics: molecular anatomy of an insulating sheath. Mol Neurobiol 40:55–72

    Article  CAS  PubMed  Google Scholar 

  121. Taylor CM, Marta CB, Claycomb RJ, Han DK, Rasband MN, Coetzee T, Pfeiffer SE (2004) Proteomic mapping provides powerful insights into functional myelin biology. Proc Natl Acad Sci USA 101:4643–4648

    Article  CAS  PubMed  Google Scholar 

  122. Dietzl G, Chen D, Schnorrer F, Su KC, Barinova Y, Fellner M, Gasser B, Kinsey K, Oppel S, Scheiblauer S, Couto A, Marra V, Keleman K, Dickson BJ (2007) A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 448:151–156

    Article  CAS  PubMed  Google Scholar 

  123. O’Brien KP, Remm M, Sonnhammer EL (2005) Inparanoid: a comprehensive database of eukaryotic orthologs. Nucleic Acids Res 33:D476–D480

    Article  PubMed  Google Scholar 

  124. Remm M, Storm CE, Sonnhammer EL (2001) Automatic clustering of orthologs and in-paralogs from pairwise species comparisons. J Mol Biol 314:1041–1052

    Article  CAS  PubMed  Google Scholar 

  125. Berglund AC, Sjolund E, Ostlund G, Sonnhammer EL (2008) InParanoid 6: eukaryotic ortholog clusters with inparalogs. Nucleic Acids Res 36:D263–D266

    Article  CAS  PubMed  Google Scholar 

  126. Freeman MR, Delrow J, Kim J, Johnson E, Doe CQ (2003) Unwrapping glial biology: Gcm target genes regulating glial development, diversification, and function. Neuron 38:567–580

    Article  CAS  PubMed  Google Scholar 

  127. Altenhein B, Becker A, Busold C, Beckmann B, Hoheisel JD, Technau GM (2006) Expression profiling of glial genes during Drosophila embryogenesis. Dev Biol 296:545–560

    Article  CAS  PubMed  Google Scholar 

  128. Larocque D, Fragoso G, Huang J, Mushynski WE, Loignon M, Richard S, Almazan G (2009) The QKI-6 and QKI-7 RNA binding proteins block proliferation and promote Schwann cell myelination. PLoS One 4:e5867

    Article  PubMed  CAS  Google Scholar 

  129. Larocque D, Richard S (2005) QUAKING KH domain proteins as regulators of glial cell fate and myelination. RNA Biol 2:37–40

    CAS  PubMed  Google Scholar 

  130. Larocque D, Galarneau A, Liu HN, Scott M, Almazan G, Richard S (2005) Protection of p27(Kip1) mRNA by quaking RNA binding proteins promotes oligodendrocyte differentiation. Nat Neurosci 8:27–33

    Article  CAS  PubMed  Google Scholar 

  131. Larocque D, Pilotte J, Chen T, Cloutier F, Massie B, Pedraza L, Couture R, Lasko P, Almazan G, Richard S (2002) Nuclear retention of MBP mRNAs in the quaking viable mice. Neuron 36:815–829

    Article  CAS  PubMed  Google Scholar 

  132. Peles E, Joho K, Plowman GD, Schlessinger J (1997) Close similarity between Drosophila neurexin IV and mammalian Caspr protein suggests a conserved mechanism for cellular interactions. Cell 88:745–746

    Article  CAS  PubMed  Google Scholar 

  133. Gilbert M, Smith J, Roskams AJ, Auld VJ (2001) Neuroligin 3 is a vertebrate gliotactin expressed in the olfactory ensheathing glia, a growth-promoting class of macroglia. Glia 34:151–164

    Article  CAS  PubMed  Google Scholar 

  134. Charles P, Tait S, Faivre-Sarrailh C, Barbin G, Gunn-Moore F, Denisenko-Nehrbass N, Guennoc A-M, Girault J-A, Brophy PJ, Lubetzki C (2002) Neurofascin is a glial receptor for the paranodin/Caspr-contactin axonal complex at the axoglial junction. Curr Biol 12:217–220

    Article  CAS  PubMed  Google Scholar 

  135. Behr M, Riedel D, Schuh R (2003) The claudin-like megatrachea is essential in septate junctions for the epithelial barrier function in Drosophila. Dev Cell 5:611–620

    Article  CAS  PubMed  Google Scholar 

  136. Furuse M, Tsukita S (2006) Claudins in occluding junctions of humans and flies. Trends Cell Biol 16:181–188

    Article  CAS  PubMed  Google Scholar 

  137. Wu VM, Schulte J, Hirschi A, Tepass U, Beitel GJ (2004) Sinuous is a Drosophila claudin required for septate junction organization and epithelial tube size control. J Cell Biol 164:313–323

    Article  CAS  PubMed  Google Scholar 

  138. Nelson KS, Furuse M and Beitel GJ (2010) The Drosophila claudin kune-kune is required for septate junction organization and tracheal tube size control. Genetics 185:831–839

    Google Scholar 

  139. Tonning A, Hemphälä J, Tång E, Nannmark U, Samakovlis C, Uv A (2005) A transient luminal chitinous matrix is required to model epithelial tube diameter in the Drosophila trachea. Dev Cell 9:423–430

    Article  CAS  PubMed  Google Scholar 

  140. Fehon RG, Dawson IA, Artavanis-Tsakonas S (1994) A Drosophila homologue of membrane-skeleton protein 4.1 is associated with septate junctions and is encoded by the coracle gene. Development 120:545–557

    CAS  PubMed  Google Scholar 

  141. Hijazi A, Masson W, Auge B, Waltzer L, Haenlin M, Roch F (2009) boudin is required for septate junction organisation in Drosophila and codes for a diffusible protein of the Ly6 superfamily. Development 136:2199–2209

    Article  CAS  PubMed  Google Scholar 

  142. Llimargas M, Strigini M, Katidou M, Karagogeos D, Casanova J (2004) Lachesin is a component of a septate junction-based mechanism that controls tube size and epithelial integrity in the Drosophila tracheal system. Development 131:181–190

    Article  CAS  PubMed  Google Scholar 

  143. Wu VM, Yu MH, Paik R, Banerjee S, Liang Z, Paul SM, Bhat MA, Beitel GJ (2007) Drosophila Varicose, a member of a new subgroup of basolateral MAGUKs, is required for septate junctions and tracheal morphogenesis. Development 134:999–1009

    Article  CAS  PubMed  Google Scholar 

  144. Stucke VM, Timmerman E, Vandekerckhove J, Gevaert K, Hall A (2007) The MAGUK protein MPP7 binds to the polarity protein hDlg1 and facilitates epithelial tight junction formation. Mol Biol Cell 18:1744–1755

    Article  CAS  PubMed  Google Scholar 

  145. Bachmann A, Timmer M, Sierralta J, Pietrini G, Gundelfinger ED, Knust E, Thomas U (2004) Cell type-specific recruitment of Drosophila Lin-7 to distinct MAGUK-based protein complexes defines novel roles for Sdt and Dlg-S97. J Cell Sci 117:1899–1909

    Article  CAS  PubMed  Google Scholar 

  146. Métais J-Y, Navarro C, Santoni M-J, Audebert S, Borg J-P (2005) hScrib interacts with ZO-2 at the cell–cell junctions of epithelial cells. FEBS Lett 579:3725–3730

    Article  PubMed  CAS  Google Scholar 

  147. Bilder D, Li M, Perrimon N (2000) Cooperative regulation of cell polarity and growth by Drosophila tumor suppressors. Science 289:113–116

    Article  CAS  PubMed  Google Scholar 

  148. Woods DF, Wu JW, Bryant PJ (1997) Localization of proteins to the apico-lateral junctions of Drosophila epithelia. Dev Genet 20:111–118

    Article  CAS  PubMed  Google Scholar 

  149. Furuse M, Hirase T, Itoh M, Nagafuchi A, Yonemura S, Tsukita S, Tsukita S (1993) Occludin: a novel integral membrane protein localizing at tight junctions. J Cell Biol 123:1777–1788

    Article  CAS  PubMed  Google Scholar 

  150. Ikenouchi J, Furuse M, Furuse K, Sasaki H, Tsukita S, Tsukita S (2005) Tricellulin constitutes a novel barrier at tricellular contacts of epithelial cells. J Cell Biol 171:939–945

    Article  CAS  PubMed  Google Scholar 

  151. Martìn-Padura I, Lostaglio S, Schneemann M, Williams L, Romano M, Fruscella P, Panzeri C, Stoppacciaro A, Ruco L, Villa A, Simmons D, Dejana E (1998) Junctional adhesion molecule, a novel member of the immunoglobulin superfamily that distributes at intercellular junctions and modulates monocyte transmigration. J Cell Biol 142:117–127

    Article  PubMed  Google Scholar 

  152. Hirabayashi S, Tajima M, Yao I, Nishimura W, Mori H, Hata Y (2003) JAM4, a junctional cell adhesion molecule interacting with a tight junction protein, MAGI-1. Mol Cell Biol 23:4267–4282

    Article  CAS  PubMed  Google Scholar 

  153. Cohen CJ, Shieh JT, Pickles RJ, Okegawa T, Hsieh JT, Bergelson JM (2001) The coxsackievirus and adenovirus receptor is a transmembrane component of the tight junction. Proc Natl Acad Sci USA 98:15191–15196

    Article  CAS  PubMed  Google Scholar 

  154. Nasdala I, Wolburg-Buchholz K, Wolburg H, Kuhn A, Ebnet K, Brachtendorf G, Samulowitz U, Kuster B, Engelhardt B, Vestweber D, Butz S (2002) A transmembrane tight junction protein selectively expressed on endothelial cells and platelets. J Biol Chem 277:16294–16303

    Article  CAS  PubMed  Google Scholar 

  155. Steed E, Rodrigues NTL, Balda MS, Matter K (2009) Identification of MarvelD3 as a tight junction-associated transmembrane protein of the occludin family. BMC Cell Biol 10:95

    Article  PubMed  CAS  Google Scholar 

  156. Haskins J, Gu L, Wittchen ES, Hibbard J, Stevenson BR (1998) ZO-3, a novel member of the MAGUK protein family found at the tight junction, interacts with ZO-1 and occludin. J Cell Biol 141:199–208

    Article  CAS  PubMed  Google Scholar 

  157. Wei X, Ellis HM (2001) Localization of the Drosophila MAGUK protein Polychaetoid is controlled by alternative splicing. Mech Dev 100:217–231

    Article  CAS  PubMed  Google Scholar 

  158. Ide N, Hata Y, Nishioka H, Hirao K, Yao I, Deguchi M, Mizoguchi A, Nishimori H, Tokino T, Nakamura Y, Takai Y (1999) Localization of membrane-associated guanylate kinase (MAGI)-1/BAI-associated protein (BAP) 1 at tight junctions of epithelial cells. Oncogene 18:7810–7815

    Article  CAS  PubMed  Google Scholar 

  159. Hamazaki Y, Itoh M, Sasaki H, Furuse M, Tsukita S (2002) Multi-PDZ domain protein 1 (MUPP1) is concentrated at tight junctions through its possible interaction with claudin-1 and junctional adhesion molecule. J Biol Chem 277:455–461

    Article  CAS  PubMed  Google Scholar 

  160. Lemmers C, Médina E, Delgrossi M-H, Michel D, Arsanto J-P, Le Bivic A (2002) hINADl/PATJ, a homolog of discs lost, interacts with crumbs and localizes to tight junctions in human epithelial cells. J Biol Chem 277:25408–25415

    Article  CAS  PubMed  Google Scholar 

  161. Citi S, Sabanay H, Jakes R, Geiger B, Kendrick-Jones J (1988) Cingulin, a new peripheral component of tight junctions. Nature 333:272–276

    Article  CAS  PubMed  Google Scholar 

  162. Ohnishi H, Nakahara T, Furuse K, Sasaki H, Tsukita S, Furuse M (2004) JACOP, a novel plaque protein localizing at the apical junctional complex with sequence similarity to cingulin. J Biol Chem 279:46014–46022

    Article  CAS  PubMed  Google Scholar 

  163. Suzuki A, Ohno S (2006) The PAR-aPKC system: lessons in polarity. J Cell Sci 119:979–987

    Article  CAS  PubMed  Google Scholar 

  164. Balda MS, Garrett MD, Matter K (2003) The ZO-1-associated Y-box factor ZONAB regulates epithelial cell proliferation and cell density. J Cell Biol 160:423–432

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We are thankful for much help from members of the laboratory for support throughout the work. The laboratory has received funding from the European Community’s Seventh Framework Programme (FP7/2007-2013) under grant agreement No. HEALTH-F2-2008-201535.

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  1. Institut für Neurobiologie, Badestr. 9, 48149, Münster, Germany

    Floriano Rodrigues, Imke Schmidt & Christian Klämbt

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  1. Floriano Rodrigues
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Correspondence to Christian Klämbt.

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Rodrigues, F., Schmidt, I. & Klämbt, C. Comparing peripheral glial cell differentiation in Drosophila and vertebrates. Cell. Mol. Life Sci. 68, 55–69 (2011). https://doi.org/10.1007/s00018-010-0512-6

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  • DOI: https://doi.org/10.1007/s00018-010-0512-6

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