Perineurial glia require notch signaling during motor nerve development but not regeneration

Journal of Neuroscience

Volumn 33, Issue 10, 2013, Pages 4241-4252

  Binari, Laura A ^a   Lewis, Gwendolyn M ^a   Kucenas, Sarah ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NOTCH RECEPTOR;

ANIMAL TISSUE; ARTICLE; CELL MIGRATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; EMBRYO; FEMALE; GLIA CELL; HEAT SHOCK; IMAGING; IMMUNOCYTOCHEMISTRY; IN SITU HYBRIDIZATION; LARVA; MALE; MICROSCOPY; MOTOR NERVE; NERVE CELL DIFFERENTIATION; NERVE GROWTH; NERVE REGENERATION; NERVE TRANSECTION; NONHUMAN; PERINEURIUM; PRIORITY JOURNAL; RNA HYBRIDIZATION; SCHWANN CELL; SIGNAL TRANSDUCTION; ZEBRA FISH;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; CELL DIFFERENTIATION; CELL MOVEMENT; DIPEPTIDES; EMBRYO, NONMAMMALIAN; ENZYME INHIBITORS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GREEN FLUORESCENT PROTEINS; HOT TEMPERATURE; LARVA; LUMINESCENT PROTEINS; MICROSCOPY, CONFOCAL; MUTATION; NERVE REGENERATION; NERVE TISSUE PROTEINS; NEUROGLIA; PERIPHERAL NERVE INJURIES; PERIPHERAL NERVES; RECEPTORS, NOTCH; SCHWANN CELLS; SIGNAL TRANSDUCTION; TIME FACTORS; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84874622290     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4893-12.2013     Document Type: Article

References (41)

1. Akert K, Sandri C, Weibel ER, Peper K, Moor H (1976) The fine structure of the perineural endothelium. Cell Tissue Res 165:281-295. Medline
2. Andersson ER, Sandberg R, Lendahl U (2011) Notch signaling: simplicity in design, versatility in function. Development 138:3593-3612. CrossRef Medline
3. Banerjee S, Gordon L, Donn TM, Berti C, Moens CB, Burden SJ, Granato M (2011) A novel role for MuSK and non-canonical Wnt signaling during segmental neural crest cell migration. Development 138:3287-3296. CrossRef Medline
4. Bourne GH (1968) The structure and function of nervous tissue. New York: Academic.
5. Bray SJ (2006) Notch signalling: a simple pathway becomes complex. Nat Rev Mol Cell Biol 7:678-689. CrossRef Medline
6. Burkel WE (1967) The histological fine structure of perineurium. Anat Rec 158:177-189. CrossRef Medline
7. Edenfeld G, Altenhein B, Zierau A, Cleppien D, Krukkert K, Technau G, Klämbt C (2007) Notch and Numb are required for normal migration of peripheral glia in Drosophila. Dev Biol 301:27-37. CrossRef Medline
8. Geling A, Steiner H, Willem M, Bally-Cuif L, Haass C (2002) A gamma secretase inhibitor blocks Notch signaling in vivo and causes a severe neurogenic phenotype in zebrafish. EMBO Rep 3:688-694. CrossRef Medline
9. Geuna S, Raimondo S, Ronchi G, Di Scipio F, Tos P, Czaja K, Fornaro M (2009) Chapter 3: Histology of the peripheral nerve and changes occur-ring during nerve regeneration. Int Rev Neurobiol 87:27-46. CrossRef Medline
10. Gilmour DT, Maischein HM, Nusslein-Volhard C (2002) Migration and function of a glial subtype in the vertebrate peripheral nervous system. Neuron 34:577-588. CrossRef Medline
11. Jessen KR, Mirsky R (2002) Signals that determine Schwann cell identity. J Anat 200:367-376. CrossRef Medline
12. Jessen KR, Mirsky R (2005) The origin and development of glial cells in peripheral nerves. Nat Rev Neurosci 6:671-682. CrossRef Medline
13. Kim H, Shin J, Kim S, Poling J, Park HC, Appel B (2008) Notch-regulated oligodendrocyte specification from radial glia in the spinal cord of zebrafish embryos. Dev Dyn 237:2081-2089. CrossRef Medline
14. Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF (1995) Stages of embryonic development of the zebrafish. Dev Dyn 203:253-310. CrossRef Medline
15. Kirby BB, Takada N, Latimer AJ, Shin J, Carney TJ, Kelsh RN, Appel B (2006) In vivo time-lapse imaging shows dynamic oligodendrocyte progenitor behavior during zebrafish development. Nat Neurosci 9:1506-1511. CrossRef Medline
16. 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. CrossRef Medline
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. CrossRef Medline
18. Kucenas S, Wang WD, Knapik EW, Appel B (2009) A selective glial barrier at motor axon exit points prevents oligodendrocyte migration from the spinal cord. J Neurosci 29:15187-15194. CrossRef Medline
19. Kuspert M, Weider M, Muller J, Hermans-Borgmeyer I, Meijer D, Wegner M (2012) Desert hedgehog links transcription factor Sox10 to perineurial development. J Neurosci 32:5472-5480. CrossRef Medline
20. Lyons DA, Pogoda HM, Voas MG, Woods IG, Diamond B, Nix R, Arana N, Jacobs J, Talbot WS (2005) erbb3 and erbb2 are essential for Schwann cell migration and myelination in zebrafish. Curr Biol 15:513-524. CrossRef Medline
21. Mirsky R, Parmantier E, McMahon AP, Jessen KR (1999) Schwann cell derived desert hedgehog signals nerve sheath formation. Ann N Y Acad Sci 883:196-202. CrossRef Medline
22. Mirsky R, Woodhoo A, Parkinson DB, Arthur-Farraj P, Bhaskaran A, Jessen KR (2008) Novel signals controlling embryonic Schwann cell development, myelination and dedifferentiation. J Peripher Nerv Syst 13:122-135. CrossRef Medline
23. Napoli I, Noon LA, Ribeiro S, Kerai AP, Parrinello S, Rosenberg LH, Collins MJ, Harrisingh MC, White IJ, Woodhoo A, Lloyd AC (2012) A central role for the ERK-signaling pathway in controlling Schwann cell plasticity and peripheral nerve regeneration in vivo. Neuron 73:729-742. CrossRef Medline
24. Newbern J, Birchmeier C (2010) Nrg1/ErbB signaling networks in Schwann cell development and myelination. Semin Cell Dev Biol 21:922-928. CrossRef Medline
25. Ninov N, Borius M, Stainier DYR (2012) Different levels of Notch signaling regulate quiescence, renewal and differentiation in pancreatic endocrine progenitors. Development 139:1557-1567. CrossRef Medline
26. Park HC, Appel B (2003) Delta-Notch signaling regulates oligodendrocyte specification. Development 130:3747-3755. CrossRef Medline
27. Park HC, Boyce J, Shin J, Appel B (2005) Oligodendrocyte specification in zebrafish requires Notch-regulated cyclin-dependent kinase inhibitor function. J Neurosci 25:6836-6844. CrossRef Medline
28. Parmantier E, Lynn B, Lawson D, Turmaine M, Namini SS, Chakrabarti L, McMahon AP, Jessen KR, Mirsky R (1999) Schwann cell-derived Desert hedgehog controls the development of peripheral nerve sheaths. Neuron 23:713-724. CrossRef Medline
29. Parrinello S, Napoli I, Ribeiro S, Digby PW, Fedorova M, Parkinson DB, Doddrell RD, Nakayama M, Adams RH, Lloyd AC (2010) EphB signaling directs peripheral nerve regeneration through Sox2-dependent Schwann cell sorting. Cell 143:145-155. CrossRef Medline
30. Parsons MJ, Pisharath H, Yusuff S, Moore JC, Siekmann AF, Lawson N, Leach SD (2009) Notch-responsive cells initiate the secondary transition in larval zebrafish pancreas. Mech Dev 126:898-912. CrossRef Medline
31. Scheer N, Groth A, Hans S, Campos-Ortega JA (2001) An instructive function for Notch in promoting gliogenesis in the zebrafish retina. Development 1099-1107.
32. Schroder JM, May R, Weis J (1993) Perineurial cells are the first to traverse gaps of peripheral nerves in silicone tubes. Clin Neurol Neurosurg 95 [Suppl]:S78-S83.
33. Sepp KJ, Schulte J, Auld VJ (2000) Developmental dynamics of peripheral glia in Drosophila melanogaster. Glia 30:122-133. CrossRef Medline
34. Sepp KJ, Schulte J, Auld VJ (2001) Peripheral glia direct axon guidance across the CNS/PNS transition zone. Dev Biol 238:47-63. CrossRef Medline
35. Shin J, Poling J, Park HC, Appel B (2007) Notch signaling regulates neural precursor allocation and binary neuronal fate decisions in zebrafish. Development 134:1911-1920. CrossRef Medline
36. Snyder JL, Kearns CA, Appel B (2012) Fbxw7 regulates Notch to control specification of neural precursors for oligodendrocyte fate. Neural Dev 7:15. CrossRef Medline
37. Takke C, Dornseifer P, Weizsäcker von E (1999) her4, a zebrafish homologue of the Drosophila neurogenic gene E(spl), is a target of NOTCH signalling. Development 1811-1821.
38. Taylor MK, Yeager K, Morrison SJ (2007) Physiological Notch signaling promotes gliogenesis in the developing peripheral and central nervous systems. Development 134:2435-2447. CrossRef Medline
39. Wang S, Barres BA (2000) Up a Notch: Instructing Gliogenesis. Neuron 27:197-200. CrossRef Medline
40. Woodhoo A, Alonso MBD, Droggiti A, Turmaine M, D'Antonio M, Parkinson DB, Wilton DK, Al-Shawi R, Simons P, Shen J, Guillemot F, Radtke F, Meijer D, Feltri ML, Wrabetz L, Mirsky R, Jessen KR (2009) Notch controls embryonic Schwann cell differentiation, postnatal myelination and adult plasticity. Nat Neurosci 12:839-847. Medline
41. Yeo SY, Kim M, Kim HS, Huh TL, Chitnis AB (2007) Fluorescent protein expression driven by her4 regulatory elements reveals the spatiotemporal pattern of Notch signaling in the nervous system of zebrafish embryos. Dev Biol 301:555-567. CrossRef Medline