Contact-Mediated Inhibition Between Oligodendrocyte Progenitor Cells and Motor Exit Point Glia Establishes the Spinal Cord Transition Zone

PLoS Biology

Volumn 12, Issue 9, 2014, Pages

  Smith, Cody J ^a   Morris, Angela D ^a   Welsh, Taylor G ^a   Kucenas, Sarah ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; FORKHEAD TRANSCRIPTION FACTOR; OLIGODENDROCYTE TRANSCRIPTION FACTOR 2; TRANSCRIPTION FACTOR FOXD3; TRANSCRIPTION FACTOR NKX2.2; TRANSCRIPTION FACTOR SOX10; UNCLASSIFIED DRUG; WNT INHIBITORY FACTOR 1; REPRESSOR PROTEIN; SIGNAL TRANSDUCING ADAPTOR PROTEIN; WIF1 PROTEIN, ZEBRAFISH; ZEBRAFISH PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL MIGRATION; CELL POPULATION; CELLULAR DISTRIBUTION; CONTACT INHIBITION; CONTROLLED STUDY; EMBRYO; GLIA; GLIA CELL; IN VIVO STUDY; MOTOR EXIT POINT GLIA; MYELINATION; NERVE FIBER; NEURAL CREST CELL; NONHUMAN; OLIGODENDROCYTE PRECURSOR CELL; PROTEIN EXPRESSION; SPINAL CORD; TIME LAPSE IMAGING; ZEBRA FISH; ANIMAL; ANTIBODY SPECIFICITY; CELL DIFFERENTIATION; CELL LINEAGE; CELL MOTION; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MORPHOGENESIS; MOTONEURON; MYELIN SHEATH; OLIGODENDROGLIA; SCHWANN CELL; STEM CELL; ULTRASTRUCTURE;

DANIO RERIO;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; AXONS; CELL DIFFERENTIATION; CELL LINEAGE; CELL MOVEMENT; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MORPHOGENESIS; MOTOR NEURONS; MYELIN SHEATH; OLIGODENDROGLIA; ORGAN SPECIFICITY; REPRESSOR PROTEINS; SCHWANN CELLS; SPINAL CORD; STEM CELLS; TIME-LAPSE IMAGING; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84920389892     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1001961     Document Type: Article

References (49)

1. Fraher JP, Rossiter JP, (1983) Cell clusters on fetal rat ventral roots: prenatal development. J Anat 136: 111–128.
2. Lu QR, Sun T, Zhu Z, Ma N, Garcia M, et al. (2002) Common developmental requirement for Olig function indicates a motor neuron/oligodendrocyte connection. Cell 109: 75–86.
3. Jessen KR, Mirsky R, (2005) The origin and development of glial cells in peripheral nerves. Nat Rev Neurosci 6: 671–682 doi:10.1038/nrn1746
4. Emery B, (2010) Regulation of oligodendrocyte differentiation and myelination. Science 330: 779–782 doi:10.1126/science.1190927
5. Sepp KJ, Schulte J, Auld VJ, (2001) Peripheral glia direct axon guidance across the CNS/PNS transition zone. Developmental Biology 238: 47–63 doi:10.1006/dbio.2001.0411
6. Kucenas S, Takada N, Park H-C, Woodruff E, Broadie K, et al. (2008) CNS-derived glia ensheath peripheral nerves and mediate motor root development. Nat Neurosci 11: 143–151 doi:10.1038/nn2025
7. Maro GS, Vermeren M, Voiculescu O, Melton L, Cohen J, et al. (2004) Neural crest boundary cap cells constitute a source of neuronal and glial cells of the PNS. Nat Neurosci 7: 930–938 doi:10.1038/nn1299
8. Itoyama Y, Webster HD, Richardson EP, Trapp BD, (1983) Schwann cell remyelination of demyelinated axons in spinal cord multiple sclerosis lesions. Ann Neurol 14: 339–346 doi:10.1002/ana.410140313
9. Coulpier F, Le Crom S, Maro GS, Manent J, Giovannini M, et al. (2009) Novel features of boundary cap cells revealed by the analysis of newly identified molecular markers. Glia 57: 1450–1457 doi:10.1002/glia.20862
10. Coulpier F, Decker L, Funalot B, Vallat JM, Garcia-Bragado F, et al. (2010) CNS/PNS boundary transgression by central glia in the absence of Schwann cells or Krox20/Egr2 function. J Neurosci 30: 5958–5967 doi:10.1523/JNEUROSCI.0017-10.2010
11. Niederländer C, Lumsden A, (1996) Late emigrating neural crest cells migrate specifically to the exit points of cranial branchiomotor nerves. Development 122: 2367–2374.
12. Duncan ID, Hoffman RL, (1997) Schwann cell invasion of the central nervous system of the myelin mutants. J Anat 190(Pt 1):35–49.
13. Bron R, Vermeren M, Kokot N, Andrews W, Little GE, et al. (2007) Boundary cap cells constrain spinal motor neuron somal migration at motor exit points by a semaphorin-plexin mechanism. Neural Development 2: 21 doi:10.1186/1749-8104-2-21
14. Vermeren M, Maro GS, Bron R, McGonnell IM, Charnay P, et al. (2003) Integrity of developing spinal motor columns is regulated by neural crest derivatives at motor exit points. Neuron 37: 403–415.
15. Fraher JP, Dockery P, O'Donoghue O, Riedewald B, O'Leary D, (2007) Initial motor axon outgrowth from the developing central nervous system. J Anat 211: 600–611 doi:10.1111/j.1469-7580.2007.00807.x
16. Rickmann M, Fawcett JW, Keynes RJ, (1985) The migration of neural crest cells and the growth of motor axons through the rostral half of the chick somite. J Embryol Exp Morphol 90: 437–455.
17. Jones DS, (1939) Studies on the origin of sheath cells and sympathetic ganglia in the chick. The Anatomical Record 73: 343–357.
18. Lunn ER, Scourfield J, Keynes RJ, Stern CD, (1987) The neural tube origin of ventral root sheath cells in the chick embryo. Development 101: 247–254.
19. Weston JA, (1963) A radioautographic analysis of the migration and localization of trunk neural crest cells in the chick. Developmental Biology 6: 279–310.
20. Fraher JP, Kaar GF, (1986) The lumbar ventral root-spinal cord transitional zone in the rat. A morphological study during development and at maturity. J Anat 145: 109–122.
21. Kirby BB, Takada N, Latimer AJ, Shin J, Carney TJ, et al. (2006) In vivo time-lapse imaging shows dynamic oligodendrocyte progenitor behavior during zebrafish development. Nat Neurosci 9: 1506–1511 doi:10.1038/nn1803
22. Hughes EG, Kang SH, Fukaya M, Bergles DE, (2013) Oligodendrocyte progenitors balance growth with self-repulsion to achieve homeostasis in the adult brain. Nat Neurosci 16: 668–676 doi:10.1038/nn.3390
23. Le Douarin N, Dulac C, Dupin E, Cameron-Curry P, (1991) Glial cell lineages in the neural crest. Glia 4: 175–184 doi:10.1002/glia.440040209
24. Raible DW, Eisen JS, (1994) Restriction of neural crest cell fate in the trunk of the embryonic zebrafish. Development 120: 495–503.
25. Honjo Y, Kniss J, Eisen JS, (2008) Neuregulin-mediated ErbB3 signaling is required for formation of zebrafish dorsal root ganglion neurons. Development 135: 2993–2993 doi:10.1242/dev.027763
26. McGraw HF, Snelson CD, Prendergast A, Suli A, Raible DW, (2012) Postembryonic neuronal addition in Zebrafish dorsal root ganglia is regulated by Notch signaling. Neural Development 7: 23 doi:10.1186/1749-8104-7-23
27. Kucenas S, Wang W-D, 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 doi:10.1523/JNEUROSCI.4193-09.2009
28. Prendergast A, Linbo TH, Swarts T, Ungos JM, McGraw HF, et al. (2012) The metalloproteinase inhibitor Reck is essential for zebrafish DRG development. Development 139: 1141–1152 doi:10.1242/dev.072439
29. Kucenas S, Snell H, Appel B, (2008) nkx2.2a promotes specification and differentiation of a myelinating subset of oligodendrocyte lineage cells in zebrafish. Neuron Glia Biol 4: 71–81 doi:10.1017/S1740925X09990123
30. McGraw HF, Nechiporuk A, Raible DW, (2008) Zebrafish dorsal root ganglia neural precursor cells adopt a glial fate in the absence of neurogenin1. J Neurosci 28: 12558–12569 doi:10.1523/JNEUROSCI.2079-08.2008
31. Park H-C, Mehta A, Richardson JS, Appel B, (2002) olig2 is required for zebrafish primary motor neuron and oligodendrocyte development. Developmental Biology 248: 356–368 doi:10.1006/dbio.2002.0738
32. Schäfer M, Kinzel D, Neuner C, Schartl M, Volff J-N, et al. (2005) Hedgehog and retinoid signalling confines nkx2.2b expression to the lateral floor plate of the zebrafish trunk. Mech Dev 122: 43–56 doi:10.1016/j.mod.2004.09.002
33. Richardson WD, Kessaris N, Pringle N, (2006) Oligodendrocyte wars. Nat Rev Neurosci 7: 11–18 doi:10.1038/nrn1826
34. Cooper MK, Porter JA, Young KE, Beachy PA, (1998) Teratogen-mediated inhibition of target tissue response to Shh signaling. Science 280: 1603–1607 doi:10.1126/science.280.5369.1603
35. Zannino DA, Appel B, (2009) Olig2+ precursors produce abducens motor neurons and oligodendrocytes in the zebrafish hindbrain. J Neurosci 29: 2322–2333 doi:10.1523/JNEUROSCI.3755-08.2009
36. Hochgreb-Hägele T, Bronner ME, (2013) A novel FoxD3 gene trap line reveals neural crest precursor movement and a role for FoxD3 in their specification. Developmental Biology 374: 1–11 doi:10.1016/j.ydbio.2012.11.035
37. Kim H, Shin J, Kim S, Poling J, Park H-C, et al. (2008) Notch-regulated oligodendrocyte specification from radial glia in the spinal cord of zebrafish embryos. Dev Dyn 237: 2081–2089 doi:10.1002/dvdy.21620
38. Lyons DA, Pogoda H-M, Voas MG, Woods IG, Diamond B, et al. (2005) erbb3 and erbb2 are essential for Schwann cell migration and myelination in zebrafish. Curr Biol 15: 513–524 doi:10.1016/j.cub.2005.02.030
39. Jessen KR, Mirsky R, (1997) Embryonic Schwann cell development: the biology of Schwann cell precursors and early Schwann cells. J Anat 191(Pt 4): 501–505.
40. Lewis GM, Kucenas S, (2013) Motor nerve transection and time-lapse imaging of glial cell behaviors in live zebrafish. J Vis Exp 76.
41. Almeida RG, Czopka T, ffrench-Constant C, Lyons DA, (2011) Individual axons regulate the myelinating potential of single oligodendrocytes in vivo. Development 138: 4443–4450 doi:10.1242/dev.071001
42. Fraher JP, (1997) Axon-glial relationships in early CNS-PNS transitional zone development: an ultrastructural study. J Neurocytol 26: 41–52.
43. Parker RJ, Auld VJ, (2006) Roles of glia in the Drosophila nervous system. Seminars in Cell and Developmental Biology 17: 66–77 doi:10.1016/j.semcdb.2005.11.012
44. Clark JK, O'keefe A, Mastracci TL, Sussel L, Matise MP, et al. (2014) Mammalian Nkx2.2(+) perineurial glia are essential for motor nerve development. Dev Dyn 243(9): 1116–1129 doi:10.1002/dvdy.24158
45. Zawadzka M, Rivers LE, Fancy SPJ, Zhao C, Tripathi R, et al. (2010) CNS-resident glial progenitor/stem cells produce Schwann cells as well as oligodendrocytes during repair of CNS demyelination. Stem Cell 6: 578–590 doi:10.1016/j.stem.2010.04.002
46. Rosenberg AF, Wolman MA, Franzini-Armstrong C, Granato M, (2012) In vivo nerve-macrophage interactions following peripheral nerve injury. J Neurosci 32: 3898–3909 doi:10.1523/JNEUROSCI.5225-11.2012
47. Bernardos RL, Raymond PA, (2006) GFAP transgenic zebrafish. Gene Expression Patterns 6: 1007–1013 doi:10.1016/j.modgep.2006.04.006
48. Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF, (1995) Stages of embryonic development of the zebrafish. Dev Dyn 203: 253–310.
49. Binari LA, Lewis GM, Kucenas S, (2013) Perineurial glia require notch signaling during motor nerve development but not regeneration. J Neurosci 33: 4241–4252 doi:10.1523/JNEUROSCI.4893-12.2013