The structural role of radial glial endfeet in confining spinal motor neuron somata is controlled by the Reelin and Notch pathways

Experimental Neurology

Volumn 249, Issue , 2013, Pages 83-94

  Lee, Hojae ^a   Song, Mi Ryoung ^a  

^a Gwangju Institute of Science and Technology (GIST)   (South Korea)

Author keywords

Motor neurons; Notch; Radial glia; Reelin

Indexed keywords

NOTCH RECEPTOR; REELIN;

ANIMAL TISSUE; ARTICLE; BASEMENT MEMBRANE; BOUNDARY CAP CELL; CHICK EMBRYO; CONTROLLED STUDY; EMBRYO; GLIA; MOUSE; NERVE CELL; NEURAL TUBE; NONHUMAN; PRIORITY JOURNAL; SCHWANN CELL PRECURSOR; SIGNAL TRANSDUCTION; SPINAL CORD MOTONEURON;

MOTOR NEURONS; NOTCH; RADIAL GLIA; REELIN;

ANIMALS; CELL ADHESION MOLECULES, NEURONAL; CHICK EMBRYO; EPENDYMOGLIAL CELLS; EXTRACELLULAR MATRIX PROTEINS; FEMALE; MICE; MICE, NEUROLOGIC MUTANTS; MOTOR NEURONS; NERVE TISSUE PROTEINS; PREGNANCY; RECEPTOR, NOTCH1; SERINE ENDOPEPTIDASES; SIGNAL TRANSDUCTION;

EID: 84884168835     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2013.08.010     Document Type: Article

References (53)

1. Bai G., Chivatakarn O., Bonanomi D., Lettieri K., Franco L., Xia C., Stein E., Ma L., Lewcock J.W., Pfaff S.L. Presenilin-dependent receptor processing is required for axon guidance. Cell 2010, 144:106-118.
2. Barry D., McDermott K. Differentiation of radial glia from radial precursor cells and transformation into astrocytes in the developing rat spinal cord. Glia 2005, 50:187-197.
3. Barry D.S., Pakan J.M., O'Keeffe G.W., McDermott K.W. The spatial and temporal arrangement of the radial glial scaffold suggests a role in axon tract formation in the developing spinal cord. J. Anat. 2012, 222:203-213.
4. Benjelloun-Touimi S., Jacque C.M., Derer P., De Vitry F., Maunoury R., Dupouey P. Evidence that mouse astrocytes may be derived from the radial glia. An immunohistochemical study of the cerebellum in the normal and reeler mouse. J. Neuroimmunol. 1985, 9:87-97.
5. Bravo-Ambrosio A., Kaprielian Z. Crossing the border: molecular control of motor axon exit. Int. J. Mol. Sci. 2012, 12:8539-8561.
6. Campbell K. Signaling to and from radial glia. Glia 2003, 43:44-46.
7. Chauvet S., Rougon G. Semaphorins deployed to repel cell migrants at spinal cord borders. J. Biol. 2008, 7:4.
8. Coulpier F., Decker L., Funalot B., Vallat J.M., Garcia-Bragado F., Charnay P., Topilko P. CNS/PNS boundary transgression by central glia in the absence of Schwann cells or Krox20/Egr2 function. J. Neurosci. 2010, 30:5958-5967.
9. D'Arcangelo G., Miao G.G., Chen S.C., Soares H.D., Morgan J.I., Curran T. A protein related to extracellular matrix proteins deleted in the mouse mutant reeler. Nature 1995, 374:719-723.
10. Dillon A.K., Jevince A.R., Hinck L., Ackerman S.L., Lu X., Tessier-Lavigne M., Kaprielian Z. UNC5C is required for spinal accessory motor neuron development. Mol. Cell. Neurosci. 2007, 35:482-489.
11. Forster E., Tielsch A., Saum B., Weiss K.H., Johanssen C., Graus-Porta D., Muller U., Frotscher M. Reelin, Disabled 1, and beta 1 integrins are required for the formation of the radial glial scaffold in the hippocampus. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:13178-13183.
12. Fraher J.P., Dockery P., O'Donoghue O., Riedewald B., O'Leary D. Initial motor axon outgrowth from the developing central nervous system. J. Anat. 2007, 211:600-611.
13. Frotscher M., Haas C.A., Forster E. Reelin controls granule cell migration in the dentate gyrus by acting on the radial glial scaffold. Cereb. Cortex 2003, 13:634-640.
14. Fukaya M., Yamada K., Nagashima M., Tanaka K., Watanabe M. Down-regulated expression of glutamate transporter GLAST in Purkinje cell-associated astrocytes of reeler and weaver mutant cerebella. Neurosci. Res. 1999, 34:165-175.
15. Gaiano N., Nye J.S., Fishell G. Radial glial identity is promoted by Notch1 signaling in the murine forebrain. Neuron 2000, 26:395-404.
16. Ghosh S., Marquardt T., Thaler J.P., Carter N., Andrews S.E., Pfaff S.L., Hunter T. Instructive role of aPKCzeta subcellular localization in the assembly of adherens junctions in neural progenitors. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:335-340.
17. Grant P.K., Moens C.B. The neuroepithelial basement membrane serves as a boundary and a substrate for neuron migration in the zebrafish hindbrain. Neural Dev. 2010, 5:9.
18. Halfter W., Dong S., Yip Y.P., Willem M., Mayer U. A critical function of the pial basement membrane in cortical histogenesis. J. Neurosci. 2002, 22:6029-6040.
19. Hartfuss E., Forster E., Bock H.H., Hack M.A., Leprince P., Luque J.M., Herz J., Frotscher M., Gotz M. Reelin signaling directly affects radial glia morphology and biochemical maturation. Development 2003, 130:4597-4609.
20. Hashimoto-Torii K., Torii M., Sarkisian M.R., Bartley C.M., Shen J., Radtke F., Gridley T., Sestan N., Rakic P. Interaction between Reelin and Notch signaling regulates neuronal migration in the cerebral cortex. Neuron 2008, 60:273-284.
21. Hatakeyama J., Bessho Y., Katoh K., Ookawara S., Fujioka M., Guillemot F., Kageyama R. Hes genes regulate size, shape and histogenesis of the nervous system by control of the timing of neural stem cell differentiation. Development 2004, 131:5539-5550.
22. Hochstim C., Deneen B., Lukaszewicz A., Zhou Q., Anderson D.J. Identification of positionally distinct astrocyte subtypes whose identities are specified by a homeodomain code. Cell 2008, 133:510-522.
23. Hu H., Yang Y., Eade A., Xiong Y., Qi Y. Breaches of the pial basement membrane and disappearance of the glia limitans during development underlie the cortical lamination defect in the mouse model of muscle-eye-brain disease. J. Comp. Neurol. 2007, 501:168-183.
24. Jankovski A., Sotelo C. Subventricular zone-olfactory bulb migratory pathway in the adult mouse: cellular composition and specificity as determined by heterochronic and heterotopic transplantation. J. Comp. Neurol. 1996, 371:376-396.
25. Joosten E.A., Gribnau A.A. Astrocytes and guidance of outgrowing corticospinal tract axons in the rat. An immunocytochemical study using anti-vimentin and anti-glial fibrillary acidic protein. Neuroscience 1989, 31:439-452.
26. Keilani S., Sugaya K. Reelin induces a radial glial phenotype in human neural progenitor cells by activation of Notch-1. BMC Dev. Biol. 2008, 8:69.
27. Kim H., Shin J., Kim S., Poling J., Park H.C., Appel B. Notch-regulated oligodendrocyte specification from radial glia in the spinal cord of zebrafish embryos. Dev. Dyn. 2008, 237:2081-2089.
28. Kucenas S., Takada N., Park H.C., Woodruff E., Broadie K., Appel B. CNS-derived glia ensheath peripheral nerves and mediate motor root development. Nat. Neurosci. 2008, 11:143-151.
29. Lois C., Garcia-Verdugo J.M., Alvarez-Buylla A. Chain migration of neuronal precursors. Science 1996, 271:978-981.
30. Louvi A., Sisodia S.S., Grove E.A. Presenilin 1 in migration and morphogenesis in the central nervous system. Development 2004, 131:3093-3105.
31. Luque J.M., Morante-Oria J., Fairen A. Localization of ApoER2, VLDLR and Dab1 in radial glia: groundwork for a new model of reelin action during cortical development. Brain Res. Dev. Brain Res. 2003, 140:195-203.
32. Maro G.S., Vermeren M., Voiculescu O., Melton L., Cohen J., Charnay P., Topilko P. Neural crest boundary cap cells constitute a source of neuronal and glial cells of the PNS. Nat. Neurosci. 2004, 7:930-938.
33. Martin-Lopez E., Blanchart A., De Carlos J.A., Lopez-Mascaraque L. Dab1 (Disable homolog-1) reelin adaptor protein is overexpressed in the olfactory bulb at early postnatal stages. PLoS One 2011, 6:e26673.
34. Mauti O., Domanitskaya E., Andermatt I., Sadhu R., Stoeckli E.T. Semaphorin6A acts as a gate keeper between the central and the peripheral nervous system. Neural Dev. 2007, 2:28.
35. McDermott K.W., Barry D.S., McMahon S.S. Role of radial glia in cytogenesis, patterning and boundary formation in the developing spinal cord. J. Anat. 2005, 207:241-250.
36. Murtaugh L.C., Stanger B.Z., Kwan K.M., Melton D.A. Notch signaling controls multiple steps of pancreatic differentiation. PNAS 2003, 100:14920-14925.
37. Noctor S.C., Flint A.C., Weissman T.A., Dammerman R.S., Kriegstein A.R. Neurons derived from radial glial cells establish radial units in neocortex. Nature 2001, 409:714-720.
38. O'Brien D., Dockery P., McDermott K., Fraher J. Early development of rat ventral root transitional zone: an immunohistochemical and morphometric study. J. Neurocytol. 2001, 30:11-20.
39. Palmesino E., Rousso D.L., Kao T.J., Klar A., Laufer E., Uemura O., Okamoto H., Novitch B.G., Kania A. Foxp1 and lhx1 coordinate motor neuron migration with axon trajectory choice by gating Reelin signalling. PLoS Biol. 2010, 8:e1000446.
40. Phelps P.E., Rich R., Dupuy-Davies S., Rios Y., Wong T. Evidence for a cell-specific action of Reelin in the spinal cord. Dev. Biol. 2002, 244:180-198.
41. Pinto-Lord M.C., Evrard P., Caviness V.S. Obstructed neuronal migration along radial glial fibers in the neocortex of the reeler mouse: a Golgi-EM analysis. Brain Res. 1982, 256:379-393.
42. Rice D.S., Curran T. Role of the reelin signaling pathway in central nervous system development. Annu. Rev. Neurosci. 2001, 24:1005-1039.
43. Shu T., Richards L.J. Cortical axon guidance by the glial wedge during the development of the corpus callosum. J. Neurosci. 2001, 21:2749-2758.
44. Sibbe M., Forster E., Basak O., Taylor V., Frotscher M. Reelin and Notch1 cooperate in the development of the dentate gyrus. J. Neurosci. 2009, 29:8578-8585.
45. Silver J., Lorenz S.E., Wahlsten D., Coughlin J. Axonal guidance during development of the great cerebral commissures: descriptive and experimental studies, in vivo, on the role of preformed glial pathways. J. Comp. Neurol. 1982, 210:10-29.
46. Thaler J.P., Koo S.J., Kania A., Lettieri K., Andrews S., Cox C., Jessell T.M., Pfaff S.L. A postmitotic role for Isl-class LIM homeodomain proteins in the assignment of visceral spinal motor neuron identity. Neuron 2004, 41:337-350.
47. Uemura O., Okada Y., Ando H., Guedj M., Higashijima S., Shimazaki T., Chino N., Okano H., Okamoto H. Comparative functional genomics revealed conservation and diversification of three enhancers of the isl1 gene for motor and sensory neuron-specific expression. Dev. Biol. 2005, 278:587-606.
48. Vermeren M., Maro G.S., Bron R., McGonnell I.M., Charnay P., Topilko P., Cohen J. Integrity of developing spinal motor columns is regulated by neural crest derivatives at motor exit points. Neuron 2003, 37:403-415.
49. Wanner I.B., Guerra N.K., Mahoney J., Kumar A., Wood P.M., Mirsky R., Jessen K.R. Role of N-cadherin in Schwann cell precursors of growing nerves. Glia 2006, 54:439-459.
50. Weimer J.M., Yokota Y., Stanco A., Stumpo D.J., Blackshear P.J., Anton E.S. MARCKS modulates radial progenitor placement, proliferation and organization in the developing cerebral cortex. Development 2009, 136:2965-2975.
51. Weiss K.H., Johanssen C., Tielsch A., Herz J., Deller T., Frotscher M., Forster E. Malformation of the radial glial scaffold in the dentate gyrus of reeler mice, scrambler mice, and ApoER2/VLDLR-deficient mice. J. Comp. Neurol. 2003, 460:56-65.
52. Yip J.W., Yip Y.P., Nakajima K., Capriotti C. Reelin controls position of autonomic neurons in the spinal cord. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:8612-8616.
53. Yip Y.P., Zhou G., Capriotti C., Yip J.W. Location of preganglionic neurons is independent of birthdate but is correlated to reelin-producing cells in the spinal cord. J. Comp. Neurol. 2004, 475:564-574.