Cerebrospinal fluid-derived Semaphorin3B orients neuroepithelial cell divisions in the apicobasal axis

Nature Communications

Volumn 6, Issue , 2015, Pages

  Arbeille, Elise ^a   Reynaud, Florie ^a   Sanyas, Isabelle ^a   Bozon, Muriel ^a   Kindbeiter, Karine ^a   Causeret, Frédéric ^b   Pierani, Alessandra ^b   Falk, Julien ^a   Moret, Frédéric ^a   Castellani, Valérie ^a  

^a CENTRE DE GÉNÉTIQUE MOLÉCULAIRE ET CELLULAIRE   (France)

^b INSTITUT JACQUES MONOD   (France)

Author keywords

[No Author keywords available]

Indexed keywords

2 (2,4 DICHLOROPHENYL) 3 (1 METHYL 3 INDOLYL)MALEIMIDE; 2 (3 CHLORO 4 HYDROXYANILINO) 3 (2 NITROPHENYL)MALEIMIDE; BROXURIDINE; COLLAPSIN RESPONSE MEDIATOR PROTEIN 2; DIMETHYL SULFOXIDE; F ACTIN; NEUROPILIN 1; NEUROPILIN 2; PROTEIN ZO1; SEMAPHORIN; SEMAPHORIN3B; UNCLASSIFIED DRUG; COLLAPSIN RESPONSE MEDIATOR PROTEIN-2; NERVE PROTEIN; NEUROPILIN; SIGNAL PEPTIDE;

BODY FLUID; EMBRYO; GERM CELL; HOMEOSTASIS; ORIENTATION; SIGNALING; SPATIAL ANALYSIS;

ANIMAL CELL; ANIMAL EXPERIMENT; APICOBASAL AXIS; ARTICLE; CELL DIVISION; CELL JUNCTION; CEREBROSPINAL FLUID; CHOROID PLEXUS; CONTROLLED STUDY; EMBRYO; FEMALE; GENETIC TRANSFECTION; HELA CELL LINE; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; IN VIVO STUDY; MICROTUBULE; MITOSIS; MITOSIS SPINDLE; MOTONEURON; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NEURAL TUBE; NEUROEPITHELIUM CELL; NONHUMAN; PROTEIN DEPLETION; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; SPATIAL ORIENTATION; SPINAL CORD; STEREOTYPY; WESTERN BLOTTING; ANIMAL; CELL POLARITY; CYTOLOGY; EMBRYOLOGY; FLUORESCENT ANTIBODY TECHNIQUE; KNOCKOUT MOUSE; METABOLISM; NONPARAMETRIC TEST; PHYSIOLOGY;

ANIMALS; BLOTTING, WESTERN; CELL DIVISION; CELL POLARITY; FLUORESCENT ANTIBODY TECHNIQUE; HELA CELLS; HUMANS; IN SITU HYBRIDIZATION; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; MICE, KNOCKOUT; NERVE TISSUE PROTEINS; NEUROEPITHELIAL CELLS; NEUROPILINS; SEMAPHORINS; SPINAL CORD; STATISTICS, NONPARAMETRIC;

EID: 84924085092     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms7366     Document Type: Article

References (63)

1. Morin, X. & Bellaiche, Y. Mitotic spindle orientation in asymmetric and symmetric cell divisions during animal development. Dev. Cell 21, 102 (2011).
2. Gillies, T. E. & Cabernard, C. Cell division orientation in animals. Curr. Biol. 21, R599 (2011).
3. Lu, M. S. & Johnston, C. A. Molecular pathways regulating mitotic spindle orientation in animal cells. Development 140, 1843 (2013).
4. Lancaster, M. A. & Knoblich, J. A. Spindle orientation in mammalian cerebral cortical development. Curr. Opin. Neurobiol. 22, 737 (2012).
5. Cayouette, M., Whitmore, A. V., Jeffery, G. & Raff, M. Asymmetric segregation of Numb in retinal development and the influence of the pigmented epithelium. J. Neurosci. 21, 5643 (2001).
6. Siegrist, S. E. & Doe, C. Q. Extrinsic cues orient the cell division axis in Drosophila embryonic neuroblasts. Development 133, 529 (2006).
7. Werts, A. D. & Goldstein, B. How signaling between cells can orient a mitotic spindle. Semin. Cell Dev. Biol. 22, 842 (2011).
8. Kiecker, C. & Lumsden, A. The role of organizers in patterning the nervous system. Annu. Rev. Neurosci. 35, 347 (2012).
9. Sauer, M. E. & Chittenden, A. C. Deoxyribonucleic acid content of cell nuclei in the neural tube of the chick embryo: evidence for intermitotic migration of nuclei. Exp. Cell Res. 16, 1 (1959).
10. Gotz, M. & Huttner, W. B. The cell biology of neurogenesis. Nat. Rev. Mol. Cell Biol. 6, 777 (2005).
11. Shitamukai, A. & Matsuzaki, F. Control of asymmetric cell division of mammalian neural progenitors. Dev. Growth Differ. 54, 277 (2012).
12. Wilcock, A. C., Swedlow, J. R. & Storey, K. G. Mitotic spindle orientation distinguishes stem cell and terminal modes of neuron production in the early spinal cord. Development 134, 1943 (2007).
13. Nawabi, H. et al. A midline switch of receptor processing regulates commissural axon guidance in vertebrates. Genes Dev. 24, 396 (2010).
14. Falk, J. et al. Dual functional activity of semaphorin 3B is required for positioning the anterior commissure. Neuron 48, 63 (2005).
15. Hebert, A. M. et al. Merlin/ERM proteins establish cortical asymmetry and centrosome position. Genes Dev. 26, 2709 (2012).
16. Noatynska, A., Gotta, M. & Meraldi, P. Mitotic spindle (DIS)orientation and DISease: cause or consequence? J. Cell Biol. 199, 1025 (2012).
17. Charoy, C. et al. gdnf activates midline repulsion by Semaphorin3B via NCAM during commissural axon guidance. Neuron 75, 1051 (2012).
18. Zou, Y., Stoeckli, E., Chen, H. & Tessier-Lavigne, M. Squeezing axons out of the gray matter: a role for slit and semaphorin proteins from midline and ventral spinal cord. Cell 102, 363 (2000).
19. Chamberlain, C. E. et al. Notochord-derived Shh concentrates in close association with the apically positioned basal body in neural target cells and forms a dynamic gradient during neural patterning. Development 135, 1097 (2008).
20. Causeret, F. et al. Dbx1-expressing cells are necessary for the survival of the mammalian anterior neural and craniofacial structures. PLoS ONE 6, e19367 (2011).
21. Jessell, T. M. Neuronal specification in the spinal cord: inductive signals and transcriptional codes. Nat. Rev. Genet. 1, 20 (2000).
22. Iacopetti, P. et al. Expression of the antiproliferative gene TIS21 at the onset of neurogenesis identifies single neuroepithelial cells that switch from proliferative to neuron-generating division. Proc. Natl Acad. Sci. USA 96, 4639 (1999).
23. Kosodo, Y. et al. Asymmetric distribution of the apical plasma membrane during neurogenic divisions of mammalian neuroepithelial cells. EMBO J. 23, 2314 (2004).
24. Konno, D. et al. Neuroepithelial progenitors undergo LGN-dependent planar divisions to maintain self-renewability during mammalian neurogenesis. Nat. Cell Biol. 10, 93 (2008).
25. Das, R. M. & Storey, K. G. Mitotic spindle orientation can direct cell fate and bias Notch activity in chick neural tube. EMBO Rep. 13, 1030 (2012).
26. Takahashi, T. et al. Semaphorins A and E act as antagonists of neuropilin-1 and agonists of neuropilin-2 receptors. Nat. Neurosci. 1, 487 (1998).
27. Giger, R. J. et al. Neuropilin-2 is required in vivo for selective axon guidance responses to secreted semaphorins. Neuron 25, 29 (2000).
28. Gu, C. et al. Neuropilin-1 conveys semaphorin and VEGF signaling during neural and cardiovascular development. Dev. Cell 5, 45 (2003).
29. Kolodkin, A. L. & Tessier-Lavigne, M. Mechanisms and molecules of neuronal wiring: a primer. Cold Spring Harb. Perspect. Biol. 3, pii: a001727 (2011).
30. Morin, X., Jaouen, F. & Durbec, P. Control of planar divisions by the G-protein regulator LGN maintains progenitors in the chick neuroepithelium. Nat. Neurosci. 10, 1440 (2007).
31. Aizawa, H. et al. Phosphorylation of cofilin by LIM-kinase is necessary for semaphorin 3A-induced growth cone collapse. Nat. Neurosci. 4, 367 (2001).
32. Kaji, N., Muramoto, A. & Mizuno, K. LIM kinase-mediated cofilin phosphorylation during mitosis is required for precise spindle positioning. J. Biol. Chem. 283, 4983 (2008).
33. Eickholt, B. J., Walsh, F. S. & Doherty, P. An inactive pool of GSK-3 at the leading edge of growth cones is implicated in Semaphorin 3A signaling. J. Cell Biol. 157, 211 (2002).
34. Uchida, Y. et al. Semaphorin3A signalling is mediated via sequential Cdk5 and GSK3beta phosphorylation of CRMP2: implication of common phosphorylating mechanism underlying axon guidance and Alzheimer's disease. Genes Cells 10, 165 (2005).
35. Fukata, Y. et al. CRMP-2 binds to tubulin heterodimers to promote microtubule assembly. Nat. Cell Biol. 4, 583 (2002).
36. Buttrick, G. J. et al. Akt regulates centrosome migration and spindle orientation in the early Drosophila melanogaster embryo. J. Cell Biol. 180, 537 (2008).
37. Lin, P. C., Chan, P. M., Hall, C. & Manser, E. Collapsin response mediator proteins (CRMPs) are a new class of microtubule-associated protein (MAP) that selectively interacts with assembled microtubules via a taxol-sensitive binding interaction. J. Biol. Chem. 286, 41466 (2011).
38. Arimura, N. et al. CRMP-2 directly binds to cytoplasmic dynein and interferes with its activity. J. Neurochem. 111, 380 (2009).
39. Jauffred, B. et al. Regulation of centrosome movements by numb and the collapsin response mediator protein during Drosophila sensory progenitor asymmetric division. Development 140, 2657 (2013).
40. Wakefield, J. G., Stephens, D. J. & Tavare, J. M. A role for glycogen synthase kinase-3 in mitotic spindle dynamics and chromosome alignment. J. Cell Sci. 116(Pt 4): 637 (2003).
41. Yang, N. et al. Cofilin phosphorylation by LIM-kinase 1 and its role in Racmediated actin reorganization. Nature 393, 809 (1998).
42. Yoshimura, T. et al. GSK-3beta regulates phosphorylation of CRMP-2 and neuronal polarity. Cell 120, 137 (2005).
43. Hammond, J. W., Cai, D. & Verhey, K. J. Tubulin modifications and their cellular functions. Curr. Opin. Cell Biol. 20, 71 (2008).
44. Habib, S. J. et al. A localized Wnt signal orients asymmetric stem cell division in vitro. Science 339, 1445 (2013).
45. Beck, B. et al. A vascular niche and a VEGF-Nrp1 loop regulate the initiation and stemness of skin tumours. Nature 478, 399 (2011).
46. Haydar, T. F., Ang, Jr E. & Rakic, P. Mitotic spindle rotation and mode of cell division in the developing telencephalon. Proc. Natl Acad. Sci. USA 100, 2890 (2003).
47. Charron, F. et al. The morphogen sonic hedgehog is an axonal chemoattractant that collaborates with netrin-1 in midline axon guidance. Cell 113, 11 (2003).
48. Borrell, V. et al. Slit/Robo signaling modulates the proliferation of central nervous system progenitors. Neuron 76, 338 (2012).
49. Wang, X. et al. Asymmetric centrosome inheritance maintains neural progenitors in the neocortex. Nature 461, 947 (2009).
50. Delaunay, D. et al. Mitotic spindle asymmetry: a Wnt/PCP-regulated mechanism generating asymmetrical division in cortical precursors. Cell Rep. 6, 400 (2014).
51. Peyre, E. & Morin, X. An oblique view on the role of spindle orientation in vertebrate neurogenesis. Dev. Growth Differ. 54, 287 (2012).
52. Tripodi, M., Stepien, A. E. & Arber, S. Motor antagonism exposed by spatial segregation and timing of neurogenesis. Nature 479, 61 (2011).
53. Lehtinen, M. K. & Walsh, C. A. Neurogenesis at the brain-cerebrospinal fluid interface. Annu. Rev. Cell Dev. Biol. 27, 653 (2011).
54. Moret, F. et al. Distribution of tyrosine hydroxylase, dopamine, and serotonin in the central nervous system of amphioxus (Branchiostoma lanceolatum): implications for the evolution of catecholamine systems in vertebrates. J. Comp. Neurol. 468, 135 (2004).
55. Goto, H. et al. Identification of a novel phosphorylation site on histone H3 coupled with mitotic chromosome condensation. J. Biol. Chem. 274, 25543 (1999).
56. Roszko, I., Afonso, C., Henrique, D. & Mathis, L. Key role played by RhoA in the balance between planar and apico-basal cell divisions in the chick neuroepithelium. Dev. Biol. 298, 212 (2006).
57. Kilmartin, J. V., Wright, B. & Milstein, C. Rat monoclonal antitubulin antibodies derived by using a new nonsecreting rat cell line. J. Cell Biol. 93, 576 (1982).
58. Pacary, E., Azzarelli, R. & Guillemot, F. Rnd3 coordinates early steps of cortical neurogenesis through actin-dependent and -independent mechanisms. Nat. Commun. 4, 1635 (2013).
59. Lobjois, V., Bel-Vialar, S., Trousse, F. & Pituello, F. Forcing neural progenitor cells to cycle is insufficient to alter cell-fate decision and timing of neuronal differentiation in the spinal cord. Neural. Dev. 3, 4 (2008).
60. Gogel, S. et al. Post-translational regulation of Crmp in developing and regenerating chick spinal cord. Dev. Neurobiol. 70, 456 (2010).
61. Sato, Y. et al. Hypoxia-ischemia induces hypo-phosphorylation of collapsin response mediator protein 2 in a neonatal rat model of periventricular leukomalacia. Brain Res. 1386, 165 (2011).
62. Peyre, E. et al. A lateral belt of cortical LGN and NuMA guides mitotic spindle movements and planar division in neuroepithelial cells. J. Cell Biol. 193, 141 (2011).
63. Goeckeler, Z. M. &Wysolmerski, R. B. Myosin phosphatase and cofilin mediate cAMP/cAMP-dependent protein kinase-induced decline in endothelial cell isometric tension and myosin II regulatory light chain phosphorylation. J. Biol. Chem. 280, 33083 (2005).