Coupling of NF-protocadherin signaling to axon guidance by cue-induced translation

Nature Neuroscience

Volumn 16, Issue 2, 2013, Pages 166-173

  Leung, Louis C ^a,b   Urbančič, Vasja ^a   Baudet, Marie Laure ^a,c   Dwivedy, Asha ^a   Bayley, Timothy G ^a   Lee, Aih Cheun ^a   Harris, William A ^a   Holt, Christine E ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b STANFORD UNIVERSITY   (United States)

^c UNIVERSITY OF TRENTO   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CADHERIN; CELL PROTEIN; NEUROPILIN 1; NF PROTOCADHERIN; PROTEIN TAF1; SEMAPHORIN 3A; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; EMBRYO; IN VITRO STUDY; IN VIVO STUDY; NERVE FIBER GROWTH; NEUROEPITHELIUM; NONHUMAN; OPTIC TRACT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; RETINA GANGLION CELL;

ANALYSIS OF VARIANCE; ANIMALS; ANISOMYCIN; AXONS; CADHERINS; CERCOPITHECUS AETHIOPS; COS CELLS; CUES; ELECTROPORATION; EMBRYO, NONMAMMALIAN; GREEN FLUORESCENT PROTEINS; MICROSCOPY, CONFOCAL; NEUROEPITHELIAL CELLS; ORGAN CULTURE TECHNIQUES; PROTEIN BIOSYNTHESIS; PROTEIN SYNTHESIS INHIBITORS; RETINA; RETINAL GANGLION CELLS; SEMAPHORIN-3A; SIGNAL TRANSDUCTION; TIME FACTORS; TRANSCRIPTION FACTORS; TRANSFECTION; VISUAL PATHWAYS; XENOPUS LAEVIS; XENOPUS PROTEINS;

EID: 84873084738     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.3290     Document Type: Article

References (50)

1. Chien, C.B., Rosenthal, D.E., Harris, W.A. & Holt, C.E. Navigational errors made by growth cones without flopodia in the embryonic Xenopus brain. Neuron 11, 237-251 (1993). (Pubitemid 23250343)
2. Harris, W.A. Local positional cues in the neuroepithelium guide retinal axons in embryonic Xenopus brain. Nature 339, 218-221 (1989). (Pubitemid 19126392)
3. Atkinson-Leadbeater, K. et al. Dynamic expression of axon guidance cues required for optic tract development is controlled by fbroblast growth factor signaling. J. Neurosci. 30, 685-693 (2010).
4. Campbell, D.S. et al. Semaphorin 3A elicits stage-dependent collapse, turning, and branching in Xenopus retinal growth cones. J. Neurosci. 21, 8538-8547 (2001). (Pubitemid 33051452)
5. Piper, M. et al. Signaling mechanisms underlying Slit2-induced collapse of Xenopus retinal growth cones. Neuron 49, 215-228 (2006). (Pubitemid 43089639)
6. Arikkath, J. & Reichardt, L.F. Cadherins and catenins at synapses: roles in synaptogenesis and synaptic plasticity. Trends Neurosci. 31, 487-494 (2008).
7. Hirano, S., Suzuki, S. & Redies, C. The cadherin superfamily in neural development: diversity, function and interaction with other molecules. Front. Biosci. 8, d306-d355 (2003).
8. Takeichi, M. The cadherin superfamily in neuronal connections and interactions. Nat. Rev. Neurosci. 8, 11-20 (2007). (Pubitemid 46011995)
9. Bradley, R.S., Espeseth, A. & Kintner, C. NF-protocadherin, a novel member of the cadherin superfamily, is required for Xenopus ectodermal differentiation. Curr. Biol. 8, 325-334 (1998). (Pubitemid 28159118)
10. Heggem, M.A. & Bradley, R.S. The cytoplasmic domain of Xenopus NF-protocadherin interacts with TAF1/set. Dev. Cell 4, 419-429 (2003). (Pubitemid 36342366)
11. Rashid, D., Newell, K., Shama, L. & Bradley, R. A requirement for NF-protocadherin and TAF1/Set in cell adhesion and neural tube formation. Dev. Biol. 291, 170-181 (2006). (Pubitemid 43343935)
12. Piper, M., Dwivedy, A., Leung, L., Bradley, R.S. & Holt, C.E. NF-protocadherin and TAF1 regulate retinal axon initiation and elongation in vivo. J. Neurosci. 28, 100-105 (2008).
13. Campbell, D.S. & Holt, C.E. Chemotropic responses of retinal growth cones mediated by rapid local protein synthesis and degradation. Neuron 32, 1013-1026 (2001). (Pubitemid 34075393)
14. Leung, K.-M. et al. Asymmetrical β-actin mRNA translation in growth cones mediates attractive turning to netrin-1. Nat. Neurosci. 9, 1247-1256 (2006). (Pubitemid 44454266)
15. Lin, A.C. & Holt, C.E. Local translation and directional steering in axons. EMBO J. 26, 3729-3736 (2007). (Pubitemid 47295875)
16. Wu, K.Y. et al. Local translation of RhoA regulates growth cone collapse. Nature 436, 1020-1024 (2005). (Pubitemid 41191685)
17. 2+-dependent growth cone guidance. Nat. Neurosci. 9, 1265-1273 (2006). (Pubitemid 44454268)
18. Falk, J. et al. Electroporation of cDNA/morpholinos to targeted areas of embryonic CNS in Xenopus. BMC Dev. Biol. 7, 107 (2007).
19. Holt, C.E. A single-cell analysis of early retinal ganglion cell differentiation in Xenopus: from soma to axon tip. J. Neurosci. 9, 3123-3145 (1989). (Pubitemid 19260829)
20. Piper, M., Salih, S., Weinl, C., Holt, C.E. & Harris, W.A. Endocytosis-dependent desensitization and protein synthesis-dependent resensitization in retinal growth cone adaptation. Nat. Neurosci. 8, 179-186 (2005). (Pubitemid 40194048)
21. Lin, A.C. et al. Cytoplasmic polyadenylation and cytoplasmic polyadenylation element-dependent mRNA regulation are involved in Xenopus retinal axon development. Neural Dev. 4, 8 (2009).
22. Leung, K.-M. & Holt, C.E. Live visualization of protein synthesis in axonal growth cones by microinjection of photoconvertible Kaede into Xenopus embryos. Nat. Protoc. 3, 1318-1327 (2008).
23. Uemura, M., Nakao, S., Suzuki, S.T., Takeichi, M. & Hirano, S. OL-protocadherin is essential for growth of striatal axons and thalamocortical projections. Nat. Neurosci. 10, 1151-1159 (2007). (Pubitemid 47342422)
24. Garrett, A.M., Schreiner, D., Lobas, M.A. & Weiner, J.A. γ-Protocadherins control cortical dendrite arborization by regulating the activity of a FAK/PKC/MARCKS signaling pathway. Neuron 74, 269-276 (2012).
25. Lefebvre, J.L., Kostadinov, D., Chen, W.V., Maniatis, T. & Sanes, J.R. Protocadherins mediate dendritic self-avoidance in the mammalian nervous system. Nature 488, 517-521 (2012).
26. Yasuda, S. et al. Activity-induced protocadherin arcadlin regulates dendritic spine number by triggering N-cadherin endocytosis via TAO2β and p38 MAP kinases. Neuron 56, 456-471 (2007). (Pubitemid 350026265)
27. Garrett, A.M. & Weiner, J.A. Control of CNS synapse development by γ-protocadherin-mediated astrocyte-neuron contact. J. Neurosci. 29, 11723-11731 (2009).
28. Williams, E.O. et al. Delta protocadherin 10 is regulated by activity in the mouse main olfactory system. Front. Neural Circuits 5, 9 (2011).
29. Lefebvre, J.L., Zhang, Y., Meister, M., Wang, X. & Sanes, J.R. γ-Protocadherins regulate neuronal survival but are dispensable for circuit formation in retina. Development 135, 4141-4151 (2008).
30. Castellani, V., De Angelis, E., Kenwrick, S. & Rougon, G. Cis and trans interactions of L1 with neuropilin-1 control axonal responses to semaphorin 3A. EMBO J. 21, 6348-6357 (2002). (Pubitemid 35448413)
31. Castellani, V., Falk, J. & Rougon, G. Semaphorin3A-induced receptor endocytosis during axon guidance responses is mediated by L1 CAM. Mol. Cell. Neurosci. 26, 89-100 (2004). (Pubitemid 38581025)
32. Bechara, A. et al. FAK-MAPK-dependent adhesion disassembly downstream of L1 contributes to semaphorin3A-induced collapse. EMBO J. 27, 1549-1562 (2008). (Pubitemid 351794032)
33. Falk, J. et al. Dual functional activity of semaphorin 3B is required for positioning the anterior commissure. Neuron 48, 63-75 (2005).
34. Wolman, M.A., Regnery, A.M., Becker, T., Becker, C.G. & Halloran, M.C. Semaphorin3D regulates axon-axon interactions by modulating levels of L1 cell adhesion molecule. J. Neurosci. 27, 9653-9663 (2007). (Pubitemid 47492177)
35. Nawabi, H. et al. A midline switch of receptor processing regulates commissural axon guidance in vertebrates. Genes Dev. 24, 396-410 (2010).
36. Kuwajima, T. et al. Optic chiasm presentation of Semaphorin6D in the context of Plexin-A1 and Nr-CAM promotes retinal axon midline crossing. Neuron 74, 676-690 (2012).
37. Lemmon, V., Burden, S.M., Payne, H.R., Elmslie, G.J. & Hlavin, M.L. Neurite growth on different substrates: permissive versus instructive infuences and the role of adhesive strength. J. Neurosci. 12, 818-826 (1992).
38. Goodman, C.S. Mechanisms and molecules that control growth cone guidance. Annu. Rev. Neurosci. 19, 341-377 (1996). (Pubitemid 26084344)
39. Barnes, S.H., Price, S.R., Wentzel, C. & Guthrie, S.C. Cadherin-7 and cadherin-6B differentially regulate the growth, branching and guidance of cranial motor axons. Development 137, 805-814 (2010).
40. Shima, Y. et al. Opposing roles in neurite growth control by two seven-pass transmembrane cadherins. Nat. Neurosci. 10, 963-969 (2007). (Pubitemid 47185201)
41. Nakao, S., Platek, A., Hirano, S. & Takeichi, M. Contact-dependent promotion of cell migration by the OL-protocadherin-Nap1 interaction. J. Cell Biol. 182, 395-410 (2008).
42. Brittis, P.A., Lu, Q. & Flanagan, J.G. Axonal protein synthesis provides a mechanism for localized regulation at an intermediate target. Cell 110, 223-235 (2002). (Pubitemid 34876550)
43. Kuwako, K. et al. Neural RNA-binding protein Musashi1 controls midline crossing of precerebellar neurons through posttranscriptional regulation of Robo3/Rig-1 expression. Neuron 67, 407-421 (2010).
44. Zivraj, K.H. et al. Subcellular profling reveals distinct and developmentally regulated repertoire of growth cone mRNAs. J. Neurosci. 30, 15464-15478 (2010).
45. Seo, S.B. et al. Regulation of histone acetylation and transcription by INHAT, a human cellular complex containing the Set oncoprotein. Cell 104, 119-130 (2001).
46. Nieuwkoop, F.J. & Faber, J. Normal Table of Xenopus laevis (Daudin) (North-Holland, 1967).
47. Scotto-Lavino, E., Du, G. & Frohman, M.A. 3′ end cDNA amplifcation using classic RACE. Nat. Protoc. 1, 2742-2745 (2006).
48. Leung, L. & Holt, C.E. Imaging axon pathfnding in Xenopus in vivo. Cold Spring Harb. Protoc. 2012, 984-991 (2012).
49. Wizenmann, A. et al. Extracellular engrailed participates in the topographic guidance of retinal axons in vivo. Neuron 64, 355-366 (2009).
50. Luo, Y., Raible, D. & Raper, J.A. Collapsin: a protein in brain that induces the collapse and paralysis of neuronal growth cones. Cell 75, 217-227 (1993). (Pubitemid 23320286)