Neuropilin-1 biases dendrite polarization in the retina

Development (Cambridge)

Volumn 140, Issue 14, 2013, Pages 2933-2941

  Kita, Elizabeth M ^a   Bertolesi, Gabriel E ^a   Hehr, Carrie L ^a   Johnston, Jillian ^a   McFarlane, Sarah ^a  

^a UNIVERSITY OF CALGARY   (Canada)

Author keywords

Plexin; Retinal ganglion cell; Semaphorin; Xenopus

Indexed keywords

NEUROPILIN 1; PLEXIN; PLEXIN A1; SEMAPHORIN 3A; SEMAPHORIN 3F; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASSOCIATION; DENDRITE; ELECTROPORATION; EMBRYO; FEMALE; HUMAN; IN SITU HYBRIDIZATION; IN VIVO STUDY; MORPHOGENESIS; NERVE CELL DIFFERENTIATION; NEUROEPITHELIUM; NONHUMAN; ORIENTATION; PHENOTYPE; POLARIZATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETINA GANGLION CELL; XENOPUS LAEVIS;

PLEXIN; RETINAL GANGLION CELL; SEMAPHORIN; XENOPUS;

ANIMALS; CELL POLARITY; DENDRITES; FEMALE; NERVE TISSUE PROTEINS; NEUROPILIN-1; RETINA; RETINAL GANGLION CELLS; SEMAPHORIN-3A; XENOPUS LAEVIS; XENOPUS PROTEINS;

EID: 84879646149     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.088286     Document Type: Article

References (42)

1. Arimura, N. and Kaibuchi, K. (2007). Neuronal polarity: from extracellular signals to intracellular mechanisms. Nat. Rev. Neurosci. 8, 194-205.
2. Atkinson-Leadbeater, K., Bertolesi, G. E., Hehr, C. L., Webber, C. A., Cechmanek, P. B. and McFarlane, S. (2010). Dynamic expression of axon guidance cues required for optic tract development is controlled by fibroblast growth factor signaling. J. Neurosci. 30, 685-693.
3. Atwal, J. K., Singh, K. K., Tessier-Lavigne, M., Miller, F. D. and Kaplan, D. R. (2003). Semaphorin 3F antagonizes neurotrophin-induced phosphatidylinositol 3-kinase and mitogen-activated protein kinase kinase signaling: a mechanism for growth cone collapse. J. Neurosci. 23, 7602-7609.
4. Barnes, A. P. and Polleux, F. (2009). Establishment of axon-dendrite polarity in developing neurons. Annu. Rev. Neurosci. 32, 347-381.
5. Callander, D. C., Lamont, R. E., Childs, S. J. and McFarlane, S. (2007). Expression of multiple class three semaphorins in the retina and along the path of zebrafish retinal axons. Dev. Dyn. 236, 2918-2924.
6. Campbell, D. S., Regan, A. G., Lopez, J. S., Tannahill, D., Harris, W. A. and Holt, C. E. (2001). Semaphorin 3A elicits stage-dependent collapse, turning, and branching in Xenopus retinal growth cones. J. Neurosci. 21, 8538-8547.
7. Chen, H., Chédotal, A., He, Z., Goodman, C. S. and Tessier-Lavigne, M. (1997). Neuropilin-2, a novel member of the neuropilin family, is a high affinity receptor for the semaphorins Sema E and Sema IV but not Sema III. Neuron 19, 547-559.
8. Choi, J. H., Law, M. Y., Chien, C. B., Link, B. A. and Wong, R. O. (2010). In vivo development of dendritic orientation in wild-type and mislocalized retinal ganglion cells. Neural Dev. 5, 29.
9. de Winter, F., Cui, Q., Symons, N., Verhaagen, J. and Harvey, A. R. (2004). Expression of class-3 semaphorins and their receptors in the neonatal and adult rat retina. Invest. Ophthalmol. Vis. Sci. 45, 4554-4562.
10. Gonthier, B., Koncina, E., Satkauskas, S., Perraut, M., Roussel, G., Aunis, D., Kapfhammer, J. P. and Bagnard, D. (2009). A PKC-dependent recruitment of MMP-2 controls semaphorin-3A growth-promoting effect in cortical dendrites. PLoS ONE 4, e5099.
11. Hocking, J. C., Hehr, C. L., Bertolesi, G. E., Wu, J. Y. and McFarlane, S. (2010). Distinct roles for Robo2 in the regulation of axon and dendrite growth by retinal ganglion cells. Mech. Dev. 127, 36-48.
12. Hocking, J. C., Hehr, C. L., Chang, R. Y., Johnston, J. and McFarlane, S. (2008). TGFbeta ligands promote the initiation of retinal ganglion cell dendrites in vitro and in vivo. Mol. Cell. Neurosci. 37, 247-260.
13. Holt, C. E. (1989). A single-cell analysis of early retinal ganglion cell differentiation in Xenopus: from soma to axon tip. J. Neurosci. 9, 3123-3145.
14. Kim, S. and Chiba, A. (2004). Dendritic guidance. Trends Neurosci. 27, 194-202.
15. Koestner, U., Shnitsar, I., Linnemannstöns, K., Hufton, A. L. and Borchers, A. (2008). Semaphorin and neuropilin expression during early morphogenesis of Xenopus laevis. Dev. Dyn. 237, 3853-3863.
16. Koncina, E., Roth, L., Gonthier, B. and Bagnard, D. (2007). Role of semaphorins during axon growth and guidance. Adv. Exp. Med. Biol. 621, 50-64.
17. Liu, Y., Berndt, J., Su, F., Tawarayama, H., Shoji, W., Kuwada, J. Y. and Halloran, M. C. (2004). Semaphorin3D guides retinal axons along the dorsoventral axis of the tectum. J. Neurosci. 24, 310-318.
18. Matsuoka, R. L., Chivatakarn, O., Badea, T. C., Samuels, I. S., Cahill, H., Katayama, K., Kumar, S. R., Suto, F., Chédotal, A., Peachey, N. S. et al. (2011a). Class 5 transmembrane semaphorins control selective mammalian retinal lamination and function. Neuron 71, 460-473.
19. Matsuoka, R. L., Nguyen-Ba-Charvet, K. T., Parray, A., Badea, T. C., Chédotal, A. and Kolodkin, A. L. (2011b). Transmembrane semaphorin signalling controls laminar stratification in the mammalian retina. Nature 470, 259-263.
20. McFarlane, S. and Lom, B. (2012). The Xenopus retinal ganglion cell as a model neuron to study the establishment of neuronal connectivity. Dev. Neurobiol. 72, 520-536.
21. McFarlane, S., McNeill, L. and Holt, C. E. (1995). FGF signaling and target recognition in the developing Xenopus visual system. Neuron 15, 1017-1028.
22. Morita, A., Yamashita, N., Sasaki, Y., Uchida, Y., Nakajima, O., Nakamura, F., Yagi, T., Taniguchi, M., Usui, H., Katoh-Semba, R. et al. (2006). Regulation of dendritic branching and spine maturation by semaphorin3A-Fyn signaling. J. Neurosci. 26, 2971-2980.
23. Nakamura, F. and Goshima, Y. (2002). Structural and functional relation of neuropilins. Adv. Exp. Med. Biol. 515, 55-69.
24. Nieuwkoop, P. D. and Faber, J. (1994). Normal Table of Xenopus Laevis. New York, NY: Garland.
25. Nishiyama, M., Togashi, K., von Schimmelmann, M. J., Lim, C. S., Maeda, S., Yamashita, N., Goshima, Y., Ishii, S. and Hong, K. (2011). Semaphorin 3A induces CaV2.3 channel-dependent conversion of axons to dendrites. Nat. Cell Biol. 13, 676-685.
26. Ohta, K., Takagi, S., Asou, H. and Fujisawa, H. (1992). Involvement of neuronal cell surface molecule B2 in the formation of retinal plexiform layers. Neuron 9, 151-161.
27. Parker, M. W., Hellman, L. M., Xu, P., Fried, M. G. and Vander Kooi, C. W. (2010). Furin processing of semaphorin 3F determines its anti-angiogenic activity by regulating direct binding and competition for neuropilin. Biochemistry 49, 4068-4075.
28. Polleux, F., Morrow, T. and Ghosh, A. (2000). Semaphorin 3A is a chemoattractant for cortical apical dendrites. Nature 404, 567-573.
29. Randlett, O., Norden, C. and Harris, W. A. (2011). The vertebrate retina: a model for neuronal polarization in vivo. Dev. Neurobiol. 71, 567-583.
30. Renzi, M. J., Feiner, L., Koppel, A. M. and Raper, J. A. (1999). A dominant negative receptor for specific secreted semaphorins is generated by deleting an extracellular domain from neuropilin-1. J. Neurosci. 19, 7870-7880.
31. Schlomann, U., Schwamborn, J. C., Müller, M., Fässler, R. and Püschel, A. W. (2009). The stimulation of dendrite growth by Sema3A requires integrin engagement and focal adhesion kinase. J. Cell Sci. 122, 2034-2042.
32. Shelly, M., Cancedda, L., Lim, B. K., Popescu, A. T., Cheng, P. L., Gao, H. and Poo, M. M. (2011). Semaphorin3A regulates neuronal polarization by suppressing axon formation and promoting dendrite growth. Neuron 71, 433-446.
33. Sive, H. L., Grainger, R. M. and Harland, R. M. (2000). Early Development of Xenopus Laevis: A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
34. Sokal, R. R. and Rohlf, F. J. (2011). Biometry: The Principles and Practices of Statistics in Biological Research. New York, NY: Freeman.
35. Steinbach, K., Volkmer, H. and Schlosshauer, B. (2002). Semaphorin 3E/collapsin-5 inhibits growing retinal axons. Exp. Cell Res. 279, 52-61.
36. Tahirovic, S. and Bradke, F. (2009). Neuronal polarity. Cold Spring Harb. Perspect. Biol. 1, a001644.
37. Takagi, S., Hirata, T., Agata, K., Mochii, M., Eguchi, G. and Fujisawa, H. (1991). The A5 antigen, a candidate for the neuronal recognition molecule, has homologies to complement components and coagulation factors. Neuron 7, 295-307.
38. Takahashi, T., Fournier, A., Nakamura, F., Wang, L. H., Murakami, Y., Kalb, R. G., Fujisawa, H. and Strittmatter, S. M. (1999). Plexin-neuropilin-1 complexes form functional semaphorin-3A receptors. Cell 99, 59-69.
39. Takahashi, T. and Strittmatter, S. M. (2001). Plexina1 autoinhibition by the plexin sema domain. Neuron 29, 429-439.
40. Tamagnone, L., Artigiani, S., Chen, H., He, Z., Ming, G. I., Song, H., Chedotal, A., Winberg, M. L., Goodman, C. S., Poo, M. et al. (1999). Plexins are a large family of receptors for transmembrane, secreted, and GPI-anchored semaphorins in vertebrates. Cell 99, 71-80.
41. Togashi, K., von Schimmelman, M. J., Nishiyama, M., Lim, C. S., Yoshkida, N., Yun, B., Molday, R. S., Goshima, Y. and Hong, K. (2008). Cyclic GMP-gated CNG channels function in Sema3A-induced growth cone repulsion. Neuron 58, 694-707.
42. Zhou, Y., Gunput, R. A. and Pasterkamp, R. J. (2008). Semaphorin signaling: progress made and promises ahead. Trends Biochem. Sci. 33, 161-170.