Phosphorylation of Collapsin Response Mediator Protein 1 (CRMP1) at Tyrosine 504 residue regulates Semaphorin 3A-induced cortical dendritic growth.
CRMP1
Fyn
Sema3A
cortical neuron
dendritic growth
tyrosine phosphorylation
Journal
Journal of neurochemistry
ISSN: 1471-4159
Titre abrégé: J Neurochem
Pays: England
ID NLM: 2985190R
Informations de publication
Date de publication:
05 2021
05 2021
Historique:
revised:
11
12
2020
received:
07
07
2020
accepted:
08
01
2021
pubmed:
16
1
2021
medline:
22
6
2021
entrez:
15
1
2021
Statut:
ppublish
Résumé
Collapsin response mediator proteins (CRMPs) have been identified as mediating proteins of repulsive axon guidance cue Semaphorin-3A (Sema3A). Phosphorylation of CRMPs plays a crucial role in the Sema3A signaling cascade. It has been shown that Fyn phosphorylates CRMP1 at Tyrosine 504 residue (Tyr504); however, the physiological role of this phosphorylation has not been examined. We found that CRMP1 was the most strongly phosphorylated by Fyn among the five members of CRMPs. We confirmed Tyr504 phosphorylation of CRMP1 by Fyn. Immunocytochemistry of mouse dorsal root ganglion (DRG) neurons showed that phosphotyrosine signal in the growth cones was transiently increased in the growth cones upon Sema3A stimulation. Tyr504-phosphorylated CRMP1 also tended to increase after Sema3A simulation. Ectopic expression of a single amino acid mutant of CRMP1 replacing Tyr504 with phenylalanine (CRMP1-Tyr504Phe) suppressed Sema3A-induced growth cone collapse response in chick DRG neurons. CRMP1-Tyr504Phe expression in mouse hippocampal neurons also suppressed Sema3A but not Sema3F-induced growth cone collapse response. Immunohistochemistry showed that Tyr504-phosphorylated CRMP1 was present in the cell bodies and in the dendritic processes of mouse cortical neurons. CRMP1-Tyr504Phe suppressed Sema3A-induced dendritic growth of primary cultured mouse cortical neurons as well as the dendritic development of cortical pyramidal neurons in vivo. Fyn
Substances chimiques
Nerve Tissue Proteins
0
Phosphoproteins
0
Semaphorin-3A
0
collapsin response mediator protein-1
0
Tyrosine
42HK56048U
Proto-Oncogene Proteins c-fyn
EC 2.7.10.2
Banques de données
RefSeq
['RRID', ':I', 'MSR_JAX', 'MSR_TAC', ':M', 'GI', ': A', 'B_631528', 'B_477171', 'B_2565455', 'B_439694', 'B_309678', 'B_2556564', ':S', 'CR_002798']
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1207-1221Informations de copyright
© 2021 International Society for Neurochemistry.
Références
Buel, G. R., Rush, J., & Ballif, B. A. (2010). Fyn promotes phosphorylation of collapsin response mediator protein 1 at tyrosine 504, a novel, isoform-specific regulatory site. Journal of Cellular Biochemistry, 111, 20-28. https://doi.org/10.1002/jcb.22659
Charrier, E., Mosinger, B., Meissirel, C., Aguera, M., Rogemond, V., Reibel, S., Salin, P., Chounlamountri, N., Perrot, V., Belin, M. F., Goshima, Y., Honnorat, J., Thomasset, N., & Kolattukudy, P. (2006). Transient alterations in granule cell proliferation, apoptosis and migration in postnatal developing cerebellum of CRMP1-/- mice. Genes to Cells, 11, 1337-1352.10.1111/j.1365-2443.2006.01024.x
Chew L. A., Khanna R. (2018). CRMP2 and voltage-gated ion channels: potential roles in neuropathic pain. Neuronal Signaling, 2, (1), http://dx.doi.org/10.1042/ns20170220.
Cole, A. R., Causeret, F., Yadirgi, G., Hastie, C. J., McLauchlan, H., McManus, E. J., Hernández, F., Eickholt, B. J., Nikolic, M., & Sutherland, C. (2006). Distinct priming kinases contribute to differential regulation of collapsin response mediator proteins by glycogen synthase kinase-3 in vivo. Journal of Biological Chemistry, 281, 16591-16598.
Feng, G., Mellor, R. H., Bernstein, M., Keller-Peck, C., Nguyen, Q. T., Wallace, M., Nerbonne, J. M., Lichtman, J. W., & Sanes, J. R. (2000). Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron, 28, 41-51.
Fenstermaker, V., Chen, Y., Ghosh, A., & Yuste, R. (2004). Regulation of dendritic length and branching by semaphorin 3A. Journal of Neurobiology, 58, 403-412.
Ferreira, T. A., Blackman, A. V., Oyrer, J., Jayabal, S., Chung, A. J., Watt, A. J., Sjostrom, P. J., & van Meyel, D. J. (2014). Neuronal morphometry directly from bitmap images. Nature Methods, 11, 982-984.
Goshima, Y., Nakamura, F., Strittmatter, P., & Strittmatter, S. M. (1995). Collapsin-induced growth cone collapse mediated by an intracellular protein related to UNC-33. Nature, 376, 509-514.
Goshima, Y., Yamashita, N., Nakamura, F., & Sasaki, Y. (2016). Regulation of dendritic development by semaphorin 3A through novel intracellular remote signaling. Cell Adhesion and Migration, 10, 627-640.
Makihara, H., Nakai, S., Ohkubo, W., Yamashita, N., Nakamura, F., Kiyonari, H., Shioi, G., Jitsuki-Takahashi, A., Nakamura, H., Tanaka, F., Akase, T., Kolattukudy, P., & Goshima, Y. (2016). CRMP1 and CRMP2 have synergistic but distinct roles in dendritic development. Genes to Cells, 21, 994-1005.
Morinaka, A., Yamada, M., Itofusa, R., Funato, Y., Yoshimura, Y., Nakamura, F., Yoshimura, T., Kaibuchi, K., Goshima, Y., Hoshino, M., Kamiguchi, H., & Miki, H. (2011). Thioredoxin mediates oxidation-dependent phosphorylation of CRMP2 and growth cone collapse. Science Signalling, 4, ra26. https://doi.org/10.1126/scisignal.2001127
Morita, A., Yamashita, N., Sasaki, Y., Uchida, Y., Nakajima, O., Nakamura, F., Yagi, T., Taniguchi, M., Usui, H., Katoh-Semba, R., Takei, K., & Goshima, Y. (2006). Regulation of dendritic branching and spine maturation by semaphorin3A-Fyn signaling. Journal of Neuroscience, 26, 2971-2980. https://doi.org/10.1523/JNEUROSCI.5453-05.2006
Nakamura, F., Kalb, R. G., & Strittmatter, S. M. (2000). Molecular basis of semaphorin-mediated axon guidance. Journal of Neurobiology, 44, 219-229. https://doi.org/10.1002/1097-4695(200008)44:2<219:AID-NEU11>3.0.CO;2-W
Nakamura, F., Kumeta, K., Hida, T., Isono, T., Nakayama, Y., Kuramata-Matsuoka, E., Yamashita, N., Uchida, Y., Ogura, K.-I., Gengyo-Ando, K., Mitani, S., Ogino, T., & Goshima, Y. (2014). Amino- and carboxyl-terminal domains of Filamin-A interact with CRMP1 to mediate Sema3A signalling. Nature Communications, 5:5325, https://doi.org/10.1038/ncomms6325
Nakamura, F., Ohshima, T., & Goshima, Y. (2020). Collapsin response mediator proteins: Their biological functions and pathophysiology in neuronal development and regeneration. Frontiers in Cellular Neuroscience, 14, 188. https://doi.org/10.3389/fncel.2020.00188
Nakamura, F., Okada, T., Shishikura, M., Uetani, N., Taniguchi, M., Yagi, T., Iwakura, Y., Ohshima, T., Goshima, Y., & Strittmatter, S. M. (2017). Protein tyrosine phosphatase delta mediates the Sema3A-induced cortical basal dendritic Arborization through the activation of Fyn tyrosine kinase. Journal of Neuroscience, 37, 7125-7139.1523/JNEUROSCI.2519-7116.2017.
Nakamura, F., Tanaka, M., Takahashi, T., Kalb, R. G., & Strittmatter, S. M. (1998). Neuropilin-1 extracellular domains mediate semaphorin D/III-induced growth cone collapse. Neuron, 21, 1093-1100. https://doi.org/10.1016/S0896-6273(00)80626-1
Polleux, F., Morrow, T., & Ghosh, A. (2000). Semaphorin 3A is a chemoattractant for cortical apical dendrites. Nature, 404, 567-573. https://doi.org/10.1038/35007001
Pozas, E., Pascual, M., Nguyen Ba-Charvet, K. T., Guijarro, P., Sotelo, C., Chédotal, A., Del Río, J. A., & Soriano, E. (2001). Age-dependent effects of secreted Semaphorins 3A, 3F, and 3E on developing hippocampal axons: In vitro effects and phenotype of Semaphorin 3A (-/-) mice. Molecular and Cellular Neurosciences, 18, 26-43. https://doi.org/10.1006/mcne.2001.0999
Quach, T. T., Honnorat, J., Kolattukudy, P. E., Khanna, R., & Duchemin, A. M. (2015). CRMPs: Critical molecules for neurite morphogenesis and neuropsychiatric diseases. Molecular Psychiatry, 20, 1037-1045. https://doi.org/10.1038/mp.2015.77
Raper, J. A. (2000). Semaphorins and their receptors in vertebrates and invertebrates. Current Opinion in Neurobiology, 10, 88-94. https://doi.org/10.1016/S0959-4388(99)00057-4
Roskoski, R. Jr (2005). Src kinase regulation by phosphorylation and dephosphorylation. Biochemical and Biophysical Research Communications, 331, 1-14. https://doi.org/10.1016/j.bbrc.2005.03.012
Sasaki, Y., Cheng, C., Uchida, Y., Nakajima, O., Ohshima, T., Yagi, T., Taniguchi, M., Nakayama, T., Kishida, R., Kudo, Y., Ohno, S., Nakamura, F., & Goshima, Y. (2002). Fyn and Cdk5 mediate semaphorin-3A signaling, which is involved in regulation of dendrite orientation in cerebral cortex. Neuron, 35, 907-920. https://doi.org/10.1016/S0896-6273(02)00857-7
Schmidt, E. F., & Strittmatter, S. M. (2007). The CRMP family of proteins and their role in Sema3A signaling. Advances in Experimental Medicine and Biology, 600, 1-11.
Sholl, D. A. (1953). Dendritic organization in the neurons of the visual and motor cortices of the cat. Journal of Anatomy, 87, 387-406.
Shvartsman, D. E., Donaldson, J. C., Diaz, B., Gutman, O., Martin, G. S., & Henis, Y. I. (2007). Src kinase activity and SH2 domain regulate the dynamics of Src association with lipid and protein targets. Journal of Cell Biology, 178, 675-686. https://doi.org/10.1083/jcb.200701133
Sumi, T., Imasaki, T., Aoki, M., Sakai, N., Nitta, E., Shirouzu, M., & Nitta, R. (2018). Structural insights into the altering function of CRMP2 by phosphorylation. Cell Structure and Function, 43, 15-23. https://doi.org/10.1247/csf.17025
Takahashi, T., Fournier, A., Nakamura, F., Wang, L. H., Murakami, Y., Kalb, R. G., Fujisawa, H., & Strittmatter, S. M. (1999). Plexin-neuropilin-1 complexes form functional semaphorin-3A receptors. Cell, 99, 59-69. https://doi.org/10.1016/S0092-8674(00)80062-8
Takahashi, T., Nakamura, F., & Strittmatter, S. M. (1997). Neuronal and non-neuronal collapsin-1 binding sites in developing chick are distinct from other semaphorin binding sites. Journal of Neuroscience, 17, 9183-9193. https://doi.org/10.1523/JNEUROSCI.17-23-09183.1997
Uchida, Y., Ohshima, T., Sasaki, Y., Suzuki, H., Yanai, S., Yamashita, N., Nakamura, F., Takei, K., Ihara, Y., Mikoshiba, K., Kolattukudy, P., Honnorat, J., & Goshima, Y. (2005). 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 to Cells, 10, 165-179.
Uchida, Y., Ohshima, T., Yamashita, N., Ogawara, M., Sasaki, Y., Nakamura, F., & Goshima, Y. (2009). Semaphorin3A signaling mediated by Fyn-dependent tyrosine phosphorylation of collapsin response mediator protein 2 at tyrosine 32. Journal of Biological Chemistry, 284, 27393-27401. https://doi.org/10.1074/jbc.M109.000240.
Wang, L. H., & Strittmatter, S. M. (1997). Brain CRMP forms heterotetramers similar to liver dihydropyrimidinase. Journal of Neurochemistry, 69, 2261-2269. https://doi.org/10.1046/j.1471-4159.1997.69062261.x
Yamashita, N., Morita, A., Uchida, Y., Nakamura, F., Usui, H., Ohshima, T., Taniguchi, M., Honnorat, J., Thomasset, N., Takei, K., Takahashi, T., Kolattukudy, P., & Goshima, Y. (2007). Regulation of spine development by semaphorin3A through cyclin-dependent kinase 5 phosphorylation of collapsin response mediator protein 1. Journal of Neuroscience, 27, 12546-12554. https://doi.org/10.1523/JNEUROSCI.3463-07.2007.
Yamashita, N., Uchida, Y., Ohshima, T., Hirai, S.-I., Nakamura, F., Taniguchi, M., Mikoshiba, K., Honnorat, J., Kolattukudy, P., Thomasset, N., Takei, K., Takahashi, T., & Goshima, Y. (2006). Collapsin response mediator protein 1 mediates reelin signaling in cortical neuronal migration. Journal of Neuroscience, 26, 13357-13362. https://doi.org/10.1523/JNEUROSCI.4276-06.2006
Yoshimura, T., Kawano, Y., Arimura, N., Kawabata, S., Kikuchi, A., & Kaibuchi, K. (2005). GSK-3beta regulates phosphorylation of CRMP-2 and neuronal polarity. Cell, 120, 137-149.1016/j.cell.2004.1011.1012