Reelin activates the small GTPase TC10 and VAMP7 to promote neurite outgrowth and regeneration of dorsal root ganglia (DRG) neurons.
Animals
Cell Adhesion Molecules, Neuronal
/ metabolism
Extracellular Matrix Proteins
/ metabolism
Ganglia, Spinal
/ metabolism
Mice
Nerve Regeneration
/ physiology
Nerve Tissue Proteins
/ metabolism
Neuronal Outgrowth
/ physiology
Neurons
/ metabolism
R-SNARE Proteins
/ metabolism
Rats, Sprague-Dawley
Reelin Protein
Serine Endopeptidases
/ metabolism
rho GTP-Binding Proteins
/ metabolism
ApoER2
RRID:AB_1079279
RRID:AB_1844090
RRID:AB_2223041
RRID:AB_2315049
RRID:AB_329827
RRID:AB_91371
RRID:SCR_003070
RRID:SCR_014213
Reelin
Rho GTPases
TC10
VAMP7
axonal outgrowth
regeneration
signaling pathway
Journal
Journal of neuroscience research
ISSN: 1097-4547
Titre abrégé: J Neurosci Res
Pays: United States
ID NLM: 7600111
Informations de publication
Date de publication:
01 2021
01 2021
Historique:
received:
19
11
2019
revised:
27
05
2020
accepted:
11
06
2020
pubmed:
12
7
2020
medline:
3
11
2021
entrez:
12
7
2020
Statut:
ppublish
Résumé
Axonal outgrowth is a fundamental process during the development of central (CNS) and peripheral (PNS) nervous system as well as in nerve regeneration and requires accurate axonal navigation and extension to the correct target. These events need proper coordination between membrane trafficking and cytoskeletal rearrangements and are under the control of the small GTPases of the Rho family, among other molecules. Reelin, a relevant protein for CNS development and synaptic function in the adult, is also present in the PNS. Upon sciatic nerve damage, Reelin expression increases and, on the other hand, mice deficient in Reelin exhibit an impaired nerve regeneration. However, the mechanism(s) involved the Reelin-dependent axonal growth is still poorly understood. In this work, we present evidence showing that Reelin stimulates dorsal root ganglia (DRG) regeneration after axotomy. Moreover, dissociated DRG neurons express the Reelin receptor Apolipoprotein E-receptor 2 and also require the presence of TC10 to develop their axons. TC10 is a Rho GTPase that promotes neurite outgrowth through the exocytic fusion of vesicles at the growth cone. Here, we demonstrate for the first time that Reelin controls TC10 activation in DRG neurons. Besides, we confirmed that the known CNS Reelin target Cdc42 is also activated in DRG and controls TC10 activity. Finally, in the process of membrane addition, we found that Reelin stimulates the fusion of membrane carriers containing the v-SNARE protein VAMP7 in vesicles that contain TC10. Altogether, our work shows a new role of Reelin in PNS, opening the option of therapeutic interventions to improve the regeneration process.
Substances chimiques
Cell Adhesion Molecules, Neuronal
0
Extracellular Matrix Proteins
0
Nerve Tissue Proteins
0
R-SNARE Proteins
0
Reelin Protein
0
Reln protein, rat
0
Sybl1 protein, mouse
0
Reln protein, mouse
EC 3.4.21.-
Serine Endopeptidases
EC 3.4.21.-
Rhoq protein, mouse
EC 3.6.1.-
rho GTP-Binding Proteins
EC 3.6.5.2
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
392-406Informations de copyright
© 2020 Wiley Periodicals LLC.
Références
Abe, T., Kato, M., Miki, H., Takenawa, T., & Endo, T. (2003). Small GTPase Tc10 and its homologue RhoT induce N-WASP-mediated long process formation and neurite outgrowth. Journal of Cell Science, 116(Pt 1), 155-168. https://doi.org/10.1242/jcs.00208
Arimura, N., & Kaibuchi, K. (2007). Neuronal polarity: From extracellular signals to intracellular mechanisms. Nature Reviews Neuroscience, 8(3), 194-205. https://doi.org/10.1038/nrn2056
Baird, D., Feng, Q. Y., & Cerione, R. A. (2005). The cool-2/alpha-Pix protein mediates a Cdc42-Rac signaling cascade. Current Biology, 15(1), 1-10. https://doi.org/10.1016/j.cub.2004.12.040
Bal, M., Leitz, J., Reese, A. L., Ramirez, D. M. O., Durakoglugil, M., Herz, J., … Kavalali, E. T. (2013). Reelin mobilizes a VAMP7-dependent synaptic vesicle pool and selectively augments spontaneous neurotransmission. Neuron, 80(4), 934-946. https://doi.org/10.1016/j.neuron.2013.08.024
Ballif, B. A., Arnaud, L., Arthur, W. T., Guris, D., Imamoto, A., & Cooper, J. A. (2004). Activation of a Dab1/CrkL/C3G/Rap1 pathway in reelin-stimulated neurons. Current Biology, 14(7), 606-610. https://doi.org/10.1016/j.cub.2004.03.038
Ballif, B. A., Arnaud, L., & Cooper, J. A. (2003). Tyrosine phosphorylation of Disabled-1 is essential for Reelin-stimulated activation of Akt and Src family kinases. Molecular Brain Research, 117(2), 152-159. https://doi.org/10.1016/S0169-328X(03)00295-X
Bisbal, M., Conde, C., Donoso, M., Bollati, F., Sesma, J., Quiroga, S., … Caceres, A. (2008). Protein kinase d regulates trafficking of dendritic membrane proteins in developing neurons. Journal of Neuroscience, 28(37), 9297-9308. https://doi.org/10.1523/JNEUROSCI.1879-08.2008
Bradke F., Fawcett J. W., & Spira M. E. (2012). Assembly of a new growth cone after axotomy: the precursor to axon regeneration. Nature Reviews Neuroscience, 13(3), 183-193. https://doi.org/10.1038/nrn3176
Burgo, A., Proux-Gillardeaux, V., Sotirakis, E., Bun, P., Casano, A., Verraes, A., … Galli, T. (2012). A molecular network for the transport of the TI-VAMP/VAMP7 vesicles from cell center to periphery. Developmental Cell, 23(1), 166-180. https://doi.org/10.1016/j.devcel.2012.04.019
Caceres, A., Ye, B., & Dotti, C. G. (2012). Neuronal polarity: Demarcation, growth and commitment. Current Opinion in Cell Biology, 24(4), 547-553. https://doi.org/10.1016/j.ceb.2012.05.011
Chai, X., Forster, E., Zhao, S., Bock, H. H., & Frotscher, M. (2009). Reelin stabilizes the actin cytoskeleton of neuronal processes by inducing n-cofilin phosphorylation at serine3. Journal of Neuroscience, 29(1), 288-299. https://doi.org/10.1523/JNEUROSCI.2934-08.2009
Chaineau, M., Danglot, L., & Galli, T. (2009). Multiple roles of the vesicular-SNARE TI-VAMP in post-Golgi and endosomal trafficking. FEBS Letters, 583(23), 3817-3826. https://doi.org/10.1016/j.febslet.2009.10.026
Chen, K. L., Ochalski, P. G., Tran, T. S., Sahir, N., Schubert, M., Pramatarova, A., & Howell, B. W. (2004). Interaction between Dab1 and CrkII is promoted by Reelin signaling. Journal of Cell Science, 117(19), 4527-4536. https://doi.org/10.1242/jcs.01320
Chiang, S. H., Hwang, J., Legendre, M., Zhang, M., Kimura, A., & Saltiel, A. R. (2003). TCGAP, a multidomain Rho GTPase-activating protein involved in insulin-stimulated glucose transport. EMBO Journal, 22(11), 2679-2691. https://doi.org/10.1093/Emboj/Cdg262
Clandinin, T. R. (2005). Surprising twists to exocyst function. Neuron, 46(2), 164-166. https://doi.org/10.1016/j.neuron.2005.04.003
Coisy-Quivy, M., Touzet, O., Bourret, A., Hipskind, R. A., Mercier, J., Fort, P., & Philips, A. (2009). TC10 controls human myofibril organization and is activated by the sarcomeric RhoGEF obscurin. Journal of Cell Science, 122(Pt 7), 947-956. https://doi.org/10.1242/jcs.040121
Cuitino, L., Matute, R., Retamal, C., Bu, G. J., Inestrosa, N. C., & Marzolo, M. P. (2005). ApoER2 is endocytosed by a clathrin-mediated process involving the adaptor protein Dab2 independent of its rafts' association. Traffic, 6(9), 820-838. https://doi.org/10.1111/j.1600-0854.2005.00320.x
D'Arcangelo, G., Miao, G. G., Chen, S. C., Soares, H. D., Morgan, J. I., & Curran, T. (1995). A protein related to extracellular matrix proteins deleted in the mouse mutant reeler. Nature, 374(6524), 719-723. https://doi.org/10.1038/374719a0
de Curtis, I. (2008). Functions of Rac GTPases during neuronal development. Developmental Neuroscience, 30(1-3), 47-58. https://doi.org/10.1159/000109851
Dent, E. W., & Gertler F. B. (2003). Cytoskeletal Dynamics and Transport in Growth Cone Motility and Axon Guidance. Neuron, 40(2), 209-227. https://doi.org/10.1016/s0896-6273(03)00633-0
Dent, E. W., Gupton S. L., & Gertler F. B. (2011). The Growth Cone Cytoskeleton in Axon Outgrowth and Guidance. Cold Spring Harbor Perspectives in Biology, 3(3), a001800. https://doi.org/10.1101/cshperspect.a001800
Donoso, M., Cancino, J., Lee, J., van Kerkhof, P., Retamal, C., Bu, G., … Marzolo, M.-P. (2009). Polarized traffic of LRP1 involves AP1B and SNX17 operating on Y-dependent sorting motifs in different pathways. Molecular Biology of the Cell, 20(1), 481-497. https://doi.org/10.1091/mbc.e08-08-0805
Dupraz, S., Grassi, D., Bernis, M. E., Sosa, L., Bisbal, M., Gastaldi, L., … Quiroga, S. (2009). The TC10-Exo70 complex is essential for membrane expansion and axonal specification in developing neurons. Journal of Neuroscience, 29(42), 13292-13301. https://doi.org/10.1523/JNEUROSCI.3907-09.2009
Etienne-Manneville, S., & Hall A. (2002). Rho GTPases in cell biology. Nature, 420(6916), 629-635. https://doi.org/10.1038/nature01148
Feng, Q., Baird, D., & Cerione, R. A. (2004). Novel regulatory mechanisms for the Dbl family guanine nucleotide exchange factor Cool-2/alpha-Pix. EMBO Journal, 23(17), 3492-3504. https://doi.org/10.1038/sj.emboj.7600331
Feng, Q., Baird, D., Peng, X., Wang, J., Ly, T., Guan, J. L., & Cerione, R. A. (2006). Cool-1 functions as an essential regulatory node for EGF receptor- and Src-mediated cell growth. Nature Cell Biology, 8(9), 945-956. https://doi.org/10.1038/ncb1453
Fujita, A., Koinuma, S., Yasuda, S., Nagai, H., Kamiguchi, H., Wada, N., & Nakamura, T. (2013). GTP hydrolysis of TC10 promotes neurite outgrowth through exocytic fusion of Rab11- and L1-containing vesicles by releasing exocyst component Exo70. PLoS One, 8(11), e79689. https://doi.org/10.1371/journal.pone.0079689
Goffinet, A. M. (1980). The cerebral cortex of the reeler mouse embryo. An electron microscopic analysis. Anatomy and Embryology, 159(2), 199-210. https://doi.org/10.1007/BF00304978
Gonzalez-Billault, C., Munoz-Llancao, P., Henriquez, D. R., Wojnacki, J., Conde, C., & Caceres, A. (2012). The role of small GTPases in neuronal morphogenesis and polarity. Cytoskeleton, 69(7), 464-485. https://doi.org/10.1002/cm.21034
Govek, E. E., Newey, S. E., & Van Aelst, L. (2005). The role of the Rho GTPases in neuronal development. Genes & Development, 19(1), 1-49. https://doi.org/10.1101/gad.1256405
Gracias, N. G., Shirkey-Son, N. J., & Hengst, U. (2014). Local translation of TC10 is required for membrane expansion during axon outgrowth. Nature Communications, 5, 3506. https://doi.org/10.1038/ncomms4506
Gupton, S. L., & Gertler, F. B. (2010). Integrin signaling switches the cytoskeletal and exocytic machinery that drives neuritogenesis. Developmental Cell, 18(5), 725-736. https://doi.org/10.1016/j.devcel.2010.02.017
Hellwig, S., Hack, I., Kowalski, J., Brunne, B., Jarowyj, J., Unger, A., … Frotscher, M. (2011). Role for Reelin in neurotransmitter release. Journal of Neuroscience, 31(7), 2352-2360. https://doi.org/10.1523/JNEUROSCI.3984-10.2011
Hertzog, M., & Chavrier, P. (2011). Cell polarity during motile processes: Keeping on track with the exocyst complex. Biochemical Journal, 433(3), 403-409. https://doi.org/10.1042/BJ20101214
Hoe, H. S., Tran, T. S., Matsuoka, Y., Howell, B. W., & Rebeck, G. W. (2006). DAB1 and Reelin effects on amyloid precursor protein and ApoE receptor 2 trafficking and processing. Journal of Biological Chemistry, 281(46), 35176-35185. https://doi.org/10.1074/jbc.M602162200
Jahn, R., & Fasshauer, D. (2012). Molecular machines governing exocytosis of synaptic vesicles. Nature, 490(7419), 201-207. https://doi.org/10.1038/nature11320
Jahn, R., Lang, T., & Sudhof, T. C. (2003). Membrane fusion. Cell, 112(4), 519-533. https://doi.org/10.1016/s0092-8674(03)00112-0
Jan, Y. N., & Jan, L. Y. (2003). The control of dendrite development. Neuron, 40(2), 229-242. https://doi.org/10.1016/S0896-6273(03)00631-7
Jan, Y. N., & Jan, L. Y. (2010). Branching out: Mechanisms of dendritic arborization. Nature Reviews Neuroscience, 11(5), 316-328. https://doi.org/10.1038/nrn2836
Jossin, Y., & Goffinet, A. M. (2007). Reelin signals through phosphatidylinositol 3-kinase and Akt to control cortical development and through mTor to regulate dendritic growth. Molecular and Cellular Biology, 27(20), 7113-7124. https://doi.org/10.1128/MCB.00928-07
Kawase, K., Nakamura, T., Takaya, A., Aoki, K., Namikawa, K., Kiyama, H., … Matsuda, M. (2006). GTP hydrolysis by the Rho family GTPase TC10 promotes exocytic vesicle fusion. Developmental Cell, 11(3), 411-421. https://doi.org/10.1016/j.devcel.2006.07.008
Kuhn, T. B., Meberg, P. J., Brown, M. D., Bernstein, L. S, Minamide, J. R, Jensen, K. O., … Bamburg, J. R. (2000). Regulating actin dynamics in neuronal growth cones by ADF/cofilin and Rho family GTPases. Journal of neurobiology, 44(2), 126-144. https://doi.org/10.1002/1097-4695(200008)44:2<126::AID-NEU4>3.0.CO;2-Z
Larios, J. A., Jausoro, I., Benitez, M. L., Bronfman, F. C., & Marzolo, M. P. (2014). Neurotrophins regulate ApoER2 proteolysis through activation of the Trk signaling pathway. BMC Neuroscience, 15, 108. https://doi.org/10.1186/1471-2202-15-108
Leemhuis, J., & Bock, H. H. (2011). Reelin modulates cytoskeletal organization by regulating Rho GTPases. Communicative & Integrative Biology, 4(3), 254-257. https://doi.org/10.4161/cib.4.3.14890
Leemhuis, J., Bouche, E., Frotscher, M., Henle, F., Hein, L., Herz, J., … Bock, H. H. (2010). Reelin signals through apolipoprotein E receptor 2 and Cdc42 to increase growth cone motility and filopodia formation. Journal of Neuroscience, 30(44), 14759-14772. https://doi.org/10.1523/JNEUROSCI.4036-10.2010
Liu, H., Nakazawa, T., Tezuka, T., & Yamamoto, T. (2006). Physical and functional interaction of Fyn tyrosine kinase with a brain-enriched Rho GTPase-activating protein TCGAP. Journal of Biological Chemistry, 281(33), 23611-23619. https://doi.org/10.1074/jbc.M511205200
Lorenzetto, E., Panteri, R., Marino, R., Keller, F., & Buffelli, M. (2008). Impaired nerve regeneration in reeler mice after peripheral nerve injury. European Journal of Neuroscience, 27(1), 12-19. https://doi.org/10.1111/j.1460-9568.2007.05978.x
Luo, L. (2000). Rho GTPases in neuronal morphogenesis. Nature Reviews Neuroscience, 1(3), 173-180. https://doi.org/10.1038/35044547
Luo, L., Jan, L. Y., & Jan, Y. N. (1997). Rho family GTP-binding proteins in growth cone signalling. Current Opinion in Neurobiology, 7(1), 81-86.
Mayer, S., Kumar, R., Jaiswal, M., Soykan, T., Ahmadian, M. R., Brose, N., … Papadopoulos, T. (2013). Collybistin activation by GTP-TC10 enhances postsynaptic gephyrin clustering and hippocampal GABAergic neurotransmission. Proceedings of the National Academy of Sciences of the United States of America, 110(51), 20795-20800. https://doi.org/10.1073/pnas.1309078110
Meseke, M., Cavus, E., & Forster, E. (2013). Reelin promotes microtubule dynamics in processes of developing neurons. Histochemistry and Cell Biology, 139(2), 283-297. https://doi.org/10.1007/s00418-012-1025-1
Meseke, M., Rosenberger, G., & Forster, E. (2013). Reelin and the Cdc42/Rac1 guanine nucleotide exchange factor alphaPIX/Arhgef6 promote dendritic Golgi translocation in hippocampal neurons. European Journal of Neuroscience, 37(9), 1404-1412. https://doi.org/10.1111/ejn.12153
Nalbant, P., Hodgson, L., Kraynov, V., Toutchkine, A., & Hahn, K. M. (2004). Activation of endogenous Cdc42 visualized in living cells. Science, 305(5690), 1615-1619. https://doi.org/10.1126/science.1100367
Ng, J., & Luo, L. (2004). Rho GTPases regulate axon growth through convergent and divergent signaling pathways. Neuron, 44(5), 779-793. https://doi.org/10.1016/j.neuron.2004.11.014
Ng, J., Nardine, T., Harms, M., Tzu, J., Goldstein, A., Sun, Y., … Luo, L. (2002). Rac GTPases control axon growth, guidance and branching. Nature, 416(6879), 442-447. https://doi.org/10.1038/416442a
Panteri, R., Mey, J., Zhelyaznik, N., D'Altocolle, A., Del Fà, A., Gangitano, C., … Keller, F. (2006). Reelin is transiently expressed in the peripheral nerve during development and is upregulated following nerve crush. Molecular and Cellular Neurosciences, 32(1-2), 133-142. https://doi.org/10.1016/j.mcn.2006.03.004
Pasten, C., Cerda, J., Jausoro, I., Court, F. A., Caceres, A., & Marzolo, M. P. (2015). ApoER2 and Reelin are expressed in regenerating peripheral nerve and regulate Schwann cell migration by activating the Rac1 GEF protein, Tiam1. Molecular and Cellular Neurosciences, 69, 1-11. https://doi.org/10.1016/j.mcn.2015.09.004
Pfenninger, K. H. (2009). Plasma membrane expansion: A neuron's Herculean task. Nature Reviews Neuroscience, 10(4), 251-261. https://doi.org/10.1038/nrn2593
Pommereit, D., & Wouters, F. S. (2007). An NGF-induced Exo70-TC10 complex locally antagonises Cdc42-mediated activation of N-WASP to modulate neurite outgrowth. Journal of Cell Science, 120(Pt 15), 2694-2705. https://doi.org/10.1242/jcs.03475
Quiroga, S., Bisbal, M., & Caceres, A. (2018). Regulation of plasma membrane expansion during axon formation. Developmental Neurobiology, 78(3), 170-180. https://doi.org/10.1002/dneu.22553
Rizo, J., Chen, X., & Arac, D. (2006). Unraveling the mechanisms of synaptotagmin and SNARE function in neurotransmitter release. Trends in Cell Biology, 16(7), 339-350. https://doi.org/10.1016/j.tcb.2006.04.006
Santana, J., & Marzolo, M. P. (2017). The functions of Reelin in membrane trafficking and cytoskeletal dynamics: Implications for neuronal migration, polarization and differentiation. Biochemical Journal, 474(18), 3137-3165. https://doi.org/10.1042/BCJ20160628
Sotelo, P., Farfan, P., Benitez, M. L., Bu, G. J., & Marzolo, M. P. (2014). Sorting Nexin 17 regulates ApoER2 recycling and Reelin signaling. PLoS One, 9(4), e93672. https://doi.org/10.1371/journal.pone.0093672
Stockinger, W., Hengstschläger-Ottnad, E., Novak, S., Matus, A., Hüttinger, M., Bauer, J., … Nimpf, J. (1998). The low density lipoprotein receptor gene family. Differential expression of two alpha2-macroglobulin receptors in the brain. Journal of Biological Chemistry, 273(48), 32213-32221. https://doi.org/10.1074/jbc.273.48.32213
Tanabe, K., Tachibana, T., Yamashita, T., Che, Y. H., Yoneda, Y., Ochi, T., … Kiyama, H. (2000). The small GTP-binding protein TC10 promotes nerve elongation in neuronal cells, and its expression is induced during nerve regeneration in rats. Journal of Neuroscience, 20(11), 4138-4144. https://doi.org/10.1523/JNEUROSCI.20-11-04138.2000
Telese, F., Ma, Q. I., Perez, P. M., Notani, D., Oh, S., Li, W., … Rosenfeld, M. G. (2015). LRP8-Reelin-regulated neuronal enhancer signature underlying learning and memory formation. Neuron, 86(3), 696-710. https://doi.org/10.1016/j.neuron.2015.03.033
Tobon, A. L., Suresh, M., Jin, J., Vitriolo, A., Pietralla, T., Tedford, K., … Puschel, A. W. (2018). The guanine nucleotide exchange factor Arhgef7/beta Pix promotes axon formation upstream of TC10. Scientific Reports, 8(1), 1-12. https://doi.org/10.1038/S41598-018-27081-1
Tojima, T., & Kamiguchi, H. (2015). Exocytic and endocytic membrane trafficking in axon development. Development, Growth & Differentiation, 57(4), 291-304. https://doi.org/10.1111/dgd.12218
Trommsdorff, M., Gotthardt, M., Hiesberger, T., Shelton, J., Stockinger, W., Nimpf, J., … Herz, J. (1999). Reeler/Disabled-like disruption of neuronal migration in knockout mice lacking the VLDL receptor and ApoE receptor 2. Cell, 97(6), 689-701. https://doi.org/10.1016/S0092-8674(00)80782-5
Weeber, E. J., Beffert, U., Jones, C., Christian, J. M., Forster, E., Sweatt, J. D., & Herz, J. (2002). Reelin and ApoE receptors cooperate to enhance hippocampal synaptic plasticity and learning. Journal of Biological Chemistry, 277(42), 39944-39952. https://doi.org/10.1074/jbc.M205147200
Xia, X. G., Zhou, H. X., Ding, H. L., Affar, E. B., Shi, Y., & Xu, Z. S. (2003). An enhanced U6 promoter for synthesis of short hairpin RNA. Nucleic Acids Research, 31(17), e100. https://doi.org/10.1093/nar/gng098
Zhao, T., Qi, Y., Li, Y., & Xu, K. (2012). PI3 Kinase regulation of neural regeneration and muscle hypertrophy after spinal cord injury. Molecular Biology Reports, 39(4), 3541-3547. https://doi.org/10.1007/s11033-011-1127-1
Zheng, N., Jeyifous, O., Munro, C., Montgomery, J. M., & Green, W. N. (2015). Synaptic activity regulates AMPA receptor trafficking through different recycling pathways. eLife, 4, e06878. https://doi.org/10.7554/eLife.06878