Endocytosis in the axon initial segment maintains neuronal polarity.
Journal
Nature
ISSN: 1476-4687
Titre abrégé: Nature
Pays: England
ID NLM: 0410462
Informations de publication
Date de publication:
09 2022
09 2022
Historique:
received:
11
05
2021
accepted:
05
07
2022
pubmed:
18
8
2022
medline:
9
9
2022
entrez:
17
8
2022
Statut:
ppublish
Résumé
Neurons are highly polarized cells that face the fundamental challenge of compartmentalizing a vast and diverse repertoire of proteins in order to function properly
Identifiants
pubmed: 35978188
doi: 10.1038/s41586-022-05074-5
pii: 10.1038/s41586-022-05074-5
pmc: PMC9433327
doi:
Substances chimiques
Receptors, Cell Surface
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
128-135Subventions
Organisme : NINDS NIH HHS
ID : R01 NS097161
Pays : United States
Organisme : Howard Hughes Medical Institute
Pays : United States
Informations de copyright
© 2022. The Author(s).
Références
Bentley, M. & Banker, G. The cellular mechanisms that maintain neuronal polarity. Nat. Rev. Neurosci. 17, 611–622 (2016).
pubmed: 27511065
doi: 10.1038/nrn.2016.100
Huang, C. Y.-M. & Rasband, M. N. Axon initial segments: structure, function, and disease. Ann. N. Y. Acad. Sci. 1420, 46–61 (2018).
pubmed: 29749636
pmcid: 5992072
doi: 10.1111/nyas.13718
Leterrier, C. The axon initial segment: an updated viewpoint. J. Neurosci. 38, 2135–2145 (2018).
pubmed: 29378864
pmcid: 6596274
doi: 10.1523/JNEUROSCI.1922-17.2018
Wheeler, R. J. & Hyman, A. A. Controlling compartmentalization by non-membrane-bound organelles. Phil. Trans. R. Soc. B 373, 20170193 (2018).
pubmed: 29632271
pmcid: 5904305
doi: 10.1098/rstb.2017.0193
Takano, T., Funahashi, Y. & Kaibuchi, K. Neuronal polarity: positive and negative feedback signals. Front. Cell Dev. Biol. 7, 69 (2019).
pubmed: 31069225
pmcid: 6491837
doi: 10.3389/fcell.2019.00069
Kiral, F. R., Kohrs, F. E., Jin, E. J. & Hiesinger, P. R. Rab GTPases and membrane trafficking in neurodegeneration. Curr. Biol. 28, R471–R486 (2018).
pubmed: 29689231
pmcid: 5965285
doi: 10.1016/j.cub.2018.02.010
Wang, D., Chan, C. C., Cherry, S. & Hiesinger, P. R. Membrane trafficking in neuronal maintenance and degeneration. Cell. Mol. Life Sci. 70, 2919–2934 (2013).
pubmed: 23132096
doi: 10.1007/s00018-012-1201-4
Palay, S. L., Sotelo, C., Peters, A. & Orkand, P. M. The axon hillock and the initial segment. J. Cell Biol. 38, 193–201 (1968).
pubmed: 5691973
pmcid: 2107452
doi: 10.1083/jcb.38.1.193
Fréal, A. et al. Feedback-driven assembly of the axon initial segment. Neuron 104, 305–321.e8 (2019).
pubmed: 31474508
pmcid: 6839619
doi: 10.1016/j.neuron.2019.07.029
Leterrier, C. et al. Nanoscale architecture of the axon initial segment reveals an organized and robust scaffold. Cell Rep. 13, 2781–2793 (2015).
pubmed: 26711344
doi: 10.1016/j.celrep.2015.11.051
Kuijpers, M. et al. Dynein regulator NDEL1 controls polarized cargo transport at the axon initial segment. Neuron 89, 461–471 (2016).
pubmed: 26844830
doi: 10.1016/j.neuron.2016.01.022
Nakata, T. & Hirokawa, N. Microtubules provide directional cues for polarized axonal transport through interaction with kinesin motor head. J. Cell Biol. 162, 1045–1055 (2003).
pubmed: 12975348
pmcid: 2172855
doi: 10.1083/jcb.200302175
Lewis, T. L., Mao, T., Svoboda, K. & Arnold, D. B. Myosin-dependent targeting of transmembrane proteins to neuronal dendrites. Nat. Neurosci. 12, 568–576 (2009).
pubmed: 19377470
pmcid: 2937175
doi: 10.1038/nn.2318
Al-Bassam, S., Xu, M., Wandless, T. J. & Arnold, D. B. Differential trafficking of transport vesicles contributes to the localization of dendritic proteins. Cell Rep. 2, 89–100 (2012).
pubmed: 22840400
pmcid: 3408588
doi: 10.1016/j.celrep.2012.05.018
Balasanyan, V. et al. Structure and function of an actin-based filter in the proximal axon. Cell Rep. 21, 2696–2705 (2017).
pubmed: 29212018
pmcid: 5783201
doi: 10.1016/j.celrep.2017.11.046
Farías, G. G., Guardia, C. M., Britt, D. J., Guo, X. & Bonifacino, J. S. Sorting of dendritic and axonal vesicles at the pre-axonal exclusion zone. Cell Rep. 13, 1221–1232 (2015).
pubmed: 26527003
pmcid: 5410646
doi: 10.1016/j.celrep.2015.09.074
Burack, M. A., Silverman, M. A. & Banker, G. The role of selective transport in neuronal protein sorting. Neuron 26, 465–472 (2000).
pubmed: 10839364
doi: 10.1016/S0896-6273(00)81178-2
Hamdan, H. et al. Mapping axon initial segment structure and function by multiplexed proximity biotinylation. Nat. Commun. 11, 100 (2020).
pubmed: 31900387
pmcid: 6941957
doi: 10.1038/s41467-019-13658-5
Winckler, B., Forscher, P. & Mellman, I. A diffusion barrier maintains distribution of membrane proteins in polarized neurons. Nature 397, 698–701 (1999).
pubmed: 10067893
doi: 10.1038/17806
Nakada, C. et al. Accumulation of anchored proteins forms membrane diffusion barriers during neuronal polarization. Nat. Cell Biol. 5, 626–632 (2003).
pubmed: 12819789
doi: 10.1038/ncb1009
Albrecht, D. et al. Nanoscopic compartmentalization of membrane protein motion at the axon initial segment. J. Cell Biol. 215, 37–46 (2016).
pubmed: 27697928
pmcid: 5057285
doi: 10.1083/jcb.201603108
Jegla, T. et al. Bilaterian giant ankyrins have a common evolutionary origin and play a conserved role in patterning the axon initial segment. PLoS Genet. 12, e1006457 (2016).
pubmed: 27911898
pmcid: 5135030
doi: 10.1371/journal.pgen.1006457
Otsuka, A. J. et al. An ankyrin-related gene (unc-44) is necessary for proper axonal guidance in Caenorhabditis elegans. J. Cell Biol. 129, 1081–1092 (1995).
pubmed: 7744957
doi: 10.1083/jcb.129.4.1081
Yau, K. W. et al. Microtubule minus-end binding protein CAMSAP2 controls axon specification and dendrite development. Neuron 82, 1058–1073 (2014).
pubmed: 24908486
doi: 10.1016/j.neuron.2014.04.019
Zhang, X., Davis, J. Q., Carpenter, S. & Bennett, V. Structural requirements for association of neurofascin with ankyrin. J. Biol. Chem. 273, 30785–30794 (1998).
pubmed: 9804856
doi: 10.1074/jbc.273.46.30785
Torii, T. et al. NuMA1 promotes axon initial segment assembly through inhibition of endocytosis. J. Cell Biol. 219, e201907048 (2020).
pubmed: 31727776
Liu, O. W. & Shen, K. The transmembrane LRR protein DMA-1 promotes dendrite branching and growth in C. elegans. Nat. Neurosci. 15, 57–63 (2012).
doi: 10.1038/nn.2978
Hedstrom, K. L., Ogawa, Y. & Rasband, M. N. AnkyrinG is required for maintenance of the axon initial segment and neuronal polarity. J. Cell Biol. 183, 635–640 (2008).
pubmed: 19001126
pmcid: 2582894
doi: 10.1083/jcb.200806112
Watanabe, K. et al. Networks of polarized actin filaments in the axon initial segment provide a mechanism for sorting axonal and dendritic proteins. Cell Rep. 2, 1546–1553 (2012).
pubmed: 23246006
pmcid: 3663144
doi: 10.1016/j.celrep.2012.11.015
Janssen, A. F. J. et al. Myosin-V induces cargo immobilization and clustering at the axon initial segment. Front. Cell. Neurosci. 11, 260 (2017).
pubmed: 28894417
pmcid: 5581344
doi: 10.3389/fncel.2017.00260
Stradal, T. E. B. et al. Regulation of actin dynamics by WASP and WAVE family proteins. Trends Cell Biol. 14, 303–311 (2004).
pubmed: 15183187
doi: 10.1016/j.tcb.2004.04.007
Li, G. Rab GTPases, membrane trafficking and diseases. Curr. Drug Targets 12, 1188 (2011).
pubmed: 21561417
pmcid: 4260923
doi: 10.2174/138945011795906561
Traub, L. M. Sorting it out: AP-2 and alternate clathrin adaptors in endocytic cargo selection. J. Cell Biol. 163, 203–208 (2003).
pubmed: 14581447
pmcid: 2173531
doi: 10.1083/jcb.200309175
Rolls, M. M., Hall, D. H., Victor, M., Stelzer, E. H. K. & Rapoport, T. A. Targeting of rough endoplasmic reticulum membrane proteins and ribosomes in invertebrate neurons. Mol. Biol. Cell 13, 1778–1791 (2002).
pubmed: 12006669
pmcid: 111143
doi: 10.1091/mbc.01-10-0514
Maycox, P. R., Link, E., Reetz, A., Morris, S. A. & Jahn, R. Clathrin-coated vesicles in nervous tissue are involved primarily in synaptic vesicle recycling. J. Cell Biol. 118, 1379–1388 (1992).
pubmed: 1325974
doi: 10.1083/jcb.118.6.1379
Conradi, S. Observations on the ultrastructure of the axon hillock and initial axon segment of lumbosacral motoneurons in the cat. Acta Physiol. Scand. Suppl. 332, 65–84 (1969).
pubmed: 5386536
Blanpied, T. A., Scott, D. B. & Ehlers, M. D. Dynamics and regulation of clathrin coats at specialized endocytic zones of dendrites and spines. Neuron 36, 435–449 (2002).
pubmed: 12408846
doi: 10.1016/S0896-6273(02)00979-0
Gaidarov, I., Santini, F., Warren, R. A. & Keen, J. H. Spatial control of coated-pit dynamics in living cells. Nat. Cell Biol. 1, 1–7 (1999).
pubmed: 10559856
doi: 10.1038/8971
Petersen, J. D., Kaech, S. & Banker, G. Selective microtubule-based transport of dendritic membrane proteins arises in concert with axon specification. J. Neurosci. 34, 4135–4147 (2014).
pubmed: 24647935
pmcid: 3960460
doi: 10.1523/JNEUROSCI.3779-13.2014
Sposini, S. et al. Imaging endocytic vesicle formation at high spatial and temporal resolutions with the pulsed-pH protocol. Nat. Protoc. 15, 3088–3104 (2020).
pubmed: 32807908
doi: 10.1038/s41596-020-0371-z
Dumitrescu, A. S., Evans, M. D. & Grubb, M. S. Evaluating tools for live imaging of structural plasticity at the axon initial segment. Front. Cell. Neurosci. 10, 268 (2016).
pubmed: 27932952
pmcid: 5120105
doi: 10.3389/fncel.2016.00268
Rosendale, M., Jullié, D., Choquet, D. & Perrais, D. Spatial and temporal regulation of receptor endocytosis in neuronal dendrites revealed by imaging of single vesicle formation. Cell Rep. 18, 1840–1847 (2017).
pubmed: 28228251
doi: 10.1016/j.celrep.2017.01.081
Patzke, C., Acuna, C., Giam, L. R., Wernig, M. & Südhof, T. C. Conditional deletion of L1CAM in human neurons impairs both axonal and dendritic arborization and action potential generation. J. Exp. Med. 213, 499–515 (2016).
pubmed: 27001749
pmcid: 4821644
doi: 10.1084/jem.20150951
Sohn, P. D. et al. Pathogenic tau impairs axon initial segment plasticity and excitability homeostasis. Neuron 104, 458–470.e5 (2019).
pubmed: 31542321
pmcid: 6880876
doi: 10.1016/j.neuron.2019.08.008
Yap, C. C., Digilio, L., McMahon, L. P., Garcia, A. D. R. & Winckler, B. Degradation of dendritic cargos requires Rab7-dependent transport to somatic lysosomes. J. Cell Biol. 217, 3141–3159 (2018).
pubmed: 29907658
pmcid: 6122995
doi: 10.1083/jcb.201711039
Ribeiro, L. F. et al. SorCS1-mediated sorting in dendrites maintains neurexin axonal surface polarization required for synaptic function. PLoS Biol. 17, e3000466 (2019).
pubmed: 31658245
pmcid: 6837583
doi: 10.1371/journal.pbio.3000466
Ju, W. et al. Activity-dependent regulation of dendritic synthesis and trafficking of AMPA receptors. Nat. Neurosci. 7, 244–253 (2004).
pubmed: 14770185
doi: 10.1038/nn1189
Jullié, D., Choquet, D. & Perrais, D. Recycling endosomes undergo rapid closure of a fusion pore on exocytosis in neuronal dendrites. J. Neurosci. 34, 11106 (2014).
pubmed: 25122907
pmcid: 6705249
doi: 10.1523/JNEUROSCI.0799-14.2014
Taylor, C. A., Yan, J., Howell, A. S., Dong, X. & Shen, K. RAB-10 regulates dendritic branching by balancing dendritic transport. PLoS Genet. 11, e1005695 (2015).
pubmed: 26633194
pmcid: 4669152
doi: 10.1371/journal.pgen.1005695
Brenner, S. The genetics of Caenorhabditis elegans. Genetics 77, 71–94 (1974).
pubmed: 4366476
pmcid: 1213120
doi: 10.1093/genetics/77.1.71
Gibson, D. G. et al. Enzymatic assembly of DNA molecules up to several hundred kilobases. Nat. Methods 6, 343–345 (2009).
pubmed: 19363495
doi: 10.1038/nmeth.1318
Davis, M. W., Morton, J. J., Carroll, D. & Jorgensen, E. M. Gene activation using FLP recombinase in C. elegans. PLoS Genet. 4, e1000028 (2008).
pubmed: 18369447
pmcid: 2265415
doi: 10.1371/journal.pgen.1000028
Schwartz, M. L. & Jorgensen, E. M. SapTrap, a toolkit for high-throughput CRISPR–Cas9 gene modification in Caenorhabditis elegans. Genetics 202, 1277–1288 (2016).
pubmed: 26837755
pmcid: 4905529
doi: 10.1534/genetics.115.184275
Dokshin, G. A., Ghanta, K. S., Piscopo, K. M. & Mello, C. C. Robust genome editing with short single-stranded and long, partially single-stranded DNA donors in Caenorhabditis elegans. Genetics 210, 781–787 (2018).
pubmed: 30213854
pmcid: 6218216
doi: 10.1534/genetics.118.301532
Schindelin, J. et al. Fiji: An open-source platform for biological-image analysis. Nat. Methods 9, 676–682 (2012).
pubmed: 22743772
doi: 10.1038/nmeth.2019
Schneider, C. A., Rasband, W. S. & Eliceiri, K. W. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671–675 (2012).
pubmed: 22930834
pmcid: 5554542
doi: 10.1038/nmeth.2089
Li, W., Kang, L., Piggott, B. J., Feng, Z. & Xu, X. Z. S. The neural circuits and sensory channels mediating harsh touch sensation in Caenorhabditis elegans. Nat. Commun. 2, 315 (2011).
pubmed: 21587232
doi: 10.1038/ncomms1308
Way, J. C. & Chalfie, M. The mec-3 gene of Caenorhabditis elegans requires its own product for maintained expression and is expressed in three neuronal cell types. Genes Dev. 3, 1823–1833 (1989).
pubmed: 2576011
doi: 10.1101/gad.3.12a.1823
Chatzigeorgiou, M. et al. Specific roles for DEG/ENaC and TRP channels in touch and thermosensation in C. elegans nociceptors. Nat. Neurosci. 13, 861 (2010).
pubmed: 20512132
pmcid: 2975101
doi: 10.1038/nn.2581
Merrifield, C. J., Perrais, D. & Zenisek, D. Coupling between clathrin-coated-pit invagination, cortactin recruitment, and membrane scission observed in live cells. Cell 121, 593–606 (2005).
pubmed: 15907472
doi: 10.1016/j.cell.2005.03.015
Kaech, S. & Banker, G. Culturing hippocampal neurons. Nat. Protoc. 1, 2406–2415 (2007).
doi: 10.1038/nprot.2006.356
Marro, S. G. et al. Neuroligin-4 regulates excitatory synaptic transmission in human neurons. Neuron 103, 617–626.e6 (2019).
pubmed: 31257103
pmcid: 6706319
doi: 10.1016/j.neuron.2019.05.043
Zhang, Y. et al. Rapid single-step induction of functional neurons from human pluripotent stem cells. Neuron 78, 785–798 (2013).
pubmed: 23764284
pmcid: 3751803
doi: 10.1016/j.neuron.2013.05.029
Cheng, S. et al. Molecular basis of synaptic specificity by immunoglobulin superfamily receptors in Drosophila. eLife 8, e41028 (2019).
pubmed: 30688651
pmcid: 6374074
doi: 10.7554/eLife.41028
Özkan, E. et al. An extracellular interactome of immunoglobulin and LRR proteins reveals receptor-ligand networks. Cell 154, 228 (2013).
pubmed: 23827685
pmcid: 3756661
doi: 10.1016/j.cell.2013.06.006
Chen, C. C. H. et al. RAB-10 is required for endocytic recycling in the Caenorhabditis elegans intestine. Mol. Biol. Cell 17, 1286–1297 (2006).
pubmed: 16394106
pmcid: 1382317
doi: 10.1091/mbc.e05-08-0787