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Cited by 43Axon Guidance and Neuronal SignalingNeuroscience and Neuropharmacology ResearchAdvanced Electron Microscopy Techniques and Applications

In situ cryo-electron tomography reveals local cellular machineries for axon branch development

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Nedozralova, Hana, Basnet, Nirakar, Ibiricu, Iosune, Bodakuntla, Satish, Biertümpfel, Christian, Mizuno, Naoko·2022·Journal of Cell Biology
DOI 10.1083/jcb.202106086PMC PMC8916118

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Abstract

Neurons are highly polarized cells forming an intricate network of dendrites and axons. They are shaped by the dynamic reorganization of cytoskeleton components and cellular organelles. Axon branching allows the formation of new paths and increases circuit complexity. However, our understanding of branch formation is sparse due to the lack of direct in-depth observations. Using in situ cellular cryo-electron tomography on primary mouse neurons, we directly visualized the remodeling of organelles and cytoskeleton structures at axon branches. Strikingly, branched areas functioned as hotspots concentrating organelles to support dynamic activities. Unaligned actin filaments assembled at the base of premature branches accompanied by filopodia-like protrusions. Microtubules and ER comigrated into preformed branches to support outgrowth together with accumulating compact, ∼500-nm mitochondria and locally clustered ribosomes. We obtained a roadmap of events supporting the hypothesis of local protein synthesis selectively taking place at axon branches, allowing them to serve as unique control hubs for axon development and downstream neural network formation.

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  • Several studies have imaged neuronal processes by cryo-EM and cryo-ET, showing neurites are accessible to cryogenic imaging but persistent challenges remain at molecular resolution due to poor contrast and cytoplasmic denseness.

    “Several studies have imaged neuronal processes by cryo-EM and cryo-ET19–25, showing that neurites are accessible to cryogenic imaging, while also revealing persistent challenges in obtaining information at a molecular resolution due to poor contrast and cytoplasmic denseness.”

    From Ghost Neuron preparation unlocks high-resolution structural mapping of intracellular architecture in axons (2026) · cites this paper as [25]

    The Results and discussion (Structural analysis of branching axons; page not provided) reports cryo-ET reconstructions of axon branches and shafts, supporting that neuronal processes are accessible to cryogenic imaging. It also notes a tomographic limitation, the “missing wedge,” but does not attribute difficulty obtaining molecular-resolution information to poor contrast or cytoplasmic denseness. (LLM, conf=0.85)

    Experimental — accuracy not yet measured

  • Thalamus neural explants produced long neurites extending from brain tissue, allowing unambiguous assignment to axonal origins at this developmental stage.

    “We used thalamus neural explants, which produced long neurites extending from brain tissue, allowing unambiguous assignment to axonal origins at this developmental stage25,33,34.”

    From Ghost Neuron preparation unlocks high-resolution structural mapping of intracellular architecture in axons (2026) · cites this paper as [25]

    The Materials and methods section describes E15.5 mouse thalamus tissue explants, and the Results and discussion section identifies axons and branches in those cultures. Neither passage says that long neurites extended from the tissue or that their axonal origin could be assigned unambiguously at that developmental stage. Page numbers are unavailable in our copy. (LLM, conf=0.83)

    Experimental — accuracy not yet measured

  • Mitochondria within Ghost Neuron regions retain short, oval morphology characteristic of axonal mitochondria, rather than elongated forms commonly observed in dendrites.

    “Mitochondria within these regions retain their short, oval morphology (Fig. 4B and Fig. S4), characteristic to axonal mitochondria, rather than the elongated forms commonly observed in dendrites25,40.”

    From Ghost Neuron preparation unlocks high-resolution structural mapping of intracellular architecture in axons (2026) · cites this paper as [25]

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Research works printed but not linked: 69

  1. Baas, P.W., J.S. Deitch, M.M. Black, and G.A. Banker. 1988. Polarity orientation of microtubules in hippocampal neurons: uniformity in the axon and nonuniformity in the dendrite. Proc. Natl. Acad. Sci. USA. 85: 8335– 8339. 10.1073/pnas.85.21.8335 3054884 PMC282424 · DOI · Paper page
  2. Baas, P.W., and S. Lin. 2011. Hooks and comets: the story of microtubule polarity orientation in the neuron. Dev. Neurobiol. 71: 403– 418. 10.1002/dneu.20818 21557497 PMC3151545 · DOI
  3. Baas, P.W., A.N. Rao, A.J. Matamoros, and L. Leo. 2016. Stability properties of neuronal microtubules. Cytoskeleton (Hoboken). 73: 442– 460. 10.1002/cm.21286 26887570 PMC5541393 · DOI
  4. Barnes, A.P., and F. Polleux. 2009. Establishment of axon-dendrite polarity in developing neurons. Annu. Rev. Neurosci. 32: 347– 381. 10.1146/annurev.neuro.31.060407.125536 19400726 PMC3170863 · DOI · Paper page
  5. Basnet, N., H. Nedozralova, A.H. Crevenna, S. Bodakuntla, T. Schlichthaerle, M. Taschner, G. Cardone, C. Janke, R. Jungmann, M.M. Magiera, C. Biertümpfel,. 2018. Direct induction of microtubule branching by microtubule nucleation factor SSNA1. Nat. Cell Biol. 20: 1172– 1180. 10.1038/s41556-018-0199-8 30250060 PMC6330057 · DOI
  6. Bassell, G.J., H. Zhang, A.L. Byrd, A.M. Femino, R.H. Singer, K.L. Taneja, L.M. Lifshitz, I.M. Herman, and K.S. Kosik. 1998. Sorting of beta-actin mRNA and protein to neurites and growth cones in culture. J. Neurosci. 18: 251– 265. 10.1523/JNEUROSCI.18-01-00251.1998 9412505 PMC6793411 · DOI
  7. Biever, A., C. Glock, G. Tushev, E. Ciirdaeva, T. Dalmay, J.D. Langer, and E.M. Schuman. 2020. Monosomes actively translate synaptic mRNAs in neuronal processes. Science. 367: eaay4991. 10.1126/science.aay4991 32001627 · DOI
  8. Bodakuntla, S., C. Janke, and M.M. Magiera. 2020. Knocking out multiple genes in cultured primary neurons to study tubulin posttranslational modifications. Methods Mol. Biol. 2101: 327– 351. 10.1007/978-1-0716-0219-5_19 31879912 · DOI
  9. Bodakuntla, S., H. Nedozralova, N. Basnet, and N. Mizuno. 2021. Cytoskeleton and membrane organization at axon branches. Front. Cell Dev. Biol. 9: 707486. 10.3389/fcell.2021.707486 34540830 PMC8440873 · DOI
  10. Brandt, F., L.A. Carlson, F.U. Hartl, W. Baumeister, and K. Grunewald. 2010. The three-dimensional organization of polyribosomes in intact human cells. Mol. Cell. 39: 560– 569. 10.1016/j.molcel.2010.08.003 20797628 · DOI
  11. Castaño-Díez, Daniel, Mikhail Kudryashev, Marcel Arheit, and Henning Stahlberg. 2012. Dynamo: a flexible, user-friendly development tool for subtomogram averaging of cryo-EM data in high-performance computing environments. J Struct Biol. 178(2): 139– 151.. 10.1016/j.jsb.2011.12.017 22245546 · DOI
  12. Chen, J., Y. Kanai, N.J. Cowan, and N. Hirokawa. 1992. Projection domains of MAP2 and tau determine spacings between microtubules in dendrites and axons. Nature. 360: 674– 677. 10.1038/360674a0 1465130 · DOI · Paper page
  13. Cioni, J.M., M. Koppers, and C.E. Holt. 2018. Molecular control of local translation in axon development and maintenance. Curr. Opin. Neurobiol. 51: 86– 94. 10.1016/j.conb.2018.02.025 29549711 · DOI
  14. Cui-Wang, T., C. Hanus, T. Cui, T. Helton, J. Bourne, D. Watson, K.M. Harris, and M.D. Ehlers. 2012. Local zones of endoplasmic reticulum complexity confine cargo in neuronal dendrites. Cell. 148: 309– 321. 10.1016/j.cell.2011.11.056 22265418 PMC3266556 · DOI
  15. Dalla Costa, I., C.N. Buchanan, M.D. Zdradzinski, P.K. Sahoo, T.P. Smith, E. Thames, A.N. Kar, and J.L. Twiss. 2021. The functional organization of axonal mRNA transport and translation. Nat. Rev. Neurosci. 22: 77– 91. 10.1038/s41583-020-00407-7 33288912 PMC8161363 · DOI
  16. Delgado, T., R.S. Petralia, D.W. Freeman, M. Sedlacek, Y.X. Wang, S.D. Brenowitz, S.H. Sheu, J.W. Gu, D. Kapogiannis, M.P. Mattson, and P.J. Yao. 2019. Comparing 3D ultrastructure of presynaptic and postsynaptic mitochondria. Biol. Open. 8: bio044834. 10.1242/bio.044834 31362947 PMC6737966 · DOI
  17. Dent, E.W., and F.B. Gertler. 2003. Cytoskeletal dynamics and transport in growth cone motility and axon guidance. Neuron. 40: 209– 227. 10.1016/s0896-6273(03)00633-0 14556705 · DOI
  18. Dent, E.W., and K. Kalil. 2001. Axon branching requires interactions between dynamic microtubules and actin filaments. J. Neurosci. 21: 9757– 9769 11739584 PMC6763027
  19. Donnelly, C.J., M. Park, M. Spillane, S. Yoo, A. Pacheco, C. Gomes, D. Vuppalanchi, M. McDonald, H.H. Kim, T.T. Merianda, G. Gallo,. 2013. Axonally synthesized beta-actin and GAP-43 proteins support distinct modes of axonal growth. J. Neurosci. 33: 3311– 3322. 10.1523/JNEUROSCI.1722-12.2013 23426659 PMC3711152 · DOI
  20. Fan, X., L. Zhao, C. Liu, J.C. Zhang, K. Fan, X. Yan, H.L. Peng, J. Lei, and H.W. Wang. 2017. Near-atomic resolution structure determination in over-focus with Volta phase plate by Cs-corrected cryo-EM. Structure. 25: 1623– 1630.e3. 10.1016/j.str.2017.08.008 28943337 · DOI
  21. Farias, G.G., A. Freal, E. Tortosa, R. Stucchi, X. Pan, S. Portegies, L. Will, M. Altelaar, and C.C. Hoogenraad. 2019. Feedback-driven mechanisms between microtubules and the endoplasmic reticulum instruct neuronal polarity. Neuron. 102: 184– 201.e8. 10.1016/j.neuron.2019.01.030 30772082 · DOI
  22. Gallo, G. 2011. The cytoskeletal and signaling mechanisms of axon collateral branching. Dev. Neurobiol. 71: 201– 220. 10.1002/dneu.20852 21308993 · DOI
  23. Gallo, G. 2013. Mechanisms underlying the initiation and dynamics of neuronal filopodia: from neurite formation to synaptogenesis. Int. Rev. Cell Mol. Biol. 301: 95– 156. 10.1016/B978-0-12-407704-1.00003-8 23317818 · DOI
  24. Goldberg, J.L. 2003. How does an axon grow? Genes Dev. 17: 941– 958. 10.1101/gad.1062303 12704078 · DOI
  25. Grant, T., and N. Grigorieff. 2015. Measuring the optimal exposure for single particle cryo-EM using a 2.6 A reconstruction of rotavirus VP6. Elife. 4: e06980. 10.7554/elife.06980 26023829 PMC4471936 · DOI
  26. Gumy, L.F., C.L. Tan, and J.W. Fawcett. 2010. The role of local protein synthesis and degradation in axon regeneration. Exp. Neurol. 223: 28– 37. 10.1016/j.expneurol.2009.06.004 19520073 PMC2864402 · DOI
  27. Hagen, W.J.H., W. Wan, and J.A.G. Briggs. 2017. Implementation of a cryo-electron tomography tilt-scheme optimized for high resolution subtomogram averaging. J. Struct. Biol. 197: 191– 198. 10.1016/j.jsb.2016.06.007 27313000 PMC5287356 · DOI
  28. Heyer, E.E., and M.J. Moore. 2016. Redefining the translational status of 80S monosomes. Cell. 164: 757– 769. 10.1016/j.cell.2016.01.003 26871635 · DOI
  29. Heymann, J.B., G. Cardone, D.C. Winkler, and A.C. Steven. 2008. Computational resources for cryo-electron tomography in Bsoft. J. Struct. Biol. 161: 232– 242. 10.1016/j.jsb.2007.08.002 17869539 PMC2409064 · DOI
  30. Holt, C.E., K.C. Martin, and E.M. Schuman. 2019. Local translation in neurons: visualization and function. Nat. Struct. Mol. Biol. 26: 557– 566. 10.1038/s41594-019-0263-5 31270476 · DOI
  31. Hutchins, B.I., and K. Kalil. 2008. Differential outgrowth of axons and their branches is regulated by localized calcium transients. J. Neurosci. 28: 143– 153. 10.1523/JNEUROSCI.4548-07.2008 18171932 PMC2474798 · DOI
  32. Kalil, K., and E.W. Dent. 2014. Branch management: mechanisms of axon branching in the developing vertebrate CNS. Nat. Rev. Neurosci. 15: 7– 18. 10.1038/nrn3650 24356070 PMC4063290 · DOI
  33. Koenig, E., R. Martin, M. Titmus, and J.R. Sotelo-Silveira. 2000. Cryptic peripheral ribosomal domains distributed intermittently along mammalian myelinated axons. J. Neurosci. 20: 8390– 8400. 10.1523/JNEUROSCI.20-22-08390.2000 11069946 PMC6773183 · DOI
  34. Kremer, J.R., D.N. Mastronarde, and J.R. McIntosh. 1996. Computer visualization of three-dimensional image data using IMOD. J. Struct. Biol. 116: 71– 76. 10.1006/jsbi.1996.0013 8742726 · DOI
  35. Lewis, S.C., L.F. Uchiyama, and J. Nunnari. 2016. ER-mitochondria contacts couple mtDNA synthesis with mitochondrial division in human cells. Science. 353: aaf5549. 10.1126/science.aaf5549 27418514 PMC5554545 · DOI · Paper page
  36. Lewis, T.L. Jr., S.K. Kwon, A. Lee, R. Shaw, and F. Polleux. 2018. MFF-dependent mitochondrial fission regulates presynaptic release and axon branching by limiting axonal mitochondria size. Nat. Commun. 9: 5008. 10.1038/s41467-018-07416-2 30479337 PMC6258764 · DOI · Paper page
  37. Li, Z., K. Okamoto, Y. Hayashi, and M. Sheng. 2004. The importance of dendritic mitochondria in the morphogenesis and plasticity of spines and synapses. Cell. 119: 873– 887. 10.1016/j.cell.2004.11.003 15607982 · DOI · Paper page
  38. Llorca, O., E.A. McCormack, G. Hynes, J. Grantham, J. Cordell, J.L. Carrascosa, K.R. Willison, J.J. Fernandez, and J.M. Valpuesta. 1999. Eukaryotic type II chaperonin CCT interacts with actin through specific subunits. Nature. 402: 693– 696. 10.1038/45294 10604479 · DOI
  39. Lowery, L.A., and D. Van Vactor. 2009. The trip of the tip: understanding the growth cone machinery. Nat. Rev. Mol. Cell Biol. 10: 332– 343. 10.1038/nrm2679 19373241 PMC2714171 · DOI
  40. Mahamid, J., S. Pfeffer, M. Schaffer, E. Villa, R. Danev, L.K. Cuellar, F. Forster, A.A. Hyman, J.M. Plitzko, and W. Baumeister. 2016. Visualizing the molecular sociology at the HeLa cell nuclear periphery. Science. 351: 969– 972. 10.1126/science.aad8857 26917770 · DOI
  41. Martinez-Sanchez, A., I. Garcia, S. Asano, V. Lucic, and J.J. Fernandez. 2014. Robust membrane detection based on tensor voting for electron tomography. J. Struct. Biol. 186: 49– 61. 10.1016/j.jsb.2014.02.015 24625523 · DOI
  42. Mastronarde, D.N., and S.R. Held. 2017. Automated tilt series alignment and tomographic reconstruction in IMOD. J. Struct. Biol. 197: 102– 113. 10.1016/j.jsb.2016.07.011 27444392 PMC5247408 · DOI
  43. Merianda, T.T., A.C. Lin, J.S. Lam, D. Vuppalanchi, D.E. Willis, N. Karin, C.E. Holt, and J.L. Twiss. 2009. A functional equivalent of endoplasmic reticulum and Golgi in axons for secretion of locally synthesized proteins. Mol. Cell. Neurosci. 40: 128– 142. 10.1016/j.mcn.2008.09.008 19022387 PMC3794446 · DOI
  44. Moores, C.A., M. Perderiset, F. Francis, J. Chelly, A. Houdusse, and R.A. Milligan. 2004. Mechanism of microtubule stabilization by doublecortin. Mol. Cell. 14: 833– 839. 10.1016/j.molcel.2004.06.009 15200960 · DOI
  45. Myasnikov, A.G., Z.A. Afonina, J.F. Menetret, V.A. Shirokov, A.S. Spirin, and B.P. Klaholz. 2014. The molecular structure of the left-handed supra-molecular helix of eukaryotic polyribosomes. Nat. Commun. 5: 5294. 10.1038/ncomms6294 25376914 · DOI
  46. Noma, K., A. Goncharov, M.H. Ellisman, and Y. Jin. 2017. Microtubule-dependent ribosome localization in C. elegans neurons. Elife. 6: e26376. 10.7554/eLife.26376 28767038 PMC5577916 · DOI
  47. Poon, M.M., S.H. Choi, C.A. Jamieson, D.H. Geschwind, and K.C. Martin. 2006. Identification of process-localized mRNAs from cultured rodent hippocampal neurons. J. Neurosci. 26: 13390– 13399. 10.1523/JNEUROSCI.3432-06.2006 17182790 PMC6675000 · DOI
  48. Popov, V., N.I. Medvedev, H.A. Davies, and M.G. Stewart. 2005. Mitochondria form a filamentous reticular network in hippocampal dendrites but are present as discrete bodies in axons: a three-dimensional ultrastructural study. J. Comp. Neurol. 492: 50– 65. 10.1002/cne.20682 16175555 · DOI
  49. Sheng, Z.H. 2017. The interplay of axonal energy homeostasis and mitochondrial trafficking and anchoring. Trends Cell Biol. 27: 403– 416. 10.1016/j.tcb.2017.01.005 28228333 PMC5440189 · DOI · Paper page
  50. Shibata, Y., T. Shemesh, W.A. Prinz, A.F. Palazzo, M.M. Kozlov, and T.A. Rapoport. 2010. Mechanisms determining the morphology of the peripheral ER. Cell. 143: 774– 788. 10.1016/j.cell.2010.11.007 21111237 PMC3008339 · DOI
  51. Shigeoka, T., M. Koppers, H.H. Wong, J.Q. Lin, R. Cagnetta, A. Dwivedy, J. de Freitas Nascimento, F.W. van Tartwijk, F. Strohl, J.M. Cioni, J. Schaeffer,. 2019. On-site ribosome remodeling by locally synthesized ribosomal proteins in axons. Cell Rep. 29: 3605– 3619.e10. 10.1016/j.celrep.2019.11.025 31825839 PMC6915326 · DOI
  52. Spillane, M., A. Ketschek, T.T. Merianda, J.L. Twiss, and G. Gallo. 2013. Mitochondria coordinate sites of axon branching through localized intra-axonal protein synthesis. Cell Rep. 5: 1564– 1575. 10.1016/j.celrep.2013.11.022 24332852 PMC3947524 · DOI
  53. Stepanova, T., J. Slemmer, C.C. Hoogenraad, G. Lansbergen, B. Dortland, C.I. De Zeeuw, F. Grosveld, G. van Cappellen, A. Akhmanova, and N. Galjart. 2003. Visualization of microtubule growth in cultured neurons via the use of EB3-GFP (end-binding protein 3-green fluorescent protein). J. Neurosci. 23: 2655– 2664. 10.1523/JNEUROSCI.23-07-02655.2003 12684451 PMC6742099 · DOI
  54. Stiess, M., N. Maghelli, L.C. Kapitein, S. Gomis-Ruth, M. Wilsch-Brauninger, C.C. Hoogenraad, I.M. Tolic-Norrelykke, and F. Bradke. 2010. Axon extension occurs independently of centrosomal microtubule nucleation. Science. 327: 704– 707. 10.1126/science.1182179 20056854 · DOI
  55. Su, Y., W. Xia, J. Li, T. Walz, M.J. Humphries, D. Vestweber, C. Cabanas, C. Lu, and T.A. Springer. 2016. Relating conformation to function in integrin α5β1. Proc. Natl. Acad. Sci. USA. 113: E3872– E3881. 10.1073/pnas.1605074113 27317747 PMC4941492 · DOI · Paper page
  56. Tang, F., and K. Kalil. 2005. Netrin-1 induces axon branching in developing cortical neurons by frequency-dependent calcium signaling pathways. J. Neurosci. 25: 6702– 6715. 10.1523/JNEUROSCI.0871-05.2005 16014732 PMC6725419 · DOI
  57. Taylor, A.M., N.C. Berchtold, V.M. Perreau, C.H. Tu, N. Li Jeon, and C.W. Cotman. 2009. Axonal mRNA in uninjured and regenerating cortical mammalian axons. J. Neurosci. 29: 4697– 4707. 10.1523/JNEUROSCI.6130-08.2009 19369540 PMC3632375 · DOI
  58. Tcherkezian, J., P.A. Brittis, F. Thomas, P.P. Roux, and J.G. Flanagan. 2010. Transmembrane receptor DCC associates with protein synthesis machinery and regulates translation. Cell. 141: 632– 644. 10.1016/j.cell.2010.04.008 20434207 PMC2881594 · DOI
  59. Tegunov, D., and P. Cramer. 2019. Real-time cryo-electron microscopy data preprocessing with Warp. Nat. Methods. 16: 1146– 1152. 10.1038/s41592-019-0580-y 31591575 PMC6858868 · DOI
  60. Tymanskyj, S.R., and L. Ma. 2019. MAP7 prevents axonal branch retraction by creating a stable microtubule boundary to rescue polymerization. J. Neurosci. 39: 7118– 7131. 10.1523/JNEUROSCI.0775-19.2019 31391261 PMC6733548 · DOI
  61. van Beuningen, S.F., and C.C. Hoogenraad. 2016. Neuronal polarity: remodeling microtubule organization. Curr. Opin. Neurobiol. 39: 1– 7. 10.1016/j.conb.2016.02.003 26945466 · DOI
  62. Vassilopoulos, S., S. Gibaud, A. Jimenez, G. Caillol, and C. Leterrier. 2019. Ultrastructure of the axonal periodic scaffold reveals a braid-like organization of actin rings. Nat. Commun. 10: 5803. 10.1038/s41467-019-13835-6 31862971 PMC6925202 · DOI · Paper page
  63. Wang, K.H., K. Brose, D. Arnott, T. Kidd, C.S. Goodman, W. Henzel, and M. Tessier-Lavigne. 1999. Biochemical purification of a mammalian slit protein as a positive regulator of sensory axon elongation and branching. Cell. 96: 771– 784. 10.1016/s0092-8674(00)80588-7 10102266 · DOI
  64. Wong, H.H., J.Q. Lin, F. Strohl, C.G. Roque, J.M. Cioni, R. Cagnetta, B. Turner-Bridger, R.F. Laine, W.A. Harris, C.F. Kaminski, and C.E. Holt. 2017. RNA docking and local translation regulate site-specific axon remodeling in vivo. Neuron. 95: 852– 868.e8. 10.1016/j.neuron.2017.07.016 28781168 PMC5563073 · DOI
  65. Wu, Y., C. Whiteus, C.S. Xu, K.J. Hayworth, R.J. Weinberg, H.F. Hess, and P. De Camilli. 2017. Contacts between the endoplasmic reticulum and other membranes in neurons. Proc. Natl. Acad. Sci. USA. 114: E4859– E4867. 10.1073/pnas.1701078114 28559323 PMC5474793 · DOI
  66. Xu, K., G. Zhong, and X. Zhuang. 2013. Actin, spectrin, and associated proteins form a periodic cytoskeletal structure in axons. Science. 339: 452– 456. 10.1126/science.1232251 23239625 PMC3815867 · DOI
  67. Yu, W., L. Qiang, J.M. Solowska, A. Karabay, S. Korulu, and P.W. Baas. 2008. The microtubule-severing proteins spastin and katanin participate differently in the formation of axonal branches. Mol. Biol. Cell. 19: 1485– 1498. 10.1091/mbc.e07-09-0878 18234839 PMC2291400 · DOI
  68. Zheng, S.Q., E. Palovcak, J.P. Armache, K.A. Verba, Y. Cheng, and D.A. Agard. 2017. MotionCor2: anisotropic correction of beam-induced motion for improved cryo-electron microscopy. Nat. Methods. 14: 331– 332. 10.1038/nmeth.4193 28250466 PMC5494038 · DOI
  69. Zivraj, K.H., Y.C. Tung, M. Piper, L. Gumy, J.W. Fawcett, G.S. Yeo, and C.E. Holt. 2010. Subcellular profiling reveals distinct and developmentally regulated repertoire of growth cone mRNAs. J. Neurosci. 30: 15464– 15478. 10.1523/jneurosci.1800-10.2010 21084603 PMC3683943 · DOI · Paper page

Cited by

Sorted by citations

Authors
Nedozralova, H., Basnet, N., Ibiricu, I., Bodakuntla, S., Biertümpfel, C., & Mizuno, N.
Affiliations
  • Department of Structural Cell Biology, Max Planck Institute of Biochemistry, Martinsried, Germany 1
  • National Institutes of Health (US)
  • Max Planck Institute of Biochemistry (DE)
Corresponding author
Mizuno, Naoko
ORCID
Venue
Journal of Cell Biology
Publisher
Rockefeller University Press
Published
2022-03-09
Volume
221
Issue
4
ISSN
  • 0021-9525 (ISSN-L)
  • 1540-8140
DOI
10.1083/jcb.202106086
PMC
PMC8916118
OpenAlex
W4221055044
Cited by
43
References
1
Citations by year
2026: 13 · 2025: 10 · 2024: 6 · 2023: 8 · 2022: 6
FWCI
3.33
Type
journal article
Language
en
Open access
Licence
Locations
  • The Journal of Cell Biology (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Research Explorer (The University of Manchester) (publishedVersion)
Funders
  • BoehringerIngelheim Stiftung
  • European Research Council (724209)
  • NHLBI
  • National Institutes of Health
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Axon Guidance and Neuronal Signaling
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Structural Biology › Advanced Electron Microscopy Techniques and Applications
Keywords
axon branching, axon development, neuronal polarity, cytoskeletal remodeling, F-actin, microtubules, endoplasmic reticulum, mitochondria, local protein synthesis, filopodia, in situ cryo-electron tomography
MeSH terms
Actins, Animals, Axons, Cytoskeleton, Endoplasmic Reticulum, Microtubules, Protein Biosynthesis, Mice, Electron Microscope Tomography, Neurogenesis

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