دورية أكاديمية

Evidence for glia-mediated, age-dependent remodeling of myelin at the axon initial segment.

التفاصيل البيبلوغرافية
العنوان: Evidence for glia-mediated, age-dependent remodeling of myelin at the axon initial segment.
المؤلفون: Furusho M; Department of Cell Biology, University of Connecticut Health Center, Farmington, Connecticut, USA., Terasaki M; Department of Cell Biology, University of Connecticut Health Center, Farmington, Connecticut, USA.
المصدر: The Journal of comparative neurology [J Comp Neurol] 2024 Feb; Vol. 532 (2), pp. e25574.
نوع المنشور: Journal Article; Research Support, Non-U.S. Gov't
اللغة: English
بيانات الدورية: Publisher: Wiley-Liss Country of Publication: United States NLM ID: 0406041 Publication Model: Print Cited Medium: Internet ISSN: 1096-9861 (Electronic) Linking ISSN: 00219967 NLM ISO Abbreviation: J Comp Neurol Subsets: MEDLINE
أسماء مطبوعة: Publication: <2003-> : Hoboken, N.J. : Wiley-Liss
Original Publication: Philadelphia Wistar Institute of Anatomy and Biology
مواضيع طبية MeSH: Myelin Sheath*/ultrastructure , Axon Initial Segment*, Mice ; Animals ; Axons/ultrastructure ; Neurons ; Microscopy, Electron
مستخلص: Due to its proximity to the axon initial segment (AIS), the paranode of the first myelin segment can influence the threshold for action potentials and how a neuron participates in a neuronal circuit. Using serial section electron microscopy, we examined its three-dimensional (3D) organization in the ventral horn of the mouse spinal cord. The myelin loops of postnatal day 18 mice resemble those at the node of Ranvier. However, in 3-month-old mice, 13 of 22 para-AIS showed 4 types of alteration: (A) A cytoplasmic foot process, with ultrastructural characteristics of an astrocyte, was interposed between the axolemma and the myelin loops. (B) A thin extension of the inner tongue was present between the foot process and axolemma. (C) The foot process was absent. The inner tongue extension was a broad lamella from which a thin extension reached beyond the loops and spiraled around axon. (D) One set of loops was adjacent to the axon, and another was further back and underlain by compact myelin. We suggest that (A)-(C) are steps in a progression toward (D). In this progression, a glial process displaces the original loops, the inner tongue reactivates and extends beneath the foot process, then wraps around the axon to form a new set of loops. This is the first study of the 3D organization of myelin at the AIS and provides evidence for glia-mediated age-dependent remodeling at this critical region.
(© 2024 The Authors. The Journal of Comparative Neurology published by Wiley Periodicals LLC.)
References: Akter, N., Fukaya, R., Adachi, R., Kawabe, H., & Kuba, H. (2020). Structural and functional refinement of the axon initial segment in avian cochlear nucleus during development. Journal of Neuroscience, 40(35), 6709-6721. https://doi.org/10.1523/JNEUROSCI.3068-19.2020.
Baena, V., Schalek, R. L., Lichtman, J. W., & Terasaki, M. (2019). Serial-section electron microscopy using automated tape-collecting ultramicrotome (ATUM). Methods in Cell Biology, 52, 41-67. https://doi.org/10.1016/bs.mcb.2019.04.004.
Bonetto, G., Kamen, Y., Evans, K. A., & Káradóttir, R. T. (2020). Unraveling myelin plasticity. Frontiers in Cellular Neuroscience, 14, 156. https://doi.org/10.3389/fncel.2020.00156.
Cardona, A., Saalfeld, S., Schindelin, J., Arganda-Carreras, I., Preibisch, S., Longair, M., Tomancak, P., Hartenstein, V., & Douglas, R. J. (2012). TrakEM2 software for neural circuit reconstruction. PLoS One, 7(6), e38011. https://doi.org/10.1371/journal.pone.0038011.
Cohen, C. C. H., Popovic, M. A., Klooster, J., Weil, M. T., Möbius, W., Nave, K. A., & Kole, M. H. P. (2020). Saltatory conduction along myelinated axons involves a periaxonal nanocircuit. Cell, 180, 311-322.e15. https://doi.org/10.1016/j.cell.2019.11.039.
Djannatian, M., Timmler, S., Arends, M., Luckner, M., Weil, M. T., Alexopoulos, I., Snaidero, N., Schmid, B., Misgeld, T., Möbius, W., Schifferer, M., Peles, E., & Simons, M. (2019). Two adhesive systems cooperatively regulate axon ensheathment and myelin growth in the CNS. Nature Communications, 10(1), 4794. https://doi.org/10.1038/s41467-019-12789-z.
Ding, Y., Chen, T., Wang, Q., Yuan, Y., & Hua, T. (2018). Axon initial segment plasticity accompanies enhanced excitation of visual cortical neurons in aged rats. NeuroReport, 29(18), 1537-1543. https://doi.org/10.1097/WNR.0000000000001145.
Dutta, D. J., Woo, D. H., Lee, P. R., Pajevic, S., Bukalo, O., Huffman, W. C., Wake, H., Basser, P. J., SheikhBahaei, S., Lazarevic, V., Smith, J. C., & Fields, R. D. (2018). Regulation of myelin structure and conduction velocity by perinodal astrocytes. Proceedings of the National Academy of Sciences of the United States of America, 115(46), 11832-11837. https://doi.org/10.1073/pnas.1811013115.
Goudriaan, A., Loos, M., Spijker, S., Smit, A. B., & Verheijen, M. H. G. (2020). Genetic variation in CNS myelination and functional brain connectivity in recombinant inbred mice. Cell, 9(9), 2119. https://doi.org/10.3390/cells9092119.
Hayden, M. R., Grant, D. G., Aroor, A., & DeMarco, V. G. (2018). Ultrastructural remodeling of the neurovascular unit in the female diabetic db/db model-Part III: Oligodendrocyte and myelin. Neuroglia, 1(2), 351-367. https://doi.org/10.3390/neuroglia1020021.
Hill, R. A., Li, A. M., & Grutzendler, J. (2018). Lifelong cortical myelin plasticity and age-related degeneration in the live mammalian brain. Nature Neuroscience, 21(5), 683-695. https://doi.org/10.1038/s41593-018-0120-6.
Höfflin, F., Jack, A., Riedel, C., Mack-Bucher, J., Roos, J., Corcelli, C., Schultz, C., Wahle, P., & Engelhardt, M. (2017). Heterogeneity of the axon initial segment in interneurons and pyramidal cells of rodent visual cortex. Frontiers in Cellular Neuroscience, 11, 332. https://doi.org/10.3389/fncel.2017.00332.
Iwakura, A., Uchigashima, M., Miyazaki, T., Yamasaki, M., & Watanabe, M. (2012). Lack of molecular-anatomical evidence for GABAergic influence on axon initial segment of cerebellar Purkinje cells by the pinceau formation. Journal of Neuroscience, 32(27), 9438-9448. https://doi.org/10.1523/JNEUROSCI.1651-12.2012.
Jorstad, A., Nigro, B., Cali, C., Wawrzyniak, M., Fua, P., & Knott, G. (2015). NeuroMorph: A toolset for the morphometric analysis and visualization of 3D models derived from electron microscopy image stacks. Neuroinformatics, 13(1), 83-92. https://doi.org/10.1007/s12021-014-9242-5.
Jorstad, A., Blanc, J., & Knott, G. (2018). NeuroMorph: A software toolset for 3D analysis of neurite morphology and connectivity. Frontiers in Neuroanatomy, 12, 59. https://doi.org/10.3389/fnana.2018.00059.
Kaller, M. S., Lazari, A., Blanco-Duque, C., Sampaio-Baptista, C., & Johansen-Berg, H. (2017). Myelin plasticity and behaviour-Connecting the dots. Current Opinion in Neurobiology, 47, 86-92. https://doi.org/10.1016/j.conb.2017.09.014.
Kasthuri, N., Hayworth, K. J., Berger, D. R., Schalek, R. L., Conchello, J. A., Knowles-Barley, S., Lee, D., Vázquez-Reina, A., Kaynig, V., Jones, T. R., Roberts, M., Morgan, J. L., Tapia, J. C., Seung, H. S., Roncal, W. G., Vogelstein, J. T., Burns, R., Sussman, D. L., Priebe, C. E., … Lichtman, J. W. (2015). Saturated reconstruction of a volume of neocortex. Cell, 162(3), 648-661. https://doi.org/10.1016/j.cell.2015.06.054.
Kerman, B. E., Kim, H. J., Padmanabhan, K., Mei, A., Georges, S., Joens, M. S., Fitzpatrick, J. A., Jappelli, R., Chandross, K. J., August, P., & Gage, F. H. (2015). In vitro myelin formation using embryonic stem cells. Development, 142(12), 2213-2225. https://doi.org/10.1242/dev.116517.
Kuba, H., Ishii, T. M., & Ohmori, H. (2006). Axonal site of spike initiation enhances auditory coincidence detection. Nature, 444(7122), 1069-1072. https://doi.org/10.1038/nature05347.
Kuba, H., Oichi, Y., & Ohmori, H. (2010). Presynaptic activity regulates Na+ channel distribution at the axon initial segment. Nature, 465(7301), 1075-1078. https://doi.org/10.1038/nature09087.
McKenzie, I. A., Ohayon, D., Li, H., de Faria, J. P., Emery, B., Tohyama, K., & Richardson, W. D. (2014). Motor skill learning requires active central myelination. Science, 346(6207), 318-322. https://doi.org/10.1126/science.1254960.
Nakamura, D. S., Lin, Y. H., Khan, D., Gothie, J.-D., Faira, O., Dixon, J. A., McBride, H. M., Antel, J. P., & Kennedy, T. E. (2020). Mitochondrial dynamics and bioenergetics regulated by netrin-1 in oligodendrocytes. Glia, 69, 392-412.
Pan, S., Mayoral, S. R., Choi, H. S., Chan, J. R., & Kheirbek, M. A. (2020). Preservation of a remote fear memory requires new myelin formation. Nature Neuroscience, 23(4), 487-499. https://doi.org/10.1038/s41593-019-0582-1.
Rasband, M. N., & Peles, E. (2021). Mechanisms of node of Ranvier assembly. Nature Reviews Neuroscience, 22(1), 7-20. https://doi.org/10.1038/s41583-020-00406-8.
Savage, J. C., Picard, K., González-Ibáñez, F., & Tremblay, M. È. (2018). A brief history of microglial ultrastructure: Distinctive features, phenotypes, and functions discovered over the past 60 years by electron microscopy. Frontiers in Immunology, 9, 803. https://doi.org/10.3389/fimmu.2018.00803.
Snaidero, N., Möbius, W., Czopka, T., Hekking, L. H., Mathisen, C., Verkleij, D., Goebbels, S., Edgar, J., Merkler, D., Lyons, D. A., Nave, K. A., & Simons, M. (2014). Myelin membrane wrapping of CNS axons by PI(3,4,5)P3-dependent polarized growth at the inner tongue. Cell, 156(1-2), 277-290. https://doi.org/10.1016/j.cell.2013.11.044.
Tapia, J. C., Kasthuri, N., Hayworth, K. J., Schalek, R., Lichtman, J. W., Smith, S. J., & Buchanan, J. (2012). High-contrast en bloc staining of neuronal tissue for field emission scanning electron microscopy. Nature Protocols, 7(2), 193-206. https://doi.org/10.1038/nprot.2011.439.
Terasaki, M. (2018). Axonal endoplasmic reticulum is very narrow. Journal of Cell Science, 131(4), jcs210450. https://doi.org/10.1242/jcs.210450.
Wang, H., Wang, J., Cai, G., Liu, Y., Qu, Y., & Wu, T. (2021). A physical perspective to the inductive function of myelin-A missing piece of neuroscience. Frontiers in Neural Circuits, 14, 562005.
Yamada, R., & Kuba, H. (2016). Structural and functional plasticity at the axon initial segment. Frontiers in Cell Neuroscience, 10, 250. https://doi.org/10.3389/fncel.2016.00250.
معلومات مُعتمدة: Connecticut Science Fund
فهرسة مساهمة: Keywords: astrocyte; axon initial segment; myelin; node of Ranvier
تواريخ الأحداث: Date Created: 20240227 Date Completed: 20240228 Latest Revision: 20240426
رمز التحديث: 20240426
DOI: 10.1002/cne.25574
PMID: 38411251
قاعدة البيانات: MEDLINE
الوصف
تدمد:1096-9861
DOI:10.1002/cne.25574