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Abstract

Myelination of axons provides the structural basis for rapid saltatory impulse propagation along vertebrate fiber tracts, a well-established neurophysiological concept. However, myelinating oligodendrocytes and Schwann cells serve additional functions in neuronal energy metabolism that are remarkably similar to those of axon-ensheathing glial cells in unmyelinated invertebrates. Here we discuss myelin evolution and physiological glial functions, beginning with the role of ensheathing glia in preventing ephaptic coupling, axoglial metabolic support, and eliminating oxidative radicals. In both vertebrates and invertebrates, axoglial interactions are bidirectional, serving to regulate cell fate, nerve conduction, and behavioral performance. One key step in the evolution of compact myelin in the vertebrate lineage was the emergence of the open reading frame for myelin basic protein within another gene. Several other proteins were neofunctionalized as myelin constituents and help maintain a healthy nervous system. Myelination in vertebrates became a major prerequisite of inhabiting new ecological niches.

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2021-07-08
2024-04-20
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Literature Cited

  1. Ackerman SD, Monk KR. 2016. The scales and tales of myelination: using zebrafish and mouse to study myelinating glia. Brain Res 1641:79–91
    [Google Scholar]
  2. Aggarwal S, Snaidero N, Pähler G, Frey S, Sánchez P et al. 2013. Myelin membrane assembly is driven by a phase transition of myelin basic proteins into a cohesive protein meshwork. PLOS Biol 11:e1001577
    [Google Scholar]
  3. Ainger K, Avossa D, Morgan F, Hill SJ, Barry C et al. 1993. Transport and localization of exogenous myelin basic protein mRNA microinjected into oligodendrocytes. J. Cell Biol. 123:431–41
    [Google Scholar]
  4. Almeida RG, Lyons DA. 2017. On myelinated axon plasticity and neuronal circuit formation and function. J. Neurosci. 37:10023–34
    [Google Scholar]
  5. Anastassiou CA, Perin R, Markram H, Koch C. 2011. Ephaptic coupling of cortical neurons. Nat. Neurosci. 14:217–23
    [Google Scholar]
  6. Arancibia-Cárcamo IL, Ford MC, Cossell L, Ishida K, Tohyama K, Attwell D. 2017. Node of Ranvier length as a potential regulator of myelinated axon conduction speed. eLife 6:e23329
    [Google Scholar]
  7. Arendt D. 2020. The evolutionary assembly of neuronal machinery. Curr. Biol. 30:R603–16
    [Google Scholar]
  8. Babetto E, Wong KM, Beirowski B. 2020. A glycolytic shift in Schwann cells supports injured axons. Nat. Neurosci. 23:1215–28
    [Google Scholar]
  9. Bailey AP, Koster G, Guillermier C, Hirst EMA, MacRae JI et al. 2015. Antioxidant role for lipid droplets in a stem cell niche of Drosophila. Cell 163:340–53
    [Google Scholar]
  10. Bakhti M, Snaidero N, Schneider D, Aggarwal S, Möbius W et al. 2013. Loss of electrostatic cell-surface repulsion mediates myelin membrane adhesion and compaction in the central nervous system. PNAS 110:3143–48
    [Google Scholar]
  11. Banerjee S, Pillai AM, Paik R, Li J, Bhat MA. 2006. Axonal ensheathment and septate junction formation in the peripheral nervous system of Drosophila. J. Neurosci. 26:3319–29
    [Google Scholar]
  12. Baumgartner S, Littleton JT, Broadie K, Bhat MA, Harbecke R et al. 1996. A Drosophila neurexin is required for septate junction and blood-nerve barrier formation and function. Cell 87:1059–68
    [Google Scholar]
  13. Bergles DE, Richardson WD. 2016. Oligodendrocyte development and plasticity. Cold Spring Harb. Perspect. Biol. 8:a020453
    [Google Scholar]
  14. Bhat MA, Rios JC, Lu Y, Garcia-Fresco GP, Ching W et al. 2001. Axon-glia interactions and the domain organization of myelinated axons requires Neurexin IV/Caspr/Paranodin. Neuron 30:369–83
    [Google Scholar]
  15. Bolzoni F, Jankowska E. 2019. Ephaptic interactions between myelinated nerve fibres of rodent peripheral nerves. Eur. J. Neurosci. 50:3101–7
    [Google Scholar]
  16. Bottelbergs A, Verheijden S, Hulshagen L, Gutmann DH, Goebbels S et al. 2010. Axonal integrity in the absence of functional peroxisomes from projection neurons and astrocytes. Glia 58:1532–43
    [Google Scholar]
  17. Brivio V, Faivre-Sarrailh C, Peles E, Sherman DL, Brophy PJ. 2017. Assembly of CNS nodes of Ranvier in myelinated nerves is promoted by the axon cytoskeleton. Curr. Biol. 27:1068–73
    [Google Scholar]
  18. Bullock TH, Moore JK, Fields RD. 1984. Evolution of myelin sheaths: Both lamprey and hagfish lack myelin. Neurosci. Lett. 48:145–48
    [Google Scholar]
  19. Buscham T, Eichel M, Siems S, Werner H. 2019. Turning to myelin turnover. Neural Regen. Res. 14:2063–66
    [Google Scholar]
  20. Buskey EJ, Strickler JR, Bradley CJ, Hartline DK, Lenz PH. 2017. Escapes in copepods: comparison between myelinate and amyelinate species. J. Exp. Biol. 220:754–58
    [Google Scholar]
  21. Castelfranco AM, Hartline DK. 2016. Evolution of rapid nerve conduction. Brain Res 1641:11–33
    [Google Scholar]
  22. Castelijns B, Baak ML, Timpanaro IS, Wiggers CRM, Vermunt MW et al. 2020. Hominin-specific regulatory elements selectively emerged in oligodendrocytes and are disrupted in autism patients. Nat. Commun. 11:301
    [Google Scholar]
  23. Chung H-L, Wangler MF, Marcogliese PC, Jo J, Ravenscroft TA et al. 2020. Loss- or gain-of-function mutations in ACOX1 cause axonal loss via different mechanisms. Neuron 106:589–606
    [Google Scholar]
  24. Claerhout H, Witters P, Régal L, Jansen K, Van Hoestenberghe MR et al. 2018. Isolated sulfite oxidase deficiency. J. Inherit. Metab. Dis. 41:101–8
    [Google Scholar]
  25. Cohen CCH, Popovic MA, Klooster J, Weil MT, Möbius W et al. 2020. Saltatory conduction along myelinated axons involves a periaxonal nanocircuit. Cell 180:311–22
    [Google Scholar]
  26. Davie K, Janssens J, Koldere D, De Waegeneer M, Pech U et al. 2018. A single-cell transcriptome atlas of the aging Drosophila brain. Cell 174:982–98
    [Google Scholar]
  27. Davis AD, Weatherby TM, Hartline DK, Lenz PH. 1999. Myelin-like sheaths in copepod axons. Nature 398:571
    [Google Scholar]
  28. de Monasterio-Schrader P, Patzig J, Möbius W, Barrette B, Wagner TL et al. 2013. Uncoupling of neuroinflammation from axonal degeneration in mice lacking the myelin protein tetraspanin-2. Glia 61:1832–47
    [Google Scholar]
  29. Doherty J, Logan MA, Taşdemir ÖE, Freeman MR. 2009. Ensheathing glia function as phagocytes in the adult Drosophila brain. J. Neurosci. 29:4768–81
    [Google Scholar]
  30. Edgar JM, McLaughlin M, Werner HB, McCulloch MC, Barrie JA et al. 2009. Early ultrastructural defects of axons and axon-glia junctions in mice lacking expression of Cnp1. Glia 57:1815–24
    [Google Scholar]
  31. Eichel MA, Gargareta VI, D'Este E, Fledrich R, Kungl T et al. 2020. CMTM6 expressed on the adaxonal Schwann cell surface restricts axonal diameters in peripheral nerves. Nat. Commun. 11:4514
    [Google Scholar]
  32. Einheber S, Zanazzi G, Ching W, Scherer S, Milner TA et al. 1997. The axonal membrane protein Caspr, a homologue of Neurexin IV, is a component of the septate-like paranodal junctions that assemble during myelination. J. Cell Biol. 139:1495–506
    [Google Scholar]
  33. Erwig MS, Patzig J, Steyer AM, Dibaj P, Heilmann M et al. 2019. Anillin facilitates septin assembly to prevent pathological outfoldings of central nervous system myelin. eLife 8:e43888
    [Google Scholar]
  34. Fornasiero EF, Mandad S, Wildhagen H, Alevra M, Rammner B et al. 2018. Precisely measured protein lifetimes in the mouse brain reveal differences across tissues and subcellular fractions. Nat. Commun. 9:4230
    [Google Scholar]
  35. Freeman MR. 2015. Drosophila central nervous system glia. Cold Spring Harb. Perspect. Biol. 7:a020552
    [Google Scholar]
  36. Frühbeis C, Kuo-Elsner WP, Müller C, Barth K, Peris L et al. 2020. Oligodendrocytes support axonal transport and maintenance via exosome secretion. PLOS Biol 18:e3000621
    [Google Scholar]
  37. Funch PG, Wood MR, Faber DS. 1984. Localization of active sites along the myelinated goldfish Mauthner axon: morphological and pharmacological evidence for saltatory conduction. J. Neurosci. 4:2397–409
    [Google Scholar]
  38. Fünfschilling U, Supplie LM, Mahad D, Boretius S, Saab AS et al. 2012. Glycolytic oligodendrocytes maintain myelin and long-term axonal integrity. Nature 485:7399517–21
    [Google Scholar]
  39. Garbern JY, Yool DA, Moore GJ, Wilds IB, Faulk MW et al. 2002. Patients lacking the major CNS myelin protein, proteolipid protein 1, develop length-dependent axonal degeneration in the absence of demyelination and inflammation. Brain 125:551–61
    [Google Scholar]
  40. Geren BB, Schmitt FO 1954. The structure of the Schwann cell and its relation to the axon in certain invertebrate nerve fibers. PNAS 40:863–70
    [Google Scholar]
  41. Gómez-Ramos P, Morán MA. 2007. Ultrastructural localization of intraneuronal Aβ-peptide in Alzheimer disease brains. J. Alzheimer's Dis. 11:53–59
    [Google Scholar]
  42. Gordon A, Adamsky K, Vainshtein A, Frechter S, Dupree JL et al. 2014. Caspr and caspr2 are required for both radial and longitudinal organization of myelinated axons. J. Neurosci. 34:14820–26
    [Google Scholar]
  43. Govind CK, Lang F. 1976. Growth of lobster giant axons: correlation between conduction velocity and axon diameter. J. Comp. Neurol. 170:421–33
    [Google Scholar]
  44. Green SA, Bronner ME. 2014. The lamprey: a jawless vertebrate model system for examining origin of the neural crest and other vertebrate traits. Differentiation 87:44–51
    [Google Scholar]
  45. Griffiths I, Klugmann M, Anderson T, Yool D, Thomson C et al. 1998. Axonal swellings and degeneration in mice lacking the major proteolipid of myelin. Science 280:1610–13
    [Google Scholar]
  46. Günther J. 1976. Impulse conduction in the myelinated giant fibers of the earthworm. Structure and function of the dorsal nodes in the median giant fiber. J. Comp. Neurol. 168:505–31
    [Google Scholar]
  47. Hama K. 1959. Some observations on the fine structure of the giant nerve fibers of the earthworm, Eisenia foetida. J. Biophys. Biochem. Cytol. 6:61–66
    [Google Scholar]
  48. Hama K. 1966. The fine structure of the Schwann cell sheath of the nerve fiber in the shrimp (Penaeus japonicus). J. Cell Biol. 31:624–32
    [Google Scholar]
  49. Hartline DK. 2011. The evolutionary origins of glia. Glia 59:1215–36
    [Google Scholar]
  50. Hartline DK, Colman DR. 2007. Rapid conduction and the evolution of giant axons and myelinated fibers. Curr. Biol. 17:1R29–35
    [Google Scholar]
  51. Herbert AL, Fu MM, Drerup CM, Gray RS, Harty BL et al. 2017. Dynein/dynactin is necessary for anterograde transport of Mbp mRNA in oligodendrocytes and for myelination in vivo. PNAS 114:E9153–62
    [Google Scholar]
  52. Heuser JE, Doggenweiler CF. 1966. The fine structural organization of nerve fibers, sheaths, and glial cells in the prawn, Palaemonetes vulgaris. J. Cell Biol. 30:381–403
    [Google Scholar]
  53. Hildebrand C, Bowe CM, Remahl IN. 1994. Myelination and myelin sheath remodelling in normal and pathological PNS nerve fibres. Prog. Neurobiol. 43:85–141
    [Google Scholar]
  54. Hildebrand C, Remahl S, Persson H, Bjartmar C. 1993. Myelinated nerve fibres in the CNS. Prog. Neurobiol. 40:319–84
    [Google Scholar]
  55. Hill AS, Nishino A, Nakajo K, Zhang G, Fineman JR et al. 2008. Ion channel clustering at the axon initial segment and node of Ranvier evolved sequentially in early chordates. PLOS Genet 4:e1000317
    [Google Scholar]
  56. Hodgkin AL. 1954. A note on conduction velocity. J. Physiol. 125:221–24
    [Google Scholar]
  57. Hursh JB. 1939. Conduction velocity and diameter of nerve fibers. Am. J. Physiol. 127:131–39
    [Google Scholar]
  58. Jacobs EC, Pribyl TM, Kampf K, Campagnoni C, Colwell CS et al. 2005. Region-specific myelin pathology in mice lacking the golli products of the myelin basic protein gene. J. Neurosci. 25:7004–13
    [Google Scholar]
  59. Jahn O, Siems SB, Kusch K, Hesse D, Jung RB et al. 2020. The CNS myelin proteome: deep profile and persistence after post-mortem delay. Front. Cell. Neurosci. 14:239
    [Google Scholar]
  60. Kaller MS, Lazari A, Blanco-Duque C, Sampaio-Baptista C, Johansen-Berg H. 2017. Myelin plasticity and behaviour—connecting the dots. Curr. Opin. Neurobiol. 47:86–92
    [Google Scholar]
  61. Kassmann CM, Lappe-Siefke C, Baes M, Brügger B, Mildner A et al. 2007. Axonal loss and neuroinflammation caused by peroxisome-deficient oligodendrocytes. Nat. Genet. 39:969–76
    [Google Scholar]
  62. Kottmeier R, Bittern J, Schoofs A, Scheiwe F, Matzat T et al. 2020. Wrapping glia regulates neuronal signaling speed and precision in the peripheral nervous system of Drosophila. Nat. Commun. 11:4491
    [Google Scholar]
  63. Kretzschmar D, Hasan G, Sharma S, Heisenberg M, Benzer S. 1997. The Swiss cheese mutant causes glial hyperwrapping and brain degeneration in Drosophila. J. Neurosci. 17:7425–32
    [Google Scholar]
  64. Kusano K. 1966. Electrical activity and structural correlates of giant nerve fibers in Kuruma shrimp (Penaeus japonicus). J. Cell. Physiol. 68:361–83
    [Google Scholar]
  65. Laquérriere A, Maluenda J, Camus A, Fontenas L, Dieterich K et al. 2014. Mutations in CNTNAP1 and ADCY6 are responsible for severe arthrogryposis multiplex congenita with axoglial defects. Hum. Mol. Genet. 23:2279–89
    [Google Scholar]
  66. Laval M, Bel C, Faivre-Sarrailh C. 2008. The lateral mobility of cell adhesion molecules is highly restricted at septate junctions in Drosophila. BMC Cell Biol 9:38
    [Google Scholar]
  67. Lee Y, Morrison BM, Li Y, Lengacher S, Farah MH et al. 2012. Oligodendroglia metabolically support axons and contribute to neurodegeneration. Nature 487:7408443–48
    [Google Scholar]
  68. Lee YI, Li Y, Mikesh M, Smith I, Nave KA et al. 2016. Neuregulin1 displayed on motor axons regulates terminal Schwann cell-mediated synapse elimination at developing neuromuscular junctions. PNAS 113:E479–87
    [Google Scholar]
  69. Li F, Sami A, Noristani HN, Slattery K, Qiu J et al. 2020. Glial metabolic rewiring promotes axon regeneration and functional recovery in the central nervous system. Cell Metab 32:767–85.e7
    [Google Scholar]
  70. Li H, Richardson WD. 2016. Evolution of the CNS myelin gene regulatory program. Brain Res 1641:111–21
    [Google Scholar]
  71. Li J. 2015. Molecular regulators of nerve conduction—lessons from inherited neuropathies and rodent genetic models. Exp. Neurol. 267:209–18
    [Google Scholar]
  72. Liu L, MacKenzie KR, Putluri N, Maletić-Savatić M, Bellen HJ. 2017. The glia-neuron lactate shuttle and elevated ROS promote lipid synthesis in neurons and lipid droplet accumulation in glia via APOE/D. Cell Metab 26:719–37
    [Google Scholar]
  73. Liu L, Zhang K, Sandoval H, Yamamoto S, Jaiswal M et al. 2015. Glial lipid droplets and ROS induced by mitochondrial defects promote neurodegeneration. Cell 160:177–90
    [Google Scholar]
  74. Lubetzki C, Sol-Foulon N, Desmazières A. 2020. Nodes of Ranvier during development and repair in the CNS. Nat. Rev. Neurol. 16:426–39
    [Google Scholar]
  75. Lüders KA, Nessler S, Kusch K, Patzig J, Jung RB et al. 2019. Maintenance of high proteolipid protein level in adult central nervous system myelin is required to preserve the integrity of myelin and axons. Glia 67:634–49
    [Google Scholar]
  76. Magistretti PJ, Allaman I. 2015. A cellular perspective on brain energy metabolism and functional imaging. Neuron 86:883–901
    [Google Scholar]
  77. Marie D, Garza P, Nartey CM, Carvunis AR. 2019. Philosophy of biology: the meanings of ‘function’ in biology and the problematic case of de novo gene emergence. eLife 8:e47014
    [Google Scholar]
  78. Marschallinger J, Iram T, Zardeneta M, Lee SE, Lehallier B et al. 2020. Lipid-droplet-accumulating microglia represent a dysfunctional and proinflammatory state in the aging brain. Nat. Neurosci. 23:194–208
    [Google Scholar]
  79. Marshall-Phelps KLH, Kegel L, Baraban M, Ruhwedel T, Almeida RG et al. 2020. Neuronal activity disrupts myelinated axon integrity in the absence of NKCC1b. J. Cell Biol. 219:e201909022
    [Google Scholar]
  80. Martini R, Mohajeri MH, Kasper S, Giese KP, Schachner M. 1995. Mice doubly deficient in the genes for P0 and myelin basic protein show that both proteins contribute to the formation of the major dense line in peripheral nerve myelin. J. Neurosci. 15:4488–95
    [Google Scholar]
  81. Matzat T, Sieglitz F, Kottmeier R, Babatz F, Engelen D, Klämbt C. 2015. Axonal wrapping in the Drosophila PNS is controlled by glia-derived neuregulin homolog Vein. Development 142:1336–45
    [Google Scholar]
  82. Meschkat M, Steyer AM, Weil M-T, Kusch K, Jahn O et al. 2020. White matter integrity requires continuous myelin synthesis at the inner tongue. bioRxiv 2020.09.02.279612. https://doi.org/10.1101/2020.09.02.279612
    [Crossref]
  83. Möbius W, Nave KA, Werner HB. 2016. Electron microscopy of myelin: structure preservation by high-pressure freezing. Brain Res 1641:92–100
    [Google Scholar]
  84. Möbius W, Patzig J, Nave KA, Werner HB. 2008. Phylogeny of proteolipid proteins: divergence, constraints, and the evolution of novel functions in myelination and neuroprotection. Neuron Glia Biol 4:111–27
    [Google Scholar]
  85. Moffett JR, Ross B, Arun P, Madhavarao CN, Namboodiri AMA. 2007. N-acetylaspartate in the CNS: from neurodiagnostics to neurobiology. Prog. Neurobiol. 81:89–131
    [Google Scholar]
  86. Monje M. 2018. Myelin plasticity and nervous system function. Annu. Rev. Neurosci. 41:61–76
    [Google Scholar]
  87. Monk KR, Feltri ML, Taveggia C. 2015. New insights on Schwann cell development. Glia 63:81376–93
    [Google Scholar]
  88. Moore JW, Joyner RW, Brill MH, Waxman SD, Najar-Joa M. 1978. Simulations of conduction in uniform myelinated fibers. Relative sensitivity to changes in nodal and internodal parameters. Biophys. J. 21:147–60
    [Google Scholar]
  89. Morris JK, Willard BB, Yin X, Jeserich G, Kinter M, Trapp BD. 2004. The 36K protein of zebrafish CNS myelin is a short-chain dehydrogenase. Glia 45:378–91
    [Google Scholar]
  90. Mukherjee C, Kling T, Russo B, Miebach K, Kess E et al. 2020. Oligodendrocytes provide antioxidant defense function for neurons by secreting ferritin heavy chain. Cell Metab 32:259–72
    [Google Scholar]
  91. Müller C, Bauer NM, Schäfer I, White R. 2013. Making myelin basic protein—from mRNA transport to localized translation. Front. Cell. Neurosci. 7:169
    [Google Scholar]
  92. Münzel EJ, Schaefer K, Obirei B, Kremmer E, Burton EA et al. 2012. Claudin k is specifically expressed in cells that form myelin during development of the nervous system and regeneration of the optic nerve in adult zebrafish. Glia 60:53–270
    [Google Scholar]
  93. Musse AA, Gao W, Homchaudhuri L, Boggs JM, Harauz G. 2008. Myelin basic protein as a “PI(4,5)P2-modulin”: a new biological function for a major central nervous system protein. Biochemistry 47:10372–82
    [Google Scholar]
  94. Myllykoski M, Seidel L, Muruganandam G, Raasakka A, Torda AE, Kursula P. 2016. Structural and functional evolution of 2′,3′-cyclic nucleotide 3′-phosphodiesterase. Brain Res 1641:64–78
    [Google Scholar]
  95. Nagarajan B, Harder A, Japp A, Häberlein F, Mingardo E et al. 2020. CNS myelin protein 36K regulates oligodendrocyte differentiation through Notch. Glia 68:509–27
    [Google Scholar]
  96. Nave K-A, Lai C, Bloom FE, Milner RJ 1987. Splice site selection in the proteolipid protein (PLP) gene transcript and primary structure of the DM-20 protein of central nervous system myelin. PNAS 84:5665–69
    [Google Scholar]
  97. Nave K-A, Salzer JL. 2006. Axonal regulation of myelination by neuregulin 1. Curr. Opin. Neurobiol. 16:492–500
    [Google Scholar]
  98. Nave K-A, Tzvetanova ID, Schirmeier S. 2017. Glial cell evolution: the origins of a lipid store. Cell Metab 26:701–2
    [Google Scholar]
  99. Nave K-A, Werner HB. 2014. Myelination of the nervous system: mechanisms and functions. Annu. Rev. Cell Dev. Biol. 30:503–33
    [Google Scholar]
  100. Nawaz S, Kippert A, Saab AS, Werner HB, Lang T et al. 2009. Phosphatidylinositol 4,5-bisphosphate-dependent interaction of myelin basic protein with the plasma membrane in oligodendroglial cells and its rapid perturbation by elevated calcium. J. Neurosci. 29:4794–807
    [Google Scholar]
  101. Nawaz S, Schweitzer J, Jahn O, Werner HB. 2013. Molecular evolution of myelin basic protein, an abundant structural myelin component. Glia 61:81364–77
    [Google Scholar]
  102. Neusch C, Papadopoulos N, Müller M, Maletzki I, Winter SM et al. 2006. Lack of the Kir4.1 channel subunit abolishes K+ buffering properties of astrocytes in the ventral respiratory group: impact on extracellular K+ regulation. J. Neurophysiol. 95:1843–52
    [Google Scholar]
  103. Neusch C, Rozengurt N, Jacobs RE, Lester HA, Kofuji P. 2001. Kir4.1 potassium channel subunit is crucial for oligodendrocyte development and in vivo myelination. J. Neurosci. 21:5429–38
    [Google Scholar]
  104. Ortega A, Olivares-Bañuelos TN. 2020. Neurons and glia cells in marine invertebrates: an update. Front. Neurosci. 14:121
    [Google Scholar]
  105. Otto N, Marelja Z, Schoofs A, Kranenburg H, Bittern J et al. 2018. The sulfite oxidase Shopper controls neuronal activity by regulating glutamate homeostasis in Drosophila ensheathing glia. Nat. Commun. 9:3514
    [Google Scholar]
  106. Pannese E. 2015. Neurocytology: Fine Structure of Neurons, Nerve Processes, and Neuroglial Cells Cham, Switz: Springer
  107. Patzig J, Erwig MS, Tenzer S, Kusch K, Dibaj P et al. 2016a. Septin/anillin filaments scaffold central nervous system myelin to accelerate nerve conduction. eLife 5:e17119
    [Google Scholar]
  108. Patzig J, Kusch K, Fledrich R, Eichel MA, Lüders KA et al. 2016b. Proteolipid protein modulates preservation of peripheral axons and premature death when myelin protein zero is lacking. Glia 64:1155–74
    [Google Scholar]
  109. Peles E, Joho K, Plowman GD, Schlessinger J. 1997. Close similarity between Drosophila neurexin IV and mammalian Caspr protein suggests a conserved mechanism for cellular interactions. Cell 88:745–46
    [Google Scholar]
  110. Ponath G, Ramanan S, Mubarak M, Housley W, Lee S et al. 2017. Myelin phagocytosis by astrocytes after myelin damage promotes lesion pathology. Brain 140:399–413
    [Google Scholar]
  111. Popko B, Puckett C, Lai E, Shine HD, Readhead C et al. 1987. Myelin deficient mice: expression of myelin basic protein and generation of mice with varying levels of myelin. Cell 48:713–21
    [Google Scholar]
  112. Pribyl TM, Campagnoni CW, Kampf K, Kashima T, Handley VW et al. 1993. The human myelin basic protein gene is included within a 179-kilobase transcription unit: expression in the immune and central nervous systems. PNAS 90:10695–99
    [Google Scholar]
  113. Pumphrey RJ, Young JZ. 1938. The rates of conduction of nerve fibres of various diameters in cephalopods. J. Exp. Biol. 15:453–66
    [Google Scholar]
  114. Querol L, Nogales-Gadea G, Rojas-Garcia R, Martinez-Hernandez E, Diaz-Manera J et al. 2013. Antibodies to contactin-1 in chronic inflammatory demyelinating polyneuropathy. Ann. Neurol. 73:370–80
    [Google Scholar]
  115. Rainier S, Bui M, Mark E, Thomas D, Tokarz D et al. 2008. Neuropathy target esterase gene mutations cause motor neuron disease. Am. J. Hum. Genet. 82:780–85
    [Google Scholar]
  116. Rovainen CM. 1967. Physiological and anatomical studies on large neurons of central nervous system of the sea lamprey (Petromyzon marinus). I. Müller and Mauthner cells. J. Neurophysiol. 30:1000–23
    [Google Scholar]
  117. Rushton WAH. 1951. A theory of the effects of fibre size in medullated nerve. J. Physiol. 115:101–22
    [Google Scholar]
  118. Saab AS, Tzvetavona ID, Trevisiol A, Baltan S, Dibaj P et al. 2016. Oligodendroglial NMDA receptors regulate glucose import and axonal energy metabolism. Neuron 91:119–32
    [Google Scholar]
  119. Saavedra RA, Lipson A, Kimbro KS, Ljubetic C. 1993. The structural complexities of the myelin basic protein gene from mouse are also present in shark. J. Mol. Neurosci. 4:215–23
    [Google Scholar]
  120. Safaiyan S, Kannaiyan N, Snaidero N, Brioschi S, Biber K et al. 2016. Age-related myelin degradation burdens the clearance function of microglia during aging. Nat. Neurosci. 19:995–98
    [Google Scholar]
  121. Schaefer K, Brösamle C. 2009. Zwilling-A and -B, two related myelin proteins of teleosts, which originate from a single bicistronic transcript. Mol. Biol. Evol. 26:495–99
    [Google Scholar]
  122. Schmidt H, Knösche TR. 2019. Action potential propagation and synchronisation in myelinated axons. PLOS Comput. Biol. 15:e1007004
    [Google Scholar]
  123. Schultz R, Berkowitz EC, Pease DC. 1956. The electron microscopy of the lamprey spinal cord. J. Morphol. 98:251–73
    [Google Scholar]
  124. Schweitzer J, Becker T, Becker CG, Schachner M. 2003. Expression of protein zero is increased in lesioned axon pathways in the central nervous system of adult zebrafish. Glia 41:301–17
    [Google Scholar]
  125. Schweitzer J, Becker T, Schachner M, Nave KA, Werner H. 2006. Evolution of myelin proteolipid proteins: gene duplication in teleosts and expression pattern divergence. Mol. Cell. Neurosci. 31:161–77
    [Google Scholar]
  126. Sheng L, Shields EJ, Gospocic J, Glastad KM, Ratchasanmuang P et al. 2020. Social reprogramming in ants induces longevity-associated glia remodeling. Sci. Adv. 6:eaba9869
    [Google Scholar]
  127. Sherman DL, Krols M, Wu LMN, Grove M, Nave KA et al. 2012. Arrest of myelination and reduced axon growth when Schwann cells lack mTOR. J. Neurosci. 32:1817–25
    [Google Scholar]
  128. Siems SB, Jahn O, Eichel MA, Kannaiyan N, Wu LMN et al. 2020. Proteome profile of peripheral myelin in healthy mice and in a neuropathy model. eLife 9:e51406
    [Google Scholar]
  129. Sies H, Jones DP. 2020. Reactive oxygen species (ROS) as pleiotropic physiological signalling agents. Nat. Rev. Mol. Cell Biol. 21:363–83
    [Google Scholar]
  130. Singhvi A, Shaham S. 2019. Glia-neuron interactions in Caenorhabditis elegans. Annu. Rev. Neurosci. 42:149–68
    [Google Scholar]
  131. Snaidero N, Simons M. 2017. The logistics of myelin biogenesis in the central nervous system. Glia 65:71021–31
    [Google Scholar]
  132. Stassart RM, Fledrich R, Velanac V, Brinkmann BG, Schwab MH et al. 2013. A role for Schwann cell-derived neuregulin-1 in remyelination. Nat. Neurosci. 16:48–54
    [Google Scholar]
  133. Stoll G, Griffin JW, Li CY, Trapp BD. 1989. Wallerian degeneration in the peripheral nervous system: participation of both Schwann cells and macrophages in myelin degradation. J. Neurocytol. 18:671–83
    [Google Scholar]
  134. Stolt CC, Wegner M. 2016. Schwann cells and their transcriptional network: evolution of key regulators of peripheral myelination. Brain Res 1641:101–10
    [Google Scholar]
  135. Stout RF, Verkhratsky A, Parpura V. 2014. Caenorhabditis elegans glia modulate neuronal activity and behavior. Front. Cell. Neurosci. 8:67
    [Google Scholar]
  136. Sturrock RR. 1980. A comparative quantitative and morphological study of ageing in the mouse neostriatum, indusium griseum and anterior commissure. Neuropathol. Appl. Neurobiol. 6:51–68
    [Google Scholar]
  137. Sunderhaus ER, Law AD, Kretzschmar D. 2019. Disease-associated PNPLA6 mutations maintain partial functions when analyzed in Drosophila. Front. Neurosci. 13:1207
    [Google Scholar]
  138. Suzuki A, Stern SA, Bozdagi O, Huntley GW, Walker RH et al. 2011. Astrocyte-neuron lactate transport is required for long-term memory formation. Cell 144:810–23
    [Google Scholar]
  139. Tanaka M. 2013. Molecular and evolutionary basis of limb field specification and limb initiation. Dev. Growth Differ. 55:149–63
    [Google Scholar]
  140. Tasaki I. 1939. The electro-saltatory transmission of the nerve impulse and the effect of narcosis upon the nerve fiber. Am. J. Physiol. Content. 127:211–27
    [Google Scholar]
  141. Tasaki I. 2007. Saltatory conduction. Scholarpedia 2:63354
    [Google Scholar]
  142. Terada N, Saitoh Y, Kamijo A, Yamauchi J, Ohno N, Sakamoto T. 2019. Structures and molecular composition of Schmidt-Lanterman incisures. Adv. Exp. Med. Biol. 1190:181–98
    [Google Scholar]
  143. Thakurela S, Garding A, Jung RB, Müller C, Goebbels S et al. 2016. The transcriptome of mouse central nervous system myelin. Sci. Rep. 6:125828
    [Google Scholar]
  144. Toyama BH, Savas JN, Park SK, Harris MS, Ingolia NT et al. 2013. Identification of long-lived proteins reveals exceptional stability of essential cellular structures. Cell 154:971–82
    [Google Scholar]
  145. Vallat JM, Nizon M, Magee A, Isidor B, Magy L et al. 2016. Contactin-associated protein 1 (CNTNAP1) mutations induce characteristic lesions of the paranodal region. J. Neuropathol. Exp. Neurol. 75:1155–59
    [Google Scholar]
  146. Varoqueaux F, Fasshauer D. 2017. Getting nervous: an evolutionary overhaul for communication. Annu. Rev. Genet. 51:455–76
    [Google Scholar]
  147. Verkhratsky A, Ho MS, Parpura V. 2019. Evolution of neuroglia. Adv. Exp. Med. Biol. 1175:15–44
    [Google Scholar]
  148. Volkenhoff A, Weiler A, Letzel M, Stehling M, Klämbt C, Schirmeier S. 2015. Glial glycolysis is essential for neuronal survival in Drosophila. Cell Metab 22:437–47
    [Google Scholar]
  149. Waehneldt TV. 1990. Phylogeny of myelin proteins. Ann. N. Y. Acad. Sci. 605:15–28
    [Google Scholar]
  150. Wan R, Cheli V, Santiago-González D, Rosenblum S, Wan Q, Paez P 2020. Impaired postnatal myelination in a conditional knock-out mouse for the ferritin heavy chain in oligodendroglial cells. J. Neurosci. 40:7609–24
    [Google Scholar]
  151. Wang E, Dimova N, Sperle K, Huang Z, Lock L et al. 2008. Deletion of a splicing enhancer disrupts PLP1/DM20 ratio and myelin stability. Exp. Neurol. 214:322–30
    [Google Scholar]
  152. Weil M-T, Heibeck S, Töpperwien M, Tom Dieck S, Ruhwedel T et al. 2018. Axonal ensheathment in the nervous system of lamprey: implications for the evolution of myelinating glia. J. Neurosci. 38:296586–96
    [Google Scholar]
  153. Werner HB. 2013. Do we have to reconsider the evolutionary emergence of myelin?. Front. Cell. Neurosci. 7:217
    [Google Scholar]
  154. Werner HB, Krämer-Albers EM, Strenzke N, Saher G, Tenzer S et al. 2013. A critical role for the cholesterol-associated proteolipids PLP and M6B in myelination of the central nervous system. Glia 61:567–86
    [Google Scholar]
  155. Wilson CH, Hartline DK. 2011. Novel organization and development of copepod myelin. II. Nonglial origin. J. Comp. Neurol. 519:3281–305
    [Google Scholar]
  156. Wu LMN, Williams A, Delaney A, Sherman DL, Brophy PJ. 2012. Increasing internodal distance in myelinated nerves accelerates nerve conduction to a flat maximum. Curr. Biol. 22:1957–61
    [Google Scholar]
  157. Xu K, Terakawa S. 1999. Fenestration nodes and the wide submyelinic space form the basis for the unusually fast impulse conduction of shrimp myelinated axons. J. Exp. Biol. 202:1979–89
    [Google Scholar]
  158. Yasargil GM, Greeff NG, Luescher HR, Akert K, Sandri C. 1982. The structural correlate of saltatory conduction along the Mauthner axon in the tench (Tinea tinea L.): identification of nodal equivalents at the axon collaterals. J. Comp. Neurol. 212:417–24
    [Google Scholar]
  159. Yergert KM, O'Rouke R, Hines JH, Appel B. 2020. Identification of 3′ UTR motifs required for mRNA localization to myelin sheaths in vivo. bioRxiv 654616. https://doi.org/10.1101/654616
    [Crossref]
  160. Yeung MSY, Zdunek S, Bergmann O, Bernard S, Salehpour M et al. 2014. Dynamics of oligodendrocyte generation and myelination in the human brain. Cell 159:766–74
    [Google Scholar]
  161. Yildirim K, Petri J, Kottmeier R, Klämbt C. 2019. Drosophila glia: few cell types and many conserved functions. Glia 67:5–26
    [Google Scholar]
  162. Yin X, Baek RC, Kirschner DA, Peterson A, Fujii Y et al. 2006. Evolution of a neuroprotective function of central nervous system myelin. J. Cell Biol. 172:469–78
    [Google Scholar]
  163. Yin X, Crawford TO, Griffin JW, Tu PH, Lee VMY et al. 1998. Myelin-associated glycoprotein is a myelin signal that modulates the caliber of myelinated axons. J. Neurosci. 18:1953–62
    [Google Scholar]
  164. Yool D, Montague P, McLaughlin M, McCulloch MC, Edgar JM et al. 2002. Phenotypic analysis of mice deficient in the major myelin protein MOBP, and evidence for a novel Mobp isoform. Glia 39:256–67
    [Google Scholar]
  165. Yoshida M, Colman DR. 1996. Parallel evolution and coexpression of the proteolipid proteins and protein zero in vertebrate myelin. Neuron 16:1115–26
    [Google Scholar]
  166. Yoshikawa F, Sato Y, Tohyama K, Akagi T, Furuse T et al. 2016. Mammalian-specific central myelin protein opalin is redundant for normal myelination: structural and behavioral assessments. PLOS ONE 11:e0166732
    [Google Scholar]
  167. Zakon HH. 2012. Adaptive evolution of voltage-gated sodium channels: the first 800 million years. PNAS 109:10619–25
    [Google Scholar]
  168. Zalc B, Colman DR. 2000. Origins of vertebrate success. Science 288:271–72
    [Google Scholar]
  169. Zalc B, Goujet D, Colman D. 2008. The origin of the myelination program in vertebrates. Curr. Biol. 18:R511–12
    [Google Scholar]
  170. Zeis T, Enz L, Schaeren-Wiemers N. 2016. The immunomodulatory oligodendrocyte. Brain Res 1641:139–48
    [Google Scholar]
  171. Zeisel A, Muñoz-Manchado AB, Codeluppi S, Lönnerberg P, La Manno G et al. 2015. Cell types in the mouse cortex and hippocampus revealed by single-cell RNA-seq. Science 347:1138–42
    [Google Scholar]
  172. Zhang Y, Chen K, Sloan SA, Bennett ML, Scholze AR et al. 2014. An RNA-sequencing transcriptome and splicing database of glia, neurons, and vascular cells of the cerebral cortex. J. Neurosci. 34:3611929–47
    [Google Scholar]
  173. Zhou T, Zheng Y, Sun L, Badea SR, Jin Y et al. 2019. Microvascular endothelial cells engulf myelin debris and promote macrophage recruitment and fibrosis after neural injury. Nat. Neurosci. 22:421–35
    [Google Scholar]
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