Remodeling myelination: implications for mechanisms of neural plasticity

One of the most significant paradigm shifts in membrane remodeling is the emerging view that membrane transformation is not exclusively controlled by cytoskeletal rearrangement, but also by biophysical constraints, adhesive forces, membrane curvature and compaction. One of the most exquisite examples of membrane remodeling is myelination. The advent of myelin was instrumental in advancing the nervous system during vertebrate evolution. With more rapid and efficient communication between neurons, faster and more complex computations could be performed in a given time and space. Our knowledge of how myelin-forming oligodendrocytes select and wrap axons has been limited by insufficient spatial and temporal resolution. By virtue of recent technological advances, progress has clarified longstanding controversies in the field. Here we review insights into myelination, from target selection to axon wrapping and membrane compaction, and discuss how understanding these processes has unexpectedly opened new avenues of insight into myelination-centered mechanisms of neural plasticity.

[1]  Yasuzo Tsukada,et al.  Fine structure of the central myelin sheath in the myelin deficient mutant Shiverer mouse, with special reference to the pattern of myelin formation by oligodendroglia , 1981, Brain Research.

[2]  M. Rasband,et al.  Subcellular patterning: axonal domains with specialized structure and function. , 2015, Developmental cell.

[3]  P. Mohler,et al.  A Distal Axonal Cytoskeleton Forms an Intra-Axonal Boundary that Controls Axon Initial Segment Assembly , 2012, Cell.

[4]  D. Görlich,et al.  Myelin Membrane Assembly Is Driven by a Phase Transition of Myelin Basic Proteins Into a Cohesive Protein Meshwork , 2013, PLoS biology.

[5]  C. Lubetzki,et al.  Axon‐oligodendrocyte interactions during developmental myelination, demyelination and repair , 2010, Journal of neurochemistry.

[6]  G. Harauz,et al.  Lateral self-assembly of 18.5-kDa myelin basic protein (MBP) charge component-C1 on membranes. , 2012, Biochimica et biophysica acta.

[7]  Mary Kay Lobo,et al.  Impaired adult myelination in the prefrontal cortex of socially isolated mice , 2012, Nature Neuroscience.

[8]  K. Young,et al.  White matter plasticity in adulthood , 2014, Neuroscience.

[9]  Samuel Bernard,et al.  Dynamics of Oligodendrocyte Generation and Myelination in the Human Brain , 2014, Cell.

[10]  Anatol C. Kreitzer,et al.  Plasticity in gray and white: neuroimaging changes in brain structure during learning , 2012, Nature Neuroscience.

[11]  Edwin W Rubel,et al.  Mechanisms for Adjusting Interaural Time Differences to Achieve Binaural Coincidence Detection , 2010, The Journal of Neuroscience.

[12]  M. Kukley,et al.  Vesicular glutamate release from axons in white matter , 2007, Nature Neuroscience.

[13]  Dwight E Bergles,et al.  Synaptic signaling between GABAergic interneurons and oligodendrocyte precursor cells in the hippocampus , 2004, Nature Neuroscience.

[14]  M. Rasband,et al.  Axon initial segments: diverse and dynamic neuronal compartments , 2014, Current Opinion in Neurobiology.

[15]  Carlos Matute,et al.  Pío del Río Hortega and the discovery of the oligodendrocytes , 2015, Front. Neuroanat..

[16]  D. Bergles,et al.  Vesicular release of glutamate from unmyelinated axons in white matter , 2007, Nature Neuroscience.

[17]  J. Friedrichs,et al.  A size barrier limits protein diffusion at the cell surface to generate lipid-rich myelin-membrane sheets. , 2011, Developmental cell.

[18]  Carmen Birchmeier,et al.  Neuregulin-1/ErbB Signaling Serves Distinct Functions in Myelination of the Peripheral and Central Nervous System , 2008, Neuron.

[19]  K. Nave,et al.  Assembly of CNS Myelin in the Absence of Proteolipid Protein , 1997, Neuron.

[20]  P. J. Basser,et al.  Role of myelin plasticity in oscillations and synchrony of neuronal activity , 2014, Neuroscience.

[21]  G. Harauz,et al.  Structural polymorphism and multifunctionality of myelin basic protein. , 2009, Biochemistry.

[22]  C. Peddie,et al.  Exploring the third dimension: volume electron microscopy comes of age. , 2014, Micron.

[23]  M. Simons,et al.  Actin filament turnover drives leading edge growth during myelin sheath formation in the central nervous system. , 2015, Developmental cell.

[24]  B. Brody,et al.  Sequence of Central Nervous System Myelination in Human Infancy. I. An Autopsy Study of Myelination , 1987, Journal of neuropathology and experimental neurology.

[25]  D. Zilberman,et al.  A Critical Period for Social Experience – Dependent Oligodendrocyte Maturation and Myelination , 2012 .

[26]  D. Foran,et al.  Myelin acquisition in the central nervous system of the mouse revealed by an MBP-Lac Z transgene , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[27]  David Strachan,et al.  Time-Lapse Imaging of the Dynamics of CNS Glial-Axonal Interactions In Vitro and Ex Vivo , 2012, PloS one.

[28]  Rita Gerardy-Schahn,et al.  Sialic acids in the brain: gangliosides and polysialic acid in nervous system development, stability, disease, and regeneration. , 2014, Physiological reviews.

[29]  C. ffrench-Constant,et al.  Individual Oligodendrocytes Have Only a Few Hours in which to Generate New Myelin Sheaths In Vivo , 2013, Developmental cell.

[30]  K. Nave,et al.  Myelination in the Absence of Galactolipids and Proteolipid Proteins , 1999, Molecular and Cellular Neuroscience.

[31]  M. Raff,et al.  Myelin-specific proteins and glycolipids in rat Schwann cells and oligodendrocytes in culture , 1980, The Journal of cell biology.

[32]  P. Somogyi,et al.  Glutamatergic synapses on oligodendrocyte precursor cells in the hippocampus , 2000, Nature.

[33]  William D. Richardson,et al.  Motor skill learning requires active central myelination , 2014, Science.

[34]  T. Chomiak,et al.  What Is the Optimal Value of the g-Ratio for Myelinated Fibers in the Rat CNS? A Theoretical Approach , 2009, PloS one.

[35]  W. Richardson,et al.  NG2-glia as Multipotent Neural Stem Cells: Fact or Fantasy? , 2011, Neuron.

[36]  J. Fraher.  A quantitative study of anterior root fibres during early myelination. II. Longitudinal variation in sheath thickness and axon circumference. , 1973, Journal of anatomy.

[37]  Christopher W Mount,et al.  Neuronal Activity Promotes Oligodendrogenesis and Adaptive Myelination in the Mammalian Brain , 2014, Science.

[38]  Stephen G. Waxman,et al.  Ultrastructure of visual callosal axons in the rabbit , 1976, Experimental Neurology.

[39]  H. Persson,et al.  Myelinated nerve fibres in the CNS , 1993, Progress in Neurobiology.

[40]  S. Waxman.  Determinants of conduction velocity in myelinated nerve fibers , 1980, Muscle & nerve.

[41]  G. Harauz,et al.  The classic basic protein of myelin--conserved structural motifs and the dynamic molecular barcode involved in membrane adhesion and protein-protein interactions. , 2009, Current protein & peptide science.

[42]  K. Nave,et al.  Myelin Membrane Wrapping of CNS Axons by PI(3,4,5)P3-Dependent Polarized Growth at the Inner Tongue , 2014, Cell.

[43]  J. Frahm,et al.  Elevated Phosphatidylinositol 3,4,5-Trisphosphate in Glia Triggers Cell-Autonomous Membrane Wrapping and Myelination , 2010, The Journal of Neuroscience.

[44]  R. Fields,et al.  White matter in learning, cognition and psychiatric disorders , 2008, Trends in Neurosciences.

[45]  M. Simons,et al.  Myelination at a glance , 2014, Journal of Cell Science.

[46]  Klaus-Armin Nave,et al.  Axonal regulation of myelination by neuregulin 1 , 2006, Current Opinion in Neurobiology.

[47]  B. Trapp,et al.  CNP overexpression induces aberrant oligodendrocyte membranes and inhibits MBP accumulation and myelin compaction , 1997, Journal of neuroscience research.

[48]  J. Israelachvili,et al.  Lipid domains control myelin basic protein adsorption and membrane interactions between model myelin lipid bilayers , 2014, Proceedings of the National Academy of Sciences.

[49]  B. Becher,et al.  CNS live imaging reveals a new mechanism of myelination: The liquid croissant model , 2011, Glia.

[50]  M. Rasband,et al.  Excitable domains of myelinated nerves: axon initial segments and nodes of Ranvier. , 2013, Current topics in membranes.

[51]  K. Nave,et al.  Phylogeny of proteolipid proteins: divergence, constraints, and the evolution of novel functions in myelination and neuroprotection. , 2008, Neuron glia biology.

[52]  J. Zuchero,et al.  CNS myelin wrapping is driven by actin disassembly. , 2015, Developmental cell.

[53]  L. Wrabetz,et al.  Signals to promote myelin formation and repair , 2010, Nature Reviews Neurology.

[54]  S. Waxman,et al.  Axon-glia interactions: Building a smart nerve fiber , 1997, Current Biology.

[55]  Ben A. Barres,et al.  Distinct Stages of Myelination Regulated by γ-Secretase and Astrocytes in a Rapidly Myelinating CNS Coculture System , 2008, Neuron.

[56]  H. Webster,et al.  THE GEOMETRY OF PERIPHERAL MYELIN SHEATHS DURING THEIR FORMATION AND GROWTH IN RAT SCIATIC NERVES , 1971, The Journal of cell biology.

[57]  J. Salzer.  Schwann cell myelination. , 2015, Cold Spring Harbor perspectives in biology.

[58]  R. Bunge,et al.  Movements of the Schwann cell nucleus implicate progression of the inner (axon-related) Schwann cell process during myelination , 1989, The Journal of cell biology.

[59]  Peter E. Braun,et al.  Overexpression of 2′,3′-Cyclic Nucleotide 3′-Phosphodiesterase in Transgenic Mice Alters Oligodendrocyte Development and Produces Aberrant Myelination , 1996, Molecular and Cellular Neuroscience.

[60]  J. Fraher.  Quantitative studies on the maturation of central and peripheral parts of individual ventral motoneuron axons. I. Myelin sheath and axon calibre. , 1978, Journal of anatomy.

[61]  D. Hartline,et al.  Rapid Conduction and the Evolution of Giant Axons and Myelinated Fibers , 2007, Current Biology.

[62]  L. Mei,et al.  Neuregulin-ERBB Signaling in the Nervous System and Neuropsychiatric Diseases , 2014, Neuron.

[63]  M. Simons,et al.  The emerging functions of oligodendrocytes in regulating neuronal network behaviour , 2015, BioEssays : news and reviews in molecular, cellular and developmental biology.

[64]  B. B. Geren.  The formation from the schwann cell surfaceof myelin in the peripheral nerves of chick embryos , 1954 .

[65]  Aiman S Saab,et al.  Phosphatidylinositol 4,5-Bisphosphate-Dependent Interaction of Myelin Basic Protein with the Plasma Membrane in Oligodendroglial Cells and Its Rapid Perturbation by Elevated Calcium , 2009, The Journal of Neuroscience.

[66]  G. Harauz,et al.  Human proteolipid protein (PLP) mediates winding and adhesion of phospholipid membranes but prevents their fusion. , 1998, Biochimica et biophysica acta.

[67]  N. Baumann,et al.  Absence of the major dense line in myelin of the mutant mouse ‘shiverer’ , 1979, Neuroscience Letters.

[68]  S. Nelson,et al.  Distinct Profiles of Myelin Distribution Along Single Axons of Pyramidal Neurons in the Neocortex , 2014 .

[69]  S. Tenzer,et al.  Myelin Proteomics: Molecular Anatomy of an Insulating Sheath , 2009, Molecular Neurobiology.

[70]  T. Howard,et al.  Myelin Proteolipid Protein-Induced Aggregation of Lipid Vesicles: Efficacy of the Various Molecular Species , 2002, Neurochemical Research.

[71]  Armin H. Seidl,et al.  Regulation of conduction time along axons , 2014, Neuroscience.

[72]  J. Chan,et al.  The geometric and spatial constraints of the microenvironment induce oligodendrocyte differentiation , 2008, Proceedings of the National Academy of Sciences.

[73]  B. B. Geren,et al.  The formation from the Schwann cell surface of myelin in the peripheral nerves of chick embryos. , 1954, Experimental cell research.

[74]  E. Peles,et al.  The making of a node: a co-production of neurons and glia , 2013, Current Opinion in Neurobiology.

[75]  H. Kinney,et al.  Sequence of Central Nervous System Myelination in Human Infancy. II. Patterns of Myelination in Autopsied Infants , 1988, Journal of neuropathology and experimental neurology.

[76]  R. Virchow.  Ueber das ausgebreitete Vorkommen einer dem Nervenmark analogen Substanz in den thierischen Geweben , 1854, Archiv für pathologische Anatomie und Physiologie und für klinische Medicin.

[77]  W. Möbius,et al.  Electron microscopy of the mouse central nervous system. , 2010, Methods in cell biology.

[78]  C. Babbs,et al.  Subtle Paranodal Injury Slows Impulse Conduction in a Mathematical Model of Myelinated Axons , 2013, PloS one.

[79]  Ethan K. Scott,et al.  Neuronal activity biases axon selection for myelination in vivo , 2015, Nature Neuroscience.

[80]  Michelle K. Leach,et al.  A culture system to study oligodendrocyte myelination-processes using engineered nanofibers , 2012, Nature Methods.

[81]  R. Bunge,et al.  Electron microscopic demonstration of connections between glia and myelin sheaths in the developing mammalian central nervous system. , 1962, The Journal of cell biology.

[82]  S. M. Sumi,et al.  Brain lipid composition of the shiverer mouse: (genetic defect in myelin development) , 1978, Journal of neurochemistry.

[83]  K. Nave,et al.  Loss of electrostatic cell-surface repulsion mediates myelin membrane adhesion and compaction in the central nervous system , 2013, Proceedings of the National Academy of Sciences.

[84]  A. Peters.  FURTHER OBSERVATIONS ON THE STRUCTURE OF MYELIN SHEATHS IN THE CENTRAL NERVOUS SYSTEM , 1964, The Journal of cell biology.

[85]  B. Zalc,et al.  The origin of the myelination program in vertebrates , 2008, Current Biology.

[86]  J. Rosenbluth,et al.  Central myelin in the mouse mutant shiverer , 1980, The Journal of comparative neurology.

[87]  John H. Martin,et al.  Electrical stimulation of the medullary pyramid promotes proliferation and differentiation of oligodendrocyte progenitor cells in the corticospinal tract of the adult rat , 2010, Neuroscience Letters.

[88]  Patrick R Hof,et al.  Functional Trade-Offs in White Matter Axonal Scaling , 2008, The Journal of Neuroscience.