Electron microscopy of myelin: Structure preservation by high-pressure freezing

Brain Research

Volumn 1641, Issue , 2016, Pages 92-100

  Möbius, Wiebke ^a,b   Nave, Klaus Armin ^a   Werner, Hauke B ^a  

^a MAX PLANCK INSTITUTE OF EXPERIMENTAL MEDICINE   (Germany)

^b Center for Nanoscale Microscopy and Molecular Physiology of the Brain (CNMPB)   (Germany)

Author keywords

Demyelination and remyelination; Earthworm lumbricus terrestris; Leukodystrophy; Mouse; Neuropathy; Oligodendrocyte; Schwann cell; Transmission electron microscopy; Xenopus; Zebrafish

Indexed keywords

ALDEHYDE; MYELIN;

AQUATIC SPECIES; AXON; BIOGENESIS; ELECTRON MICROSCOPY; FREEZE SUBSTITUTION; FREEZING; HIGH PRESSURE FREEZING; INVERTEBRATE; LUMBRICUS TERRESTRIS; MYELINATION; NERVE CONDUCTION; NEUROPATHOLOGY; NONHUMAN; PRESERVATION; PRIORITY JOURNAL; REVIEW; ULTRASTRUCTURE; VENTRAL ROOT; ANIMAL; CRYOPRESERVATION; HUMAN; METABOLISM; MYELIN SHEATH; PROCEDURES;

ANIMALS; CRYOPRESERVATION; HUMANS; MYELIN SHEATH;

EID: 84959287676     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2016.02.027     Document Type: Review

References (78)

1. Ackerman, S.D., Monk, K.R., The scales and tales of myelination: using zebrafish and mouse to study myelinating glia. Brain Res, 2015.
2. Bakhti, M., Snaidero, N., Schneider, D., Aggarwal, S., Mobius, W., Janshoff, A., Eckhardt, M., Nave, K.A., Simons, M., Loss of electrostatic cell-surface repulsion mediates myelin membrane adhesion and compaction in the central nervous system. Proc. Natl. Acad. Sci. USA 110 (2013), 3143–3148.
3. Baraban, M., Mensch, S., Lyons, D.A., Adaptive myelination from fish to man. Brain Res, 2015.
4. Beirowski, B., Babetto, E., Golden, J.P., Chen, Y.J., Yang, K., Gross, R.W., Patti, G.J., Milbrandt, J., Metabolic regulator LKB1 is crucial for Schwann cell-mediated axon maintenance. Nat. Neurosci. 17 (2014), 1351–1361.
5. Birling, M.C., Tait, S., Hardy, R.J., Brophy, P.J., A novel rat tetraspan protein in cells of the oligodendrocyte lineage. J. Neurochem. 73 (1999), 2600–2608.
6. Bizzozero, O.A., Bixler, H.A., Davis, J.D., Espinosa, A., Messier, A.M., Chemical deacylation reduces the adhesive properties of proteolipid protein and leads to decompaction of the myelin sheath. J. Neurochem. 76 (2001), 1129–1141.
7. Brosamle, C., Halpern, M.E., Characterization of myelination in the developing zebrafish. Glia 39 (2002), 47–57.
8. Castelfranco A.M., Hartline D.K., Evolution of rapid nerve conduction, Brain Res. 2016, 10.1016/j.brainres.2016.02.015.
9. Czopka, T., Insights into mechanisms of central nervous system myelination using zebrafish. Glia 64 (2016), 333–349.
10. Czopka, T., Lyons, D.A., Dissecting mechanisms of myelinated axon formation using zebrafish. Methods Cell. Biol. 105 (2011), 25–62.
11. de Bellard, M.E., Myelin in cartilaginous fish. Brain Res, 2016.
12. Davis, A.D., Weatherby, T.M., Hartline, D.K., Lenz, P.H., Myelin-like sheaths in copepod axons. Nature, 398, 1999, 571.
13. Dutta, S., Rieche, F., Eckl, N., Duch, C., Kretzschmar, D., Glial expression of Swiss-cheese (SWS), the Drosophila orthologue of Neuropathy Target Esterase, is required for neuronal ensheathment and function. Dis. Model. Mech, 2015.
14. de Monasterio-Schrader, P., Jahn, O., Tenzer, S., Wichert, S.P., Patzig, J., Werner, H.B., Systematic approaches to central nervous system myelin. Cell. Mol. Life Sci. 69 (2012), 2879–2894.
15. de Monasterio-Schrader, P., Patzig, J., Mobius, W., Barrette, B., Wagner, T.L., Kusch, K., Edgar, J.M., Brophy, P.J., Werner, H.B., Uncoupling of neuroinflammation from axonal degeneration in mice lacking the myelin protein tetraspanin-2. Glia 61 (2013), 1832–1847.
16. Funfschilling, U., Supplie, L.M., Mahad, D., Boretius, S., Saab, A.S., Edgar, J., Brinkmann, B.G., Kassmann, C.M., Tzvetanova, I.D., Mobius, W., et al. Glycolytic oligodendrocytes maintain myelin and long-term axonal integrity. Nature 485 (2012), 517–521.
17. Garrod, D., Chidgey, M., Desmosome structure, composition and function. Biochim. Biophys. Acta 1778 (2008), 572–587.
18. Goebbels, S., Oltrogge, J.H., Kemper, R., Heilmann, I., Bormuth, I., Wolfer, S., Wichert, S.P., Mobius, W., Liu, X., Lappe-Siefke, C., et al. Elevated phosphatidylinositol 3,4,5-trisphosphate in glia triggers cell-autonomous membrane wrapping and myelination. J. Neurosci. 30 (2010), 8953–8964.
19. Gould, R.M., Morrison, H.G., Gilland, E., Campbell, R.K., Myelin tetraspan family proteins but no non-tetraspan family proteins are present in the ascidian (Ciona intestinalis) genome. Biol. Bull. 209 (2005), 49–66.
20. Hartline, D.K., Colman, D.R., Rapid conduction and the evolution of giant axons and myelinated fibers. Curr. Biol. 17 (2007), R29–R35.
21. Hayat, M.A., Principles and Techniques of Electron Microscopy. 2000, Cambridge University Press, Cambridge, UK.
22. Heuser, J.E., Doggenweiler, C.F., The fine structural organization of nerve fibers, sheaths, and glial cells in the prawn, Palaemonetes vulgaris. J. Cell Biol. 30 (1966), 381–403.
23. Hines, J.H., Ravanelli, A.M., Schwindt, R., Scott, E.K., Appel, B., Neuronal activity biases axon selection for myelination in vivo. Nat. Neurosci. 18 (2015), 683–689.
24. Inouye, H., Kirschner, D.A., Evolution of myelin ultrastructure and the major structural myelin proteins. Brain Res, 2015.
25. Ivanovic, A., Horresh, I., Golan, N., Spiegel, I., Sabanay, H., Frechter, S., Ohno, S., Terada, N., Mobius, W., Rosenbluth, J., et al. The cytoskeletal adapter protein 4.1G organizes the internodes in peripheral myelinated nerves. J. Cell Biol. 196 (2012), 337–344.
26. Jahn, O., Tenzer, S., Werner, H.B., Myelin proteomics: molecular anatomy of an insulating sheath. Mol. Neurobiol. 40 (2009), 55–72.
27. Jessen, K.R., Mirsky, R., Arthur-Farraj, P., The role of cell plasticity in tissue repair: adaptive cellular reprogramming. Dev. Cell 34 (2015), 613–620.
28. Kaya, F., Mannioui, A., Chesneau, A., Sekizar, S., Maillard, E., Ballagny, C., Houel-Renault, L., Dupasquier, D., Bronchain, O., Holtzmann, I., et al. Live imaging of targeted cell ablation in Xenopus: a new model to study demyelination and repair. J. Neurosci. 32 (2012), 12885–12895.
29. Kazakova, N., Li, H., Mora, A., Jessen, K.R., Mirsky, R., Richardson, W.D., Smith, H.K., A screen for mutations in zebrafish that affect myelin gene expression in Schwann cells and oligodendrocytes. Dev. Biol. 297 (2006), 1–13.
30. Kitagawa, K., Sinoway, M.P., Yang, C., Gould, R.M., Colman, D.R., A proteolipid protein gene family: expression in sharks and rays and possible evolution from an ancestral gene encoding a pore-forming polypeptide. Neuron 11 (1993), 433–448.
31. Klein, D., Martini, R., Myelin and macrophages in the PNS: an intimate relationship in trauma and disease. Brain Res, 2015.
32. Klugmann, M., Schwab, M.H., Puhlhofer, A., Schneider, A., Zimmermann, F., Griffiths, I.R., Nave, K.A., Assembly of CNS myelin in the absence of proteolipid protein. Neuron 18 (1997), 59–70.
33. Kretzschmar, D., Hasan, G., Sharma, S., Heisenberg, M., Benzer, S., The swiss cheese mutant causes glial hyperwrapping and brain degeneration in Drosophila. J. Neurosci. 17 (1997), 7425–7432.
34. Kuratani, S., Evolution of the vertebrate jaw from developmental perspectives. Evol. Dev. 14 (2012), 76–92.
35. Lappe-Siefke, C., Goebbels, S., Gravel, M., Nicksch, E., Lee, J., Braun, P.E., Griffiths, I.R., Nave, K.A., Disruption of Cnp1 uncouples oligodendroglial functions in axonal support and myelination. Nat. Genet. 33 (2003), 366–374.
36. Lee, J., Gravel, M., Zhang, R., Thibault, P., Braun, P.E., Process outgrowth in oligodendrocytes is mediated by CNP, a novel microtubule assembly myelin protein. J. Cell Biol. 170 (2005), 661–673.
37. Lee, Y., Morrison, B.M., Li, Y., Lengacher, S., Farah, M.H., Hoffman, P.N., Liu, Y., Tsingalia, A., Jin, L., Zhang, P.W., et al. Oligodendroglia metabolically support axons and contribute to neurodegeneration. Nature 487 (2012), 443–448.
38. Lenz, P.H., Hartline, D.K., Davis, A.D., The need for speed. I. Fast reactions and myelinated axons in copepods. J. Comp. Physiol. A 186 (2000), 337–345.
39. Li, H., Richardson, W.D., Evolution of the CNS myelin gene regulatory program. Brain Res, 2015.
40. Möbius, W., Patzig, J., Nave, K.A., Werner, H.B., Phylogeny of proteolipid proteins: divergence, constraints, and the evolution of novel functions in myelination and neuroprotection. Neuron Glia Biol. 4 (2008), 111–127.
41. Möbius, W., Cooper, B., Kaufmann, W.A., Imig, C., Ruhwedel, T., Snaidero, N., Saab, A.S., Varoqueaux, F., Electron microscopy of the mouse central nervous system. Methods Cell. Biol. 96 (2010), 475–512.
42. Magistretti, P.J., Allaman, I., A cellular perspective on brain energy metabolism and functional imaging. Neuron 86 (2015), 883–901.
43. Mensch, S., Baraban, M., Almeida, R., Czopka, T., Ausborn, J., El Manira, A., Lyons, D.A., Synaptic vesicle release regulates myelin sheath number of individual oligodendrocytes in vivo. Nat. Neurosci. 18 (2015), 628–630.
44. Myllykoski, M., Raasakka, A., Han, H., Kursula, P., Myelin 2′,3′-cyclic nucleotide 3′-phosphodiesterase: active-site ligand binding and molecular conformation. PLoS One, 7, 2012, e32336.
45. Myllykoski, M., Seidel, L., Muruganandam, G., Raasakka, A., Torda, A.E., Kursula, P., Structural and functional evolution of 2′,3′-cyclic nucleotide 3′-phosphodiesterase. Brain Res, 2015.
46. Nave, K.A., Werner, H.B., Myelination of the nervous system: mechanisms and functions. Annu. Rev. Cell Dev. Biol. 30 (2014), 503–533.
47. Nawaz, S., Schweitzer, J., Jahn, O., Werner, H.B., Molecular evolution of myelin basic protein, an abundant structural myelin component. Glia 61 (2013), 1364–1377.
48. Patzig, J., Jahn, O., Tenzer, S., Wichert, S.P., de Monasterio-Schrader, P., Rosfa, S., Kuharev, J., Yan, K., Bormuth, I., Bremer, J., et al. Quantitative and integrative proteome analysis of peripheral nerve myelin identifies novel myelin proteins and candidate neuropathy loci. J. Neurosci. 31 (2011), 16369–16386.
49. Patzig, J., Kusch, K., Fledrich, R., Eichel, M.A., Luders, K.A., Mobius, W., Sereda, M.W., Nave, K.A., Martini, R., Werner, H.B., Proteolipid protein modulates preservation of peripheral axons and premature death when myelin protein zero is lacking. Glia 64 (2016), 155–174.
50. Pinzon-Olejua, A., Welte, C., Abdesselem, H., Malaga-Trillo, E., Stuermer, C.A., Essential roles of zebrafish rtn4/Nogo paralogues in embryonic development. Neural Dev., 9, 2014, 8.
51. Pogoda, H.M., Sternheim, N., Lyons, D.A., Diamond, B., Hawkins, T.A., Woods, I.G., Bhatt, D.H., Franzini-Armstrong, C., Dominguez, C., Arana, N., et al. A genetic screen identifies genes essential for development of myelinated axons in zebrafish. Dev. Biol. 298 (2006), 118–131.
52. Preston, M.A., Macklin, W.B., Zebrafish as a model to investigate CNS myelination. Glia 63 (2015), 177–193.
53. Roach, A., Takahashi, N., Pravtcheva, D., Ruddle, F., Hood, L., Chromosomal mapping of mouse myelin basic protein gene and structure and transcription of the partially deleted gene in shiverer mutant mice. Cell 42 (1985), 149–155.
54. Roots, B.I., Lane, N.J., Myelinating glia of earthworm giant axons: thermally induced intramembranous changes. Tissue Cell. 15 (1983), 695–709.
55. Rosenbluth, J., Schiff, R., Lam, P., Effects of osmolality on PLP-null myelin structure: implications re axon damage. Brain Res. 1253 (2009), 191–197.
56. Salzer, J.L., Schwann cell myelination. Cold Spring Harb. Perspect. Biol., 7, 2015, a020529.
57. Saugier-Veber, P., Munnich, A., Bonneau, D., Rozet, J.M., Le Merrer, M., Gil, R., Boespflug-Tanguy, O., X-linked spastic paraplegia and Pelizaeus-Merzbacher disease are allelic disorders at the proteolipid protein locus. Nat. Genet. 6 (1994), 257–262.
58. Schirmeier, S., Matzat, T., Klambt, C., Axon ensheathment and metabolic supply by glial cells in Drosophila. Brain Res, 2015.
59. Schweitzer, J., Becker, T., Schachner, M., Nave, K.A., Werner, H., Evolution of myelin proteolipid proteins: gene duplication in teleosts and expression pattern divergence. Mol. Cell. Neurosci. 31 (2006), 161–177.
60. Sekizar, S., Mannioui, A., Azoyan, L., Colin, C., Thomas, J.L., Du Pasquier, D., Mallat, M., Zalc, B., Remyelination by resident oligodendrocyte precursor cells in a Xenopus laevis inducible model of demyelination. Dev. Neurosci. 37 (2015), 232–242.
61. Shypitsyna, A., Malaga-Trillo, E., Reuter, A., Stuermer, C.A., Origin of Nogo-A by domain shuffling in an early jawed vertebrate. Mol. Biol. Evol. 28 (2011), 1363–1370.
62. Snaidero, N., Mobius, W., Czopka, T., Hekking, L.H., Mathisen, C., Verkleij, D., Goebbels, S., Edgar, J., Merkler, D., Lyons, D.A., et al. Myelin membrane wrapping of CNS axons by PI(3,4,5)P3-dependent polarized growth at the inner tongue. Cell 156 (2014), 277–290.
63. Stolt, C.C., Wegner, M., Schwann cells and their transcriptional network: evolution of key regulators of peripheral myelination. Brain Res, 2015.
64. Suzuki, A., Stern, S.A., Bozdagi, O., Huntley, G.W., Walker, R.H., Magistretti, P.J., Alberini, C.M., Astrocyte-neuron lactate transport is required for long-term memory formation. Cell 144 (2011), 810–823.
65. Verrier, J.D., Jackson, T.C., Gillespie, D.G., Janesko-Feldman, K., Bansal, R., Goebbels, S., Nave, K.A., Kochanek, P.M., Jackson, E.K., Role of CNPase in the oligodendrocytic extracellular 2′,3′-cAMP-adenosine pathway. Glia 61 (2013), 1595–1606.
66. Viader, A., Sasaki, Y., Kim, S., Strickland, A., Workman, C.S., Yang, K., Gross, R.W., Milbrandt, J., Aberrant Schwann cell lipid metabolism linked to mitochondrial deficits leads to axon degeneration and neuropathy. Neuron 77 (2013), 886–898.
67. Volkenhoff, A., Weiler, A., Letzel, M., Stehling, M., Klambt, C., Schirmeier, S., Glial Glycolysis is essential for neuronal survival in Drosophila. Cell Metab. 22 (2015), 437–447.
68. Weber, B., Barros, L.F., The astrocyte: powerhouse and recycling center. Cold Spring Harb. Perspect. Biol., 7, 2015.
69. Werner, H.B., Do we have to reconsider the evolutionary emergence of myelin?. Front. Cell. Neurosci., 7, 2013, 217.
70. Werner, H.B., Kuhlmann, K., Shen, S., Uecker, M., Schardt, A., Dimova, K., Orfaniotou, F., Dhaunchak, A., Brinkmann, B.G., Mobius, W., et al. Proteolipid protein is required for transport of sirtuin 2 into CNS myelin. J. Neurosci. 27 (2007), 7717–7730.
71. Werner, H.B., Kramer-Albers, E.M., Strenzke, N., Saher, G., Tenzer, S., Ohno-Iwashita, Y., de Monasterio-Schrader, P., Mobius, W., Moser, T., Griffiths, I.R., et al. A critical role for the cholesterol-associated proteolipids PLP and M6B in myelination of the central nervous system. Glia 61 (2013), 567–586.
72. Wilson, C.H., Hartline, D.K., Novel organization and development of copepod myelin. ii. nonglial origin. J. Comp. Neurol. 519 (2011), 3281–3305.
73. Xu, K., Terakawa, S., Fenestration nodes and the wide submyelinic space form the basis for the unusually fast impulse conduction of shrimp myelinated axons. J. Exp. Biol. 202 (1999), 1979–1989.
74. Yin, X., Baek, R.C., Kirschner, D.A., Peterson, A., Fujii, Y., Nave, K.A., Macklin, W.B., Trapp, B.D., Evolution of a neuroprotective function of central nervous system myelin. J. Cell Biol. 172 (2006), 469–478.
75. Yoshida, M., Colman, D.R., Parallel evolution and coexpression of the proteolipid proteins and protein zero in vertebrate myelin. Neuron 16 (1996), 1115–1126.
76. Zalc, B., The acquisition of myelin: an evolutionary perspective. Brain Res, 2015.
77. Zalc, B., Goujet, D., Colman, D., The origin of the myelination program in vertebrates. Curr. Biol. 18 (2008), R511–R512.
78. Zeis, T., Enz, L., Schaeren-Wiemers, N., The immunomodulatory oligodendrocyte. Brain Res, 2015.