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Phylogeny of proteolipid proteins: divergence, constraints, and the evolution of novel functions in myelination and neuroprotection

Published online by Cambridge University Press:  05 June 2009

Wiebke Möbius ,
Julia Patzig ,
Klaus-Armin Nave  and
Hauke B. Werner
Wiebke Möbius
Affiliation:
Department of Neurogenetics, Max-Planck Institute of Experimental Medicine, Göttingen, Germany
Julia Patzig
Affiliation:
Department of Neurogenetics, Max-Planck Institute of Experimental Medicine, Göttingen, Germany
Klaus-Armin Nave
Affiliation:
Department of Neurogenetics, Max-Planck Institute of Experimental Medicine, Göttingen, Germany
Hauke B. Werner*
Affiliation:
Department of Neurogenetics, Max-Planck Institute of Experimental Medicine, Göttingen, Germany
*
Correspondence should be addressed to: Hauke B. Werner, Department of Neurogenetics, Max-Planck Institute of Experimental Medicine, Hermann-Rein-Str. 3, D-37075 Goettingen, Germany phone: ++49551 389-9759 fax: ++49 551 389-9758 email: hauke@em.mpg.de
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Abstract

The protein composition of myelin in the central nervous system (CNS) has changed at the evolutionary transition from fish to tetrapods, when a lipid-associated transmembrane-tetraspan (proteolipid protein, PLP) replaced an adhesion protein of the immunoglobulin superfamily (P0) as the most abundant constituent. Here, we review major steps of proteolipid evolution. Three paralog proteolipids (PLP/DM20/DMα, M6B/DMγ and the neuronal glycoprotein M6A/DMβ) exist in vertebrates from cartilaginous fish to mammals, and one (M6/CG7540) can be traced in invertebrate bilaterians including the planktonic copepod Calanus finmarchicus that possess a functional myelin equivalent. In fish, DMα and DMγ are coexpressed in oligodendrocytes but are not major myelin components. PLP emerged at the root of tetrapods by the acquisition of an enlarged cytoplasmic loop in the evolutionary older DMα/DM20. Transgenic experiments in mice suggest that this loop enhances the incorporation of PLP into myelin. The evolutionary recruitment of PLP as the major myelin protein provided oligodendrocytes with the competence to support long-term axonal integrity. We suggest that the molecular shift from P0 to PLP also correlates with the concentration of adhesive forces at the radial component, and that the new balance between membrane adhesion and dynamics was favorable for CNS myelination.

Keywords

MyelinoligodendrocyteSchmidt–Lanterman incisurePelizaeus-Merzbacher diseasespastic paraplegianeurite outgrowthPLP/DM20M6OSP/claudin-11P0/MPZ
Type
Research Article
Information
Neuron Glia Biology , Volume 4 , Issue 2 , May 2008 , pp. 111 - 127
Copyright
Copyright © Cambridge University Press 2009

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References

REFERENCES

Alfonso, J., Fernández, M.E., Cooper, B., Flugge, G. and Frasch, A.C. (2005) The stress-regulated protein M6a is a key modulator for neurite outgrowth and filopodium/spine formation. Proceedings of the National Academy of Sciences of the U.S.A. 102, 17196–17201.Google Scholar
Alfonso, J., Frick, L.R., Silberman, D.M., Palumbo, M.L., Genaro, A.M. and Frasch, A.C. (2006) Regulation of hippocampal gene expression is conserved in two species subjected to different stressors and antidepressant treatments. Biological Psychiatry 59, 244–251.CrossRefGoogle ScholarPubMed
Alfonso, J., Pollevick, G.D., Van Der Hart, M.G., Flügge, G., Fuchs, E. and Frasch, A.C. (2004) Identification of genes regulated by chronic psychosocial stress and antidepressant treatment in the hippocampus. European Journal of Neuroscience 19, 659–666.Google Scholar
Arroyo, E.J. and Scherer, S.S. (2000) On the molecular architecture of myelinated fibers. Histochemistry and Cell Biology 113, 1–18.CrossRefGoogle ScholarPubMed
Avila, R.L., Tevlin, B.R., Lees, J.P., Inouye, H. and Kirschner, D.A. (2007) Myelin structure and composition in zebrafish. Neurochemical Research 32, 197–209.CrossRefGoogle ScholarPubMed
Banik, N.L. and Smith, M.E. (1977) Protein determinants of myelination in different regions of developing rat central nervous system. Biochemical Journal 162, 247–255.CrossRefGoogle ScholarPubMed
Baumrind, N.L., Parkinson, D., Wayne, D.B., Heuser, J.E. and Pearlman, A.L. (1992) EMA: a developmentally regulated cell-surface glycoprotein of CNS neurons that is concentrated at the leading edge of growth cones. Developmental Dynamics 194, 311–325.CrossRefGoogle Scholar
Berndt, J.A., Kim, J.G., Tosic, M., Kim, C. and Hudson, L.D. (2001) The transcriptional regulator Yin Yang 1 activates the myelin PLP gene. Journal of Neurochemistry 77, 935–942.Google Scholar
Bifulco, M., Laezza, C., Stingo, S. and Wolff, J. (2002) 2′,3′-Cyclic nucleotide 3′-phosphodiesterase: a membrane-bound, microtubule-associated protein and membrane anchor for tubulin. Proceedings of the National Academy of Sciences of the U.S.A. 99, 1807–1812.CrossRefGoogle ScholarPubMed
Bischoff, A. and Moor, H. (1967) Ultrastructural differences between the myelin sheaths of peripheral nerve fibres and CNS white matter. Zeitschrift für Zellforschung und Mikroskopische Anatomie 81, 303–310.CrossRefGoogle ScholarPubMed
Bizzozero, O.A., Bixler, H.A., Davis, J.D., Espinosa, A. and Messier, A.M. (2001) Chemical deacylation reduces the adhesive properties of proteolipid protein and leads to decompaction of the myelin sheath. Journal of Neurochemistry 76, 1129–1141.Google Scholar
Blair, J.E. and Hedges, S.B. (2005) Molecular phylogeny and divergence times of deuterostome animals. Molecular Biology and Evolution 22, 2275–2284.Google Scholar
Boggs, J.M. (2006) Myelin basic protein: a multifunctional protein. Cellular and Molecular Life Sciences 63, 1945–1961.CrossRefGoogle ScholarPubMed
Boison, D. and Stoffel, W. (1989) Myelin-deficient rat: a point mutation in exon III (A-C, Thr75-Pro) of the myelin proteolipid protein causes dysmyelination and oligodendrocyte death. EMBO Journal 8, 3295–3302.CrossRefGoogle Scholar
Boison, D. and Stoffel, W. (1994) Disruption of the compacted myelin sheath of axons of the central nervous system in proteolipid protein-deficient mice. Proceedings of the National Academy of Sciences of the U.S.A. 91, 11709–11713.Google Scholar
Boks, M.P., Hoogendoorn, M., Jungerius, B.J., Bakker, S.C., Sommer, I.E., Sinke, R.J. et al. (2008) Do mood symptoms subdivide the schizophrenia phenotype? Association of the GMP6A gene with a depression subgroup. American Journal of Medical Genetics 147B, 707–711.Google Scholar
Bonnet-Dupeyron, M.N., Combes, P., Santander, P., Cailloux, F., Boespflug-Tanguy, O. and Vaurs-Barrière, C. (2008) PLP1 splicing abnormalities identified in Pelizaeus-Merzbacher disease and SPG2 fibroblasts are associated with different types of mutations. Human Mutation 29, 1028–1036.CrossRefGoogle ScholarPubMed
Brophy, P.J., Horváth, L.I. and Marsh, D. (1984) Stoichiometry and specificity of lipid-protein interaction with myelin proteolipid protein studied by spin-label electron spin resonance. Biochemistry 23, 860–865.CrossRefGoogle ScholarPubMed
Brösamle, C. and Halpern, M.E. (2002) Characterization of myelination in the developing zebrafish. Glia 39, 47–57.Google Scholar
Casari, G. and Rugarli, E. (2001) Molecular basis of inherited spastic paraplegias. Current Opinion in Genetics and Development 11, 336–342.CrossRefGoogle ScholarPubMed
Celio, M.R. (1976) The Schmidt-Lantermann incisures of the myelin sheath of Mauthner axons: site of longitudinal myelin growth. Brain Research 108, 221–235.CrossRefGoogle ScholarPubMed
Combes, P., Bonnet-Dupeyron, M.N., Gauthier-Barichard, F., Schiffmann, R., Bertini, E., Rodriguez, D. et al. (2006) PLP1 and GPM6B intragenic copy number analysis by MAPH in 262 patients with hypomyelinating leukodystrophies: identification of one partial triplication and two partial deletions of PLP1. Neurogenetics 7, 31–37.Google Scholar
Cooper, B., Werner, H.B. and Flügge, G. (2008) Glycoprotein M6a is present in glutamatergic axons in adult rat forebrain and cerebellum. Brain Research 1197, 1–12.Google Scholar
Corcoran, C., Walker, E., Huot, R., Mittal, V., Tessner, K. Kestler, L. et al. (2003) The stress cascade and schizophrenia: etiology and onset. Schizophrenia Bulletin 29, 671–692.Google Scholar
D'Antonio, M., Michalovich, D., Paterson, M., Droggiti, A., Woodhoo, A., Mirsky, R. et al. (2006) Gene profiling and bioinformatic analysis of Schwann cell embryonic development and myelination. Glia 53, 501–515.Google Scholar
D'Urso, D., Brophy, P.J., Staugaitis, S.M., Gillespie, C.S., Frey, A.B., Stempak, J.G. et al. (1990) Protein zero of peripheral nerve myelin: biosynthesis, membrane insertion, and evidence for homotypic interaction. Neuron 4, 449–460.CrossRefGoogle ScholarPubMed
Davis, A.D., Weatherby, T.M., Hartline, D.K. and Lenz, P.H. (1999) Myelin-like sheaths in copepod axons. Nature 398, 571.Google Scholar
Deber, C.M. and Reynolds, S.J. (1991) Central nervous system myelin: structure, function, and pathology. Clinical Biochemistry 24, 113–134.Google Scholar
De Cózar, M., Lucas, M. and Monreal, J. (1987) Ionophoric properties of the proteolipid apoprotein from bovine brain myelin. International Journal of Biochemistry 14, 833–841.Google Scholar
Dehal, P. and Boore, J.L. (2005) Two rounds of whole genome duplication in the ancestral vertebrate. PLoS Biology 3, e314.Google Scholar
Dermietzel, R. (1974) Junctions in the central nervous system of the cat. I. Membrane fusion in central myelin. Cell and Tissue Research 148, 565–576.CrossRefGoogle ScholarPubMed
Devaux, J. and Gow, A. (2008) Tight junctions potentiate the insulative properties of small CNS myelinated axons. Journal of Cell Biology 183, 909–921.Google Scholar
Dhaunchak, A.S. and Nave, K.A. (2007) A common mechanism of PLP/DM20 misfolding causes cysteine-mediated endoplasmic reticulum retention in oligodendrocytes and Pelizaeus-Merzbacher disease. Proceedings of the National Academy of Sciences of the U.S.A. 104, 17813–17818.Google Scholar
Díaz, R.S., Monreal, J. and Lucas, M. (1990) Calcium movements mediated by proteolipid protein and nucleotides in liposomes prepared with the endogenous lipids from brain white matter. Journal of Neurochemistry 55, 1304–1309.Google Scholar
Dobretsova, A., Johnson, J.W., Jones, R.C., Edmondson, R.D. and Wight, P.A. (2008) Proteomic analysis of nuclear factors binding to an intronic enhancer in the myelin proteolipid protein gene. Journal of Neurochemistry 105, 1979–1995.CrossRefGoogle Scholar
Dugas, J.C., Tai, Y.C., Speed, T.P., Ngai, J. and Barres, B.A. (2006) Functional genomic analysis of oligodendrocyte differentiation. Journal of Neuroscience 26, 10967–10983.CrossRefGoogle ScholarPubMed
Duncan, I.D. (2005) The PLP mutants from mouse to man. Journal of the Neurological Sciences 228, 204–205.Google Scholar
Duncan, I.D., Hammang, J.P., and Trapp, B.D. (1987) Abnormal compact myelin in the myelin-deficient rat: absence of proteolipid protein correlates with a defect in the intraperiod line. Proceedings of the National Academy of Sciences of the U.S.A. 84, 6287–6291.Google Scholar
Edgar, J.M., McLaughlin, M., Yool, D., Zhang, S.C., Fowler, J.H., Montague, P. et al. (2004) Oligodendroglial modulation of fast axonal transport in a mouse model of hereditary spastic paraplegia. Journal of Cell Biology 166, 121–131.Google Scholar
Filbin, M.T., Walsh, F.S., Trapp, B.D., Pizzey, J.A. and Tennekoon, G.I. (1990) Role of myelin P0 protein as a homophilic adhesion molecule. Nature 344, 871–872.Google Scholar
Fitzner, D., Schneider, A., Kippert, A., Möbius, W., Willig, K.I., Hell, S.W. et al. (2006) Myelin basic protein-dependent plasma membrane reorganization in the formation of myelin. EMBO Journal 25, 5037–5048.CrossRefGoogle ScholarPubMed
Fjorback, A.W., Müller, H.K. and Wiborg, O. (2008) Membrane glycoprotein M6B interacts with the human serotonin transporter. Journal of Molecular Neuroscience 37, 191–200.CrossRefGoogle ScholarPubMed
Folch, J. and Lees, M. (1951) Proteolipides, a new type of tissue lipoproteins; their isolation from brain. Journal of Biological Chemistry 191, 807–817.CrossRefGoogle ScholarPubMed
Franz, T., Waehneldt, T.V., Neuhoff, V. and Wächtler, K. (1981) Central nervous system myelin proteins and glycoproteins in vertebrates: a phylogenetic study. Brain Research 226, 245–258.CrossRefGoogle ScholarPubMed
Garbern, J.Y. (2007) Pelizaeus-Merzbacher disease: Genetic and cellular pathogenesis. Cellular and Molecular Life Sciences 64, 50–65.CrossRefGoogle ScholarPubMed
Garbern, J.Y., Cambi, F., Tang, X.M., Sima, A.A., Vallat, J.M., Bosch, E.P. et al. (1997) Proteolipid protein is necessary in peripheral as well as central myelin. Neuron 19, 205–218.Google Scholar
Giese, K.P., Martini, R., Lemke, G., Soriano, P. and Schachner, M. (1992) Mouse P0 gene disruption leads to hypomyelination, abnormal expression of recognition molecules, and degeneration of myelin and axons. Cell 71, 565–576.CrossRefGoogle ScholarPubMed
Gould, R.M., Morrison, H.G., Gilland, E. and Campbell, R.K. (2005) Myelin tetraspan family proteins but no non-tetraspan family proteins are present in the ascidian (Ciona intestinalis) genome. Biological Bulletin 209, 49–66.CrossRefGoogle ScholarPubMed
Gow, A., Southwood, C.M., Li, J.S., Pariali, M., Riordan, G.P., Brodie, S.E. et al. (1999) CNS myelin and sertoli cell tight junction strands are absent in Osp/claudin-11 null mice. Cell 99, 649–659.Google Scholar
Griffiths, I., Klugmann, M., Anderson, T., Yool, D., Thomson, C., Schwab, M.H. et al. (1998) Axonal swellings and degeneration in mice lacking the major proteolipid of myelin. Science 280, 1610–1613.Google Scholar
Gudz, T.I., Komuro, H. and Macklin, W.B. (2006) Glutamate stimulates oligodendrocyte progenitor migration mediated via an alphav integrin/myelin proteolipid protein complex. Journal of Neuroscience 26, 2458–2466.CrossRefGoogle ScholarPubMed
Gudz, T.I., Schneider, T.E., Haas, T.A. and Macklin, W.B. (2002) Myelin proteolipid protein forms a complex with integrins and may participate in integrin receptor signaling in oligodendrocytes. Journal of Neuroscience 22, 7398–7407.CrossRefGoogle ScholarPubMed
Hartline, D.K. and Colman, D.R. (2007) Rapid conduction and the evolution of giant axons and myelinated fibers. Current Biology 17, R29–R35.Google Scholar
Hartsock, A. and Nelson, W.J. (2008) Adherens and tight junctions: structure, function and connections to the actin cytoskeleton. Biochimica et Biophysica Acta 1778, 660–669.Google Scholar
Hayasaka, K., Himoro, M., Sato, W., Takada, G., Uyemura, K., Shimizu, N. et al. (1993) Charcot-Marie-Tooth neuropathy type 1B is associated with mutations of the myelin P0 gene. Nature Genetics 5, 31–34.Google Scholar
Hayat, M.A. (2000) Principles and Techniques of Electron Microscopy. Fourth Edition. Cambridge University Press. Cambridge, UK.Google Scholar
Henneke, M., Wehner, L.E., Hennies, H.C., Preuss, N. and Gärtner, J. (2004) Mutation analysis of the M6b gene in patients with Pelizaeus-Merzbacher-like syndrome. American Journal of Medical Genetics 128A, 156–158.Google Scholar
Hildebrand, C., Bowe, C.M. and Remahl, I.N. (1994) Myelination and myelin sheath remodelling in normal and pathological PNS nerve fibres. Progress in Neurobiology 43, 85–141.Google Scholar
Hildebrand, C., Remahl, S., Persson, H. and Bjartmar, C. (1993) Myelinated nerve fibres in the CNS. Progress in Neurobiology 40, 319–384.CrossRefGoogle ScholarPubMed
Inoue, K. (2005) PLP1-related inherited dysmyelinating disorders: Pelizaeus-Merzbacher disease and spastic paraplegia type 2. Neurogenetics 6, 1–16.CrossRefGoogle ScholarPubMed
Inoue, K., Osaka, H., Imaizumi, K., Nezu, A., Takanashi, J., Arii, J. et al. (1999) Proteolipid protein gene duplications causing Pelizaeus-Merzbacher disease: molecular mechanism and phenotypic manifestations. Annals of Neurology 45, 624–632.Google Scholar
Inouye, H. and Kirschner, D.A. (1994) Membrane topology of PLP in CNS myelin: evaluation of models. Neurochemical Research 19, 975–981.Google Scholar
Isensee, J., Witt, H., Pregla, R., Hetzer, R., Regitz-Zagrosek, V. and Ruiz Noppinger, P. (2008) Sexually dimorphic gene expression in the heart of mice and men. Journal of Molecular Medicine 86, 61–74.Google Scholar
Jahn, O., Tenzer, S. and Werner, H.B. (2009) Myelin proteomics: molecular anatomy of an insulating sheath. Molecular Neurobiology, accepted for publication.Google Scholar
Jeserich, G., Strelau, J. and Lanwert, C. (1997) Partial characterization of the 5′-flanking region of trout IP: a Po-like gene containing a PLP-like promoter. Journal of Neuroscience Research 50, 781–790.3.0.CO;2-4>CrossRefGoogle Scholar
Jessen, K.R. and Mirsky, R. (2005) The origin and development of glial cells in peripheral nerves. Nature Reviews Neuroscience 6, 671–682.CrossRefGoogle ScholarPubMed
Kagawa, T., Ikenaka, K., Inoue, Y., Kuriyama, S., Tsujii, T., Nakao, J. et al. (1994) Glial cell degeneration and hypomyelination caused by overexpression of myelin proteolipid protein gene. Neuron 13, 427–442.CrossRefGoogle ScholarPubMed
Karlsson, U. (1966) Comparison of the myelin period of peripheral and central origin by electron microscopy. Journal of Ultrastructure Research 15, 451–468.Google Scholar
Kassmann, C.M., Lappe-Siefke, C., Baes, M., Brügger, B., Mildner, A., Werner, H.B. et al. (2007) Axonal loss and neuroinflammation caused by peroxisome-deficient oligodendrocytes. Nature Genetics 39, 969–976.Google Scholar
Kassmann, C.M. and Nave, K.A. (2008) Oligodendroglial impact on axonal function and survival – a hypothesis. Current Opinion in Neurology 21, 235–241.Google Scholar
Kim, S.C., Sprung, R., Chen, Y., Xu, Y., Ball, H., Pei, J. et al. (2006) Substrate and functional diversity of lysine acetylation revealed by a proteomics survey. Molecular Cell 23, 607–618.CrossRefGoogle ScholarPubMed
Kirby, B.B., Takada, N., Latimer, A.J., Shin, J., Carney, T.J., Kelsh, R.N. et al. (2006) In vivo time-lapse imaging shows dynamic oligodendrocyte progenitor behavior during zebrafish development. Nature Neuroscience 9, 1506–1511.Google Scholar
Kirschner, D.A., Inouye, H., Ganser, A.L. and Mann, V. (1989) Myelin membrane structure and composition correlated: a phylogenetic study. Journal of Neurochemistry 53, 1599–1609.CrossRefGoogle ScholarPubMed
Kitagawa, K., Sinoway, M.P., Yang, C., Gould, R.M. and Colman, D.R. (1993) A proteolipid protein gene family: expression in sharks and rays and possible evolution from an ancestral gene encoding a pore-forming polypeptide. Neuron 11, 433–448.Google Scholar
Klugmann, M., Schwab, M.H., Pühlhofer, A., Schneider, A., Zimmermann, F., Griffiths, I.R. et al. (1997) Assembly of CNS myelin in the absence of proteolipid protein. Neuron 18, 59–70.Google Scholar
Kosaras, B. and Kirschner, D.A. (1990) Radial component of CNS myelin: junctional subunit structure and supramolecular assembly. Journal of Neurocytology 19, 187–199.CrossRefGoogle ScholarPubMed
Kronquist, K.E., Crandall, B.F., Macklin, W.B. and Campagnoni, A.T. (1987) Expression of myelin proteins in the developing human spinal cord: cloning and sequencing of human proteolipid protein cDNA. Journal of Neuroscience Research 18, 395–401.CrossRefGoogle ScholarPubMed
Kruger, L. and Maxwell, D.S. (1966) Electron microscopy of oligodendrocytes in normal rat cerebrum. American Journal of Anatomy 118, 411–435.Google Scholar
Kulkens, T., Bolhuis, P.A., Wolterman, R.A., Kemp, S., te Nijenhuis, S., Valentijn, L.J. et al. (1993) Deletion of the serine 34 codon from the major peripheral myelin protein P0 gene in Charcot-Marie-Tooth disease type 1B. Nature Genetics 5, 35–39.Google Scholar
Kurihara, T., Sakuma, M. and Gojobori, T. (1997) Molecular evolution of myelin proteolipid protein. Biochemical and Biophysical Research Communications 237, 559–561.CrossRefGoogle ScholarPubMed
Lagenaur, C., Kunemund, V., Fischer, G., Fushiki, S. and Schachner, M. (1992) Monoclonal M6 antibody interferes with neurite extension of cultured neurons. Journal of Neurobiology 23, 71–88.Google Scholar
Lanwert, C. and Jeserich, G. (2001) Structure, heterologous expression, and adhesive properties of the P(0)-like myelin glycoprotein IP1 of trout CNS. Microscopy Research and Technique 52, 637–644.Google Scholar
Lappe-Siefke, C., Goebbels, S., Gravel, M., Nicksch, E., Lee, J., Braun, P.E. et al. (2003) Disruption of Cnp1 uncouples oligodendroglial functions in axonal support and myelination. Nature Genetics 33, 366–374.Google Scholar
Lee, J., Gravel, M., Zhang, R., Thibault, P. and Braun, P.E. (2005) Process outgrowth in oligodendrocytes is mediated by CNP, a novel microtubule assembly myelin protein. Journal of Cell Biology 170, 661–673.Google Scholar
Lee, J.A., Carvalho, C.M. and Lupski, J.R. (2007) A DNA replication mechanism for generating nonrecurrent rearrangements associated with genomic disorders. Cell 131, 1235–1247.CrossRefGoogle ScholarPubMed
Lees, M.B. (1998) A history of proteolipids: a personal memoir. Neurochemical Research 23, 261–271.Google Scholar
Lemke, G. and Axel, R. (1985) Isolation and sequence of a cDNA encoding the major structural protein of peripheral myelin. Cell 40, 501–508.Google Scholar
Lenz, P.H., Hartline, D.K. and Davis, A.D. (2000) The need for speed. I. Fast reactions and myelinated axons in copepods. Journal of Comparative Physiology 186, 337–345.Google Scholar
Li, W., Zhang, B., Tang, J., Cao, Q., Wu, Y., Wu, C. et al. (2007) Sirtuin 2, a mammalian homolog of yeast silent information regulator-2 longevity regulator, is an oligodendroglial protein that decelerates cell differentiation through deacetylating alpha-tubulin. Journal of Neuroscience 27, 2606–2616.Google Scholar
Liang, Y.J., Wu, D.F., Stumm, R., Höllt, V. and Koch, T. (2008) Membrane glycoprotein M6A promotes mu-opioid receptor endocytosis and facilitates receptor sorting into the recycling pathway. Cell Research 18, 768–779.Google Scholar
Lin, L.F. and Lees, M.B. (1982) Interactions of dicyclohexylcarbodiimide with myelin proteolipid. Proceedings of the National Academy of Sciences of the U.S.A. 79, 941–945.CrossRefGoogle ScholarPubMed
Lund, R.D., Perry, V.H. and Lagenaur, C.F. (1986) Cell surface changes in the developing optic nerve of mice. Journal of Comparative Neurology 247, 439–446.Google Scholar
Luxoro, M. (1958) Observations in myelin structure: incisures and nodal regions. Proceedings of the National Academy of Sciences of the U.S.A. 44, 152–156.CrossRefGoogle ScholarPubMed
Martini, L. and Whistler, J.L. (2007) The role of mu opioid receptor desensitization and endocytosis in morphine tolerance and dependence. Current Opinion in Neurobiology 17, 556–564.Google Scholar
Martini, R., Zielasek, J., Toyka, K.V., Giese, K.P. and Schachner, M. (1995a) Protein zero (P0)-deficient mice show myelin degeneration in peripheral nerves characteristic of inherited human neuropathies. Nature Genetics 11, 281–286.CrossRefGoogle ScholarPubMed
Martini, R., Mohajeri, M.H., Kasper, S., Giese, K.P. and Schachner, M. (1995b) 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. Journal of Neuroscience 15, 4488–4495.Google Scholar
Mi, Z.P., Weng, W., Hankin, M.H., Narayanan, V. and Lagenaur, C.F. (1998) Maturational changes in cell surface antigen expression in the mouse retina and optic pathway. Developmental Brain Research 106, 145–154.CrossRefGoogle ScholarPubMed
Michibata, H., Okuno, T., Konishi, N., Wakimoto, K., Kyono, K., Aoki, K. et al. (2008) Inhibition of mouse GPM6A expression leads to decreased differentiation of neurons derived from mouse embryonic stem cells. Stem Cells and Development 17, 641–651.Google Scholar
Milner, R.J., Lai, C., Nave, K.A., Lenoir, D., Ogata, J. and Sutcliffe, J.G. (1985) Nucleotide sequences of two mRNAs for rat brain myelin proteolipid protein. Cell 42, 931–939.Google Scholar
Möbius, W. (2009) Cryopreparation of biological specimens for immunoelectron microscopy. Annals of Anatomy Jan 20. [Epub ahead of print] PMID: 19264467.CrossRefGoogle ScholarPubMed
Moll, W., Lanwert, C., Stratmann, A., Strelau, J. and Jeserich, G. (2003) Molecular cloning, tissue expression, and partial characterization of the major fish CNS myelin protein 36 k. Glia 44, 57–66.Google Scholar
Morell, P., Greenfield, S., Costantino-Ceccarini, E. and Wisniewski, H. (1972) Changes in the protein composition of mouse brain myelin during development. Journal of Neurochemistry 19, 2545–2554.Google Scholar
Morris, J.K., Willard, B.B., Yin, X., Jeserich, G., Kinter, M. and Trapp, B.D. (2004) The 36K protein of zebrafish CNS myelin is a short-chain dehydrogenase. Glia 45, 378–391.Google Scholar
Mugnaini, E. and Schnapp, B. (1974) Possible role of zonula occludens of the myelin sheath in demyelinating conditions. Nature 251, 725–727.Google Scholar
Mukobata, S., Hibino, T., Sugiyama, A., Urano, Y., Inatomi, A., Kanai, Y. et al. (2002) M6a acts as a nerve growth factor-gated Ca(2+) channel in neuronal differentiation. Biochemical and Biophysical Research Communications 297, 722–728.Google Scholar
Musse, A.A., Gao, W., Homchaudhuri, L., Boggs, J.M. and 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, 10372–10382.Google Scholar
Musse, A.A., Gao, W., Rangaraj, G., Boggs, J.M. and Harauz, G. (2009) Myelin basic protein co-distributes with other PI(4,5)P(2)-sequestering proteins in Triton X-100 detergent-resistant membrane microdomains. Neuroscience Letters 450, 32–36.Google Scholar
Nadon, N.L., Duncan, I.D. and Hudson, L.D. (1990) A point mutation in the proteolipid protein gene of the ‘shaking pup’ interrupts oligodendrocyte development. Development 110, 529–537.Google Scholar
Nagarajan, R., Le, N., Mahoney, H., Araki, T. and Milbrandt, J. (2002) Deciphering peripheral nerve myelination by using Schwann cell expression profiling. Proceedings of the National Academy of Sciences of the U.S.A. 99, 8998–9003.Google Scholar
Narayanan, V., Olinsky, S., Dahle, E. and Naidu, S. (1998) Mutation analysis of the M6b gene in patients with Rett syndrome. American Journal of Medical Genetics 78, 165–168.Google Scholar
Nave, K.A., Lai, C., Bloom, F.E. and Milner, R.J. (1986) Jimpy mutant mouse: a 74-base deletion in the mRNA for myelin proteolipid protein and evidence for a primary defect in RNA splicing. Proceedings of the National Academy of Sciences of the U.S.A. 83, 9264–9268.CrossRefGoogle Scholar
Nave, K.A., Lai, C., Bloom, F.E. and Milner, R.J. (1987) Splice site selection in the proteolipid protein (PLP) gene transcript and primary structure of the DM-20 protein of central nervous system myelin. Proceedings of the National Academy of Sciences of the U.S.A. 84, 5665–5669.Google Scholar
Nave, K.A. and Trapp, B.D. (2008) Axon-glial signaling and the glial support of axon function. Annual Reviews in Neuroscience 31, 535–561.Google Scholar
Nawaz, S., Kippert, A., Saab, A.S., Werner, H.B., Lang, T., Nave, K.A. and Simons, M. (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. Journal of Neuroscience 29, 4794–4807.Google Scholar
North, B.J., Marshall, B.L., Borra, M.T., Denu, J.M. and Verdin, E. (2003) The human Sir2 ortholog, SIRT2, is an NAD+-dependent tubulin deacetylase. Molecular Cell 11, 437–444.Google Scholar
Norton, W.T. and Poduslo, S.E. (1973) Myelination in rat brain: changes in myelin composition during brain maturation. Journal of Neurochemistry 21, 759–773.CrossRefGoogle ScholarPubMed
Olinsky, S., Loop, B.T., DeKosky, A., Ripepi, B., Weng, W., Cummins, J. et al. (1996) Chromosomal mapping of the human M6 genes. Genomics 33, 532–536.Google Scholar
Pannese, E. (1994) Neurocytology. Georg Thieme Verlag.Google Scholar
Peters, A. (1961) A radial component of central myelin sheaths. The Journal of Biophysical and Biochemical Cytology 11, 733–735.Google Scholar
Plotkowski, M.L., Kim, S., Phillips, M.L., Partridge, A.W., Deber, C.M. and Bowie, J.U. (2007) Transmembrane domain of myelin protein zero can form dimers: possible implications for myelin construction. Biochemistry 46, 12164–12173.Google Scholar
Pogoda, H.M., Sternheim, N., Lyons, D.A., Diamond, B., Hawkins, T.A., Woods, I.G. et al. (2006) A genetic screen identifies genes essential for development of myelinated axons in zebrafish. Developmental Biology 298, 118–131.Google Scholar
Polevoda, B. and Sherman, F. (2002) The diversity of acetylated proteins. Genome Biology, reviews0006 Vol. 3, No. 5, Pages 1–6, PMID: 12049668.Google Scholar
Popko, B., Puckett, C., Lai, E., Shine, H.D., Readhead, C., Takahashi, N. et al. (1987) Myelin deficient mice: expression of myelin basic protein and generation of mice with varying levels of myelin. Cell 48, 713–721.Google Scholar
Popot, J.L., Pham Dinh, D. and Dautigny, A. (1991) Major Myelin proteolipid: the 4-alpha-helix topology. Journal of Membrane Biology 120, 233–246.CrossRefGoogle ScholarPubMed
Postlethwait, J., Amores, A., Cresko, W., Singer, A. and Yan, Y.L. (2004) Subfunction partitioning, the teleost radiation and the annotation of the human genome. Trends in Genetics 20, 481–490.Google Scholar
Rasband, M.N., Tayler, J., Kaga, Y., Yang, Y., Lappe-Siefke, C., Nave, K.A. et al. (2005) CNP is required for maintenance of axon-glia interactions at nodes of Ranvier in the CNS. Glia 50, 86–90.Google Scholar
Readhead, C., Popko, B., Takahashi, N., Shine, H.D., Saavedra, R.A., Sidman, R.L. et al. (1987) Expression of a myelin basic protein gene in transgenic shiverer mice: correction of the dysmyelinating phenotype. Cell 48, 703–712.CrossRefGoogle ScholarPubMed
Readhead, C., Schneider, A., Griffiths, I. and Nave, K.A. (1994) Premature arrest of myelin formation in transgenic mice with increased proteolipid protein gene dosage. Neuron 12, 583–595.Google Scholar
Reynolds, E.S. (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. Journal of Cell Biology 17, 208–212.CrossRefGoogle ScholarPubMed
Roach, A., Takahashi, N., Pravtcheva, D., Ruddle, F. and Hood, L. (1985) Chromosomal mapping of mouse myelin basic protein gene and structure and transcription of the partially deleted gene in shiverer mutant mice. Cell 42, 149–155.Google Scholar
Robertson, J.D. (1958) The ultrastructure of Schmidt–Lanterman clefts and related shearing defects of the myelin sheath. The Journal of Biophysical and Biochemical Cytology 4, 39–46.CrossRefGoogle ScholarPubMed
Rosenbluth, J., Nave, K.A., Mierzwa, A. and Schiff, R. (2006) Subtle myelin defects in PLP-null mice. Glia 54, 172–182.Google Scholar
Rosenbluth, J., Schiff, R. and Lam, P. (2009) Effects of osmolality on PLP-null myelin structure: implications re axon damage. Brain Research 1253, 191–197.CrossRefGoogle ScholarPubMed
Rosenbluth, J., Stoffel, W. and Schiff, R. (1996) Myelin structure in proteolipid protein (PLP)-null mouse spinal cord. Journal of Comparative Neurology 371, 336–344.Google Scholar
Rotenstein, L., Herath, K., Gould, R.M. and de Bellard, M.E. (2008) Characterization of the shark myelin Po protein. Brain, Behavior and Evolution 72, 48–58.Google Scholar
Roth, A.D., Ivanova, A. and Colman, D.R. (2006) New observations on the compact myelin proteome. Neuron Glia Biology 2, 15–21.CrossRefGoogle ScholarPubMed
Roussel, G., Trifilieff, E., Lagenaur, C. and Nussbaum, J.L. (1998) Immunoelectron microscopic localization of the M6a antigen in rat brain. Journal of Neurocytology 27, 695–703.Google Scholar
Saavedra, R.A., Fors, L., Aebersold, R.H., Arden, B., Horvath, S., Sanders, J. et al. (1989) The myelin proteins of the shark brain are similar to the myelin proteins of the mammalian peripheral nervous system. Journal of Molecular Evolution 29, 149–156.Google Scholar
Salinas, S., Proukakis, C., Crosby, A., Warner, T.T. (2008) Hereditary spastic paraplegia: clinical features and pathogenetic mechanisms. Lancet Neurology 7, 1127–1138.Google Scholar
Saugier-Veber, P., Munnich, A., Bonneau, D., Rozet, J.M., Le Merrer, M., Gil, R. et al. (1994) X-linked spastic paraplegia and Pelizaeus-Merzbacher disease are allelic disorders at the proteolipid protein locus. Nature Genetics 6, 257–262.Google Scholar
Schaefer, K. and Brösamle, C. (2009) Zwilling-A and -B, two related myelin proteins of teleosts, which originate from a single, bicistronic transcript. Molecular Biology and Evolution 26, 495–499.CrossRefGoogle Scholar
Schliess, F. and Stoffel, W. (1991) Evolution of the myelin integral membrane proteins of the central nervous system. Biological Chemistry Hoppe Seyler 372, 865–874.Google Scholar
Schneider, A., Länder, H., Schulz, G., Wolburg, H., Nave, K.A., Schulz, J.B. et al. (2005) Palmitoylation is a sorting determinant for transport to the myelin membrane. Journal of Cell Science 118, 2415–2423.CrossRefGoogle Scholar
Schneider, A., Montague, P., Griffiths, I., Fanarraga, M., Kennedy, P., Brophy, P. et al. (1992) Uncoupling of hypomyelination and glial cell death by a mutation in the proteolipid protein gene. Nature 358, 758–761.Google Scholar
Schneider, A.M., Griffiths, I.R., Readhead, C. and Nave, K.A. (1995) Dominant-negative action of the jimpy mutation in mice complemented with an autosomal transgene for myelin proteolipid protein. Proceedings of the National Academy of Sciences of the U.S.A. 92, 4447–4451.Google Scholar
Schneider-Schaulies, J., von Brunn, A. and Schachner, M. (1990) Recombinant peripheral myelin protein P0 confers both adhesion and neurite outgrowth-promoting properties. Journal of Neuroscience Research 27, 286–297.Google Scholar
Schweigreiter, R., Roots, B.I., Bandtlow, C.E. and Gould, R.M. (2006) Understanding myelination through studying its evolution. International Reviews in Neurobiology 73, 219–273.CrossRefGoogle ScholarPubMed
Schweitzer, J., Becker, T., Becker, C.G. and Schachner, M. (2003) Expression of protein zero is increased in lesioned axon pathways in the central nervous system of adult zebrafish. Glia 41, 301–317.Google Scholar
Schweitzer, J., Becker, T., Schachner, M., Nave, K.A. and Werner, H. (2006) Evolution of myelin proteolipid proteins: gene duplication in teleosts and expression pattern divergence. Molecular and Cellular Neuroscience 31, 161–177.Google Scholar
Sebastiani, P., Wang, L., Nolan, V.G., Melista, E., Ma, Q., Baldwin, C.T. et al. (2008) Fetal hemoglobin in sickle cell anemia: Bayesian modeling of genetic associations. American Journal of Hematology 83, 189–195.Google Scholar
Shapiro, L., Doyle, J.P., Hensley, P., Colman, D.R. and Hendrickson, W.A. (1996) Crystal structure of the extracellular domain from P0, the major structural protein of peripheral nerve myelin. Neuron 17, 435–449.Google Scholar
Sheetz, M.P., Baumrind, N.L., Wayne, D.B. and Pearlman, A.L. (1990) Concentration of membrane antigens by forward transport and trapping in neuronal growth cones. Cell 61, 231–241.Google Scholar
Sherman, D.L. and Brophy, P.J. (2005) Mechanisms of axon ensheathment and myelin growth. Nature Reviews Neuroscience 6, 683–690.Google Scholar
Shimizu, F., Watanabe, T.K., Fujiwara, T., Takahashi, E., Nakamura, Y. and Maekawa, H. (1996) Isolation and mapping of the human glycoprotein M6 gene (GPM6A) to 4q33–>q34. Cytogenetic and Cell Genetics 74, 138–139.Google Scholar
Shy, M.E., Jáni, A., Krajewski, K., Grandis, M., Lewis, R.A., Li, J. et al. (2004) Phenotypic clustering in MPZ mutations. Brain 127, 371–384.Google Scholar
Simons, M., Krämer, E.M., Thiele, C., Stoffel, W. and Trotter, J. (2000) Assembly of myelin by association of proteolipid protein with cholesterol- and galactosylceramide-rich membrane domains. Journal of Cell Biology 151, 143–154.Google Scholar
Simons, R., Alon, N. and Riordan, J.R. (1987) Human myelin DM-20 proteolipid protein deletion defined by cDNA sequence. Biochemical and Biophysical Research Communications 146, 666–671.Google Scholar
Southwood, C.M., Peppi, M., Dryden, S., Tainsky, M.A. and Gow, A. (2007) Microtubule deacetylases, SirT2 and HDAC6, in the nervous system. Neurochemical Research 32, 187–195.Google Scholar
Spörkel, O., Uschkureit, T., Büssow, H. and Stoffel, W. (2002) Oligodendrocytes expressing exclusively the DM20 isoform of the proteolipid protein gene: myelination and development. Glia 37, 19–30.CrossRefGoogle ScholarPubMed
Stecca, B., Southwood, C.M., Gragerov, A., Kelley, K.A., Friedrich, V.L. Jr. and Gow, A. (2000) The evolution of lipophilin genes from invertebrates to tetrapods: DM-20 cannot replace proteolipid protein in CNS myelin. Journal of Neuroscience 20, 4002–4010.Google Scholar
Stratmann, A. and Jeserich, G. (1995) Molecular cloning and tissue expression of a cDNA encoding IP1 – a P0-like glycoprotein of trout CNS myelin. Journal of Neurochemistry 64, 2427–2436.Google Scholar
Studer, D., Humbel, B.M. and Chiquet, M. (2008) Electron microscopy of high pressure frozen samples: bridging the gap between cellular ultrastructure and atomic resolution. Histochemistry and Cell Biology 130, 877–889.Google Scholar
Subramaniam, S. (1998) The Biology Workbench – a seamless database and analysis environment for the biologist. Proteins 32, 1–2.Google Scholar
Swamy, M.J., Horváth, L.I., Brophy, P.J. and Marsh, D. (1999) Interactions between lipid-anchored and transmembrane proteins. Spin-label ESR studies on avidin-biotinyl phosphatidylethanolamine in membrane recombinants with myelin proteolipid proteins. Biochemistry 38, 16333–16339.Google Scholar
Takamori, S., Holt, M., Stenius, K., Lemke, E.A., Grønborg, M., Riedel, D. et al. (2006) Molecular anatomy of a trafficking organelle. Cell 127, 831–846.Google Scholar
Takei, K. and Uyemura, K. (1993) Expression of a P0-like glycoprotein in central nervous system myelin of amphibians (Ambystoma mexicanus, Xenopus laevis and Rana catesbeiana). Comparative Biochemistry and Physiology 106, 873–882.Google Scholar
Taylor, C.M., Marta, C.B., Claycomb, R.J., Han, D.K., Rasband, M.N., Coetzee, T. et al. (2004) Proteomic mapping provides powerful insights into functional myelin biology. Proceedings of the National Academy of Sciences of the U.S.A. 101, 4643–4648.Google Scholar
Tosic, M., Dolivo, M., Amiguet, P., Domanska-Janik, K. and Matthieu, J.M. (1993) Paralytic tremor (pt) rabbit: a sex-linked mutation affecting proteolipid protein-gene expression. Brain Research 625, 307–312.Google Scholar
Trapp, B.D. and Nave, K.A. (2008) Multiple sclerosis: an immune or neurodegenerative disorder? Annual Reviews in Neuroscience 31, 247–269.Google Scholar
Trapp, B.D., Nishiyama, A., Cheng, D. and Macklin, W. (1997) Differentiation and death of premyelinating oligodendrocytes in developing rodent brain. Journal of Cell Biology 137, 459–468.Google Scholar
Tsukita, S., Furuse, M. and Itoh, M. (2001) Multifunctional strands in tight junctions. Nature Reviews Molecular Cell Biology 2, 285–93.Google Scholar
Tuason, M.C., Rastikerdar, A., Kuhlmann, T., Goujet-Zalc, C., Zalc, B., Dib, S. et al. (2008) Separate proteolipid protein/DM20 enhancers serve different lineages and stages of development. Journal of Neuroscience 28, 6895–6903.Google Scholar
Turner, G., Gedeon, A., Kerr, B., Bennett, R., Mulley, J. and Partington, M. (2003) Syndromic form of X-linked mental retardation with marked hypotonia in early life, severe mental handicap, and difficult adult behavior maps to Xp22. American Journal of Medical Genetics 117A, 245–250.Google Scholar
Vanrobaeys, F., Van Coster, R., Dhondt, G., Devreese, B. and Van Beeumen, J. (2005) Profiling of myelin proteins by 2D-gel electrophoresis and multidimensional liquid chromatography coupled to MALDI TOF-TOF mass spectrometry. Journal of Proteome Research 4, 2283–2293.Google Scholar
Venkatesh, B., Erdmann, M.V. and Brenner, S. (2001) Molecular synapomorphies resolve evolutionary relationships of extant jawed vertebrates. Proceedings of the National Academy of Sciences of the U.S.A. 98, 11382–11387.Google Scholar
Verheijen, M.H., Chrast, R., Burrola, P. and Lemke, G. (2003) Local regulation of fat metabolism in peripheral nerves. Genes and Development 17, 2450–2464.Google Scholar
Volff, J.N. (2005) Genome evolution and biodiversity in teleost fish. Heredity 94, 280–294.Google Scholar
Waehneldt, T.V. (1990) Phylogeny of myelin proteins. Annals of the New York Academy of Sciences 605, 15–28.CrossRefGoogle ScholarPubMed
Waehneldt, T.V., Malotka, J., Karin, N.J. and Matthieu, J.M. (1985) Phylogenetic examination of vertebrate central nervous system myelin proteins by electro-immunoblotting. Neuroscience Letters 57, 97–102.Google Scholar
Waehneldt, T.V., Stoklas, S., Jeserich, G. and Matthieu, J.M. (1986) Central nervous system myelin of teleosts: comparative electrophoretic analysis of its proteins by staining and immunoblotting. Comparative Biochemistry and Physiology 84, 273–278.Google Scholar
Wang, E., Dimova, N., Sperle, K., Huang, Z., Lock, L., McCulloch, M.C. et al. (2008) Deletion of a splicing enhancer disrupts PLP1/DM20 ratio and myelin stability. Experimental Neurology 214, 322–330.Google Scholar
Weatherby, T.M., Davis, A.D., Hartline, D.K. and Lenz, P.H. (2000) The need for speed. II. Myelin in calanoid copepods. Journal of Comparative Physiology 186, 347–357.Google Scholar
Weimbs, T. and Stoffel, W. (1992) Proteolipid protein (PLP) of CNS myelin: positions of free, disulfide-bonded, and fatty acid thioester-linked cysteine residues and implications for the membrane topology of PLP. Biochemistry 31, 12289–12296.CrossRefGoogle ScholarPubMed
Werner, H., Dimou, L., Klugmann, M., Pfeiffer, S. and Nave, K.A. (2001) Multiple splice isoforms of proteolipid M6B in neurons and oligodendrocytes. Molecular and Cellular Neuroscience 18, 593–605.Google Scholar
Werner, H., Jung, M., Klugmann, M., Sereda, M., Griffiths, I.R. and Nave, K.A. (1998) Mouse models of myelin diseases. Brain Pathology 8, 771–793.CrossRefGoogle ScholarPubMed
Werner, H.B., Krämer-Albers, E.M., Strenzke, N., Saher, G., de Monasterio, Schrader P., Möbius, W., Tenzer, S., Ohno-lwashita, Y., Moser, T., Griffiths, I.R. and Nave, K.A. Oligodendroglial proteolipid proteins PLP and M6B are required for normal myelin composition and biogenesis. Submitted for publication.Google Scholar
Werner, H.B., Kuhlmann, K., Shen, S., Uecker, M., Schardt, A., Dimova, K. et al. (2007) Proteolipid protein is required for transport of sirtuin 2 into CNS myelin. Journal of Neuroscience 27, 7717–7730.Google Scholar
White, J., Lagenaur, C., Yan, Y. and Salama, G. (1993) A novel cation channel involved in neurite extension. Biophysical Journal [Suppl.] 64, A98.Google Scholar
Woodward, K.J. (2008) The molecular and cellular defects underlying Pelizaeus-Merzbacher disease. Expert Reviews in Molecular Medicine 10, e14.Google Scholar
Wu, D.F., Koch, T., Liang, Y.J., Stumm, R., Schulz, S., Schröder, H. et al. (2007) Membrane glycoprotein M6a interacts with the micro-opioid receptor and facilitates receptor endocytosis and recycling. Journal of Biological Chemistry 282, 22239–22247.Google Scholar
Yamaguchi, Y., Ikenaka, K., Niinobe, M., Yamada, H. and Mikoshiba, K. (1996) Myelin proteolipid protein (PLP), but not DM-20, is an inositol hexakisphosphate-binding protein. Journal of Biological Chemistry 271, 27838–46.Google Scholar
Yan, Y., Lagenaur, C. and Narayanan, V. (1993) Molecular cloning of M6: identification of a PLP/DM20 gene family. Neuron 11, 423–431.Google Scholar
Yan, Y., Narayanan, V. and Lagenaur, C. (1996) Expression of members of the proteolipid protein gene family in the developing murine central nervous system. Journal of Comparative Neurology 370, 465–478.Google Scholar
Yin, X., Baek, R.C., Kirschner, D.A., Peterson, A., Fujii, Y., Nave, K.A. et al. (2006) Evolution of a neuroprotective function of central nervous system myelin. Journal of Cell Biology 172, 469–478.Google Scholar
Yin, X., Kidd, G.J., Nave, K.A. and Trapp, B.D. (2008) P0 protein is required for and can induce formation of Schmidt–Lantermann incisures in myelin internodes. Journal of Neuroscience 28, 7068–7073.CrossRefGoogle ScholarPubMed
Yoshida, M. and Colman, D.R. (1996) Parallel evolution and coexpression of the proteolipid proteins and protein zero in vertebrate myelin. Neuron 16, 1115–1126.Google Scholar
Yoshida, M. and Colman, D.R. (2000) Glial-defined rhombomere boundaries in developing Xenopus hindbrain. Journal of Comparative Neurology 424, 47–57.Google Scholar
Yoshida, M. and Macklin, W.B. (2005) Oligodendrocyte development and myelination in GFP-transgenic zebrafish. Journal of Neuroscience Research 81, 1–8.Google Scholar
Yoshida, M., Shan, W.S. and Colman, D.R. (1999) Conserved and divergent expression patterns of the proteolipid protein gene family in the amphibian central nervous system. Journal of Neuroscience Research 57, 13–22.Google Scholar
Zalc, B., Goujet, D. and Colman, D. (2008) The origin of the myelination program in vertebrates. Current Biology 18, R511–R512.Google Scholar
Zhao, J., Iida, A., Ouchi, Y., Satoh, S. and Watanabe, S. (2008) M6a is expressed in the murine neural retina and regulates neurite extension. Molecular Vision 14, 1623–1630.Google Scholar