Defects in myelination, paranode organization and Purkinje cell innervation in the ether lipid-deficient mouse cerebellum

Human Molecular Genetics

Volumn 18, Issue 11, 2009, Pages 1897-1908

  Teigler, Andre ^a   Komljenovic, Dorde ^a,b   Draguhn, Andreas ^a   Gorgas, Karin ^a   Just, Wilhelm W ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

DIHYDROXYACETONE PHOSPHATE ACYLTRANSFERASE; ETHER LIPID; MYELIN BASIC PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CELL MIGRATION; CEREBELLUM; CEREBELLUM DISEASE; CONTROLLED STUDY; CORPUS CALLOSUM; GENE DELETION; GRANULE CELL; MOUSE; MYELINATED NERVE; MYELINATION; NERVE CONDUCTION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PURKINJE CELL;

ACYLTRANSFERASES; ANIMALS; AXONS; CELL MOVEMENT; CEREBELLUM; INTERCELLULAR JUNCTIONS; KIDNEY; MICE; MICE, KNOCKOUT; MYELIN BASIC PROTEINS; MYELIN SHEATH; PHOSPHOLIPID ETHERS; PURKINJE CELLS;

ANIMALIA; MAMMALIA; MUS;

EID: 65549163117     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddp110     Document Type: Article

References (77)

1. Moser, H.W. (2000) Molecular genetics of peroxisomal disorders. Front. Biosci., 5, D298-D306.
2. Wanders, R.J. and Waterham, H.R. (2005) Peroxisomal disorders I: biochemistry and genetics of peroxisome biogenesis disorders. Clin. Genet., 67, 107-133.
3. Gorgas, K., Teigler, A., Komljenovic, D. and Just, W.W. (2006) The ether lipid-deficient mouse: Tracking down plasmalogen functions. Biochim. Biophys. Acta, 1763, 1511-1526.
4. Nagan, N. and Zoeller, R.A. (2001) Plasmalogens: Biosynthesis and functions. Prog. Lipid Res., 40, 199-229.
5. Zoeller, R.A., Morand, O.H. and Raetz, C.R. (1988) A possible role for plasmalogens in protecting animal cells against photosensitized killing. J. Biol. Chem., 263, 11590-11596.
6. Diagne, A., Fauvel, J., Record, M., Chap, H. and Douste-Blazy, L. (1984) Studies on ether phospholipids. II. Comparative composition of various tissues from human, rat and guinea pig. Biochim. Biophys. Acta, 793, 221-231.
7. Han, X., Holtzman, D.M. and McKeel, D.W. Jr. (2001) Plasmalogen deficiency in early Alzheimer's disease subjects and in animal models: molecular characterization using electrospray ionization mass spectrometry. J. Neurochem., 77, 1168-1180.
8. Honke, K., Zhang, Y., Cheng, X., Kotani, N. and Taniguchi, N. (2004) Biological roles of sulfoglycolipids and pathophysiology of their deficiency. Glycoconj. J., 21, 59-62.
9. Ishii, S. and Shimizu, T. (2000) Platelet-activating factor (PAF) receptor and genetically engineered PAF receptor mutant mice. Prog. Lipid Res., 39, 41-82.
10. Tokuoka, S.M., Ishii, S., Kawamura, N., Satoh, M., Shimada, A., Sasaki, S., Hirotsune, S., Wynshaw-Boris, A. and Shimizu, T. (2003) Involvement of platelet-activating factor and LIS1 in neuronal migration. Eur. J. Neurosci., 18, 563-570.
11. Ikezawa, H. (2002) Glycosylphosphatidylinositol (GPI)-anchored proteins. Biol. Pharm. Bull., 25, 409-417.
12. Kinoshita, T. and Inoue, N. (2000) Dissecting and manipulating the pathway for glycosylphos-phatidylinositol-anchor biosynthesis. Curr. Opin. Chem. Biol., 4, 632-638.
13. Glaser, P.E. and Gross, R.W. (1994) Plasmenylethanolamine facilitates rapid membrane fusion: A stopped-flow kinetic investigation correlating the propensity of a major plasma membrane constituent to adopt an HII phase with its ability to promote membrane fusion. Biochemistry, 33, 5805-5812.
14. Chilton, F.H. and Murphy, R.C. (1986) Remodeling of arachidonate-containing phosphoglycerides within the human neutrophil. J. Biol. Chem., 261, 7771-7777.
15. Hale, C.C., Ebeling, E.G., Hsu, F.F. and Ford, D.A. (1998) The selective activation of the cardiac sarcolemmal sodium-calcium exchanger by plasmalogenic phosphatidic acid produced by phospholipase D. FEBS Lett., 422, 247-251.
16. Kubota, M., Nakane, M., Nakagomi, T., Tamura, A., Hisaki, H., Shimasaki, H. and Ueta, N. (2001) Regional distribution of ethanolamine plasmalogen in the hippocampal CA1 and CA3 regions and cerebral cortex of the gerbil. Neurosci. Lett., 301, 175-178.
17. Munn, N.J., Arnio, E., Liu, D., Zoeller, R.A. and Liscum, L. (2003) Deficiency in ethanolamine plasmalogen leads to altered cholesterol transport. J. Lipid Res., 44, 182-192.
18. Thai, T.P., Rodemer, C., Jauch, A., Hunziker, A., Moser, A., Gorgas, K. and Just, W.W. (2001) Impaired membrane traffic in defective ether lipid biosynthesis. Hum. Mol. Genet., 10, 127-136.
19. Brites, P., Motley, A.M., Gressens, P., Mooyer, P.A., Ploegaert, I., Everts, V., Evrard, P., Carmeliet, P., Dewerchin, M., Schoonjans, L. et al. (2003) Impaired neuronal migration and endochondral ossification in Pex7 knockout mice: A model for rhizomelic chondrodysplasia punctata. Hum. Mol. Genet., 12, 2255-2267.
20. Faust, P.L. and Hatten, M.E. (1997) Targeted deletion of the PEX2 peroxisome assembly gene in mice provides a model for Zellweger syndrome, a human neuronal migration disorder. J. Cell Biol., 139, 1293-1305.
21. Faust, P.L., Su, H.M., Moser, A. and Moser, H.W. (2001) The peroxisome deficient PEX2 Zellweger mouse: Pathologic and biochemical correlates of lipid dysfunction. J. Mol. Neurosci., 16, 289-297.
22. Hulshagen, L., Krysko, O., Bottelbergs, A., Huyghe, S., Klein, R., Van Veldhoven, P.P., De Deyn, P.P., D'Hooge, R., Hartmann, D. and Baes, M. (2008) Absence of functional peroxisomes from mouse CNS causes dysmyelination and axon degeneration. J. Neurosci., 28, 4015-4027.
23. Janssen, A., Gressens, P., Grabenbauer, M., Baumgart, E., Schad, A., Vanhorebeek, I., Brouwers, A., Declercq, P.E., Fahimi, D., Evrard, P. et al. (2003) Neuronal migration depends on intact peroxisomal function in brain and in extraneuronal tissues. J. Neurosci., 23, 9732-9741.
24. Krysko, O., Hulshagen, L., Janssen, A., Schutz, G., Klein, R., De Bruycker, M., Espeel, M., Gressens, P. and Baes, M. (2007) Neocortical and cerebellar developmental abnormalities in conditions of selective elimination of peroxisomes from brain or from liver. J. Neurosci. Res., 85, 58-72.
25. Maxwell, M., Bjorkman, J., Nguyen, T., Sharp, P., Finnie, J., Paterson, C., Tonks, I., Paton, B.C., Kay, G.F. and Crane, D.I. (2003) Pex13 inactivation in the mouse disrupts peroxisome biogenesis and leads to a Zellweger syndrome phenotype. Mol. Cell. Biol., 23, 5947-5957.
26. Rodemer, C., Thai, T.P., Brugger, B., Kaercher, T., Werner, H., Nave, K.A., Wieland, F., Gorgas, K. and Just, W.W. (2003) Inactivation of ether lipid biosynthesis causes male infertility, defects in eye development and optic nerve hypoplasia in mice. Hum. Mol. Genet., 12, 1881-1895.
27. Sudarov, A. and Joyner, A.L. (2007) Cerebellum morphogenesis: The foliation pattern is orchestrated by multi-cellular anchoring centers. Neural Dev., 2, 26.
28. Andersen, P., Silfvenius, H., Sundberg, S.H., Sveen, O. and Wigstrom, H. (1978) Functional characteristics of unmyelinated fibres in the hippocampal cortex. Brain Res., 144, 11-18.
29. Spiegel, I. and Peles, E. (2002) Cellular junctions of myelinated nerves (Review). Mol. Membr. Biol., 19, 95-101.
30. Falk, J., Bonnon, C., Girault, J.A. and Faivre-Sarrailh, C. (2002) F3/ contactin, a neuronal cell adhesion molecule implicated in axogenesis and myelination. Biol. Cell, 94, 327-334.
31. Hedstrom, K.L. and Rasband, M.N. (2006) Intrinsic and extrinsic determinants of ion channel localization in neurons. J. Neurochem. 98, 1345-1352.
32. Hashimoto, K. and Kano, M. (2005) Postnatal development and synapse elimination of climbing fiber to Purkinje cell projection in the cerebellum. Neurosci. Res., 53, 221-218.
33. Hioki, H., Fujiyama, F., Taki, K., Tomioka, R., Furuta, T., Tamamaki, N. and Kaneko, T. (2003) Differential distribution of vesicular glutamate transporters in the rat cerebellar cortex. Neuroscience, 117 1-6.
34. Sotelo, C. (1990) Cerebellar synaptogenesis: What we can learn from mutant mice. J. Exp. Biol., 153, 225-249.
35. Yuste, R. and Bonhoeffer, T. (2004) Genesis of dendritic spines: insights from ultrastructural and imaging studies. Nat. Rev., 5 24-34.
36. Sotelo, C. and Arsenio-Nunes, M.L. (1976) Development of Purkinje cells in absence of climbing fibers. Brain Res., 111, 289-295.
37. Sugihara, I. (2006) Organization and remodeling of the olivocerebellar climbing fiber projection. Cerebellum, 5, 15-22.
38. Takei, K., Mignery, G.A., Mugnaini, E., Sudhof, T.C. and De Camilli, P. (1994) Inositol 1,4,5-trisphosphate receptor causes formation of ER cisternal stacks in transfected fibroblasts and in cerebellar Purkinje cells. Neuron, 12, 327-342.
39. Sillitoe, R.V. and Joyner, A.L. (2007) Morphology, molecular codes, and circuitry produce the three-dimensional complexity of the cerebellum. Ann. Rev. Cell Dev. Biol., 23, 549-577.
40. Nagy, A., Rossant, J., Nagy, R., Abramow-Newerly, W. and Roder, J.C. (1993) Derivation of completely cell culture-derived mice from early-passage embryonic stem cells. Proc. Natl Acad. Sci. USA, 90, 8424-8428.
41. Gressens, P. (2006) Pathogenesis of migration disorders. Curr. Opin. Neurol., 19, 135-140.
42. Komuro, H. and Yacubova, E. (2003) Recent advances in cerebellar granule cell migration. Cell. Mol. Life Sci., 60, 1084-1098.
43. Bollinger, C.R., Teichgraber, V. and Gulbins, E. (2005) Ceramide-enriched membrane domains. Biochim. Biophys. Acta, 1746, 284-294.
44. Meyer, S., Orso, E., Schmitz, G., Landthaler, M. and Vogt, T. (2007) Lubrol-RAFTs in melanoma cells: A molecular platform for tumor-promoting ephrin-B2-integrin-beta1 interaction. J. Invest. Dermatol., 127 1615-1621.
45. Nguyen, D.H. and Taub, D. (2002) CXCR4 function requires membrane cholesterol: Implications for HIV infection. J. Immunol., 168 4121-4126.
46. Suzuki, S., Numakawa, T., Shimazu, K., Koshimizu, H., Hara, T., Hatanaka, H., Mei, L., Lu, B. and Kojima, M. (2004) BDNF-induced recruitment of TrkB receptor into neuronal lipid rafts: Roles in synaptic modulation. J. Cell Biol., 167, 1205-1215.
47. Yang, X.L., Xiong, W.C. and Mei, L. (2004) Lipid rafts in neuregulin signaling at synapses. Life Sci., 75, 2495-2504.
48. Boyle, M.E., Berglund, E.O., Murai, K.K., Weber, L., Peles, E. and Ranscht, B. (2001) Contactin orchestrates assembly of the septate-like junctions at the paranode in myelinated peripheral nerve. Neuron, 30, 385-397.
49. Collard, J.F., Cote, F. and Julien, J.P. (1995) Defective axonal transport in a transgenic mouse model of amyotrophic lateral sclerosis. Nature, 375, 61-64.
50. Garcia-Fresco, G.P., Sousa, A.D., Pillai, A.M., Moy, S.S., Crawley, J.N., Tessarollo, L., Dupree, J.L. and Bhat, M.A. (2006) Disruption of axo-glial junctions causes cytoskeletal disorganization and degeneration of Purkinje neuron axons. Proc. Natl Acad. Sci. USA, 103, 5137-5142.
51. Poliak, S. and Peles, E. (2003) The local differentiation of myelinated axons at nodes of Ranvier. Nat. Rev., 4, 968-980.
52. Ogawa, Y., Schafer, D.P., Horresh, I., Bar, V., Hales, K., Yang, Y., Susuki, K., Peles, E., Stankewich, M.C. and Rasband, M.N. (2006) Spectrins and ankyrinB constitute a specialized paranodal cytoskeleton. J. Neurosci., 26, 5230-5239.
53. Bosio, A., Bussow, H., Adam, J. and Stoffel, W. (1998) Galactosphingolipids and axono-glial interaction in myelin of the central nervous system. Cell Tiss. Res., 292, 199-210.
54. Coetzee, T., Fujita, N., Dupree, J., Shi, R., Blight, A., Suzuki, K. and Popko, B. (1996) Myelination in the absence of galactocerebroside and sulfatide: Normal structure with abnormal function and regional instability. Cell, 86, 209-219.
55. Schaeren-Wiemers, N., Bonnet, A., Erb, M., Erne, B., Bartsch, U., Kern, F., Mantei, N., Sherman, D. and Suter, U. (2004) The raft-associated protein MAL is required for maintenance of proper axon-glia interactions in the central nervous system. J. Cell Biol., 166, 731-742.
56. More, M.I., Kirsch, F.P. and Rathjen, F.G. (2001) Targeted ablation of NrCAM or ankyrin-B results in disorganized lens fibers leading to cataract formation. J. Cell Biol., 154, 187-196.
57. Berglund, E.O., Murai, K.K., Fredette, B., Sekerkova, G., Marturano, B., Weber, L., Mugnaini, E. and Ranscht, B. (1999) Ataxia and abnormal cerebellar microorganization in mice with ablated contactin gene expression. Neuron, 24, 739-750.
58. Honsho, M., Yagita, Y., Kinoshita, N. and Fujiki, Y. (2008) Isolation and characterization of mutant animal cell line defective in alkyl-dihydroxyacetonephosphate synthase: Localization and transport of plasmalogens to post-Golgi compartments. Biochim. Biophys. Acta, 1783, 1857-1865.
59. Houjou, T., Hayakawa, J., Watanabe, R., Tashima, Y., Maeda, Y., Kinoshita, T. and Taguchi, R. (2007) Changes in molecular species profiles of glycosylphosphatidylinositol anchor precursors in early stages of biosynthesis. J. Lipid Res., 48, 1599-1606.
60. De Benedictis, L., Bizzoca, A., Corsi, P., Albieri, I., Consalez, G.G. and Gennarini, G. (2006) Activation profile of the F3/contactin gene in the developing mouse cerebellum. Mol. Cell Neurosci., 32, 403-418.
61. Snyder, F., Hibbs, M. and Malone, B. (1971) Enzymic synthesis of O-alkyl glycerolipids in brain and liver of rats during fetal and postnatal development. Biochim. Biophys. Acta, 231, 409-411.
62. Honke, K., Hirahara, Y., Dupree, J., Suzuki, K., Popko, B., Fukushima, K., Fukushima, J., Nagasawa, T., Yoshida, N., Wada, Y. et al. (2002) Paranodal junction formation and spermatogenesis require sulfoglycolipids. Proc. Natl Acad. Sci. USA, 99, 4227-4232.
63. Ishibashi, T., Dupree, J.L., Ikenaka, K., Hirahara, Y., Honke, K., Peles, E., Popko, B., Suzuki, K., Nishino, H. and Baba, H. (2002) A myelin galactolipid, sulfatide, is essential for maintenance of ion channels on myelinated axon but not essential for initial cluster formation. J. Neurosci., 22, 6507-6514.
64. Ichikawa, R., Miyazaki, T., Kano, M., Hashikawa, T., Tatsumi, H., Sakimura, K., Mishina, M., Inoue, Y. and Watanabe, M. (2002) Distal extension of climbing fiber territory and multiple innervation caused by aberrant wiring to adjacent spiny branchlets in cerebellar Purkinje cells lacking glutamate receptor delta 2. J. Neurosci., 22, 8487-8503.
65. Miyazaki, T., Hashimoto, K., Shin, H.S., Kano, M. and Watanabe, M. (2004) P/Q-type Ca2+ channel alpha1A regulates synaptic competition on developing cerebellar Purkinje cells. J. Neurosci., 24, 1734-1743.
66. Rhyu, I.J., Abbott, L.C., Walker, D.B. and Sotelo, C. (1999) An ultrastructural study of granule cell/Purkinje cell synapses in tottering (tg/tg), leaner (tg(la)/tg(la)) and compound heterozygous tottering/leaner (tg/tg(la)) mice. Neuroscience, 90, 717-728.
67. Rhyu, I.J., Oda, S., Uhm, C.S., Kim, H., Suh, Y.S. and Abbott, L.C. (1999) Morphologic investigation of rolling mouse Nagoya (tg(rol)/ tg(rol)) cerebellar Purkinje cells: An ataxic mutant, revisited. Neurosci. Lett., 266, 49-52.
68. Takagishi, Y., Hashimoto, K., Kayahara, T., Watanabe, M., Otsuka, H., Mizoguchi, A., Kano, M. and Murata, Y. (2007) Diminished climbing fiber innervation of Purkinje cells in the cerebellum of myosin Va mutant mice and rats. Dev. Neurobiol., 67, 909-923.
69. Langford, G.M. (2002) Myosin-V, a versatile motor for short-range vesicle transport. Traffic, 3, 859-865.
70. Paschen, W. and Mengesdorf, T. (2005) Endoplasmic reticulum stress response and neurodegeneration. Cell Calcium, 38, 409-415.
71. Banno, T. and Kohno, K. (1998) Conformational changes of the smooth endoplasmic reticulum are facilitated by L-glutamate and its receptors in rat Purkinje cells. J. Comp. Neurol., 402, 252-263.
72. Lappe-Siefke, C., Goebbels, S., Gravel, M., Nicksch, E., Lee, J., Braun, P.E., Griffiths, I.R. and Nave, K.A. (2003) Disruption of Cnp1 uncouples oligodendroglial functions in axonal support and myelination. Nat. Genet., 33, 366-374.
73. Steffensen, I., Waxman, S.G., Mills, L. and Stys, P.K. (1997) Immunolocalization of the Na(+)Ca2+ exchanger in mammalian myelinated axons. Brain Res., 776, 1-9.
74. Condrescu, M., Opuni, K., Hantash, B.M. and Reeves, J.P. (2002) Cellular regulation of sodium-calcium exchange. Ann. N. Y. Acad. Sci., 976, 214-223.
75. Franklin, K. and Paxinos, G. (1997) The Mouse Brain in Stereotaxic Coordinates. Academic Press, San Diego, CF, 1997.
76. Daughaday, W.H., Lowry, O.H., Rosebrough, N.J. and Fields, W.S. (1952) Determination of cerebrospinal fluid protein with the Folin phenol reagent. J. Lab. Clin. Med., 39, 663-665.
77. Nimmrich, V., Maier, N., Schmitz, D. and Draguhn, A. (2005) Induced sharp wave-ripple complexes in the absence of synaptic inhibition in mouse hippocampal slices. J. Physiol., 563, 663-670.