Npc1 Acting in Neurons and Glia Is Essential for the Formation and Maintenance of CNS Myelin

PLoS Genetics

Volumn 9, Issue 4, 2013, Pages

  Yu, Ting ^a   Lieberman, Andrew P ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MYELIN; MYELIN PROTEIN; PROTEIN KINASE FYN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL CYCLE ARREST; CELL MATURATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENZYME REGULATION; EXPERIMENTAL MOUSE; FEMALE; GENE; GENE DELETION; GENE FUNCTION; GENE IDENTIFICATION; GLIA CELL; INTRACELLULAR TRANSPORT; LIPID STORAGE; LIPID TRANSPORT; LOSS OF FUNCTION MUTATION; MALE; MOUSE; MYELIN DEFICIENCY; NERVE CELL; NERVE CELL NECROSIS; NERVE DEGENERATION; NERVE FIBER DEGENERATION; NEUROPATHOLOGY; NIEMANN PICK DISEASE; NONHUMAN; NPC1 GENE; NULL ALLELE; OLIGODENDROGLIA; PHENOTYPE; PURKINJE CELL; SEX DIFFERENCE; SIGNAL TRANSDUCTION;

ANIMALS; CELLS, CULTURED; CENTRAL NERVOUS SYSTEM; CHOLESTEROL; ENDOCYTOSIS; HUMANS; MICE; MYELIN SHEATH; NEUROGLIA; NEURONS; NIEMANN-PICK DISEASE, TYPE C; OLIGODENDROGLIA; PROTEINS; PROTO-ONCOGENE PROTEINS C-FYN; PURKINJE CELLS;

MUS;

EID: 84876855611     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1003462     Document Type: Article

References (54)

1. Baumann N, Pham-Dinh D, (2001) Biology of oligodendrocyte and myelin in the mammalian central nervous system. Physiol Rev 81: 871-927.
2. Dietschy JM, Turley SD, (2004) Thematic review series: brain Lipids. Cholesterol metabolism in the central nervous system during early development and in the mature animal. J Lipid Res 45: 1375-1397.
3. Saher G, Brugger B, Lappe-Siefke C, Mobius W, Tozawa R, et al. (2005) High cholesterol level is essential for myelin membrane growth. Nat Neurosci 8: 468-475.
4. Carstea ED, Morris JA, Coleman KG, Loftus SK, Zhang D, et al. (1997) Niemann-Pick C1 disease gene: homology to mediators of cholesterol homeostasis. Science 277: 228-231.
5. Loftus SK, Morris JA, Carstea ED, Gu JZ, Cummings C, et al. (1997) Murine model of Niemann-Pick C disease: mutation in a cholesterol homeostasis gene. Science 277: 232-235.
6. Neufeld EB, Wastney M, Patel S, Suresh S, Cooney AM, et al. (1999) The Niemann-Pick C1 protein resides in a vesicular compartment linked to retrograde transport of multiple lysosomal cargo. J Biol Chem 274: 9627-9635.
7. Higgins ME, Davies JP, Chen FW, Ioannou YA, (1999) Niemann-Pick C1 is a late endosome-resident protein that transiently associates with lysosomes and the trans-Golgi network. Mol Genet Metab 68: 1-13.
8. Davies JP, Ioannou YA, (2000) Topological analysis of Niemann-Pick C1 protein reveals that the membrane orientation of the putative sterol-sensing domain is identical to those of 3-hydroxy-3-methylglutaryl-CoA reductase and sterol regulatory element binding protein cleavage-activating protein. J Biol Chem 275: 24367-24374.
9. Garver WS, Heidenreich RA, Erickson RP, Thomas MA, Wilson JM, (2000) Localization of the murine Niemann-Pick C1 protein to two distinct intracellular compartments. J Lipid Res 41: 673-687.
10. Kwon HJ, Abi-Mosleh L, Wang ML, Deisenhofer J, Goldstein JL, et al. (2009) Structure of N-terminal domain of NPC1 reveals distinct subdomains for binding and transfer of cholesterol. Cell 137: 1213-1224.
11. Deffieu MS, Pfeffer SR, (2011) Niemann-Pick type C 1 function requires lumenal domain residues that mediate cholesterol-dependent NPC2 binding. Proc Natl Acad Sci U S A 108: 18932-18936.
12. Karten B, Peake KB, Vance JE, (2009) Mechanisms and consequences of impaired lipid trafficking in Niemann-Pick type C1-deficient mammalian cells. Biochim Biophys Acta 1791: 659-670.
13. Vanier MT, (2010) Niemann-Pick disease type C. Orphanet J Rare Dis 5: 16.
14. German DC, Liang CL, Song T, Yazdani U, Xie C, et al. (2002) Neurodegeneration in the Niemann-Pick C mouse: glial involvement. Neuroscience 109: 437-450.
15. Weintraub H, Abramovici A, Sandbank U, Pentchev PG, Brady RO, et al. (1985) Neurological mutation characterized by dysmyelination in NCTR-Balb/C mouse with lysosomal lipid storage disease. J Neurochem 45: 665-672.
16. Weintraub H, Abramovici A, Sandbank U, Booth AD, Pentchev PG, et al. (1987) Dysmyelination in NCTR-Balb/C mouse mutant with a lysosomal storage disorder. Morphological survey. Acta Neuropathol 74: 374-381.
17. Takikita S, Fukuda T, Mohri I, Yagi T, Suzuki K, (2004) Perturbed myelination process of premyelinating oligodendrocyte in Niemann-Pick type C mouse. J Neuropathol Exp Neurol 63: 660-673.
18. Trouard TP, Heidenreich RA, Seeger JF, Erickson RP, (2005) Diffusion tensor imaging in Niemann-Pick Type C disease. Pediatr Neurol 33: 325-330.
19. Walterfang M, Fahey M, Desmond P, Wood A, Seal ML, et al. (2010) White and gray matter alterations in adults with Niemann-Pick disease type C: a cross-sectional study. Neurology 75: 49-56.
20. Elrick MJ, Pacheco CD, Yu T, Dadgar N, Shakkottai VG, et al. (2010) Conditional Niemann-Pick C mice demonstrate cell autonomous Purkinje cell neurodegeneration. Hum Mol Genet 19: 837-847.
21. Lakso M, Pichel JG, Gorman JR, Sauer B, Okamoto Y, et al. (1996) Efficient in vivo manipulation of mouse genomic sequences at the zygote stage. Proc Natl Acad Sci U S A 93: 5860-5865.
22. Hayashi S, McMahon AP, (2002) Efficient recombination in diverse tissues by a tamoxifen-inducible form of Cre: a tool for temporally regulated gene activation/inactivation in the mouse. Dev Biol 244: 305-318.
23. Yu T, Shakkottai VG, Chung C, Lieberman AP, (2011) Temporal and cell-specific deletion establishes that neuronal Npc1 deficiency is sufficient to mediate neurodegeneration. Hum Mol Genet 20: 4440-4451.
24. Zhu Y, Romero MI, Ghosh P, Ye Z, Charnay P, et al. (2001) Ablation of NF1 function in neurons induces abnormal development of cerebral cortex and reactive gliosis in the brain. Genes Dev 15: 859-876.
25. Bornig H, Geyer G, (1974) Staining of cholesterol with the fluorescent antibiotic "filipin". Acta Histochem 50: 110-115.
26. Soriano P, (1999) Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat Genet 21: 70-71.
27. Weng Q, Chen Y, Wang H, Xu X, Yang B, et al. (2012) Dual-mode modulation of Smad signaling by Smad-interacting protein Sip1 is required for myelination in the central nervous system. Neuron 73: 713-728.
28. Charles P, Hernandez MP, Stankoff B, Aigrot MS, Colin C, et al. (2000) Negative regulation of central nervous system myelination by polysialylated-neural cell adhesion molecule. Proc Natl Acad Sci U S A 97: 7585-7590.
29. Lee X, Yang Z, Shao Z, Rosenberg SS, Levesque M, et al. (2007) NGF regulates the expression of axonal LINGO-1 to inhibit oligodendrocyte differentiation and myelination. J Neurosci 27: 220-225.
30. Wang S, Sdrulla AD, diSibio G, Bush G, Nofziger D, et al. (1998) Notch receptor activation inhibits oligodendrocyte differentiation. Neuron 21: 63-75.
31. Baudry M, Yao Y, Simmons D, Liu J, Bi X, (2003) Postnatal development of inflammation in a murine model of Niemann-Pick type C disease: immunohistochemical observations of microglia and astroglia. Exp Neurol 184: 887-903.
32. Umemori H, Sato S, Yagi T, Aizawa S, Yamamoto T, (1994) Initial events of myelination involve Fyn tyrosine kinase signalling. Nature 367: 572-576.
33. Kramer-Albers EM, White R, (2011) From axon-glial signalling to myelination: the integrating role of oligodendroglial Fyn kinase. Cell Mol Life Sci 68: 2003-2012.
34. Lappe-Siefke C, Goebbels S, Gravel M, Nicksch E, Lee J, et al. (2003) Disruption of Cnp1 uncouples oligodendroglial functions in axonal support and myelination. Nat Genet 33: 366-374.
35. Liao G, Cheung S, Galeano J, Ji AX, Qin Q, et al. (2009) Allopregnanolone treatment delays cholesterol accumulation and reduces autophagic/lysosomal dysfunction and inflammation in Npc1-/- mouse brain. Brain Res 1270: 140-151.
36. Schuller U, Heine VM, Mao J, Kho AT, Dillon AK, et al. (2008) Acquisition of granule neuron precursor identity is a critical determinant of progenitor cell competence to form Shh-induced medulloblastoma. Cancer Cell 14: 123-134.
37. Ko DC, Milenkovic L, Beier SM, Manuel H, Buchanan J, et al. (2005) Cell-autonomous death of cerebellar purkinje neurons with autophagy in Niemann-Pick type C disease. PLoS Genet 1: e7 doi:10.1371/journal.pgen.0010007.
38. Lopez ME, Klein AD, Dimbil UJ, Scott MP, (2011) Anatomically defined neuron-based rescue of neurodegenerative Niemann-Pick type C disorder. J Neurosci 31: 4367-4378.
39. Borbon I, Totenhagen J, Fiorenza MT, Canterini S, Ke W, et al. (2012) Niemann-Pick C1 mice, a model of "juvenile Alzheimer's disease", with normal gene expression in neurons and fibrillary astrocytes show long term survival and delayed neurodegeneration. J Alzheimers Dis 30: 875-887.
40. Lopez ME, Klein AD, Hong J, Dimbil UJ, Scott MP, (2012) Neuronal and epithelial cell rescue resolves chronic systemic inflammation in the lipid storage disorder Niemann-Pick C. Hum Mol Genet 21: 2946-2960.
41. Chen G, Li HM, Chen YR, Gu XS, Duan S, (2007) Decreased estradiol release from astrocytes contributes to the neurodegeneration in a mouse model of Niemann-Pick disease type C. Glia 55: 1509-1518.
42. Zhang M, Strnatka D, Donohue C, Hallows JL, Vincent I, et al. (2008) Astrocyte-only Npc1 reduces neuronal cholesterol and triples life span of Npc1-/- mice. J Neurosci Res 86: 2848-2856.
43. Emery B, (2010) Regulation of oligodendrocyte differentiation and myelination. Science 330: 779-782.
44. Sperber BR, Boyle-Walsh EA, Engleka MJ, Gadue P, Peterson AC, et al. (2001) A unique role for Fyn in CNS myelination. J Neurosci 21: 2039-2047.
45. Wake H, Lee PR, Fields RD, (2011) Control of local protein synthesis and initial events in myelination by action potentials. Science 333: 1647-1651.
46. Winters JJ, Ferguson CJ, Lenk GM, Giger-Mateeva VI, Shrager P, et al. (2011) Congenital CNS hypomyelination in the Fig4 null mouse is rescued by neuronal expression of the PI(3,5)P(2) phosphatase Fig4. J Neurosci 31: 17736-17751.
47. Verheijen MH, Camargo N, Verdier V, Nadra K, de Preux Charles AS, et al. (2009) SCAP is required for timely and proper myelin membrane synthesis. Proc Natl Acad Sci U S A 106: 21383-21388.
48. Sun X, Marks DL, Park WD, Wheatley CL, Puri V, et al. (2001) Niemann-Pick C variant detection by altered sphingolipid trafficking and correlation with mutations within a specific domain of NPC1. Am J Hum Genet 68: 1361-1372.
49. Karten B, Vance DE, Campenot RB, Vance JE, (2002) Cholesterol accumulates in cell bodies, but is decreased in distal axons, of Niemann-Pick C1-deficient neurons. J Neurochem 83: 1154-1163.
50. Wojtanik KM, Liscum L, (2003) The transport of low density lipoprotein-derived cholesterol to the plasma membrane is defective in NPC1 cells. J Biol Chem 278: 14850-14856.
51. Hawes CM, Wiemer H, Krueger SR, Karten B, (2010) Pre-synaptic defects of NPC1-deficient hippocampal neurons are not directly related to plasma membrane cholesterol. J Neurochem 114: 311-322.
52. Yazawa I, Giasson BI, Sasaki R, Zhang B, Joyce S, et al. (2005) Mouse model of multiple system atrophy alpha-synuclein expression in oligodendrocytes causes glial and neuronal degeneration. Neuron 45: 847-859.
53. Lee Y, Morrison BM, Li Y, Lengacher S, Farah MH, et al. (2012) Oligodendroglia metabolically support axons and contribute to neurodegeneration. Nature 487: 443-448.
54. Richardson WD, Kessaris N, Pringle N, (2006) Oligodendrocyte wars. Nat Rev Neurosci 7: 11-18.