The Niemann-Pick C1 protein in recycling endosomes of presynaptic nerve terminals

Journal of Lipid Research

Volumn 47, Issue 3, 2006, Pages 504-514

  Karten, Barbara ^a,b   Campenot, Robert B ^b   Vance, Dennis E ^a,b   Vance, Jean E ^a,b  

^a CANADIAN INSTITUTES OF HEALTH RESEARCH   (Canada)

^b UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Cholesterol; Synaptic vesicles; Synaptosomes

Indexed keywords

CHOLESTEROL;

ANIMAL TISSUE; ARTICLE; CELL TYPE; CELL VACUOLE; CHEMICAL ANALYSIS; CONTROLLED STUDY; ENDOSOME; MORPHOLOGY; MOUSE; MOUSE STRAIN; NERVE CELL; NERVE CELL LESION; NERVE FIBER; NIEMANN PICK DISEASE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEFICIENCY; PROTEIN LOCALIZATION; SYMPATHETIC NERVE; SYNAPSE VESICLE; SYNAPTOSOME;

ANIMALS; CELLS, CULTURED; CEREBELLUM; CHOLESTEROL; ENDOSOMES; LIPID METABOLISM; LYSOSOMES; MICE; MICE, INBRED BALB C; MODELS, MOLECULAR; NEURONS; PRESYNAPTIC TERMINALS; PROTEINS; SYNAPTOPHYSIN; TRANSFECTION; VESICULAR TRANSPORT PROTEINS;

EID: 33644783621     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M500482-JLR200     Document Type: Article

References (45)

1. Ikonen, E., and M. Holtta-Vuori. 2004. Cellular pathology of Niemann-Pick type C disease. Semin. Cell Dev. Biol. 15: 445-454.
2. Chang, T. Y., P. C. Reid, S. Sugii, N. Ohgami, J. C. Cruz, and C. C. Chang. 2005. Niemann-Pick type C disease and intracellular cholesterol trafficking. J. Biol. Chem. 280: 20917-20920.
3. Liscum, L. 2000. Niemann-Pick type C mutations cause lipid traffic jam. Traffic. 1: 218-225.
4. Pentchev, P. G., M. T. Vanier, K. Suzuki, and M. C. Patterson. 1995. Niemann-Pick disease type C: a cellular cholesterol lipidosis. In The Metabolic and Molecular Bases of Inherited Disease. A. L. Beaudet, C. R. Scriver, W. S. Sly, and D. Valle, editors. McGraw Hill, New York. 2625-2639.
5. Sturley, S. L., M. C. Patterson, W. Balch, and L. Liscum. 2004. The pathophysiology and mechanisms of NP-C disease. Biochim. Biophys. Acta. 1685: 83-87.
6. Neufeld, E. B., M. Wastney, S. Patel, S. Suresh, A. M. Cooney, N. K. Dwyer, C. F. Roff, K. Ohno, J. A. Morris, E. D. Carstea, 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, M. E., J. P. Davies, F. W. Chen, and Y. A. Ioannou. 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. Loftus, S. K., J. A. Morris, E. D. Carstea, J. Z. Gu, C. Cummings, A. Brown, J. Ellison, K. Ohno, M. A. Rosenfeld, D. A. Tagle, et al. 1997. Murine model of Niemann-Pick C disease: mutation in a cholesterol homeostasis gene. Science. 277: 232-235.
9. Carstea, E. D., J. A. Morris, K. G. Coleman, S. K. Loftus, D. Zhang, C. Cummings, J. Gu, M. A. Rosenfeld, W. J. Pavan, D. B. Krizman, et al. 1997. Niemann-Pick C1 disease gene: homology to mediators of cholesterol momeostasis. Science. 277: 228-231.
10. Sokol, J., E. J. Blanchette-Mackie, H. S. Kruth, N. K. Dwyer, L. M. Amende, J. D. Butler, E. Robinson, S. Patel, R. O. Brady, M. E. Comly, et al. 1988. Type C Niemann-Pick disease. J. Biol. Chem. 263: 3411-3417.
11. Liscum, L., R. M. Ruggiero, and J. R. Faust. 1989. The intracellular transport of low density-derived cholesterol is defective in Niemann-Pick type C fibroblasts. J. Cell Biol. 108: 1625-1636.
12. Naureckiene, S., D. E. Sleat, H. Lackland, A. Fensom, M. T. Vanier, R. Wattiaux, M. Jadot, and P. Lobel. 2000. Identification of HE1 as the second gene of Niemann-Pick C disease. Science. 290: 2298-2301.
13. Friedland, N., H. L. Liou, P. Lobel, and A. M. Stock. 2003. Structure of a cholesterol-binding protein deficient in Niemann-Pick type C2 disease. Proc. Natl. Acad. Sci. USA. 100: 2512-2517.
14. Ko, D. C., J. Binkley, A. Sidow, and M. P. Scott. 2003. The integrity of a cholesterol-binding pocket in Niemann-Pick C2 protein is necessary to control lysosome cholesterol levels. Proc. Natl. Acad. Sci. USA. 100: 2518-2525.
15. Liscum, L., and S. L. Sturley. 2004. Intracellular trafficking of Niemann-Pick C proteins 1 and 2: obligate components of subcellular lipid transport. Biochim. Biophys. Acta. 1685: 22-27.
16. Cruz, J. C., S. Sugii, C. Yu, and T-Y. Chang. 2000. Role of Niemann-Pick type C1 protein in intracellular trafficking of low density lipoprotein-derived cholesterol. J. Biol. Chem. 275: 4013-4021.
17. Cruz, J. C., and T-Y. Chang. 2000. Fate of endogenously synthesized cholesterol in Niemann Pick type C1 cells. J. Biol. Chem. 275: 41309-41316.
18. Goldin, E., C. F. Roff, S. P. F. Miller, C. Rodriguez-Lafrasse, M. T. Vanier, R. O. Brady, and P. G. Pentchev. 1992. Type C Niemann-Pick disease: a murine model of the lysosomal cholesterol lipidosis accumulates sphingosine and sphinganine in liver. Biochim. Biophys. Acta. 1127: 303-311.
19. Zervas, M., K. L. Somers, M. A. Thrall, and S. U. Walkley. 2001. Critical role for glycosphingolipids in Niemann-Pick disease type C. Curr. Biol. 11: 1283-1287.
20. Watanabe, Y., S. Akaboshi, G. Ishida, T. Takeshima, T. Yano, M. Taniguchi, K. Ohno, and K. Nakashima. 1998. Increased levels of GM2 ganglioside in fibroblasts from a patient with juvenile Niemann-Pick disease type C. Brain Dev. 20: 95-97.
21. Karten, B., H. Hayashi, G. A. Francis, R. B. Campenot, D. E. Vance, and J. E. Vance. 2005. Generation and function of astroglial lipoproteins from Niemann-Pick type C1-deficient mice. Biochem. J. 387: 779-788.
22. Karten, B., D. E. Vance, R. B. Campenot, and J. E. Vance. 2002. Cholesterol accumulates in cell bodies, but is decreased in distal axons, of Niemann-Pick C1-deficient neurons. J. Neurochem. 83: 1154-1163.
23. Karten, B., D. E. Vance, R. B. Campenot, and J. E. Vance. 2003. Trafficking of cholesterol from cell bodies to distal axons in Niemann Pick C1-deficient neurons. J. Biol. Chem. 278: 4168-4175.
24. Parton, R. G., K. Simons, and C. G. Dotti. 1992. Axonal and dendritic endocytic pathways in cultured neurons. J. Cell Biol. 119: 123-137.
25. Parton, R. G., and C. G. Dotti. 1993. Cell biology of neuronal endocytosis. J. Neurosci. Res. 36: 1-9.
26. Paul, C. A., P. C. Reid, A. K. Boegle, B. Karten, M. Zhang, Z. G. Jiang, D. Franz, L. Lin, T. Y. Chang, J. E. Vance, et al. 2005. Adenovirus expressing an NPC1-GFP fusion gene corrects neuronal and nonneuronal defects associated with Niemann Pick type C disease. J. Neurosci. Res. 81: 706-719.
27. Dunkley, P. R., J. W. Heath, S. M. Harrison, P. E. Jarvie, P. J. Glenfield, and J. A. Rostas. 1988. A rapid Percoll gradient procedure for isolation of synaptosomes directly from an S1 fraction: homogeneity and morphology of subcellular fractions. Brain Res. 441: 59-71.
28. Goncalves, P. P., and A. P. Carvalho. 1997. Membrane potential manipulation in synaptic plasma membrane vesicles for studying neurotransmitter uptake and release. Brain Res. Brain Res. Protoc. 1: 1-12.
29. Clift-O'Grady, L., A. D. Linstedt, A. W. Lowe, E. Grote, and R. B. Kelly. 1990. Biogenesis of synaptic vesicle-like structures in a pheochromocytoma cell line PC-12. J. Cell Biol. 110: 1693-1703.
30. Zhou, X., and G. Arthur. 1992. Improved procedures for the determination of lipid phosphorus by malachite green. J. Lipid Res. 33: 1233-1236.
31. Spurr, A. R. 1969. A low-viscosity epoxy resin embedding medium for electron microscopy. J. Ultrastruct. Res. 26: 31-43.
32. Bednarski, E., C. E. Ribak, and G. Lynch. 1997. Suppression of cathepsins B and L causes a proliferation of lysosomes and the formation of meganeurites in hippocampus. J. Neurosci. 17: 4006-4021.
33. Sahenk, Z., J. N. Whitaker, and J. R. Mendell. 1990. Immunocytochemical evidence for the retrograde transport of intraaxonal cathepsin D: possible relevance to the dying-back process. Brain Res. 510: 1-6.
34. Buckley, K. M., and S. C. Landis. 1983. Morphological studies of synapses and varicosities in dissociated cell cultures of sympathetic neurons. J. Neurocytol. 12: 67-92.
35. Buckley, K. M., and S. C. Landis. 1983. Morphological studies of neurotransmitter release and membrane recycling in sympathetic nerve terminals in culture. J. Neurocytol. 12: 93-116.
36. Van Lookeren Campagne, M., A. B. Oestreicher, P. M. Van Bergen en Henegouwen, and W. H. Gispen. 1990. Ultrastructural double localization of B-50/GAP43 and synaptophysin (p38) in the neonatal and adult rat hippocampus. J. Neurocytol. 19: 948-961.
37. Phillips, S. N., J. W. Benedict, J. M. Weimer, and D. A. Pearce. 2005. CLN3, the protein associated with Batten disease: structure, function and localization. J. Neurosci. Res. 79: 573-583.
38. Luiro, K., O. Kopra, M. Lehtovirta, and A. Jalanko. 2001. CLN3 protein is targeted to neuronal synapses but excluded from synaptic vesicles: new clues to Batten disease. Hum. Mol. Genet. 10: 2123-2131.
39. Sudhof, T. C. 2004. The synaptic vesicle cycle. Annu. Rev. Neurosci. 27: 509-547.
40. Paul, C. A., A. K. Boegle, and R. A. Maue. 2004. Before the loss: neuronal dysfunction in Niemann-Pick type C disease. Biochim. Biophys. Acta. 1685: 63-76.
41. Thiele, C., M. J. Hannah, F. Fahrenholz, and W. B. Huttner. 2000. Cholesterol binds to synaptophysin and is required for biogenesis of synaptic vesicles. Nat. Cell Biol. 2: 42-49.
42. Mitter, D., C. Reisinger, B. Hinz, S. Hollmann, S. V. Yelamanchili, S. Treiber-Held, T. G. Ohm, A. Herrmann, and G. Ahnert-Hilger. 2003. The synaptophysin/synaptobrevin interaction critically depends on the cholesterol content. J. Neurochem. 84: 35-42.
43. Marxen, M., W. Volknandt, and H. Zimmermann. 1999. Endocytic vacuoles formed following a short pulse of K+-stimulation contain a plethora of presynaptic membrane proteins. Neuroscience. 94: 985-996.
44. Shimizu, H., S. Kawamura, and K. Ozaki. 2003. An essential role of Rab5 in uniformity of synaptic vesicle size. J. Cell Sci. 116: 3583-3590.
45. Sugimoto, Y., H. Ninomiya, Y. Ohsaki, K. Higaki, J. P. Davies, Y. A. Ioannou, and K. Ohno. 2001. Accumulation of cholera toxin and GM1 ganglioside in the early endosome of Niemann-Pick C1-deficient cells. Proc. Natl. Acad. Sci. USA. 98: 12391-12396.