A novel cholesterol stain reveals early neuronal cholesterol accumulation in the Niemann-Pick type C1 mouse brain

Journal of Lipid Research

Volumn 45, Issue 3, 2004, Pages 582-591

  Reid, Patrick C ^a   Sakashita, Naomi ^a   Sugii, Shigeki ^a   Ohno Iwashita, Yoshiko ^b   Shimada, Yukiko ^b   Hickey, William F ^a   Chang, Ta Yuan ^a  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

^b TOKYO METROPOLITAN INSTITUTE OF GERONTOLOGY   (Japan)

Author keywords

Astrocyte; BC ; Intracellular cholesterol accumulation; Neurodegeneration; Neuron; Niemann Pick Disease; Purkinje cell

Indexed keywords

CHOLESTEROL; FILIPIN; GANGLIOSIDE; LIPID;

ADOLESCENT; ANIMAL TISSUE; ARTICLE; CENTRAL NERVOUS SYSTEM; CHOLESTEROL METABOLISM; CONFOCAL MICROSCOPY; DENDRITIC CELL; GLIA CELL; MOUSE; NERVE CELL NECROSIS; NERVE DEGENERATION; NERVE INJURY; NEWBORN; NIEMANN PICK DISEASE; NONHUMAN; PRIORITY JOURNAL; PURKINJE CELL; THALAMUS;

ANIMALS; ANIMALS, NEWBORN; BRAIN CHEMISTRY; CHOLESTEROL; MICE; MICE, NEUROLOGIC MUTANTS; NEURONS; NIEMANN-PICK DISEASES; PROTEINS; STAINING AND LABELING; TIME FACTORS;

EID: 1542513994     PISSN: 00222275     EISSN: None     Source Type: Journal    
DOI: 10.1194/jlr.D300032-JLR200     Document Type: Article

References (41)

1. Patterson, M. C., M. T. Vanier, K. Suzuki, J. A. Morris, E. Carstea, E. B. Neufeld, J. E. Blanchette-Mackie, and P. G. Pentchev. 2001. Niemann-Pick disease type C: a lipid trafficking disorder. In The Metabolic and Molecular Bases of Inherited Disease. C. R. Scriver, A. L. Beaudet, W. S. Sly, and D. Valle, editors. McGraw-Hill, New York. 3611-3633.
2. 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, J. Nagle, M. H. Polymeropoulos, S. L. Sturley, Y. A. Ioannou, M. E. Higgins, M. Comly, A. Cooney, A. Brown, C. R. Kaneski, E. J. Blanchette-Mackie, N. K. Dwyer, E. B. Neufeld, T. Y. Chang, L. Liscum, J. F. Strauss III, K. Ohno, M. Zeigler, R. Carmi, J. Sokol, D. Markie, R. R. O'Neill, O. P. van Diggelen, M. Elleder, M. C. Patterson, R. O. Brady, M. T. Vanier, P. G. Pentchev, and D. A. Tagle. 1997. Niemann-Pick C1 disease gene: homology to mediators of cholesterol homeostasis. Science. 277: 228-231.
3. Ko, D. C., M. D. Gordon, J. Y. Jin, and M. P. Scott. 2002. Dynamic movements of organelles containing Niemann-Pick C1 protein: NPC1 involvement in late endocytic events. Mol. Biol. Cell. 12: 601-614.
4. Zhang, M., N. K. Dwyer, D. C. Love, A. Cooney, M. Comly, E. B. Neufeld, P. G. Pentchev, E. J. Blanchette-Mackie, and J. A. Hanover. 2001. Cessation of rapid late endosomal tubulovesicular trafficking in Niemann-Pick type C1 disease. Proc. Natl. Acad. Sci. USA. 98: 4466-4471.
5. Wojtanik, K. M., and L. Liscum. 2003. The transport of LDL-derived cholesterol to the plasma membrane is defective in NPC1 cells. J. Biol. Chem. 278: 14850-14856.
6. Sugii, S., P. C. Reid, N. Ohgami, H. Du, and T. Y. Chang. 2003. Distinct endosomal compartments in early trafficking of low density lipoprotein-derived cholesterol. J. Biol. Chem. 278: 27180-27189.
7. Lange, Y., J. Ye, and T. L. Steck. 1998. Circulation of cholesterol between lysosomes and the plasma membrane. J. Biol. Chem. 273: 18915-18922.
8. 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.
9. 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.
10. Reid, P. C., S. Sugii, and T. Y. Chang. 2003. Trafficking defects in endogenously synthesized cholesterol in fibroblasts, macrophages, hepatocytes, and glial cells from Niemann-Pick type C1 mice. J. Lipid Res. 44: 1010-1019.
11. 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, J. P. Incardona, J. F. Strauss III, M. T. Vanier, M. C. Patterson, R. O. Brady, P. G. Pentchev, and E. J. Blanchette-Mackie. 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.
12. Liscum, L. 2000. Niemann-Pick type C mutations cause lipid traffic jam. Traffic. 1: 218-225.
13. Davies, J. P., F. W. Chen, and Y. A. Ioannou. 2000. Transmembrane molecular pump activity of Niemann-Pick C1 protein. Science. 290: 2295-2298.
14. 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.
15. 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.
16. Xie, C., S. D. Turley, P. G. Pentchev, and J. M. Dietschy. 1999. Cholesterol balance and metabolism in mice with loss of function Niemann-Pick C protein. Am. J. Physiol. 276: E336-E344.
17. Vanier, M. T. 1999. Lipid changes in Niemann-Pick disease type C brain: personal experience and review of the literature. Neurochem. Res. 24: 481-489.
18. Zervas, M., K. Dobrenis, and S. U. Walkley. 2001. Neurons in Niemann-Pick disease type C accumulate gangliosides as well as unesterified cholesterol and undergo dendritic and axonal alterations. J. Neuropathol. Exp. Neurol. 60: 49-64.
19. Zervas, M., K. L. Somers, M. A. Thrall, and S. U. Walkley. 2001. Critical role of glycosphingolipids in Niemann-Pick disease type C. Curr. Biol. 11: 1283-1287.
20. Treiber-Held, S., R. Distl, V. Meske, F. Albert, and T. G. Ohm. 2003. Spatial and temporal distribution of intracellular free cholesterol in brains of a Niemann-pick type C mouse model showing hyper-phosphorylated tau protein. Implications for Alzherimer's disease. J. Pathol. 200: 95-103.
21. Ong, W-Y., U. Kumar, R. C. Switzer, A. Sidhu, G. Suresh, C-Y. Hu, and S. C. Patel. 2001. Neurodegeneration in Niemann-Pick type C disease mice. Exp. Brain Res. 141: 218-231.
22. German, D. C., C-L. Liang, T. Song, U. Yazdani, C. Xie, and J. M. Dietschy. 2002. Neurodegeneration in the Niemann-Pick C mouse: glial involvement. Neuroscience. 109: 437-450.
23. Iwamoto, M., I. Morita, M. Fukuda, S. Murota, S. Ando, and Y. Ohno-Iwashita. 1997. A biotinylated perfringolysin O derivative: a new probe for detection of cell surface cholesterol. Biochim. Biophys. Acta. 1327: 222-230.
24. Waheed, A. A., Y. Shimada, H. F. Heijnen, M. Nakamura, M. Inomata, M. Hayashi, S. Iwashita, J. W. Slot, and Y. Ohno-Iwashita. 2001. Selective binding of perfringolysin O derivative to cholesterol-rich membrane microdomains (rafts). Proc. Natl. Acad. Sci. USA. 98: 4926-4931.
25. Sugii, S., P. C. Reid, N. Ohgami, Y. Shimada, R. A. Maue, H. Ninomiya, Y. Ohno-Iwashita, and T. Y. Chang. 2003. Biotinylated theta toxin derivative as a probe to examine intracellular cholesterol domains in normal and Niemann-Pick type C1 cells. J. Lipid Res. 44: 1033-1041.
26. Mobius, W., Y. Ohno-Iwashita, E. G. van Donselaar, V. M. Oorschot, Y. Shimada, T. Fujimoto, H. F. Heijnen, H. J. Geuze, and J. W. Slot. 2002. Immunoelectron microscopic localization of cholesterol using biotinylated and non-cytolytic perfringolysin O. J. Histochem. Cytochem. 50: 43-55.
27. 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, P. G. Pentchev, and W.J. Pavan. 1997. Murine model of Niemann-Pick C disease: mutation in a cholesterol homeostasis gene. Science. 277: 232-235.
28. Taniguchi, M., Y. Shinoda, H. Ninomiya, M. T. Vanier, and K. Ohno. 2001. Sites and temporal changes of gangliosides GM1/GM2 storage in the Niemann-Pick disease type C mouse brain. BrainDev. 23: 414-421.
29. Gondre-Lewis, M. C., R. McGlynn, and S. U. Walkley. 2003. Cholesterol accumulation in NPC1-deficient neurons is ganglioside dependent. Curr. Biol. 13: 1324-1329.
30. Liu, Y., Y. P. Wu, R. Wada, E. B. Neufeld, K. A. Mullin, A. C. Howard, P. G. Pentchev, M. T. Vanier, K. Suzuki, and R. L. Proia. 2000. Alleviation of neuronal ganglioside storage does not improve the clinical course of the Niemann-Pick C disease mouse. Hum. Mol. Genet. 9: 1087-1092.
31. 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 type C1-deficient neurons. J. Neurochem. 83: 1154-1163.
32. Higashi, Y., S. Murayama, P. G. Pentchev, and K. Suzuki. 1993. Cerebellar degeneration in the Niemann-Pick type C mouse. Acta. Neuropathol.(Berl). 85: 175-184.
33. Hu, C. Y., W. Y. Ong, and S. C. Patel. 2000. Regional distribution of NPC1 protein in monkey brain. J. Neurocytol. 29: 765-773.
34. Patel, S. C., S. Suresh, U. Kumar, C. Y. Hu, A. Cooney, E. J. Blanchette-Mackie, E. B. Neufeld, R. C. Patel, R. O. Brady, Y. C. Patel, P. G. Pentchev, and W. Y. Ong. 1999. Localization of Niemann-pick C1 proteins in astrocytes: implications for neuronal degeneration in Niemann-Pick type C disease. Proc. Natl. Acad. Sci. USA. 96: 1657-1662.
35. German, D. C., E. M. Quintero, C. L. Liang, C. Xie, and J. M. Dietschy. 2001. Degeneration of neurons and glia in the Niemann-Pick C mouse is unrelated to the low-density lipoprotein receptor. Neuroscience. 105: 999-1005.
36. Mauch, D. H., K. Nagler, S. Schumacher, C. Goritz, E. C. Muller, A. Otto, and F. W. Pfieger. 2001. CNS synaptogenesis promoted by glia-derived cholesterol. Science. 294: 1354-1357.
37. Simons, K., and E. Ikonen. 1997. Functional rafts in cell membranes. Nature. 387: 569-572.
38. Brown, D. A., and E. London. 1998. Function of lipid rafts in biological membranes. Annu. Rev. Cell Dev. Biol. 14: 111-136.
39. Simons, K., and J. Gruenberg. 2000. Jamming the endosomal system: lipid rafts and lysosomal storage diseases. Trends Cell Biol. 10: 459-462.
40. Puri, V., R. Watanabe, M. Dominguez, X. Sun, C. L. Wheatley, D. L. Marks, and R. E. Pagano. 1999. Cholesterol modulates membrane traffic along the endocytic pathway in sphingolipid-storage diseases. Nat. Cell Biol. 1: 386-388.
41. Reagan, J. W., Jr., M. L. Hubbert, and G. S. Shelness. 2000. Post-translational regulation of acid sphingomyelinase in Niemann-Pick type C1 fibroblasts and free cholesterol-enriched Chinese hamster ovary cells. J. Biol. Chem. 275: 38104-38110.