Inhibition of intracellular cholesterol transport alters presenilin localization and amyloid precursor protein processing in neuronal cells

Journal of Neuroscience

Volumn 22, Issue 5, 2002, Pages 1679-1689

  Runz, Heiko ^a,b   Rietdorf, Jens ^b   Tomic, Inge ^a   De Bernard, Marina ^c   Beyreuther, Konrad ^a   Pepperkok, Rainer ^b   Hartmann, Tobias ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^c UNIVERSITY OF PADOVA   (Italy)

Author keywords

ACAT; Amyloid ; APP processing; Cholesterol; NPC1; Presenilin; Rab7

Indexed keywords

3BETA (2 DIETHYLAMINOETHOXY)ANDROST 5 EN 17 ONE; AMYLOID PRECURSOR PROTEIN; CELL PROTEIN; CHOLESTEROL; GAMMA SECRETASE; PRESENILIN 1; RAB7 PROTEIN; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; ARTICLE; CELL COMPARTMENTALIZATION; CELL ORGANELLE; CELL SELECTION; CELLULAR DISTRIBUTION; CHINESE HAMSTER; CHOLESTEROL TRANSPORT; CONTROLLED STUDY; ENDOCYTOSIS; ENZYME ACTIVITY; HUMAN; HUMAN CELL; INTRACELLULAR TRANSPORT; LYSOSOME; NERVE CELL; NIEMANN PICK DISEASE; OVARY CELL; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN LOCALIZATION; PROTEIN PROCESSING; PROTEIN SYNTHESIS; RISK FACTOR;

EID: 0036523031     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.22-05-01679.2002     Document Type: Article

References (50)

1. Annaert WG, Levesque L, Craessaerts K, Dierinck I, Snellings G, Westaway D, St. George-Hyslop P, Cordell B, Fraser P, De Strooper B (1999) Presenilin 1 controls γ-secretase processing of amyloid precursor protein in pre-Golgi compartments of hippocampal neurons. J Cell Biol 147:277-294.
2. Armogida M, Petit A, Vincent B, Scarzello S, Alves da Costa C, Checler F (2001) Endogenous β-amyloid production in presenilin-deficient embryonic mouse fibroblasts. Nat Cell Biol 3:1030-1033.
3. Bouillot C, Prochiantz A, Rougon G, Allinquant B (1996) Axonal damyloid precursor protein expressed by neurons in vitro is present in a membrane fraction with caveolae-like properties. J Biol Chem 271:7640-7644.
4. Carstea ED, Morris JA, Coleman KG, Loftus SK, Zhang D, Cummings C, Gu J, Rosenfeld MA, Pavan WJ, Krizman DB, Nagle J, Polymeropoulos MH, Sturley SL, Ioannou YA, Higgins ME, Comly M, Cooney A, Brown A, Kaneski CR, Blanchette-Mackie EJ, et al. (1997) Niemann-Pick C1 disease gene: Homology to mediators of cholesterol homeostasis. Science 277:228-231.
5. Corder EH, Saunders AM, Strittmatter WJ, Schmechel DE, Gaskell PC, Small GW, Roses AD, Haines JL, Periak-Vance MA (1993) Gene dose of apolipoprotein type 4 allele and the risk of Alzheimer's disease in late onset families. Science 261:921-923.
6. Cruz JC, Sugii S, Yu C, Chang TY (2000) Role of Niemann-Pick type C1 protein in intracellular trafficking of low density lipoprotein-derived cholesterol. J Biol Chem 275:4013-4021.
7. Culvenor JG, Maher F, Evin G, Malchiodi-Albedi F, Cappai R, Underwood JR, Davis JB, Karran EH, Roberts GW, Beyreuther K, Masters CL (1997) Alzheimer's disease-associated presenilin 1 in neuronal cells: Evidence for localization to the endoplasmic reticulum-Golgi intermediate compartment. J Neurosci Res 49:719-731.
8. DeBose-Boyd RA, Brown MS, Li WP, Nohturfft A, Goldstein JL, Espenshade PJ (1999) Transport-dependent proteolysis of SREBP: Relocation of site-1 protease from Golgi to ER obviates the need for SREBP transport to Golgi. Cell 99:703-712.
9. De Strooper B, Annaert W (2000) Proteolytic processing and cell biological functions of the amyloid precursor protein. J Cell Sci 113:1857-1870.
10. De Strooper B, Annaert W (2001) Presenilins and the intramembrane proteolysis of proteins: Facts and fiction. Nat Cell Biol 3:E221-E225.
11. De Strooper B, Saftig P, Craessaerts K, Vanderstichele H, Guhde G, Annaert W, Von Figura K, Van Leuven F (1998) Deficiency of presenilin-1 inhibits the normal cleavage of amyloid precursor protein. Nature 391:387-390.
12. Dyrks T, Dyrks E, Monning U, Urmoneit B, Turner J, Beyreuther K (1993) Generation of βA4 from the amyloid protein precursor and fragments thereof. FEBS Lett 335:89-93.
13. Falk T, Garver WS, Erickson EP, Wilson JM, Yool AJ (1999) Expression of Niemann-Pick type C transcript in rodent cerebellum in vivo and in vitro. Brain Res 839:49-57.
14. Fassbender K, Simons M, Bergmann C, Stroick M, Lütjohann D, Keller P, Runz H, Kühl S, Bertsch T, von Bergmann K, Hennerici M, Beyreuther K, Hartmann T (2001) Simvastatin strongly reduces levels of Alzheimer's disease β-amyloid peptides Aβ42 and Aβ40 levels in vitro and in vivo. Proc Natl Acad Sci USA 98:5856-5861.
15. Frears ER, Stephens DJ, Walters CE, Davies H, Austin BM (1999) The role of cholesterol in the biosynthesis of β-amyloid. NeuroReport 10:1699-1705.
16. Goslin K, Banker G (1991) Rat hippocampal neurons in low-density culture. In: Cultivating Nerve Cells (Banker G, Goslin K, eds), pp 251-281. Cambridge, MA: MIT.
17. Herz J, Hamann U, Rogne S, Mykelbost O, Gausepohl H, Stanley KK (1988) Surface location and high affinity for calcium of a 500 kD liver membrane protein related to the LDL receptor suggest a physiological role as lipoprotein receptor. EMBO J 7:4119-4127.
18. Ida N, Hartmann T, Pantel J, Schroeder J, Zerfass R, Foerstel H, Sandbrink R, Masters CL, Beyreuther K (1996) Analysis of heterogeneous βA4 peptides in human cerebrospinal fluid and blood by a newly developed sensitive Western blot assay. J Biol Chem 271:22908-22914.
19. Jensen M, Hartmann T, Engvall B, Wang R, Uljon SN, Sennvik K, Naslund J, Muehlhauser F, Nordstedt C, Beyreuther K, Lannfelt L (2000) Quantification of Alzheimer amyloid β-peptides ending at residues 40 and 42 by novel ELISA systems. Mol Med 6:291-302.
20. Jick H, Zornberg GL, Jick SS, Seshadri S, Drachman DA (2000) Statins and the risk of dementia. Lancet 356:1627-1631.
21. Ko DC, Gordon MD, Jin JY, Scott MP (2001) Dynamic movements of organelles containing Niemann-Pick C1 protein: NPC1 involvement in late endocytic events. Mol Biol Cell 12:601-614.
22. Kobayashi T, Stang E, Fang KS, De Moerloose P, Parton RG, Gruenberg J (1998) A lipid associated with the anti-phospholipid syndrome regulates endosome structure and function. Nature 392:193-197.
23. Kojro E, Gimpl G, Lammich S, März W, Fahrenholz F (2001) Low cholesterol stimulates the nonamyloidogenic pathway by its effect on the α-secretase ADAM10. Proc Natl Acad Sci USA 98:5815-5820.
24. Kounnas MZ, Moir RD, Rebeck GW, Bush AI, Argraves WS, Tanzi RE, Hyman BT, Strickland DK (1995) LDL receptor-related protein, a multifunctional ApoE receptor, binds secreted β-amyloid precursor protein and mediates its degradation. Cell 82:331-340.
25. Kovacs DM, Fausett HJ, Page KJ, Kim TW, Moir RD, Merriam DE, Hollister RD, Hallmark OG, Mancini R, Felsenstein KM, Hyman BT, Tanzi RE, Wasco W (1996) Alzheimer-associated presenilins 1 and 2: Neuronal expression in brain and localization to intracellular membranes in mammalian cells. Nat Med 2:224-229.
26. Lange Y, Ye J, Rigney M, Steck T (2000) Cholesterol movement in Niemann-Pick type C cells and in cells treated with amphiphiles. J Biol Chem 275:17468-17475.
27. Liscum L, Ruggiero RM, Faust JR (1989) The intracellular transport of low-density lipoprotein-derived cholesterol is defective in Niemann-Pick type C fibroblasts. J Cell Biol 108:1625-1636.
28. Lusa S, Blom TS, Eskelinen EL, Kuismanen E, Mansson JE, Simons K, Ikonen E (2001) Depletion of rafts in late endocytic membranes is controlled by NPC1-dependent recycling of cholesterol to the plasma membrane. J Cell Sci 114:1893-1900.
29. 24S-hydroxycholesterol from the brain into the circulation. Proc Natl Acad Sci USA 93:9799-9804.
30. Naureckiene S, Sleat DE, Lackland H, Fensom A, Vanier MT, Wattiaux R, Jadot M, Lobel P (2000) Identification of HE1 as the second gene of Niemann-Pick C disease. Science 290:2298-2301.
31. Neufeld EB, Wastney M, Patel S, Suresh S, Cooney AM, Dwyer NK, Roff CF, Ohno K, Morris JA, Carstea ED, Incardona JP, Strauss III JF, Vanier MT, Patterson MC, Brady RO, Pentchev PG, Blanchette-Mackie EJ (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.
32. Orci L, Brown MS, Goldstein JL, Garcia-Segura LM, Anderson G (1984) Increase in membrane cholesterol: A possible trigger for degradation of HMG-CoA reductase and crystalloid endoplasmic reticulum in UT-1 cells. Cell 36:835-845.
33. Papini E, Gottardi E, Satin B, de Bernard M, Massari P, Telford J, Rappuoli R, Sato SB, Montecucco C (1996) The vacuolar ATPase proton pump is present on intracellular vacuoles induced by Helicobacter pylori. J Med Microbiol 45:84-89.
34. Pentchev PG, Comly ME, Kruth HS, Tokoro T, Butler J, Sokol J, Filling-Katz M, Quirk JM, Marshall DC, Patel S, Vanier MT, Brady RO (1987) Group C Niemann-Pick disease: Faulty regulation of lipoprotein uptake and cholesterol storage in cultured fibroblasts. FASEB J 1:40-45.
35. Pol A, Luetterforst R, Lindsay M, Heino S, Ikonen E, Parton R (2001) A caveolin dominant negative mutant associates with lipid bodies and induces intracellular cholesterol imbalance. J Cell Biol 152:1057-1070.
36. Puglielli L, Konopka G, Pack-Chung E, MacKenzie Ingano LA, Berezovska O, Hyman BT, Chang TY, Tanzi RE, Kovacs DM (2001) Acyl-coenzyme A:cholesterol acyltransferase modulates the generation of the amyloid β-peptide. Nat Cell Biol 3:905-912.
37. Refolo LM, Malester B, LaFrancois J, Bryant-Thomas T, Wang R, Tint GS, Sambamurti K, Duff KE, Pappolla MA (2000) Hypercholesteremia accelerates the Alzheimer's amyloid pathology in a transgenic mouse model. Neurobiol Dis 7:321-331.
38. Refolo LM, Pappolla MA, LaFrancois J, Malester B, Schmidt SD, Thomas-Bryant T, Tint GS, Wang R, Mercken M, Petanceska SS, Duff KE (2001) A cholesterol-lowering drug reduces β-amyloid pathology in a transgenic mouse model of Alzheimer's disease. Neurobiol Dis 8:890-899.
39. Riddell DR, Christie G, Hussain I, Dingwall C (2001) Compartmentalization of β-secretase (Asp2) into low-buoyant density, noncaveolar lipid rafts. Curr Biol 11:1288-1293.
40. Sakashita N, Miyazaki A, Takeya M, Horiuchi S, Chang CCY, Chang TY, Takahashi K (2000) Localization of human acyl-CoA:cholesterol acyltransferase-1 in macrophages and in various tissues. Am J Pathol 156:227-236.
41. Scales SJ, Pepperkok R, Kreis TE (1997) Visualization of ER-to-Golgi transport in living cells reveals a sequential mode of action for COPII and COPI. Cell 90:1137-1148.
42. Simons M, Keller P, De Strooper B, Beyreuther K, Dotti CG, Simons K (1998) Cholesterol depletion inhibits the generation of β-amyloid in hippocampal neurons. Proc Natl Acad Sci USA 95:6460-6464.
43. Skovronsky DM, Doms RW, Lee VM (1998) Detection of a novel intraneuronal pool of insoluble amyloid β-protein that accumulates with time in culture. J Cell Biol 141:1031-1039.
44. Subtil A, Gaidarov I, Kobylarz K, Lampson MA, Keen JH, McGraw TE (1999) Acute cholesterol depletion inhibits clathrin-coated pit budding. Proc Natl Acad Sci USA 96:6775-6780.
45. Tabas I, Rosoff WJ, Boykow GC (1988) Acyl-coenzyme A:cholesterol acyltransferase in macrophages utilizes a cellular pool of cholesterol oxidase-accessible cholesterol as substrate. J Biol Chem 263:1266-1272.
46. Tienari PJ, De Strooper B, Ikonen E, Simons M, Weidemann A, Czech C, Hartmann T, Ida N, Multhaup G, Masters CL, van Leuven F, Beyreuther K, Dotti CG (1996) The β-amyloid domain is essential for axonal sorting of amyloid precursor protein. EMBO J 15:5218-5229.
47. Wolozin B, Kellman W, Rousseau P, Celesia GG, Siegel G (2000) Decreased prevalence of Alzheimer disease associated with 3-hydroxy-3-methylglutaryl coenzyme A reductase inhibitors. Arch Neurol 57:1439-1443.
48. Xia W, Ray WJ, Ostaszewski BL, Rahmati T, Kimberly WT, Wolfe MS, Zhang J, Goate AM, Selkoe DJ (2000) Presenilin complexes with the C-terminal fragments of amyloid precursor protein at the sites of amyloid β-protein generation. Proc Natl Acad Sci USA 97:9299-9304.
49. Yamazaki T, Chang TY, Haass C, Ihara Y (2001) Accumulation and aggregation of amyloid β-protein in late endosomes of Niemann-Pick type C cells. J Biol Chem 276:4454-4460.
50. Zhang M, Dwyer NK, Neufeld EB, Love DC, Cooney A, Comly M, Patel S, Watari H, Strauss III JF, Pentchev PG, Hanover JA, Blanchette-Mackie EJ (2001) Sterol-modulated glycolipid sorting occurs in Niemann-Pick C1 late endosomes. J Biol Chem 276:3417-3425.