Cholesterol-depletion corrects APP and BACE1 misstrafficking in NPC1-deficient cells

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1822, Issue 8, 2012, Pages 1270-1283

  Malnar, Martina ^a   Kosicek, Marko ^a   Lisica, Ana ^a   Posavec, Melanija ^a   Krolo, Ana ^a   Njavro, Jasenka ^a   Omerbasic, Damir ^a   Tahirovic, Sabina ^b   Hecimovic, Silva ^a  

^a RUDER BO KOVI INSTITUTE   (Croatia)

^b GERMAN CENTER FOR NEURODEGENERATIVE DISEASES DZNE   (Germany)

Author keywords

Alzheimer's disease; APP; BACE1; Cholesterol; Endocytosis; NPC1

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; BETA SECRETASE; BETA SECRETASE 1; CHOLESTEROL;

ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL MIGRATION; CELL SURFACE; ENDOCYTOSIS; ENDOSOME; FEMALE; INTERNALIZATION; NIEMANN PICK DISEASE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN LOCALIZATION; RAT;

AMYLOID BETA-PROTEIN PRECURSOR; AMYLOID PRECURSOR PROTEIN SECRETASES; ANDROSTENES; ANIMALS; CHO CELLS; CHOLESTEROL; CRICETINAE; ENDOCYTOSIS; ENDOSOMES; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MICROSCOPY, CONFOCAL; NEURONS; NIEMANN-PICK DISEASE, TYPE C; RATS; TRANSFECTION;

EID: 84861388527     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2012.04.002     Document Type: Article

References (55)

1. Hardy J. Testing times for the "amyloid cascade hypothesis". Neurobiol. Aging 2002, 23:1073-1074.
2. Vassar R., Bennett B.D., Babu-Khan S., Kahn S., Mendiaz E.A., Denis P., Teplow D.B., Ross S., Amarante P., Loeloff R., Luo Y., Fisher S., Fuller J., Edenson S., Lile J., Jarosinski M.A., Biere A.L., Curran E., Burgess T., Louis J.C., Collins F., Treanor J., Rogers G., Citron M. Beta-secretase cleavage of Alzheimer's amyloid precursor protein by the transmembrane aspartic protease BACE. Science 1999, 286:735-741.
3. Scheuner D., Eckman C., Jensen M., Song X., Citron M., Suzuki N., Bird T.D., Hardy J., Hutton M., Kukull W., Larson E., Levy-Lahad E., Viitanen M., Peskind E., Poorkaj P., Schellenberg G., Tanzi R., Wasco W., Lannfelt L., Selkoe D., Younkin S. Secreted amyloid beta-protein similar to that in the senile plaques of Alzheimer's disease is increased in vivo by the presenilin 1 and 2 and APP mutations linked to familial Alzheimer's disease. Nat. Med. 1996, 2:864-870.
4. Xia W., Ray W.J., Ostaszewski B.L., Rahmati T., Kimberly W.T., Wolfe M.S., Zhang J., Goate A.M., Selkoe D.J. Presenilin complexes with the C-terminal fragments of amyloid precursor protein at the sites of amyloid beta-protein generation. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:9299-9304.
5. Edbauer D., Winkler E., Regula J.T., Pesold B., Steiner H., Haass C. Reconstitution of gamma-secretase activity. Nat. Cell Biol. 2003, 5:486-488.
6. Kimberly W.T., LaVoie M.J., Ostaszewski B.L., Ye W., Wolfe M.S., Selkoe D.J. Gamma-secretase is a membrane protein complex comprised of presenilin, nicastrin, Aph-1, and Pen-2. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:6382-6387.
7. Refolo L.M., Sambamurti K., Efthimiopoulos S., Pappolla M.A., Robakis N.K. Evidence that secretase cleavage of cell surface Alzheimer amyloid precursor occurs after normal endocytic internalization. J. Neurosci. Res. 1995, 40:694-706.
8. Perez R.G., Soriano S., Hayes J.D., Ostaszewski B., Xia W., Selkoe D.J., Chen X., Stokin G.B., Koo E.H. Mutagenesis identifies new signals for beta-amyloid precursor protein endocytosis, turnover, and the generation of secreted fragments, including Abeta42. J. Biol. Chem. 1999, 274:18851-18856.
9. Cirrito J.R., Kang J.E., Lee J., Stewart F.R., Verges D.K., Silverio L.M., Bu G., Mennerick S., Holtzman D.M. Endocytosis is required for synaptic activity-dependent release of amyloid-beta in vivo. Neuron 2008, 58:42-51.
10. Sisodia S.S. Beta-amyloid precursor protein cleavage by a membrane-bound protease. Proc. Natl. Acad. Sci. U. S. A. 1992, 89:6075-6079.
11. Lichtenthaler S.F., Haass C., Steiner H. Regulated intramembrane proteolysis - lessons from amyloid precursor protein processing. J. Neurochem. 2011, 117:779-796.
12. Sannerud R., Annaert W. Trafficking, a key player in regulated intramembrane proteolysis. Semin. Cell Dev. Biol. 2009, 20:183-190.
13. Cataldo A.M., Peterhoff C.M., Troncoso J.C., Gomez-Isla T., Hyman B.T., Nixon R.A. Endocytic pathway abnormalities precede amyloid beta deposition in sporadic Alzheimer's disease and Down syndrome: differential effects of APOE genotype and presenilin mutations. Am. J. Pathol. 2000, 157:277-286.
14. Cataldo A.M., Petanceska S., Terio N.B., Peterhoff C.M., Durham R., Mercken M., Mehta P.D., Buxbaum J., Haroutunian V., Nixon R.A. Abeta localization in abnormal endosomes: association with earliest Abeta elevations in AD and Down syndrome. Neurobiol. Aging 2004, 25:1263-1272.
15. Ginsberg S.D., Alldred M.J., Counts S.E., Cataldo A.M., Neve R.L., Jiang Y., Wuu J., Chao M.V., Mufson E.J., Nixon R.A., Che S. Microarray analysis of hippocampal CA1 neurons implicates early endosomal dysfunction during Alzheimer's disease progression. Biol. Psychiatry 2010, 68:885-893.
16. Grbovic O.M., Mathews P.M., Jiang Y., Schmidt S.D., Dinakar R., Summers-Terio N.B., Ceresa B.P., Nixon R.A., Cataldo A.M. Rab5-stimulated up-regulation of the endocytic pathway increases intracellular beta-cleaved amyloid precursor protein carboxyl-terminal fragment levels and Abeta production. J. Biol. Chem. 2003, 278:31261-31268.
17. Laifenfeld D., Patzek L.J., McPhie D.L., Chen Y., Levites Y., Cataldo A.M., Neve R.L. Rab5 mediates an amyloid precursor protein signaling pathway that leads to apoptosis. J. Neurosci. 2007, 27:7141-7153.
18. Cossec J.C., Simon A., Marquer C., Moldrich R.X., Leterrier C., Rossier J., Duyckaerts C., Lenkei Z., Potier M.C. Clathrin-dependent APP endocytosis and Abeta secretion are highly sensitive to the level of plasma membrane cholesterol. Biochim. Biophys. Acta 2010, 1801:846-852.
19. Yamazaki T., Chang T.Y., Haass C., Ihara Y. Accumulation and aggregation of amyloid beta-protein in late endosomes of Niemann-Pick type C cells. J. Biol. Chem. 2001, 276:4454-4460.
20. Burns M., Gaynor K., Olm V., Mercken M., LaFrancois J., Wang L., Mathews P.M., Noble W., Matsuoka Y., Duff K. Presenilin redistribution associated with aberrant cholesterol transport enhances beta-amyloid production in vivo. J. Neurosci. 2003, 23:5645-5649.
21. Runz H., Rietdorf J., Tomic I., de Bernard M., Beyreuther K., Pepperkok R., Hartmann T. Inhibition of intracellular cholesterol transport alters presenilin localization and amyloid precursor protein processing in neuronal cells. J. Neurosci. 2002, 22:1679-1689.
22. Kodam A., Maulik M., Peake K., Amritraj A., Vetrivel K.S., Thinakaran G., Vance J.E., Kar S. Altered levels and distribution of amyloid precursor protein and its processing enzymes in Niemann-Pick type C1-deficient mouse brains. Glia 2010, 58:1267-1281.
23. Malnar M., Kosicek M., Mitterreiter S., Omerbasic D., Lichtenthaler S.F., Goate A., Hecimovic S. Niemann-Pick type C cells show cholesterol dependent decrease of APP expression at the cell surface and its increased processing through the beta-secretase pathway. Biochim. Biophys. Acta 2010, 1802:682-691.
24. Mattsson N., Zetterberg H., Bianconi S., Yanjanin N.M., Fu R., Mansson J.E., Porter F.D., Blennow K. Gamma-secretase-dependent amyloid-beta is increased in Niemann-Pick type C: a cross-sectional study. Neurology 2011, 76:366-372.
25. Jin L.W., Shie F.S., Maezawa I., Vincent I., Bird T. Intracellular accumulation of amyloidogenic fragments of amyloid-beta precursor protein in neurons with Niemann-Pick type C defects is associated with endosomal abnormalities. Am. J. Pathol. 2004, 164:975-985.
26. Boland B., Smith D.A., Mooney D., Jung S.S., Walsh D.M., Platt F.M. Macroautophagy is not directly involved in the metabolism of amyloid precursor protein. J. Biol. Chem. 2010, 285:37415-37426.
27. Tamboli I.Y., Hampel H., Tien N.T., Tolksdorf K., Breiden B., Mathews P.M., Saftig P., Sandhoff K., Walter J. Sphingolipid storage affects autophagic metabolism of the amyloid precursor protein and promotes Abeta generation. J. Neurosci. 2011, 31:1837-1849.
28. Borbon I.A., Erickson R.P. Interactions of Npc1 and amyloid accumulation/deposition in the APP/PS1 mouse model of Alzheimer's. J. Appl. Genet. 2010, 52:213-218.
29. Kagedal K., Kim W.S., Appelqvist H., Chan S., Cheng D., Agholme L., Barnham K., McCann H., Halliday G., Garner B. Increased expression of the lysosomal cholesterol transporter NPC1 in Alzheimer's disease. Biochim. Biophys. Acta 2010, 1801:831-838.
30. Kosicek M., Malnar M., Goate A., Hecimovic S. Cholesterol accumulation in Niemann Pick type C (NPC) model cells causes a shift in APP localization to lipid rafts. Biochem. Biophys. Res. Commun. 2010, 293:404-409.
31. Hecimovic S., Wang J., Dolios G., Martinez M., Wang R., Goate A.M. Mutations in APP have independent effects on Abeta and CTFgamma generation. Neurobiol. Dis. 2004, 17:205-218.
32. Tienari P.J., De S.B., Ikonen E., Simons M., Weidemann A., Czech C., Hartmann T., Ida N., Multhaup G., Masters C.L., Van L.F., Beyreuther K., Dotti C.G. The beta-amyloid domain is essential for axonal sorting of amyloid precursor protein. EMBO J. 1996, 15:5218-5229.
33. Lichtenthaler S.F., Dominguez D.I., Westmeyer G.G., Reiss K., Haass C., Saftig P., De S.B., Seed B. The cell adhesion protein P-selectin glycoprotein ligand-1 is a substrate for the aspartyl protease BACE1. J. Biol. Chem. 2003, 278:48713-48719.
34. Kaech S., Banker G. Culturing hippocampal neurons. Nat. Protoc. 2006, 1:2406-2415.
35. van der Goot F.G. Separation of early steps in endocytic membrane transport. Electrophoresis 1997, 18:2689-2693.
36. Christian A.E., Haynes M.P., Phillips M.C., Rothblat G.H. Use of cyclodextrins for manipulating cellular cholesterol content. J. Lipid Res. 1997, 38:2264-2272.
37. Neufeld E.B., Wastney M., Patel S., Suresh S., Cooney A.M., Dwyer N.K., Roff C.F., Ohno K., Morris J.A., Carstea E.D., Incardona J.P., Strauss J.F., Vanier M.T., Patterson M.C., Brady R.O., Pentchev P.G., Blanchette-Mackie E.J. The Niemann-Pick C1 protein resides in a vesicular compartment linked to retrograde transport of multiple lysosomal cargo. J. Biol. Chem. 1999, 274:9627-9635.
38. Puri V., Watanabe R., Dominguez M., Sun X., Wheatley C.L., Marks D.L., Pagano R.E. Cholesterol modulates membrane traffic along the endocytic pathway in sphingolipid-storage diseases. Nat. Cell Biol. 1999, 1:386-388.
39. Pipalia N.H., Hao M., Mukherjee S., Maxfield F.R. Sterol, protein and lipid trafficking in Chinese hamster ovary cells with Niemann-Pick type C1 defect. Traffic 2007, 8:130-141.
40. Cutler R.G., Kelly J., Storie K., Pedersen W.A., Tammara A., Hatanpaa K., Troncoso J.C., Mattson M.P. Involvement of oxidative stress-induced abnormalities in ceramide and cholesterol metabolism in brain aging and Alzheimer's disease. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:2070-2075.
41. Xiong H., Callaghan D., Jones A., Walker D.G., Lue L.F., Beach T.G., Sue L.I., Woulfe J., Xu H., Stanimirovic D.B., Zhang W. Cholesterol retention in Alzheimer's brain is responsible for high beta- and gamma-secretase activities and Abeta production. Neurobiol. Dis. 2008, 29:422-437.
42. Panchal M., Loeper J., Cossec J.C., Perruchini C., Lazar A., Pompon D., Duyckaerts C. Enrichment of cholesterol in microdissected Alzheimer's disease senile plaques as assessed by mass spectrometry. J. Lipid Res. 2010, 51:598-605.
43. Puglielli L., Tanzi R.E., Kovacs D.M. Alzheimer's disease: the cholesterol connection. Nat. Neurosci. 2003, 6:345-351.
44. Wolozin B. Cholesterol and the biology of Alzheimer's disease. Neuron 2004, 41:7-10.
45. Zou L., Wang Z., Shen L., Bao G.B., Wang T., Kang J.H., Pei G. Receptor tyrosine kinases positively regulate BACE activity and Amyloid-beta production through enhancing BACE internalization. Cell Res. 2007, 17:389-401.
46. Cossec J.C., Marquer C., Panchal M., Lazar A.N., Duyckaerts C., Potier M.C. Cholesterol changes in Alzheimer's disease: methods of analysis and impact on the formation of enlarged endosomes. Biochim. Biophys. Acta 2010, 1801:839-845.
47. Marquer C., Devauges V., Cossec J.C., Liot G., Lecart S., Saudou F., Duyckaerts C., Leveque-Fort S., Potier M.C. Local cholesterol increase triggers amyloid precursor protein-Bace1 clustering in lipid rafts and rapid endocytosis. FASEB J. 2011, 25:1295-1305.
48. te Vruchte D., Lloyd-Evans E., Veldman R.J., Neville D.C., Dwek R.A., Platt F.M., van Blitterswijk W.J., Sillence D.J. Accumulation of glycosphingolipids in Niemann-Pick C disease disrupts endosomal transport. J. Biol. Chem. 2004, 279:26167-26175.
49. Davidson C.D., Ali N.F., Micsenyi M.C., Stephney G., Renault S., Dobrenis K., Ory D.S., Vanier M.T., Walkley S.U. Chronic cyclodextrin treatment of murine Niemann-Pick C disease ameliorates neuronal cholesterol and glycosphingolipid storage and disease progression. PLoS One 2009, 4:e6951.
50. Devlin C., Pipalia N.H., Liao X., Schuchman E.H., Maxfield F.R., Tabas I. Improvement in lipid and protein trafficking in Niemann-Pick C1 cells by correction of a secondary enzyme defect. Traffic 2010, 11:601-615.
51. Grimm M.O., Grimm H.S., Patzold A.J., Zinser E.G., Halonen R., Duering M., Tschape J.A., De S.B., Muller U., Shen J., Hartmann T. Regulation of cholesterol and sphingomyelin metabolism by amyloid-beta and presenilin. Nat. Cell Biol. 2005, 7:1118-1123.
52. Umeda T., Mori H., Zheng H., Tomiyama T. Regulation of cholesterol efflux by amyloid beta secretion. J. Neurosci. Res. 2010, 88:1985-1994.
53. Cataldo A.M., Mathews P.M., Boiteau A.B., Hassinger L.C., Peterhoff C.M., Jiang Y., Mullaney K., Neve R.L., Gruenberg J., Nixon R.A. Down syndrome fibroblast model of Alzheimer-related endosome pathology: accelerated endocytosis promotes late endocytic defects. Am. J. Pathol. 2008, 173:370-384.
54. Umeda T., Tomiyama T., Sakama N., Tanaka S., Lambert M.P., Klein W.L., Mori H. Intraneuronal amyloid beta oligomers cause cell death via endoplasmic reticulum stress, endosomal/lysosomal leakage, and mitochondrial dysfunction in vivo. J. Neurosci. Res. 2011, 89:1031-1042.
55. Jiang Y., Mullaney K.A., Peterhoff C.M., Che S., Schmidt S.D., Boyer-Boiteau A., Ginsberg S.D., Cataldo A.M., Mathews P.M., Nixon R.A. Alzheimer's-related endosome dysfunction in Down syndrome is Abeta-independent but requires APP and is reversed by BACE-1 inhibition. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:1630-1635.