Cholesterol metabolism is associated with soluble amyloid precursor protein production in Alzheimer's disease

Journal of Neurochemistry

Volumn 123, Issue 2, 2012, Pages 310-316

  Popp, Julius ^a,b   Lewczuk, Piotr ^c   Kölsch, Heike ^b   Meichsner, Sabrina ^d   Maier, Wolfgang ^b   Kornhuber, Johannes ^c   Jessen, Frank ^b,e   Lütjohann, Dieter ^d  

^a LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

^b UNIVERSITY OF BONN   (Germany)

^c UNIVERSITY HOSPITAL ERLANGEN   (Germany)

^d UNIVERSITY HOSPITAL BONN   (Germany)

^e GERMAN CENTER FOR NEURODEGENERATIVE DISEASES DZNE   (Germany)

Author keywords

24S hydroxycholesterol; 27 hydroxycholesterol; amyloid beta; cerebrospinal fluid; cholesterol; soluble amyloid precursor protein

Indexed keywords

24 HYDROXYCHOLESTEROL; 26 HYDROXYCHOLESTEROL; ALBUMIN; AMYLOID BETA PROTEIN[1-42]; AMYLOID PRECURSOR PROTEIN; APOLIPOPROTEIN E4; CHOLESTEROL DERIVATIVE; SOLUBLE AMYLOID PRECURSOR PROTEIN; SOLUBLE AMYLOID PRECURSOR PROTEIN ALPHA; SOLUBLE AMYLOID PRECURSOR PROTEIN BETA; UNCLASSIFIED DRUG;

ADULT; ALZHEIMER DISEASE; ARTICLE; BIOACCUMULATION; CEREBROSPINAL FLUID; CEREBROSPINAL FLUID LEVEL; CHOLESTEROL BLOOD LEVEL; CHOLESTEROL METABOLISM; CONTROLLED STUDY; DISEASE ASSOCIATION; FEMALE; HETEROZYGOTE; HUMAN; HYPERCHOLESTEROLEMIA; MAJOR CLINICAL STUDY; MALE; METABOLITE; NEUROCHEMISTRY; PRIORITY JOURNAL; PROTEIN SYNTHESIS; RISK FACTOR; UPREGULATION;

AGED; ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN PRECURSOR; BIOLOGICAL MARKERS; CHOLESTEROL; FEMALE; HUMANS; HYDROXYCHOLESTEROLS; MALE; MIDDLE AGED; UP-REGULATION;

EID: 84867091169     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2012.07893.x     Document Type: Article

References (46)

1. Babiker A., Andersson O., Lund E., Xiu R. J., Deeb S., Reshef A., Leitersdorf E., Diczfalusy U., and, Bjorkhem I., (1997) Elimination of cholesterol in macrophages and endothelial cells by the sterol 27-hydroxylase mechanism. Comparison with high density lipoprotein-mediated reverse cholesterol transport. J. Biol. Chem. 272, 26253-26261.
2. Bjorkhem I., (2006) Crossing the barrier: oxysterols as cholesterol transporters and metabolic modulators in the brain. J. Intern. Med. 260, 493-508.
3. Bodovitz S., and, Klein W. L., (1996) Cholesterol modulates alpha-secretase cleavage of amyloid precursor protein. J. Biol. Chem. 271, 4436-4440.
4. Brown J. III, Theisler C., Silberman S., et al,. (2004) Differential expression of cholesterol hydroxylases in Alzheimer's disease. J. Biol. Chem. 279, 34674-34681.
5. Bu G., (2009) Apolipoprotein E and its receptors in Alzheimer's disease: pathways, pathogenesis and therapy. Nat. Rev. Neurosci. 10, 333-344.
6. Canepa E., Borghi R., Vina J., Traverso N., Gambini J., Domenicotti C., Marinari U. M., Poli G., Pronzato M. A., and, Ricciarelli R., (2011) Cholesterol and amyloid-beta: evidence for a cross-talk between astrocytes and neuronal cells. J. Alzheimers Dis. 25, 645-653.
7. Cordy J. M., Hussain I., Dingwall C., Hooper N. M., and, Turner A. J., (2003) Exclusively targeting beta-secretase to lipid rafts by GPI-anchor addition up-regulates beta-site processing of the amyloid precursor protein. Proc. Natl Acad. Sci. USA 100, 11735-11740.
8. Dasari B., Prasanthi J. R., Marwarha G., Singh B. B., and, Ghribi O., (2010) The oxysterol 27-hydroxycholesterol increases beta-amyloid and oxidative stress in retinal pigment epithelial cells. BMC Ophthalmol. 10, 22.
9. Ehehalt R., Keller P., Haass C., Thiele C., and, Simons K., (2003) Amyloidogenic processing of the Alzheimer beta-amyloid precursor protein depends on lipid rafts. J. Cell Biol. 160, 113-123.
10. Famer D., Meaney S., Mousavi M., Nordberg A., Bjorkhem I., and, Crisby M., (2007) Regulation of alpha- and beta-secretase activity by oxysterols: cerebrosterol stimulates processing of APP via the alpha-secretase pathway. Biochem. Biophys. Res. Commun. 359, 46-50.
11. Fassbender K., Simons M., Bergmann C., et al,. (2001) Simvastatin strongly reduces levels of Alzheimer's disease beta -amyloid peptides Abeta 42 and Abeta 40 in vitro and in vivo. Proc. Natl Acad. Sci. USA 98, 5856-5861.
12. Folstein M. F., Folstein S. E., and, McHugh P. R., (1975) "Mini-mental state". A practical method for grading the cognitive state of patients for the clinician. J. Psychiat. Res. 12, 189-198.
13. Fukumoto H., Deng A., Irizarry M. C., Fitzgerald M. L., and, Rebeck G. W., (2002) Induction of the cholesterol transporter ABCA1 in central nervous system cells by liver X receptor agonists increases secreted Abeta levels. J. Biol. Chem. 277, 48508-48513.
14. Grimm M. O., Grimm H. S., Patzold A. J., et al,. (2005) Regulation of cholesterol and sphingomyelin metabolism by amyloid-beta and presenilin. Nat. Cell Biol. 7, 1118-1123.
15. Grimm M. O., Rothhaar T. L., and, Hartmann T., (2012) The role of APP proteolytic processing in lipid metabolism. Exp. Brain Res. 217, 365-375.
16. Hardy J., and, Selkoe D. J., (2002) The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 297, 353-356.
17. Heverin M., Bogdanovic N., Lutjohann D., Bayer T., Pikuleva I., Bretillon L., Diczfalusy U., Winblad B., and, Bjorkhem I., (2004) Changes in the levels of cerebral and extracerebral sterols in the brain of patients with Alzheimer's disease. J. Lipid Res. 45, 186-193.
18. Heverin M., Meaney S., Lutjohann D., Diczfalusy U., Wahren J., and, Bjorkhem I., (2005) Crossing the barrier: net flux of 27-hydroxycholesterol into the human brain. J. Lipid Res. 46, 1047-1052.
19. Hixson J. E., and, Vernier D. T., (1990) Restriction isotyping of human apolipoprotein E by gene amplification and cleavage with HhaI. J. Lipid Res. 31, 545-548.
20. Jones L., Holmans P. A., Hamshere M. L., et al,. (2010) Genetic evidence implicates the immune system and cholesterol metabolism in the aetiology of Alzheimer's disease. PLoS ONE 5, e13950.
21. Kojro E., Gimpl G., Lammich S., Marz W., and, Fahrenholz F., (2001) Low cholesterol stimulates the nonamyloidogenic pathway by its effect on the alpha -secretase ADAM 10. Proc. Natl Acad. Sci. USA 98, 5815-5820.
22. Kok E., Haikonen S., Luoto T., Huhtala H., Goebeler S., Haapasalo H., and, Karhunen P. J., (2009) Apolipoprotein E-dependent accumulation of Alzheimer disease-related lesions begins in middle age. Ann. Neurol. 65, 650-657.
23. Kolsch H., Heun R., Jessen F., Popp J., Hentschel F., Maier W., and, Lutjohann D., (2010) Alterations of cholesterol precursor levels in Alzheimer's disease. Biochim. Biophys. Acta 1801, 945-950.
24. Launer L. J., White L. R., Petrovitch H., Ross G. W., and, Curb J. D., (2001) Cholesterol and neuropathologic markers of AD: a population-based autopsy study. Neurology 57, 1447-1452.
25. Leoni V., Masterman T., Mousavi F. S., Wretlind B., Wahlund L. O., Diczfalusy U., Hillert J., and, Bjorkhem I., (2004) Diagnostic use of cerebral and extracerebral oxysterols. Clin. Chem. Lab. Med. 42, 186-191.
26. Lewczuk P., Kamrowski-Kruck H., Peters O., et al,. (2010) Soluble amyloid precursor proteins in the cerebrospinal fluid as novel potential biomarkers of Alzheimer's disease: a multicenter study. Mol. Psychiatry 15, 138-145.
27. Lewczuk P., Popp J., Lelental N., Kolsch H., Maier W., Kornhuber J., and, Jessen F., (2012) Cerebrospinal Fluid Soluble Amyloid-beta Protein Precursor as a Potential Novel Biomarkers of Alzheimer's Disease. J. Alzheimers Dis. 28, 119-125.
28. Lutjohann D., (2006) Cholesterol metabolism in the brain: importance of 24S-hydroxylation. Acta Neurol. Scand. Suppl. 185, 33-42.
29. Lutjohann D., Papassotiropoulos A., Bjorkhem I., et al,. (2000) Plasma 24S-hydroxycholesterol (cerebrosterol) is increased in Alzheimer and vascular demented patients. J. Lipid Res. 41, 195-198.
30. Marwarha G., Dasari B., Prasanthi J. R., Schommer J., and, Ghribi O., (2010) Leptin reduces the accumulation of Abeta and phosphorylated tau induced by 27-hydroxycholesterol in rabbit organotypic slices. J. Alzheimers Dis. 19, 1007-1019.
31. Matsuzaki T., Sasaki K., Hata J., Hirakawa Y., Fujimi K., Ninomiya T., Suzuki S. O., Kanba S., Kiyohara Y., and, Iwaki T., (2011) Association of Alzheimer disease pathology with abnormal lipid metabolism: the Hisayama Study. Neurology 77, 1068-1075.
32. McKhann G., Drachman D., Folstein M., Katzman R., Price D., and, Stadlan E. M., (1984) Clinical diagnosis of Alzheimer's disease: report of the NINCDS-ADRDA Work Group under the auspices of Department of Health and Human Services Task Force on Alzheimer's Disease. Neurology 34, 939-944.
33. Papassotiropoulos A., Lutjohann D., Bagli M., Locatelli S., Jessen F., Buschfort R., Ptok U., Bjorkhem I., von Bergmann K., and, Heun R., (2002) 24S-hydroxycholesterol in cerebrospinal fluid is elevated in early stages of dementia. J. Psychiatr. Res. 36, 27-32.
34. Pappolla M. A., Bryant-Thomas T. K., Herbert D., et al,. (2003) Mild hypercholesterolemia is an early risk factor for the development of Alzheimer amyloid pathology. Neurology 61, 199-205.
35. Popp J., Lewczuk P., Frommann I., Kolsch H., Kornhuber J., Maier W., and, Jessen F., (2010) Cerebrospinal fluid markers for Alzheimer's disease over the lifespan: effects of age and the APOEepsilon4 genotype. J. Alzheimers Dis. 22, 459-468.
36. Popp J., Lewczuk P., Kolsch H., Giannakopoulos P., Maier W. Kornhuber J., Jessen F., and, Lutjohann D., (2011) CNS cholesterol metabolism is associated with soluble amyloid precursor protein production in Alzheimer's disease. Alzheimers Dement. 7, 395.
37. Prasanthi J. R., Huls A., Thomasson S., Thompson A., Schommer E., and, Ghribi O., (2009) Differential effects of 24-hydroxycholesterol and 27-hydroxycholesterol on beta-amyloid precursor protein levels and processing in human neuroblastoma SH-SY5Y cells. Mol. Neurodegener. 4, 1.
38. Prasanthi J. R., Larson T., Schommer J., and, Ghribi O., (2011) Silencing GADD153/CHOP Gene Expression Protects against Alzheimer's Disease-Like Pathology Induced by 27-Hydroxycholesterol in Rabbit Hippocampus. PLoS ONE 6, e26420.
39. Refolo L. M., Malester B., LaFrancois J., Bryant-Thomas T., Wang R., Tint G. S., Sambamurti K., Duff K., and, Pappolla M. A., (2000) Hypercholesterolemia accelerates the Alzheimer's amyloid pathology in a transgenic mouse model. Neurobiol. Dis. 7, 321-331.
40. Sharma S., Prasanthi R. P. J., Schommer E., Feist G., and, Ghribi O., (2008) Hypercholesterolemia-induced Abeta accumulation in rabbit brain is associated with alteration in IGF-1 signaling. Neurobiol. Dis. 32, 426-432.
41. Shie F. S., Jin L. W., Cook D. G., Leverenz J. B., and, LeBoeuf R. C., (2002) Diet-induced hypercholesterolemia enhances brain A beta accumulation in transgenic mice. NeuroReport 13, 455-459.
42. Simons M., Keller P., De Strooper B., Beyreuther K., Dotti C. G., and, Simons K., (1998) Cholesterol depletion inhibits the generation of beta-amyloid in hippocampal neurons. Proc. Natl Acad. Sci. USA 95, 6460-6464.
43. Sjogren M., Gustafsson K., Syversen S., Olsson A., Edman A., Davidsson P., Wallin A., and, Blennow K., (2003) Treatment with simvastatin in patients with Alzheimer's disease lowers both alpha- and beta-cleaved amyloid precursor protein. Dement. Geriatr. Cogn. Disord. 16, 25-30.
44. Vanmierlo T., Popp J., Kolsch H., et al,. (2011) The plant sterol brassicasterol as additional CSF biomarker in Alzheimer's disease. Acta Psychiatr. Scand. 124, 184-192.
45. Wirths O., Thelen K., Breyhan H., Luzon-Toro B., Hoffmann K. H., Falkai P., Lutjohann D., and, Bayer T. A., (2006) Decreased plasma cholesterol levels during aging in transgenic mouse models of Alzheimer's disease. Exp. Gerontol. 41, 220-224.
46. Xiong H., Callaghan D., Jones A., et al,. (2008) Cholesterol retention in Alzheimer's brain is responsible for high beta- and gamma-secretase activities and Abeta production. Neurobiol. Dis. 29, 422-437.