Pharmacological activation of LXRs decreases amyloid-β levels in niemann-pick type C model cells

Current Pharmaceutical Biotechnology

Volumn 14, Issue 6, 2013, Pages 582-593

  Stefulj, Jasminka ^a   Perica, Maja ^a   Malnar, Martina ^a   Kosicek, Marko ^a   Schweinzer, Cornelia ^b   Zivkovic, Jelena ^a   Scholler, Monika ^b   Panzenboeck, Ute ^b   Hecimovic, Silva ^a  

^a RUDER BO KOVI INSTITUTE   (Croatia)

^b MEDICAL UNIVERSITY OF GRAZ   (Austria)

Author keywords

ABCA1; Alzheimer's disease; APP; A ; Cholesterol; Liver X receptors; NPC1

Indexed keywords

3 [3 [[2 CHLORO 3 (TRIFLUOROMETHYL) BENZYL] (2 DIPHENYLETHYL) AMINO] PROPOXY] PHENYLACETIC ACID; 3 [3 [[2 CHLORO 3 (TRIFLUOROMETHYL)BENZYL](2 DIPHENYLETHYL)AMINO]PROPOXY]PHENYLACETIC ACID; AMYLOID BETA PROTEIN [1-40]; AMYLOID PRECURSOR PROTEIN; APOLIPOPROTEIN A1; HIGH DENSITY LIPOPROTEIN; LIVER X RECEPTOR; N (2, 2, 2 TRIFLUOROETHYL) N [4 (2, 2, 2 TRIFLUORO 1 HYDROXY 1 TRIFLUOROMETHYLETHYL) PHENYL] BENZENESULFONAMIDE; N (2,2,2 TRIFLUOROETHYL) N [4 (2,2,2 TRIFLUORO 1 HYDROXY 1 TRIFLUOROMETHYLETHYL)PHENYL]BENZENESULFONAMIDE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL VIABILITY; CHOLESTEROL ESTERIFICATION; CHOLESTEROL SYNTHESIS; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE; IMMUNOBLOTTING; IMMUNOPRECIPITATION; MOUSE; NERVE DEGENERATION; NIEMANN PICK DISEASE; NONHUMAN; NPC1 GENE;

MUS;

AMYLOID BETA-PEPTIDES; ANIMALS; CHO CELLS; CHOLESTEROL; CRICETULUS; HYDROCARBONS, FLUORINATED; NIEMANN-PICK DISEASE, TYPE C; ORPHAN NUCLEAR RECEPTORS; PEPTIDE FRAGMENTS; SULFONAMIDES;

EID: 84888259389     PISSN: 13892010     EISSN: 18734316     Source Type: Journal    
DOI: 10.2174/138920101131400224     Document Type: Article

References (49)

1. Tang, Y.; Li, H.; Liu, J. P., Niemann-Pick disease Type C: from molecule to clinic. Clin. Exp. Pharmacol. Physiol., 2010, 37(1), 132-140.
2. Carstea, E. D.; Morris, J. A.; Coleman, K. G.; Loftus, S. K.; Zhang, D.; Cummings, C.; Gu, J.; Rosenfeld, M. A.; Pavan, W. J.; Krizman, D. B.; Nagle, J.; Polymeropoulos, M. H.; Sturley, S. L.; Ioannou, Y. A.; Higgins, M. E.; Comly, M.; Cooney, A.; Brown, A.; Kaneski, C. R.; BlanchetteMackie, E. J.; Dwyer, N. K.; Neufeld, E. B.; Chang, T. Y.; Liscum, L.; Strauss, J. F.; Ohno, K.; Zeigler, M.; Carmi, R.; Sokol, J.; Markie, D.; Oneill, R. R.; vanDiggelen, O. P.; Elleder, M.; Patterson, M. C.; Brady, R. O.; Vanier, M. T.; Pentchev, P. G.; Tagle, D. A., Niemann-Pick C1 disease gene: homology to mediators of cholesterol homeostasis. Science, 1997, 277 (5323), 228-231.
3. Frolov, A.; Zielinski, S. E.; Crowley, J. R.; Dudley-Rucker, N.; Schaffer, J. E.; Ory, D. S., NPC1 and NPC2 regulate cellular cholesterol homeostasis through generation of low density lipoprotein cholesterol-derived oxysterols. J. Biol. Chem., 2003, 278 (28), 25517-25525.
4. Karten, B.; Peake, K. B.; Vance, J. E., Mechanisms and consequences of impaired lipid trafficking in Niemann-Pick type C1-deficient mammalian cells. Biochim. Biophys. Acta., 2009, 1791 (7), 659-670.
5. Rosenbaum, A. I.; Maxfield, F. R., Niemann-Pick type C disease: molecular mechanisms and potential therapeutic approaches. J. Neurochem., 2011, 116 (5), 789-795.
6. 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 (6), 4454-4460.
7. 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 (5), 1679-1689.
8. Burns, M.; Gaynor, K.; Olm, V.; Mercken, M.; LaFrancois, J.; Wang, L. 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 (13), 5645-5649.
9. Jin, L. W.; 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 (3), 975-985.
10. 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 betasecretase pathway. Biochim. Biophys. Acta., 2010, 1802 (7-8), 682-691.
11. Mattsson, N.; Zetterberg, H.; Bianconi, S.; Yanjanin, N. M.; Fu, R.; Mansson, J. E.; Porter, F. D.; Blennow, K., Gamma-secretasedependent amyloid-beta is increased in Niemann-Pick type C: a cross-sectional study. Neurology, 2011, 76 (4), 366-372.
12. 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 (11), 1267-1281.
13. Shoji, M.; Golde, T. E.; Ghiso, J.; Cheung, T. T.; Estus, S.; Shaffer, L. M.; Cai, X. D.; McKay, D. M.; Tintner, R.; Frangione, B.; Younkin, S. G., Production of the alzheimer amyloid-beta protein by normal proteolytic processing. Science, 1992, 258 (5079), 126-129.
14. Burns, M. P.; Rebeck, G. W., Intracellular cholesterol homeostasis and amyloid precursor protein processing. Biochim. Biophys. Acta., 2010, 1801 (8), 853-859.
15. Zhao, C.; Dahlman-Wright, K., Liver X receptor in cholesterol metabolism. J. Endocrinol., 2010, 204 (3), 233-240.
16. Repa, J. J.; Turley, S. D.; Lobaccaro, J. M. A.; Medina, J.; Li, L.; Lustig, K.; Shan, B.; Heyman, R. A.; Dietschy, J. M.; Mangelsdorf, D. J., Regulation of absorption and ABC1-mediated efflux of cholesterol by RXR heterodimers. Science, 2000, 289 (5484), 1524-1529.
17. Langmade, S. J.; Gale, S. E.; Frolov, A.; Mohri, I.; Suzuki, K.; Mellon, S. H.; Walkley, S. U.; Covey, D. F.; Schaffer, J. E.; Ory, D. S., Pregnane X receptor (PXR) activation: a mechanism for neuroprotection in a mouse model of Niemann-Pick C disease. Proc. Natl. Acad. Sci. USA., 2006, 103 (37), 13807-13812.
18. Repa, J. J.; Li, H.; Frank-Cannon, T. C.; Valasek, M. A.; Turley, S. D.; Tansey, M. G.; Dietschy, J. M., Liver X receptor activation enhances cholesterol loss from the brain, decreases neuroinflammation, and increases survival of the NPC1 mouse. J. Neurosci., 2007, 27 (52), 14470-14480.
19. Liu, B.; Li, H.; Repa, J. J.; Turley, S. D.; Dietschy, J. M., Genetic variations and treatments that affect the lifespan of the NPC1 mouse. J. Lipid. Res., 2008, 49 (3), 663-669.
20. Koldamova, R. P.; Lefterov, L. M.; Ikonomovic, M. D.; Skoko, J.; Lefterov, P. I.; Isanskis, B. A.; DeKosky, S. T.; Lazo, J. S., 22RHydroxycholesterol and 9-cis-retinoic acid induce ATPbinding cassette transporter A1 expression and cholesterol efflux in brain cells and decrease amyloid beta secretion. J. Biol. Chem., 2003, 278 (15), 13244-13256.
21. Sun, Y.; Yao, J.; Kim, T. W.; Tall, A. R., Expression of liver X receptor target genes decreases cellular amyloid beta peptide secretion. J. Biol. Chem., 2003, 278 (30), 27688-27694.
22. Koldamova, T.; Lefterov, I. M.; Staufenbiel, M.; Wolfe, D.; Huang, S. H.; Glorioso, J. C.; Walter, M.; Roth, M. G.; Lazo, J. S., The liver X receptor ligand T0901317 decreases amyloid beta production in vitro and in a mouse model of Alzheimer's disease. J. Biol. Chem., 2005, 280 (6), 4079-4088.
23. Burns, M. P.; Vardanian, L.; Pajoohesh-Ganji, A.; Wang, L. L.; Cooper, M.; Harris, D. C.; Duff, K.; Rebeck, G. W., The effects of ABCA1 on cholesterol efflux and A beta levels in vitro and in vivo. Neurochem., 2006, 98 (3), 792-800.
24. Lefterov, I.; Bookout, A.; Wang, Z.; Staufenbiel, M.; Mangelsdorf, D.; Koldamova, R., Expression profiling in APP23 mouse brain: inhibition of A beta amyloidosis and inflammation in response to LXR agonist treatment. Mol. Neurodegener., 2007, 2, 20.
25. Riddell, D. R.; Zhou, H.; Comery, T. A.; Kouranova, E.; Lo, C. F.; Warwick, H. K.; Ring, R. H.; Kirksey, Y.; Aschmies, S.; Xu, J.; Kubek, K.; Hirst, W. D.; Gonzales, C.; Chen, Y.; Murphy, E.; Leonard, S.; Vasylyev, D.; Oganesian, A.; Martone, R. L.; Pangalos, M. N.; Remhart, P. H.; Jacobsen, J. S., The LXR agonist TO901317 selectively lowers hippocampal A beta 42 and improves memory in the Tg2576 mouse model of Alzheimer's disease. Mol. Cell. Neurosci., 2007, 34 (4), 621-628.
26. Jiang, Q.; Lee, C. Y. D.; Mandrekar, S.; Wilkinson, B.; Cramer, P.; Zelcer, N.; Mann, K.; Lamb, B.; Willson, T. M.; Collins, J. L.; Richardson, J. C.; Smith, J. D.; Comery, T. A.; Riddell, D.; Holtzman, D. M.; Tontonoz, P.; Landreth, G. E., ApoE promotes the proteolytic degradation of A beta. Neuron, 2008, 58 (5), 681-693.
27. Kim, W. S.; Chan, S. L.; Hill, A. F.; Guillemin, G. J.; Garner, B., Impact of 27-Hydroxycholesterol on Amyloid-beta Peptide Production and ATP-Binding Cassette Transporter Expression in Primary Human Neurons. J. Alzheimers Dis., 2009, 16 (1), 121-131.
28. Fitz, N. F.; Cronican, A.; Pham, T.; Fogg, A.; Fauq, A. H.; Chapman, R.; Lefterov, I.; Koldamova, R., Liver X receptor agonist treatment ameliorates amyloid pathology and memory deficits caused by high-fat diet in APP23 mice. J. Neurosci., 2010, 30 (20), 6862-6872.
29. Donkin, J. J.; Stukas, S.; Hirsch-Reinshagen, V.; Namjoshi, D.; Wilkinson, A.; May, S.; Chan, J.; Fan, J. J.; Collins, J.; Wellington, C. L., ATP-binding cassette transporter A1 mediates the beneficial effects of the liver X receptor agonist GW3965 on object recognition memory and amyloid burden in amyloid precursor protein/ presenilin 1 mice. J. Biol. Chem., 2010, 285 (44), 34144-34154.
30. Cui, W. G.; Sun, Y.; Wang, Z. P.; Xu, C. C.; Xu, L.; Wang, F.; Chen, Z. L.; Peng, Y. W.; Li, R. X., Activation of liver X receptor decreases BACE1 expression and activity by reducing membrane cholesterol levels. Neurochem. Res., 2011, 36 (10), 1910-1921.
31. Terwel, D.; Steffensen, K. R.; Verghese, P. B.; Kummer, M. P.; Gustafsson, J. A.; Holtzman, D. M.; Heneka, M. T., Critical role of astroglial apolipoprotein E and liver X receptor-alpha expression for microglial A beta phagocytosis. J. Neurosci., 2011, 31 (19), 7049-7059.
32. Sattler, W.; Mohr, D.; Stocker, R., Rapid isolation of lipoproteins and assessment of their peroxidation by high-performance liquidchromatography postcolumn chemiluminescence. Methods Enzymol., 1994, 233, 469-489.
33. Bergt, C.; Oettl, K.; Keller, W.; Andreae, F.; Leis, H. J.; Malle, E.; Sattler, W. G., Reagent or myeloperoxidase-generated hypochlorite affects discrete regions in lipid-free and lipid-associated human apolipoprotein A-1. Biochem. J., 2000, 346, 345-354.
34. Millard, E. E.; Srivastava, K.; Traub, L. M.; Schaffer, J. E.; Ory, D. S., Niemann-Pick type C1 (NPC1) overexpression alters cellular cholesterol homeostasis. J. Biol. Chem., 2000, 275 (49), 38445-38451.
35. Hecimovic, S.; Wang, J.; Dolios, G.; Martinez, M.; Wang, R.; Goate, A. M., Mutations in APP have independent effects on A beta and CTF gamma generation. Neurobiol. Dis., 2004, 17 (2), 205-218.
36. Schagger, H.; Vonjagow, G., Tricine sodium dodecyl-sulfate polyacrylamide-gel electrophoresis for the separation of proteins in the range from 1-KDA TO 100-KDA. Anal. Biochem., 1987, 166 (2), 368-379.
37. Stefulj, J.; Panzenboeck, U.; Becker, T.; Hirschmugl, B.; Schweinzer, C.; Lang, I.; Marsche, G.; Sadjak, A.; Lang, U.; Desoye, G.; Wadsack, C., Human endothelial cells of the placental barrier efficiently deliver cholesterol to the fetal circulation via ABCA1 and ABCG1. Circ. Res., 2009, 104 (5), 600-608.
38. Schweinzer, C.; Kober, A.; Lang, I.; Etschmaier, K.; Scholler, M.; Kresse, A.; Sattler, W.; Panzenboeck, U., Processing of endogenous A beta PP in blood-brain barrier endothelial cells is modulated by liver-X receptor agonists and altered cellular cholesterol homeostasis. J. Alzheimers Dis., 2011, 27 (2), 341-360.
39. 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 (14), 9627-9635.
40. Czech, C.; Burns, M. P.; Vardanian, L.; Augustin, A.; Jacobsen, H.; Baumann, K.; Rebeck, G. W., Cholesterol independent effect of LXR agonist TO-901317 on gamma-secretase. J. Neurochem., 2007, 101 (4), 929-936.
41. Prasanthi, J. R. P.; Huls, A.; Thomasson, S.; Thompson, A.; Schommer, E.; Ghribi, O., Differential effects of 24-hydroxycholesterol and 27-hydroxycholesterol on beta-amyloid precursor protein levels and processing in human neuroblastoma SH-SY5Y cells. Mol. Neurodegener., 2009, 4, 1.
42. Nunes, A.; Pressey, S. N. R.; Cooper, J. D.; Soriano, S., Loss of amyloid precursor protein in a mouse model of Niemann-Pick type C disease exacerbates its phenotype and disrupts tau homeostasis. Neurobiology of Disease 2011, 42 (3), 349-359.
43. Rigamonti, E.; Helin, L.; Lestavel, S.; Mutka, A. L.; Lepore, M.; Fontaine, C.; Bouhlel, M. A.; Bultel, S.; Fruchart, J. C.; Ikonen, E.; Clavey, V.; Staels, B.; Gbaguidi, G. C., Liver X receptor activation controls intracellular cholesterol trafficking and esterification in human macrophages. Circulation Res., 2005, 97 (7), 682-689.
44. Pagler, T. A.; Neuhofer, A.; Laggner, H.; Strobl, W.; Stangl, H., Cholesterol efflux via HDL resecretion occurs when cholesterol transport out of the lysosome is impaired. J. Lipid Res., 2007, 48 (10), 2141-2150.
45. Kim, W.S.; Rahmanto, A. S.; Kamili, A.; Rye, K.-A.; Guillemin, G. J.; Gelissen, I. C.; Jessup, W.; Hill, A. F.; Garner, B., Role of ABCG1 and ABCA1 in regulation of neuronal cholesterol efflux to apolipoprotein E discs and suppression of amyloid-beta peptide generation. J. Biol. Chem., 2007, 282 (5), 2851-2861.
46. Kim, W. S.; Hill, A. F.; Fitzgerald, M. L.; Freeman, M. W.; Evin, G.; Garner, B., Wild type and Tangier disease ABCA1 mutants modulate cellular amyloid-beta production independent of cholesterol efflux activity. J. Alzheimers Dis., 2011, 27 (2), 441-452.
47. Fassbender, K.; Simons, M.; Bergmann, C.; Stroick, M.; Lutjohann, D.; Keller, P.; Runz, H.; Kuhl, S.; Bertsch, T.; von Bergmannn, K.; Hennerici, M.; Beyreuther, K.; Hartmann, T., Simvastatin strongly reduces levels of Alzheimer's disease betaamyloid peptides A beta 42 and A beta 40 in vitro and in vivo. Proceedings of the National Academy of Sciences of the United States of America, 2001, 98 (10), 5856-5861.
48. Refolo, L. M.; Pappolla, M. A.; LaFrancois, J.; Malester, B.; Schmidt, S. D.; Thomas-Bryant, T.; Tint, G. S.; Wang, R.; Mercken, M.; Petanceska, S. S.; Duff, K. E., A cholesterollowering drug reduces beta-amyloid pathology in a transgenic mouse model of Alzheimer's disease. Neurobiol. Dis., 2001, 8 (5), 890-899.
49. Bhattacharyya, R.; Kovacs, D. M., ACAT inhibition and amyloid beta reduction. Biochim. Biophys. Acta., 2010, 1801 (8), 960-965.