Neuroprotection by cyclodextrin in cell and mouse models of Alzheimer disease

Journal of Experimental Medicine

Volumn 209, Issue 13, 2012, Pages 2501-2513

  Yao, Jiaqi ^a   Ho, Daniel ^a   Calingasan, Noel Y ^a   Pipalia, Nina H ^a   Lin, Michael T ^a   Beal, Flint ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 HYDROXYPROPYL BETA CYCLODEXTRIN; AMYLOID BETA PROTEIN; CHOLESTEROL; CYCLODEXTRIN; MEMBRANE LIPID; TAU PROTEIN;

ALZHEIMER DISEASE; AMNESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL MEMBRANE; CHOLESTEROL TRANSPORT; CLINICAL FEATURE; CONTROLLED STUDY; GENE EXPRESSION; MOUSE; NEURITE; NEUROPROTECTION; NIEMANN PICK DISEASE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; SENILE PLAQUE; SPATIAL LEARNING;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; BETA-CYCLODEXTRINS; BRAIN; CELL LINE; CHOLESTEROL; DISEASE MODELS, ANIMAL; HUMANS; LEARNING; LYSOSOMES; MEMORY; MICE; MICE, 129 STRAIN; MICE, TRANSGENIC; NEUROPROTECTIVE AGENTS; PEPTIDE FRAGMENTS; PLAQUE, AMYLOID; TAU PROTEINS;

EID: 84871905647     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20121239     Document Type: Article

References (60)

1. Aqul, A., B. Liu, C.M. Ramirez, A.A. Pieper, S.J. Estill, D.K. Burns, B. Liu, J.J. Repa, S.D. Turley, and J.M. Dietschy. 2011. Unesterified cholesterol accumulation in late endosomes/lysosomes causes neuro-degeneration and is prevented by driving cholesterol export from this compartment. J. Neurosci. 31:9404-9413. http://dx.doi.org/10.1523/ JNEUROSCI.1317-11.2011
2. Bahr, B.A., B. Abai, C.M. Gall, P.W. Vanderklish, K.B. Hoffman, and G. Lynch. 1994. Induction of beta-amyloid-containing polypeptides in hippocampus: evidence for a concomitant loss of synaptic proteins and interactions with an excitotoxin. 129:81.94. http://dx.doi.org/10.1006/exnr.1994.1149
3. Barrett, P.J., Y. Song, W.D. Van Horn, E.J. Hustedt, J.M. Schafer, A.Hadziselimovic, A.J. Beel, and C.R. Sanders. 2012. The amyloid precursorprotein has a flexible transmembrane domain and binds cholesterol.Science. 336:1168-1171. http://dx.doi.org/10.1126/science.1219988
4. Beltowski, J. 2008. Liver X receptors (LXR) as therapeutic targets in dyslipidemia.Cardiovasc Ther. 26:297-316. http://dx.doi.org/10.1111/j.1755-5922.2008.00062.x
5. Blauw, G.J., J. Shepherd, and M.B. Murphy; PROSPER study group. 2001. Dementia and statins. PROSPER study group. Lancet. 357:881. http://dx.doi.org/10.1016/S0140-6736(05)71808-0
6. Brown, M.S., and J.L. Goldstein. 1997. The SREBP pathway: regulation of cholesterol metabolism by proteolysis of a membrane-bound transcription factor. Cell. 89:331-340. http://dx.doi.org/10.1016/S0092-8674(00)80213-5
7. Cordy, J.M., N.M. Hooper, and A.J. Turner. 2006. The involvement of lipid rafts in Alzheimer's disease. Mol. Membr. Biol. 23:111-122. http://dx.doi.org/10.1080/09687860500496417
8. Coskun, U., and K. Simons. 2010. Membrane rafting: from apical sortingto phase segregation. FEBS Lett. 584:1685-1693. http://dx.doi.org/10.1016/j.febslet.2009.12.043
9. Cramer, P.E., J.R. Cirrito, D.W. Wesson, C.Y. Lee, J.C. Karlo, A.E. Zinn, B.T. Casali, J.L. Restivo, W.D. Goebel, M.J. James, et al.2012. ApoE-directed therapeutics rapidly clear Β-amyloid and reverse deficits in AD mouse models. Science. 335:1503-1506. http://dx.doi.org/10.1126/science.1217697
10. Davidson, C.D., N.F. Ali, M.C. Micsenyi, G. Stephney, S. Renault, K. Dobrenis,D.S. Ory, M.T. Vanier, and S.U. Walkley. 2009. Chronic cyclodextrin treatment of murine Niemann-Pick C disease ameliorates neuronal cholesterol and glycosphingolipid storage and disease progression. PLoS ONE. 4:e6951. http://dx.doi.org/10.1371/journal.pone.0006951
11. Di Paolo, G., and T.W. Kim. 2011. Linking lipids to Alzheimer'fs disease: cholesterol and beyond. Nat. Rev. Neurosci. 12:284-296. http://dx.doi.org/10.1038/nrn3012
12. Dickson, T.C., C.E. King, G.H. McCormack, and J.C. Vickers. 1999. Neurochemical diversity of dystrophic neurites in the early and late stages of Alzheimer's disease. Exp. Neurol. 156:100-110. http://dx.org/10.1006/exnr.1998.7010
13. Ehehalt, R., P. Keller, C. Haass, C. Thiele, and K. Simons. 2003. Amyloidogenic processing of the Alzheimer Β-amyloid precursor protein depends on lipid rafts. J. Cell Biol. 160:113-123. http://dx.doi.org/10.1jcb.200207113
14. Fontaine, C., E. Rigamonti, B. Pourcet, H. Duez, C. Duhem, J.C. Fruchart, G. Chinetti-Gbaguidi, and B. Staels. 2008. The nuclear receptor Reverbalphais a liver X receptor (LXR) target gene driving a negative feedback loop on select LXR-induced pathways in human macrophages. Mol. Endocrinol. 22:1797-1811. http://dx.doi.org/10.1210/me.2007-0439
15. Guirland, C., S. Suzuki, M. Kojima, B. Lu, and J.Q. Zheng. 2004. Lipid rafts mediate chemotropic guidance of nerve growth cones. Neuron. 42:51-62. http://dx.doi.org/10.1016/S0896-6273(04)00157-6
16. Hartmann, T., J. Kuchenbecker, and M.O. Grimm. 2007. Alzheimer'fs disease: the lipid connection. J. Neurochem. 103(Suppl 1):159-170. http://dx.doi.org/10.1111/j.1471-4159.2007.04715.x
17. Hastings, C. 2010. Request for intrathecal delivery of Hpbcd for Niemann Pick type C patients. http://addiandcassi.com/wordpress/wp-content/ uploads/Hempel-Cyclodextrin-Intrathecal-FDA-Filing-2010-Aug.pdf Accessed. September 2010.
18. Hirsch-Reinshagen, V., L.F. Maia, B.L. Burgess, J.F. Blain, K.E. Naus, S.A. McIsaac, P.F. Parkinson, J.Y. Chan, G.H. Tansley, M.R. Hayden, et al. 2005. The absence of ABCA1 decreases soluble ApoE levels but does not diminish amyloid deposition in two murine models of Alzheimer disease. J. Biol. Chem. 280:43243-43256. http://dx.doi.org/10.1074/jbc.M508781200
19. Jessup, W., I.C. Gelissen, K. Gaus, and L. Kritharides. 2006. Roles of ATP binding cassette transporters A1 and G1, scavenger receptor BI and membrane lipid domains in cholesterol export from macrophages. Curr. Opin. Lipidol. 17:247-257. http://dx.doi.org/10.1097/01.mol.0000226116 .35555.eb
20. Jick, H., G.L. Zornberg, S.S. Jick, S. Seshadri, and D.A. Drachman. 2000. Statins and the risk of dementia. Lancet. 356:1627-1631. http://dx.doi.org/10.1016/S0140-6736(00)03155-X
21. Kågedal, K., W.S. Kim, H. Appelqvist, S. Chan, D. Cheng, L. Agholme, K. Barnham, H. McCann, G. Halliday, and B. Garner. 2010. Increased expression of the lysosomal cholesterol transporter NPC1 in Alzheimer's disease. Biochim. Biophys. Acta. 1801:831-838. http://dx.doi.org/10.1016/ j.bbalip.2010.05.005
22. Kim, W.S., A.S. Rahmanto, A. Kamili, K.A. Rye, G.J. Guillemin, I.C. Gelissen, W. Jessup, A.F. Hill, and B. Garner. 2007. 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. 282:2851-2861. http://dx.doi.org/10.1074/jbc.M607831200
23. Kivipelto, M., E.L. Helkala, M.P. Laakso, T. Hänninen, M. Hallikainen, K. Alhainen, H. Soininen, J. Tuomilehto, and A. Nissinen. 2001. Midlife vascular risk factors and Alzheimer's disease in later life: longitudinal, population based study. BMJ. 322:1447-1451. http://dx.doi.org/10.1136/ bmj.322.7300.1447
24. Kodam, A., M. Maulik, K. Peake, A. Amritraj, K.S. Vetrivel, G. Thinakaran, J.E. Vance, and S. Kar. 2010. Altered levels and distribution of amyloid precursor protein and its processing enzymes in Niemann-Pick type C1-deficient mouse brains. Glia. 58:1267-1281. http://dx.doi.org/10.1002/glia.21001
25. Koldamova, R., M. Staufenbiel, and I. Lefterov. 2005a. Lack of ABCA1 considerably decreases brain ApoE level and increases amyloid deposi- tion in APP23 mice. J. Biol. Chem. 280:43224-43235. http://dx.doi.org/10.1074/jbc.M504513200
26. Koldamova, R.P., I.M. Lefterov, M. Staufenbiel, D. Wolfe, S. Huang, J.C. Glorioso, M. Walter, M.G. Roth, and J.S. Lazo. 2005b. The liver X receptor ligand T0901317 decreases amyloid beta production in vitro and in a mouse model of Alzheimer's disease. J. Biol. Chem. 280:4079- 4088. http://dx.doi.org/10.1074/jbc.M411420200
27. Lee, S.J., U. Liyanage, P.E. Bickel, W. Xia, P.T. Lansbury Jr., and K.S. Kosik. 1998. A detergent-insoluble membrane compartment contains A beta in vivo. Nat. Med. 4:730-734. http://dx.doi.org/10.1038/ nm0698-730
28. Liu, B., H. Li, J.J. Repa, S.D. Turley, and J.M. Dietschy. 2008. Genetic variations and treatments that affect the lifespan of the NPC1 mouse. J. Lipid Res. 49:663-669. http://dx.doi.org/10.1194/jlr.M700525-JLR200
29. -/- mouse. Proc. Natl. Acad. Sci. USA. 106:2377-2382. http://dx.doi.org/10.1073/ pnas.0810895106
30. Liu, B., C.M. Ramirez, A.M. Miller, J.J. Repa, S.D. Turley, and J.M. Dietschy. 2010. Cyclodextrin overcomes the transport defect in nearly every organ of NPC1 mice leading to excretion of sequestered cholesterol as bile acid. J. Lipid Res. 51:933-944. http://dx.doi.org/10.1194/jlr.M000257
31. Maulik, M., B. Ghoshal, J. Kim, Y. Wang, J. Yang, D. Westaway, and S. Kar. 2012. Mutant human APP exacerbates pathology in a mouse model of NPC and its reversal by a β-cyclodextrin. Hum. Mol. Genet. 21:4857.4875. http://dx.doi.org/10.1093/hmg/dds322
32. Maxwell, K.N., R.E. Soccio, E.M. Duncan, E. Sehayek, and J.L. Breslow. 2003. Novel putative SREBP and LXR target genes identified by microarray analysis in liver of cholesterol-fed mice. J. Lipid Res. 44:2109- 2119. http://dx.doi.org/10.1194/jlr.M300203-JLR200
33. McGuinness, B., D. Craig, R. Bullock, and P. Passmore. 2009. Statins for the prevention of dementia. Cochrane Database Syst. Rev. (2): CD003160.
34. Mesmin, B., and F.R. Maxfield. 2009. Intracellular sterol dynamics. Biochim. Biophys. Acta. 1791:636-645. http://dx.doi.org/10.1016/j.bbalip.2009 .03.002
35. Meyer-Luehmann, M., T.L. Spires-Jones, C. Prada, M. Garcia-Alloza, A. de Calignon, A. Rozkalne, J. Koenigsknecht-Talboo, D.M. Holtzman, B.J. Bacskai, and B.T. Hyman. 2008. Rapid appearance and local toxicity of amyloid-beta plaques in a mouse model of Alzheimer's disease. Nature. 451:720-724. http://dx.doi.org/10.1038/nature06616
36. Mondal, M., B. Mesmin, S. Mukherjee, and F.R. Maxfield. 2009. Sterols are mainly in the cytoplasmic leaflet of the plasma membrane and the endocytic recycling compartment in CHO cells. Mol. Biol. Cell. 20:581-588. http://dx.doi.org/10.1091/mbc.E08-07-0785
37. Morgan, D. 2011. Immunotherapy for Alzheimer's disease. J. Intern. Med. 269:54-63. http://dx.doi.org/10.1111/j.1365-2796.2010.02315.x
38. Nixon, R.A. 2004. Niemann-Pick Type C disease and Alzheimer's disease: the APP-endosome connection fattens up. Am. J. Pathol. 164:757-761. http://dx.doi.org/10.1016/S0002-9440(10)63163-X
39. Nixon, R.A., A.M. Cataldo, and P.M. Mathews. 2000. The endosomallysosomal system of neurons in Alzheimer's disease pathogenesis: a review. Neurochem. Res. 25:1161-1172. http://dx.doi.org/10.1023/ A:1007675508413
40. Peake, K.B., and J.E. Vance. 2012. Normalization of cholesterol homeostasis by 2-hydroxypropyl-β-cyclodextrin in neurons and glia from Niemann-Pick C1 (NPC1)-deficient mice. J. Biol. Chem. 287:9290-9298. http://dx.doi.org/10.1074/jbc.M111.326405
41. Puglielli, L., R.E. Tanzi, and D.M. Kovacs. 2003. Alzheimer's disease: the cholesterol connection. Nat. Neurosci. 6:345-351. http://dx.doi.org/10.1038/nn0403-345
42. Ramirez, C.M., B. Liu, A.M. Taylor, J.J. Repa, D.K. Burns, A.G. Weinberg, S.D. Turley, and J.M. Dietschy. 2010. Weekly cyclodextrin administration normalizes cholesterol metabolism in nearly every organ of the Niemann-Pick type C1 mouse and markedly prolongs life. Pediatr. Res. 68:309-315. http://dx.doi.org/10.1203/PDR.0b013e3181ee4dd2
43. Ramirez, C.M., B. Liu, A. Aqul, A.M. Taylor, J.J. Repa, S.D. Turley, and J.M. Dietschy. 2011. Quantitative role of LAL, NPC2, and NPC1 in lysosomal cholesterol processing defined by genetic and pharmacological manipulations. J. Lipid Res. 52:688-698. http://dx.doi.org/10.1194/jlr.M013789
44. Rigamonti, E., L. Helin, S. Lestavel, A.L. Mutka, M. Lepore, C. Fontaine, M.A. Bouhlel, S. Bultel, J.C. Fruchart, E. Ikonen, et al. 2005. Liver X receptor activation controls intracellular cholesterol trafficking and esterification in human macrophages. Circ. Res. 97:682-689. http://dx.doi.org/10.1161/01.RES.0000184678.43488.9f
45. Sato, R. 2010. Sterol metabolism and SREBP activation. Arch. Biochem. Biophys. 501:177-181. http://dx.doi.org/10.1016/j.abb.2010.06.004
46. Schmitz, G., and W. Drobnik. 2002. ATP-binding cassette transporters in macrophages: promising drug targets for treatment of cardiovascular disease. Curr. Opin. Investig. Drugs. 3:853-858.
47. Simons, M., P. Keller, B. De Strooper, K. Beyreuther, C.G. Dotti, and K. Simons. 1998. Cholesterol depletion inhibits the generation of betaamyloid in hippocampal neurons. Proc. Natl. Acad. Sci. USA. 95:6460-6464. http://dx.doi.org/10.1073/pnas.95.11.6460
48. Sparks, D.L., R.J. Kryscio, D.J. Connor, M.N. Sabbagh, L.M. Sparks, Y. Lin, and C. Liebsack. 2010. Cholesterol and cognitive performance in normal controls and the influence of elective statin use after conversion to mild cognitive impairment: results in a clinical trial cohort. Neurodegener. Dis. 7:183-186. http://dx.doi.org/10.1159/000295660
49. Terwel, D., K.R. Steffensen, P.B. Verghese, M.P. Kummer, J.A. Gustafsson, D.M. Holtzman, and M.T. Heneka. 2011. Critical role of astroglial apolipoprotein E and liver X receptor-α expression for microglial Aβ phagocytosis. J. Neurosci. 31:7049-7059. http://dx.doi.org/10.1523/ JNEUROSCI.6546-10.2011
50. Vetrivel, K.S., and G. Thinakaran. 2010. Membrane rafts in Alzheimer's disease beta-amyloid production. Biochim. Biophys. Acta. 1801:860-867. http://dx.doi.org/10.1016/j.bbalip.2010.03.007
51. Wahrle, S., P. Das, A.C. Nyborg, C. McLendon, M. Shoji, T. Kawarabayashi, L.H. Younkin, S.G. Younkin, and T.E. Golde. 2002. Cholesterol-dependent gamma-secretase activity in buoyant cholesterolrich membrane microdomains. Neurobiol. Dis. 9:11-23. http://dx.doi.org/10.1006/nbdi.2001.0407
52. Wahrle, S.E., H. Jiang, M. Parsadanian, R.E. Hartman, K.R. Bales, S.M. Paul, and D.M. Holtzman. 2005. Deletion of Abca1 increases Abeta deposition in the PDAPP transgenic mouse model of Alzheimer disease. J. Biol. Chem. 280:43236-43242. http://dx.doi.org/10.1074/jbc.M508780200
53. Wahrle, S.E., H. Jiang, M. Parsadanian, J. Kim, A. Li, A. Knoten, S. Jain, V. Hirsch-Reinshagen, C.L. Wellington, K.R. Bales, et al. 2008. Overexpression of ABCA1 reduces amyloid deposition in the PDAPP mouse model of Alzheimer disease. J. Clin. Invest. 118:671-682.
54. Wyss-Coray, T. 2006. Inflammation in Alzheimer disease: driving force, bystander or beneficial response? Nat. Med. 12:1005-1015.
55. Xiong, H., D. Callaghan, A. Jones, D.G. Walker, L.F. Lue, T.G. Beach, L.I. Sue, J. Woulfe, H. Xu, D.B. Stanimirovic, and W. Zhang. 2008. Cholesterol retention in Alzheimer's brain is responsible for high betaand gamma-secretase activities and Abeta production. Neurobiol. Dis. 29:422-437. http://dx.doi.org/10.1016/j.nbd.2007.10.005
56. Yang, D.S., P. Stavrides, P.S. Mohan, S. Kaushik, A. Kumar, M. Ohno, S.D. Schmidt, D. Wesson, U. Bandyopadhyay, Y. Jiang, et al. 2011. Reversal of autophagy dysfunction in the TgCRND8 mouse model of Alzheimer's disease ameliorates amyloid pathologies and memory deficits. Brain. 134:258-277. http://dx.doi.org/10.1093/brain/awq341
57. Yao, J., Y. Sasaki, Z. Wen, G.J. Bassell, and J.Q. Zheng. 2006. An essential role for beta-actin mRNA localization and translation in Ca2+-dependent growth cone guidance. Nat. Neurosci. 9:1265-1273. http://dx.doi.org/10.1038/nn1773
58. Yao, J., T. Hennessey, A. Flynt, E. Lai, M.F. Beal, and M.T. Lin. 2010. MicroRNA-related cofilin abnormality in Alzheimer's disease. PLoS ONE. 5:e15546. http://dx.doi.org/10.1371/journal.pone.0015546
59. Zhang, L., R. Sheng, and Z. Qin. 2009. The lysosome and neurodegenerative diseases. Acta Biochim. Biophys. Sin. (Shanghai). 41:437-445. http://dx.doi.org/10.1093/abbs/gmp031
60. Zidovetzki, R., and I. Levitan. 2007. Use of cyclodextrins to manipulate plasma membrane cholesterol content: evidence, misconceptions and control strategies. Biochim. Biophys. Acta. 1768:1311-1324. http://dx.doi.org/10.1016/j.bbamem.2007.03.026