24(S)-Hydroxycholesterol as a Modulator of Neuronal Signaling and Survival

Neuroscientist

Volumn 22, Issue 2, 2016, Pages 132-144

  Sun, Min Yu ^a   Linsenbardt, Andrew J ^a   Emnett, Christine M ^a   Eisenman, Lawrence N ^a   Izumi, Yukitoshi ^a   Zorumski, Charles F ^a   Mennerick, Steve ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Alzheimer's disease; apoptosis; cholesterol. 24(S) hydroxycholesterol; glutamate; NMDA

Indexed keywords

24 HYDROXYCHOLESTEROL; BIOLOGICAL MARKER; CHOLESTEROL DERIVATIVE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; OXYSTEROL; UNCLASSIFIED DRUG; CHOLESTEROL 24 HYDROXYLASE; TRANSCRIPTOME;

ALZHEIMER DISEASE; CELL SURVIVAL; DEGENERATIVE DISEASE; DOWN REGULATION; HUNTINGTON CHOREA; INTRACELLULAR SIGNALING; METABOLIC REGULATION; MOLECULAR MIMICRY; NERVE CELL PLASTICITY; NEUROMODULATION; NIEMANN PICK DISEASE; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; REVIEW; TRANSCRIPTION REGULATION; UPREGULATION; ANIMAL; BRAIN DISEASES; DRUG EFFECTS; GENETICS; HUMAN; METABOLISM; MOUSE; NERVE CELL; SIGNAL TRANSDUCTION;

ANIMALS; BRAIN DISEASES; CELL SURVIVAL; CHOLESTEROL 24-HYDROXYLASE; HUMANS; HYDROXYCHOLESTEROLS; MICE; NEURONS; RECEPTORS, N-METHYL-D-ASPARTATE; SIGNAL TRANSDUCTION; TRANSCRIPTOME;

EID: 84962598388     PISSN: 10738584     EISSN: 10894098     Source Type: Journal    
DOI: 10.1177/1073858414568122     Document Type: Review

References (84)

1. Abildayeva K, Jansen PJ, Hirsch-Reinshagen V, Bloks VW, Bakker AH, Ramaekers FC, and others. 2006. 24(S)-hydroxycholesterol participates in a liver X receptor-controlled pathway in astrocytes that regulates apolipoprotein E-mediated cholesterol efflux. J Biol Chem 281 (18): 12799-808.
2. Allen JA, Halverson-Tamboli RA, Rasenick MM,. 2007. Lipid raft microdomains and neurotransmitter signalling. Nat Rev Neurosci 8 (2): 128-40.
3. Bartzokis G,. 2011. Alzheimer's disease as homeostatic responses to age-related myelin breakdown. Neurobiol Aging 32 (8): 1341-71.
4. A receptor. Br J Pharmacol 117 (1): 87-92.
5. Bielska AA, Olsen BN, Gale SE, Mydock-McGrane L, Krishnan K, Baker NA, and others. 2014. Side-chain oxysterols modulate cholesterol accessibility through membrane remodeling. Biochemistry 53 (18): 3042-51.
6. Bielska AA, Schlesinger P, Covey DF, Ory DS,. 2012. Oxysterols as non-genomic regulators of cholesterol homeostasis. Trends Endocrinol Metab 23 (3): 99-106.
7. Björkhem I, Lövgren-Sandblom A, Leoni V, Meaney S, Brodin L, Salveson L, and others. 2013. Oxysterols and Parkinson's disease: evidence that levels of 24S-hydroxycholesterol in cerebrospinal fluid correlates with the duration of the disease. Neurosci Lett 555: 102-5.
8. Björkhem I, Meaney S,. 2004. Brain cholesterol: long secret life behind a barrier. Arterioscler Thromb Vasc Biol 24 (5): 806-15.
9. Bogdanovic N, Bretillon L, Lund EG, Diczfalusy U, Lannfelt L, Winblad B, and others. 2001. On the turnover of brain cholesterol in patients with Alzheimer's disease. Abnormal induction of the cholesterol-catabolic enzyme CYP46 in glial cells. Neurosci Lett 314 (1-2): 45-8.
10. Brown J 3rd, Theisler C, Silberman S, Magnuson D, Gottardi-Littell N, Lee JM, and others. 2004. Differential expression of cholesterol hydroxylases in Alzheimer's disease. J Biol Chem 279 (33): 34674-81.
11. Brown MS, Goldstein JL,. 1974. Suppression of 3-hydroxy-3-methylglutaryl coenzyme A reductase activity and inhibition of growth of human fibroblasts by 7-ketocholesterol. J Biol Chem 249 (22): 7306-14.
12. Calkin AC, Tontonoz P,. 2012. Transcriptional integration of metabolism by the nuclear sterol-activated receptors LXR and FXR. Nat Rev Mol Cell Biol 13 (4): 213-24.
13. A receptors. Trends Neurosci 33 (7): 299-306.
14. Cioffi CL,. 2013. Modulation of NMDA receptor function as a treatment for schizophrenia. Bioorg Med Chem Lett 23 (18): 5034-44.
15. Collingridge GL, Bliss TV,. 1995. Memories of NMDA receptors and LTP. Trends Neurosci 18 (2): 54-56.
16. Collingridge GL, Volianskis A, Bannister N, France G, Hanna L, Mercier M, and others. 2013. The NMDA receptor as a target for cognitive enhancement. Neuropharmacology 64: 13-26.
17. Cyster JG, Dang EV, Reboldi A, Yi T,. 2014. 25-Hydroxy cholesterols in innate and adaptive immunity. Nat Rev Immunol 14 (11): 731-43.
18. Dietschy JM, Turley SD,. 2004. Thematic review series: brain lipids. Cholesterol metabolism in the central nervous system during early development and in the mature animal. J Lipid Res 45 (8): 1375-97.
19. Emnett CM, Eisenman LN, Mohan J, Taylor AA, Doherty JJ, Paul SM, and others. 2014. Interaction between positive allosteric modulators and trapping blockers of the NMDA receptor channel. Br J Pharmacol 6. doi: 10.1111/bph.13007. [Epub ahead of print]
20. Emnett CM, Eisenman LN, Taylor AM, Izumi Y, Zorumski CF, Mennerick S,. 2013. Indistinguishable synaptic pharmacodynamics of the N -methyl- d -aspartate receptor channel blockers memantine and ketamine. Mol Pharmacol 84 (6): 935-47.
21. Famer D, Meaney S, Mousavi M, Nordberg A, Bjorkhem I, Crisby M,. 2007. Regulation of α- and β-secretase activity by oxysterols: cerebrosterol stimulates processing of APP via the alpha-secretase pathway. Biochem Biophys Res Commun 359 (1): 46-50.
22. Fantini J, Carlus D, Yahi N,. 2011. The fusogenic tilted peptide (67-78) of α-synuclein is a cholesterol binding domain. Biochim Biophys Acta 1808 (10): 2343-51.
23. Ferrera P, Mercado-Gomez O, Silva-Aguilar M, Valverde M, Arias C,. 2008. Cholesterol potentiates beta-amyloid-induced toxicity in human neuroblastoma cells: involvement of oxidative stress. Neurochem Res 33 (8): 1509-17.
24. Gamba P, Leonarduzzi G, Tamagno E, Guglielmotto M, Testa G, Sottero B, and others. 2011. Interaction between 24-hydroxycholesterol, oxidative stress, and amyloid-beta in amplifying neuronal damage in Alzheimer's disease: three partners in crime. Aging Cell 10 (3): 403-17.
25. Gamba P, Testa G, Sottero B, Gargiulo S, Poli G, Leonarduzzi G,. 2012. The link between altered cholesterol metabolism and Alzheimer's disease. Ann N Y Acad Sci 1259: 54-64.
26. Garcia AN, Muniz MT, Souza e Silva HR, da Silva HA, Athayde-Junior L,. 2009. Cyp46 polymorphisms in Alzheimer's disease: a review. J Mol Neurosci 39 (3): 342-5.
27. Halford RW, Russell DW,. 2009. Reduction of cholesterol synthesis in the mouse brain does not affect amyloid formation in Alzheimer's disease, but does extend lifespan. Proc Natl Acad Sci U S A 106 (9): 3502-6.
28. Hardingham GE, Bading H,. 2010. Synaptic versus extrasynaptic NMDA receptor signalling: implications for neurodegenerative disorders. Nat Rev Neurosci 11 (10): 682-96.
29. Hedegaard M, Hansen KB, Andersen KT, Brauner-Osborne H, Traynelis SF,. 2012. Molecular pharmacology of human NMDA receptors. Neurochem Int 61 (4): 601-9.
30. Hogins J, Crawford DC, Jiang X, Mennerick S,. 2011. Presynaptic silencing is an endogenous neuroprotectant during excitotoxic insults. Neurobiol Dis 43 (2): 516-25.
31. Hong C, Tontonoz P,. 2014. Liver X receptors in lipid metabolism: opportunities for drug discovery. Nat Rev Drug Discov 13 (6): 433-44.
32. Hu H, Zhou Y, Leng T, Liu A, Wang Y, You X, and others. 2014. The major cholesterol metabolite cholestane-3beta,5alpha,6beta-triol functions as an endogenous neuroprotectant. J Neurosci 34 (34): 11426-38.
33. Hughes TM, Rosano C, Evans RW, Kuller LH,. 2013. Brain cholesterol metabolism, oxysterols, and dementia. J Alzheimers Dis 33 (4): 891-911.
34. Izumi Y, Zorumski CF,. 2014. Metaplastic effects of subanesthetic ketamine on CA1 hippocampal function. Neuropharmacology 86: 273-81.
35. Kandutsch AA, Chen HW,. 1974. Inhibition of sterol synthesis in cultured mouse cells by cholesterol derivatives oxygenated in the side chain. J Biol Chem 249 (19): 6057-61.
36. Kotti T, Head DD, McKenna CE, Russell DW,. 2008. Biphasic requirement for geranylgeraniol in hippocampal long-term potentiation. Proc Natl Acad Sci U S A 105 (32): 11394-9.
37. Kotti TJ, Ramirez DM, Pfeiffer BE, Huber KM, Russell DW,. 2006. Brain cholesterol turnover required for geranylgeraniol production and learning in mice. Proc Natl Acad Sci U S A 103 (10): 3869-74.
38. Lang T, Bruns D, Wenzel D, Riedel D, Holroyd P, Thiele C, and others. 2001. SNAREs are concentrated in cholesterol-dependent clusters that define docking and fusion sites for exocytosis. EMBO J. 20 (9): 2202-2213.
39. Lee CY, Seet RC, Huang SH, Long LH, Halliwell B,. 2009. Different patterns of oxidized lipid products in plasma and urine of dengue fever, stroke, and Parkinson's disease patients: cautions in the use of biomarkers of oxidative stress. Antioxid Redox Signal 11 (3): 407-20.
40. Leoni V, Caccia C,. 2013. Potential diagnostic applications of side chain oxysterols analysis in plasma and cerebrospinal fluid. Biochem Pharmacol 86 (1): 26-36.
41. Leoni V, Caccia C,. 2014. Study of cholesterol metabolism in Huntington's disease. Biochem Biophys Res Commun 446 (3): 697-701.
42. Leoni V, Long JD, Mills JA, Di Donato S, Paulsen JS, PREDICT-HD study group. 2013a. Plasma 24S-hydroxycholesterol correlation with markers of Huntington disease progression. Neurobiol Dis 55: 37-43.
43. Leoni V, Mariotti C, Nanetti L, Salvatore E, Squitieri F, Bentivoglio AR, and others. 2011. Whole body cholesterol metabolism is impaired in Huntington's disease. Neurosci Lett 494 (3): 245-9.
44. Leoni V, Solomon A, Lovgren-Sandblom A, Minthon L, Blennow K, Hansson O, and others. 2013b. Diagnostic power of 24S-hydroxycholesterol in cerebrospinal fluid: candidate marker of brain health. J Alzheimers Dis 36 (4): 739-47.
45. Linsenbardt AJ, Taylor A, Emnett CM, Doherty JJ, Krishnan K, Covey DF, and others. 2014. Different oxysterols have opposing actions at N -methyl- d -aspartate receptors. Neuropharmacology 85C: 232-42.
46. Lund EG, Xie C, Kotti T, Turley SD, Dietschy JM, Russell DW,. 2003. Knockout of the cholesterol 24-hydroxylase gene in mice reveals a brain-specific mechanism of cholesterol turnover. J Biol Chem 278 (25): 22980-8.
47. Lutjohann D, Breuer O, Ahlborg G, Nennesmo I, Siden A, Diczfalusy U, and others. 1996. Cholesterol homeostasis in human brain: evidence for an age-dependent flux of 24S-hydroxycholesterol from the brain into the circulation. Proc Natl Acad Sci U S A 93 (18): 9799-804.
48. Lutjohann D, Papassotiropoulos A, Bjorkhem I, Locatelli S, Bagli M, Oehring RD, and others. 2000. Plasma 24S-hydroxycholesterol (cerebrosterol) is increased in Alzheimer and vascular demented patients. J Lipid Res 41 (2): 195-8.
49. Mast N, Charvet C, Pikuleva IA, Stout CD,. 2010. Structural basis of drug binding to CYP46A1, an enzyme that controls cholesterol turnover in the brain. J Biol Chem 285 (41): 31783-95.
50. Meaney S,. 2014. Epigenetic regulation of cholesterol homeostasis. Front Genet 5: 311.
51. Meljon A, Theofilopoulos S, Shackleton CH, Watson GL, Javitt NB, Knolker HJ, and others. 2012. Analysis of bioactive oxysterols in newborn mouse brain by LC/MS. J Lipid Res 53 (11): 2469-83.
52. Meljon A, Wang Y, Griffiths WJ,. 2014. Oxysterols in the brain of the cholesterol 24-hydroxylase knockout mouse. Biochem Biophys Res Commun 446 (3): 768-74.
53. Moghaddam B, Javitt D,. 2012. From revolution to evolution: the glutamate hypothesis of schizophrenia and its implication for treatment. Neuropsychopharmacology 37 (1): 4-15.
54. Mohn AR, Gainetdinov RR, Caron MG, Koller BH,. 1999. Mice with reduced NMDA receptor expression display behaviors related to schizophrenia. Cell 98 (4): 427-36.
55. Ohtsuki S, Ito S, Matsuda A, Hori S, Abe T, Terasaki T,. 2007. Brain-to-blood elimination of 24S-hydroxycholesterol from rat brain is mediated by organic anion transporting polypeptide 2 (oatp2) at the blood-brain barrier. J Neurochem 103 (4): 1430-8.
56. Okabe A, Urano Y, Itoh S, Suda N, Kotani R, Nishimura Y, and others. 2013. Adaptive responses induced by 24S-hydroxycholesterol through liver X receptor pathway reduce 7-ketocholesterol-caused neuronal cell death. Redox Biol 2: 28-35.
57. Olsen BN, Schlesinger PH, Ory DS, Baker NA,. 2012. Side-chain oxysterols: from cells to membranes to molecules. Biochim Biophys Acta 1818 (2): 330-6.
58. Ory DS,. 2000. Niemann-Pick type C: a disorder of cellular cholesterol trafficking. Biochim Biophys Acta 1529 (1-3): 331-9.
59. Papassotiropoulos A, Lutjohann D, Bagli M, Locatelli S, Jessen F, Buschfort R, and others. 2002. 24S-hydroxycholesterol in cerebrospinal fluid is elevated in early stages of dementia. J Psychiatr Res 36 (1): 27-32.
60. Papassotiropoulos A, Streffer JR, Tsolaki M, Schmid S, Thal D, Nicosia F, and others. 2003. Increased brain beta-amyloid load, phosphorylated tau, and risk of Alzheimer disease associated with an intronic CYP46 polymorphism. Arch Neurol 60 (1): 29-35.
61. Paul SM, Doherty JJ, Robichaud AJ, Belfort GM, Chow BY, Hammond RS, and others. 2013. The major brain cholesterol metabolite 24(S)-hydroxycholesterol is a potent allosteric modulator of N -methyl- d -aspartate receptors. J Neurosci 33 (44): 17290-300.
62. Pfrieger FW, Ungerer N,. 2011. Cholesterol metabolism in neurons and astrocytes. Prog Lipid Res 50 (4): 357-71.
63. Poli G, Biasi F, Leonarduzzi G,. 2013. Oxysterols in the pathogenesis of major chronic diseases. Redox Biol 1 (1): 125-30.
64. Porter FD, Scherrer DE, Lanier MH, Langmade SJ, Molugu V, Gale SE, and others. 2010. Cholesterol oxidation products are sensitive and specific blood-based biomarkers for Niemann-Pick C1 disease. Sci Transl Med 2 (56): 56ra81.
65. Ramirez DM, Andersson S, Russell DW,. 2008. Neuronal expression and subcellular localization of cholesterol 24-hydroxylase in the mouse brain. J Comp Neurol 507 (5): 1676-93.
66. Rankin SE, Addona GH, Kloczewiak MA, Bugge B, Miller KW,. 1997. The cholesterol dependence of activation and fast desensitization of the nicotinic acetylcholine receptor. Biophys J 73 (5): 2446-55.
67. Rothman S,. 1984. Synaptic release of excitatory amino acid neurotransmitter mediates anoxic neuronal death. J Neurosci 4 (7): 1884-91.
68. Rothman SM, Olney JW,. 1987. Excitotoxicity and the NMDA receptor. Trends Neurosci 10: 299-302.
69. Russell DW,. 2000. Oxysterol biosynthetic enzymes. Biochim Biophys Acta 1529 (1-3): 126-35.
70. Russell DW, Halford RW, Ramirez DM, Shah R, Kotti T,. 2009. Cholesterol 24-hydroxylase: an enzyme of cholesterol turnover in the brain. Annu Rev Biochem 78: 1017-40.
71. Shafaati M, Mast N, Beck O, Nayef R, Heo GY, Bjorkhem-Bergman L, and others. 2010. The antifungal drug voriconazole is an efficient inhibitor of brain cholesterol 24S-hydroxylase in vitro and in vivo. J Lipid Res 51 (2): 318-23.
72. Spann NJ, Glass CK,. 2013. Sterols and oxysterols in immune cell function. Nat Immunol 14 (9): 893-900.
73. Sturley SL, Patterson MC, Pentchev P,. 2009. Unraveling the sterol-trafficking defect in Niemann-Pick C disease. Proc Natl Acad Sci U S A 106 (7): 2093-4.
74. Traynelis SF, Wollmuth LP, McBain CJ, Menniti FS, Vance KM, Ogden KK, and others. 2010. Glutamate receptor ion channels: structure, regulation, and function. Pharmacol Rev 62 (3): 405-96.
75. Urano Y, Ochiai S, Noguchi N,. 2013. Suppression of amyloid-beta production by 24S-hydroxycholesterol via inhibition of intracellular amyloid precursor protein trafficking. FASEB J 27 (10): 4305-15.
76. Valdez CM, Smith MA, Perry G, Phelix CF, Santamaria F,. 2010. Cholesterol homeostasis markers are localized to mouse hippocampal pyramidal and granule layers. Hippocampus 20 (8): 902-5.
77. Valenza M, Leoni V, Tarditi A, Mariotti C, Bjorkhem I, Di Donato S, and others. 2007. Progressive dysfunction of the cholesterol biosynthesis pathway in the R6/2 mouse model of Huntington's disease. Neurobiol Dis 28 (1): 133-42.
78. Valenza M, Rigamonti D, Goffredo D, Zuccato C, Fenu S, Jamot L, and others. 2005. Dysfunction of the cholesterol biosynthetic pathway in Huntington's disease. J Neurosci 25 (43): 9932-9.
79. Wang L, Schuster GU, Hultenby K, Zhang Q, Andersson S, Gustafsson JA,. 2002. Liver X receptors in the central nervous system: from lipid homeostasis to neuronal degeneration. Proc Natl Acad Sci U S A 99 (21): 13878-83.
80. Wasser CR, Ertunc M, Liu X, Kavalali ET,. 2007. Cholesterol-dependent balance between evoked and spontaneous synaptic vesicle recycling. J Physiol 579 (Pt 2): 413-29.
81. Yamanaka K, Saito Y, Yamamori T, Urano Y, Noguchi N,. 2011. 24(S)-hydroxycholesterol induces neuronal cell death through necroptosis, a form of programmed necrosis. J Biol Chem 286 (28): 24666-73.
82. Yamanaka K, Urano Y, Takabe W, Saito Y, Noguchi N,. 2014. Induction of apoptosis and necroptosis by 24(S)-hydroxycholesterol is dependent on activity of acyl-CoA:cholesterol acyltransferase 1. Cell Death Dis 5: e990.
83. Zampieri S, Mellon SH, Butters TD, Nevyjel M, Covey DF, Bembi B, and others. 2009. Oxidative stress in NPC1 deficient cells: protective effect of allopregnanolone. J Cell Mol Med 13 (9B): 3786-96.
84. Zhang JR, Coleman T, Langmade SJ, Scherrer DE, Lane L, Lanier MH, and others. 2008. Niemann-Pick C1 protects against atherosclerosis in mice via regulation of macrophage intracellular cholesterol trafficking. J Clin Invest 118 (6): 2281-90.