The major cholesterol metabolite cholestane-3β,5α,6β-triol functions as an endogenous neuroprotectant

Journal of Neuroscience

Volumn 34, Issue 34, 2014, Pages 11426-11438

  Hu, Haiyan ^b   Zhou, Yuehan ^a   Leng, Tiandong ^a   Liu, Ailing ^a   Wang, Youqiong ^a   You, Xiuhua ^b   Chen, Jingkao ^a   Tang, Lipeng ^a   Chen, Wenli ^a   Qiu, Pengxin ^a   Yin, Wei ^a   Huang, Yijun ^a   Zhang, Jingxia ^a   Wang, Liwei ^c   Sang, Hanfei ^a,d   Yan, Guangmei ^a  

^a SUN YAT SEN UNIVERSITY   (China)

^b SUN YAT SEN UNIVERSITY   (China)

^c MEDICAL COLLEGE OF JINAN UNIVERSITY   (China)

^d FOURTH MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

Calcium; Cerebral ischemia; Cholestane 3 ,5 ,6 triol; NMDA; Spinal cord ischemia; Steroid

Indexed keywords

CHOLESTANE 3BETA, 5ALPHA, 6BETA TRIOL; CHOLESTEROL; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; UNCLASSIFIED DRUG; AMINO ACID RECEPTOR BLOCKING AGENT; CHOLESTANE-3,5,6-TRIOL; CHOLESTANOL; DIZOCILPINE MALEATE; GLUTAMIC ACID; NEUROPROTECTIVE AGENT; PROTEIN BINDING;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN ISCHEMIA; CALCIUM CURRENT; FEMALE; HUMAN; HUMAN CELL; ISCHEMIC PRECONDITIONING; LIQUID CHROMATOGRAPHY; MALE; MASS SPECTROMETRY; NERVE INJURY; NEUROMODULATION; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; NORMAL HUMAN; PRIORITY JOURNAL; RABBIT; RAT; SPINAL CORD ISCHEMIA; ANIMAL; BLOOD; BRAIN INJURIES; CELL CULTURE; CENTRAL NERVOUS SYSTEM; CEREBRAL ARTERY DISEASE; COMPLICATION; CYTOLOGY; DISEASE MODEL; DRUG EFFECTS; NERVE CELL; PHYSIOLOGY; SPRAGUE DAWLEY RAT; TIME; TISSUE DISTRIBUTION; YOUNG ADULT;

ADULT; ANIMALS; BRAIN INJURIES; CELLS, CULTURED; CENTRAL NERVOUS SYSTEM; CHOLESTANOLS; DISEASE MODELS, ANIMAL; DIZOCILPINE MALEATE; EXCITATORY AMINO ACID ANTAGONISTS; FEMALE; GLUTAMIC ACID; HUMANS; INFARCTION, MIDDLE CEREBRAL ARTERY; MALE; NEURONS; NEUROPROTECTIVE AGENTS; PROTEIN BINDING; RABBITS; RATS; RATS, SPRAGUE-DAWLEY; SPINAL CORD ISCHEMIA; TIME FACTORS; TISSUE DISTRIBUTION; YOUNG ADULT;

EID: 84906276029     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0344-14.2014     Document Type: Article

References (58)

1. Al Hasan M., Murugan R (2012) Stenting versus aggressive medical therapy for intracranial arterial stenosis: more harm than good. Crit Care 16:310. CrossRef Medline
2. Berman F. W, Murray TF (1996) Characterization of glutamate toxicity in cultured rat cerebellar granule neurons at reduced temperature. J Biochem Toxicol 11:111-119. CrossRef Medline
3. Budd S. L (1998) Mechanisms of neuronal damage in brain hypoxia/ischemia: focus on the role of mitochondrial calcium accumulation. Pharmacol Ther 80:203-229. CrossRef Medline
4. Celik M., Gökmen N, Erbayraktar S, Akhisaroglu M, Konakc S, Ulukus C, Genc S., Genc K, Sagiroglu E, Cerami A, BrinesM (2002) Erythropoietin prevents motor neuron apoptosis and neurologic disability in experimental spinal cord ischemic injury. Proc Natl Acad Sci U S A 99:2258-2263. CrossRef Medline
5. Chen W. Q, Jin H, Nguyen M, Carr J, Lee YJ, Hsu CC, Faiman MD, Schloss JV, Wu J. Y (2001) Role of taurine in regulation of intracellular calcium level and neuroprotective function in cultured neurons. J Neurosci Res 66: 612-619. CrossRef Medline
6. Clarkson A. N (2007) Anesthetic-mediated protection/preconditioning during cerebral ischemia. Life Sci 80:1157-1175. CrossRef Medline
7. Cross J. L, Meloni BP, Bakker AJ, Lee S, Knuckey NW (2010) Modes of neuronal calcium entry and homeostasis following cerebral ischemia. Stroke Res Treat 2010:316862. CrossRef Medline
8. Dichter M. A (1978) Rat cortical neurons in cell culture: culture methods, cell morphology, electrophysiology, and synapse formation. Brain Res 149:279-293. CrossRef Medline
9. Dirnagl U., Meisel A (2008) Endogenous neuroprotection: mitochondria as gateways to cerebral preconditioning? Neuropharmacology 55:334-344. CrossRef Medline
10. Dyker A. G, Weir CJ, Lees KR (1997) Influence of cholesterol on survival after stroke: retrospective study. BMJ 314:1584-1588. CrossRef Medline
11. Evans R. C, Morera-Herreras T, Cui Y, Du K, Sheehan T, Kotaleski JH, Venance L, Blackwell KT (2012) The effects of NMDA subunit composition on calcium influx and spike timing-dependent plasticity in striatal medium spiny neurons. PLoS Comput Biol 8:e1002493. CrossRef Medline
12. Fahey J. M, Lindquist DG, Pritchard GA, Miller LG (1995) Pregnenolone sulfate potentiation of NMDA-mediated increases in intracellular calcium in cultured chick cortical neurons. Brain Res 669:183-188. CrossRef Medline
13. Fang B., Li XM, Sun XJ, Bao NR, Ren XY, Lv HW, Ma H (2013) Ischemic preconditioning protects against spinal cord ischemia-reperfusion injury in rabbits by attenuating blood spinal cord barrier disruption. Int J Mol Sci 14:10343-10354. CrossRef Medline
14. Földes-Papp Z., Demel U, Tilz GP (2003) Laser scanning confocal fluorescence microscopy: an overview. Int Immunopharmacol 3:1715-1729. CrossRef Medline
15. Giffard R. G, Swanson RA (2005) Ischemia-induced programmed cell death in astrocytes. Glia 50:299-306. CrossRef Medline
16. Gu G. (1955) Shen Nong's herbal classic. Peking, China: People's Medical Publishing House.
17. Guo Z. Y, Li CZ, Li XJ, Wang YL, Mattson MP, Lu CB (2013) The developmental regulation of glutamate receptor-mediated calcium signaling in primary cultured rat hippocampal neurons. Neuroreport 24:492-497. CrossRef Medline
18. Huang H., Zhang L, Wang Y, Yao J, Weng H, Wu H, Chen Z, Liu J (2007) Effect of ischemic post-conditioning on spinal cord ischemic-reperfusion injury in rabbits. Can J Anaesth 54:42-48. CrossRef Medline
19. Huettner J. E, Bean BP (1988) Block of N-methyl-D-aspartate-activated current by the anticonvulsant MK-801: selective binding to open channels. Proc Natl Acad Sci U S A 85:1307-1311. CrossRef Medline
20. Hughes R. A, Sendtner M, Thoenen H (1993) Members of several gene families influence survival of rat motoneurons in vitro and in vivo. J Neurosci Res 36:663-671. CrossRef Medline
21. Iso H., Jacobs DR Jr, Wentworth D, Neaton JD, Cohen JD (1989) Serum cholesterol levels and six-year mortality from stroke in 350,977 men screened for the multiple risk factor intervention trial. N Engl J Med 320:904-910. CrossRef Medline
22. Javitt N. B (1994) Bile acid synthesis from cholesterol: regulatory and auxiliary pathways. FASEB J 8:1308-1311. Medline
23. Johnson S. H, Kraimer JM, GraeberGM (1993) Effects of flunarizine on neurological recovery and spinal cord blood flow in experimental spinal cord ischemia in rabbits. Stroke 24:1547-1553. CrossRef Medline
24. Kirihara Y., Hamazaki K, Hamazaki T, Ogushi Y, Tsuji H, Shirasaki S (2008) The relationship between total blood cholesterol levels and all-cause mortality in Fukui city, and meta-analysis of this relationship in Japan. J Lipid Nutr 17:67-78.
25. Kocaeli H., Korfali E, Oztürk H, Kahveci N, Yilmazlar S (2005) MK-801 improves neurological and histological outcomes after spinal cord ischemia induced by transient aortic cross-clipping in rats. Surg Neurol 64 [Suppl 2]:S22-S26; discussion S27.
26. Lai T. W, Shyu WC, Wang YT (2011) Stroke intervention pathways: NMDA receptors and beyond. Trends Mol Med 17:266-275. CrossRef Medline
27. Leonarduzzi G., Gamba P, Sottero B, Kadl A, Robbesyn F, Calogero RA, Biasi F, Chiarpotto E, Leitinger N, Sevanian A, Poli G (2005) Oxysterolinduced up-regulation of MCP-1 expression and synthesis in macrophage cells. Free Radical Bio Med 39:1152-1161. CrossRef Medline
28. Longa E. Z, Weinstein PR, Carlson S, Cummins R (1989) Reversible middle cerebral artery occlusion without craniectomy in rats. Stroke 20:84-91. CrossRef Medline
29. Matthias D., Becker CH, Gödicke W, Schmidt R, Ponsold K (1987) Action of cholestane-3 beta,5 alpha,6 beta-triol on rats with particular reference to the aorta. Atherosclerosis 63:115-124. CrossRef Medline
30. Mauch D. H, Nägler K, Schumacher S, Göritz C, Müller EC, Otto A, Pfrieger FW (2001) CNS synaptogenesis promoted by glia-derived cholesterol. Science 294:1354-1357. CrossRef Medline
31. Mori T., Tateishi N, Kagamiishi Y, Shimoda T, Satoh S, Ono S, Katsube N, Asano T. (2004) Attenuation of a delayed increase in the extracellular glutamate level in the peri-infarct area following focal cerebral ischemia by a novel agent ONO-2506. Neurochem Int 45:381-387. CrossRef Medline
32. Murphy S. N, Miller RJ (1988) A glutamate receptor regulates Ca2+ mobilization in hippocampal neurons. Proc Natl Acad Sci U S A 85:8737-8741. CrossRef Medline
33. Nashed N. T, Michaud DP, Levin W, Jerina DM (1985) Properties of liver microsomal cholesterol 5,6-oxide hydrolase. Arch Biochem Biophys 241: 149-162. CrossRef Medline
34. Olsen T. S, Christensen RH, Kammersgaard LP, Andersen KK (2007) Higher total serum cholesterol levels are associated with less severe strokes and lower all-cause mortality: ten-year follow-up of ischemic strokes in the Copenhagen Stroke Study. Stroke 38:2646-2651. CrossRef Medline
35. Palkovits M., Elekes I, Láng T, Patthy A (1986) Taurine levels in discrete brain nuclei of rats. J Neurochem 47:1333-1335. CrossRef Medline
36. Paoletti P., Neyton J (2007) NMDA receptor subunits: function and pharmacology. Curr Opin Pharmacol 7:39-47. CrossRef Medline
37. Paul S. M, Doherty JJ, Robichaud AJ, Belfort GM, Chow BY, Hammond RS, Crawford D. C, Linsenbardt AJ, Shu HJ, Izumi Y, Mennerick SJ, Zorumski CF (2013) The major brain cholesterol metabolite 24(S)-hydroxycholesterol is a potent allosteric modulator of N-methyl-D-aspartate receptors. J Neurosci 33:17290-17300. CrossRef Medline
38. Payne A. H, HalesDB (2004) Overview of steroidogenic enzymes in the pathway from cholesterol to active steroid hormones. Endocr Rev 25:947-970. CrossRef Medline
39. Piccolini V. M, Bottone MG, Bottiroli G, De Pascali SA, Fanizzi FP, Bernocchi G (2013) Platinum drugs and neurotoxicity: effects on intracellular calcium homeostasis. Cell Biol Toxicol 29:339-353. CrossRef Medline
40. Porcellati G. (1963) On the occurence and distribution of free phospholipid phosphoric esters and some amino acid compounds in the nervous tissues of some animal species. Riv Biol 56:209-226.
41. Qiu S., Hua YL, Yang F, Chen YZ, Luo JH (2005) Subunit assembly of N-methyl-D-aspartate receptors analyzed by fluorescence resonance energy transfer. J Biol Chem 280:24923-24930. CrossRef Medline
42. Razzazi-Fazeli E., Kleineisen S, Luf W (2000) Determination of cholesterol oxides in processed food using high performance liquid chromatography-mass spectrometry with atmospheric pressure chemical ionization. J Chromatog A 896:321-334. Medline
43. Rodríguez-Moreno A., Kohl MM, Reeve JE, Eaton TR, Collins HA, Anderson HL, Paulsen O (2011) Presynaptic induction and expression of timingdependent long-term depression demonstrated by compartment-specific photorelease of a use-dependent NMDA receptor antagonist. J Neurosci 31:8564-8569. CrossRef Medline
44. Schroepfer G. J Jr (2000) Oxysterols: modulators of cholesterol metabolism and other processes. Physiol Rev 80:361-554. Medline
45. Sevanian A., McLeod LL (1986) Catalytic properties and inhibition of hepatic cholesterol-epoxide hydrolase. J Biol Chem 261:54-59. Medline
46. Sevanian A., Seraglia R, Traldi P, Rossato P, Ursini F, Hodis H (1994) Analysis of plasma cholesterol oxidation products using gas-and highperformance liquid chromatography/mass spectrometry. Free Radical Bio Med 17:397-409. CrossRef Medline
47. Steck T. L, Lange Y (2010) Cell cholesterol homeostasis: mediation by active cholesterol. Trends Cell Biol 20:680-687. CrossRef Medline
48. Stetler R. A, Leak RK, Gan Y, Li P, Zhang F, Hu X, Jing Z, Chen J, Zigmond MJ, Gao Y. (2014) Preconditioning provides neuroprotection in models of CNS disease: paradigms and clinical significance. Prog Neurobiol 114: 58-83. CrossRef Medline
49. Sun H., Zheng X, Zhou Y, Zhu W, Ou Y, Shu M, Gao X, Leng T, Qiu P, Yan G (2013) Alphaxalone inhibits growth, migration and invasion of rat C6 malignant glioma cells. Steroids 78:1041-1045. CrossRef Medline
50. Swanson R. A, Morton MT, Tsao-Wu G, Savalos RA, Davidson C, Sharp FR. A (1990) Semiautomated method for measuring brain infarct volume. J Cereb Blood Flow Metab 10: 290-293. CrossRef Medline
51. Szydlowska K., Tymianski M (2010) Calcium, ischemia and excitotoxicity. Cell Calcium 47:122-129. CrossRef Medline
52. Thiyagarajan R., Sunderrajan A (1992) Gunapadam thatu jeeva vagupp. In: Gunapadam thatu jeeva vagupp, pp 474-478. Chennai, India: Directorate of Indian Medicine and Homeopathy.
53. Villmann C., Becker CM (2007) On the hypes and falls in neuroprotection: targeting the NMDA receptor. Neuroscientist 13:594-615. CrossRef Medline
54. Xiong Z. G, Zhu XM, Chu XP, Minami M, Hey J, Wei WL, MacDonald JF, WemmieJA, Price MP, Welsh MJ, Simon RP (2004) Neuroprotection in ischemia: Blocking calcium-permeable acid-sensing ion channels. Cell 118:687-698. CrossRef Medline
55. WuH, Jin Y, Wei J, Jin H, Sha D, WuJY (2005) Mode of action of taurine as a neuroprotector. Brain Res 1038:123-131. CrossRef Medline
56. Yang C., Ren Y, Liu F, Cai W, Zhang N, Nagel DJ, Yin G (2008) Ischemic preconditioning suppresses apoptosis of rabbit spinal neurocytes by inhibiting ASK1-14-3-3 dissociation. Neurosci Lett 441:267-271. CrossRef Medline
57. Yu Q. J, Wang YL, Zhou QS, Huang HB, Tian SF, Duan DM (2006) Effect of repetitive ischemic preconditioning on spinal cord ischemia in a rabbit model. Life Sci 79:1479-1483. CrossRef Medline
58. Zhao L., Liu X, Liang J, Han S, Wang Y, Yin Y, Luo Y, Li J (2013) Phosphorylation of p38 MAPK mediates hypoxic preconditioning-induced neuroprotection against cerebral ischemic injury via mitochondria translocation of Bcl-xL in mice. Brain Res 1503:78-88. CrossRef Medline