Allopregnanolone promotes regeneration and reduces β-amyloid burden in a preclinical model of Alzheimer's disease

PLoS ONE

Volumn 6, Issue 8, 2011, Pages

  Chen, Shuhua ^a   Wang, Jun Ming ^b   Irwin, Ronald W ^a   Yao, Jia ^a   Liu, Lifei ^a   Brinton, Roberta Diaz ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b UNIVERSITY OF MISSISSIPPI SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2',3' CYCLIC NUCLEOTIDE 3' PHOSPHODIESTERASE; 3ALPHA HYDROXY 5ALPHA PREGNAN 20 ONE; AMYLOID BETA PROTEIN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE; LIVER X RECEPTOR; PREGNANE X RECEPTOR; TAU PROTEIN; AMYLOID; ELTANOLONE;

ALZHEIMER DISEASE; AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CELLULAR DISTRIBUTION; CHOLESTEROL METABOLISM; CONTROLLED STUDY; DOWN REGULATION; DRUG EFFICACY; DRUG TARGETING; HIPPOCAMPUS; LEARNING; MALE; MEMORY; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NEUROPATHOLOGY; NONHUMAN; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; REGENERATION; SURVIVAL RATE; TISSUE DISTRIBUTION; TRANSGENIC MOUSE; UPREGULATION; ANIMAL; DRUG EFFECT; FLOW CYTOMETRY; GENETICS; HUMAN; IMMUNOBLOTTING; METABOLISM; MICROGLIA;

MUS MUSCULUS; RODENTIA;

2',3'-CYCLIC-NUCLEOTIDE PHOSPHODIESTERASES; ALZHEIMER DISEASE; AMYLOID; AMYLOID BETA-PEPTIDES; ANIMALS; FLOW CYTOMETRY; HUMANS; HYDROXYMETHYLGLUTARYL COA REDUCTASES; IMMUNOBLOTTING; MALE; MICE; MICROGLIA; PREGNANOLONE;

EID: 80052279560     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0024293     Document Type: Article

References (58)

1. Selkoe DJ, (2001) Alzheimer's disease results from the cerebral accumulation and cytotoxicity of amyloid beta-protein. J Alzheimers Dis 3: 75-80.
2. Bartzokis G, (2004) Age-related myelin breakdown: a developmental model of cognitive decline and Alzheimer's disease. Neurobiol Aging 25: 5-18; author reply 9-62.
3. Bartzokis G, Cummings JL, Sultzer D, Henderson VW, Nuechterlein KH, et al. (2003) White matter structural integrity in healthy aging adults and patients with Alzheimer disease: a magnetic resonance imaging study. Arch Neurol 60: 393-398.
4. Bartzokis G, Lu PH, Tingus K, Mendez MF, Richard A, et al. (2010) Lifespan trajectory of myelin integrity and maximum motor speed. Neurobiol Aging 31: 1554-1562.
5. Oddo S, Caccamo A, Shepherd JD, Murphy MP, Golde TE, et al. (2003) Triple-transgenic model of Alzheimer's disease with plaques and tangles: intracellular Abeta and synaptic dysfunction. Neuron 39: 409-421.
6. Desai MK, Sudol KL, Janelsins MC, Mastrangelo MA, Frazer ME, et al. (2009) Triple-transgenic Alzheimer's disease mice exhibit region-specific abnormalities in brain myelination patterns prior to appearance of amyloid and tau pathology. Glia 57: 54-65.
7. Wang JM, Johnston PB, Ball BG, Brinton RD, (2005) The neurosteroid allopregnanolone promotes proliferation of rodent and human neural progenitor cells and regulates cell-cycle gene and protein expression. J Neurosci 25: 4706-4718.
8. Wang JM, Singh C, Liu L, Irwin RW, Chen S, et al. (2010) Allopregnanolone reverses neurogenic and cognitive deficits in mouse model of Alzheimer's disease. Proc Natl Acad Sci U S A 107: 6498-6503.
9. Marx CE, Trost WT, Shampine LJ, Stevens RD, Hulette CM, et al. (2006) The Neurosteroid Allopregnanolone Is Reduced in Prefrontal Cortex in Alzheimer's Disease. Biol Psychiatry 60: 1287-1294.
10. Naylor JC, Kilts JD, Hulette CM, Steffens DC, Blazer DG, et al. (2010) Allopregnanolone levels are reduced in temporal cortex in patients with Alzheimer's disease compared to cognitively intact control subjects. Biochim Biophys Acta 1801: 951-959.
11. Schumacher M, Guennoun R, Robert F, Carelli C, Gago N, et al. (2004) Local synthesis and dual actions of progesterone in the nervous system: neuroprotection and myelination. Growth Hormone & Igf Research 14 (Suppl A): S18-33.
12. Mellon SH, Gong W, Schonemann MD, (2008) Endogenous and synthetic neurosteroids in treatment of Niemann-Pick Type C disease. Brain Res Rev 57: 410-420.
13. Oosterveer MH, Grefhorst A, Boesjes M, Bos T, Kuipers F, et al. (2010) Time-dependent effects of pharmacological Liver X Receptor activation in mice. European Journal of Clinical Investigation 40: 64-64.
14. Zhou H, Li Z, Silver DL, Jiang XC, (2006) Cholesteryl ester transfer protein (CETP) expression enhances HDL cholesteryl ester liver delivery, which is independent of scavenger receptor BI, LDL receptor related protein and possibly LDL receptor. Biochim Biophys Acta 1761: 1482-1488.
15. Koldamova RP, Lefterov IM, Staufenbiel M, Wolfe D, Huang S, et al. (2005) 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.
16. Lustbader JW, Cirilli M, Lin C, Xu HW, Takuma K, et al. (2004) ABAD directly links Abeta to mitochondrial toxicity in Alzheimer's disease. Science 304: 448-452.
17. Takuma K, Yao J, Huang J, Xu H, Chen X, et al. (2005) ABAD enhances Abeta-induced cell stress via mitochondrial dysfunction. FASEB J 19: 597-598.
18. Yan SD, Stern DM, (2005) Mitochondrial dysfunction and Alzheimer's disease: role of amyloid-beta peptide alcohol dehydrogenase (ABAD). Int J Exp Pathol 86: 161-171.
19. Yao J, Irwin RW, Zhao L, Nilsen J, Hamilton RT, et al. (2009) Mitochondrial bioenergetic deficit precedes Alzheimer's pathology in female mouse model of Alzheimer's disease. Proc Natl Acad Sci U S A 106: 14670-14675.
20. Oddo S, Caccamo A, Kitazawa M, Tseng BP, LaFerla FM, (2003) Amyloid deposition precedes tangle formation in a triple transgenic model of Alzheimer's disease. Neurobiol Aging 24: 1063-1070.
21. Lamba V, Yasuda K, Lamba JK, Assem M, Davila J, et al. (2004) PXR (NR1I2): splice variants in human tissues, including brain, and identification of neurosteroids and nicotine as PXR activators. Toxicol Appl Pharmacol 199: 251-265.
22. Langmade SJ, Gale SE, Frolov A, Mohri I, Suzuki K, et al. (2006) Pregnane X receptor (PXR) activation: a mechanism for neuroprotection in a mouse model of Niemann-Pick C disease. Proc Natl Acad Sci U S A 103: 13807-13812.
23. Ahmad I, Lope-Piedrafita S, Bi X, Hicks C, Yao Y, et al. (2005) Allopregnanolone treatment, both as a single injection or repetitively, delays demyelination and enhances survival of Niemann-Pick C mice. J Neurosci Res 82: 811-821.
24. Jacobs HI, Visser PJ, Van Boxtel MP, Frisoni GB, Tsolaki M, et al. (2010) The association between white matter hyperintensities and executive decline in mild cognitive impairment is network dependent. Neurobiol Aging. [Aug 23, Epub ahead of print] PMID: 20739101.
25. Kuczynski B, Targan E, Madison C, Weiner M, Zhang Y, et al. (2010) White matter integrity and cortical metabolic associations in aging and dementia. Alzheimers Dement 6: 54-62.
26. Singh C, Liu L, Wang JM, Irwin RW, Yao J, et al. (2011) Allopregnanolone restores hippocampal-dependent learning and memory and enhances neural progenitor survival in aging 3xTgAD and nonTg mice. Neurobiol Aging. [July 29, Epub ahead of print] PMID: 21803451.
27. Lesne S, Koh MT, Kotilinek L, Kayed R, Glabe CG, et al. (2006) A specific amyloid-beta protein assembly in the brain impairs memory. Nature 440: 352-357.
28. Oda T, Wals P, Osterburg HH, Johnson SA, Pasinetti GM, et al. (1995) Clusterin (apoJ) alters the aggregation of amyloid beta-peptide (A beta 1-42) and forms slowly sedimenting A beta complexes that cause oxidative stress. Exp Neurol 136: 22-31.
29. Lambert MP, Barlow AK, Chromy BA, Edwards C, Freed R, et al. (1998) Diffusible, nonfibrillar ligands derived from Abeta1-42 are potent central nervous system neurotoxins. Proc Natl Acad Sci U S A 95: 6448-6453.
30. Klyubin I, Walsh DM, Lemere CA, Cullen WK, Shankar GM, et al. (2005) Amyloid beta protein immunotherapy neutralizes Abeta oligomers that disrupt synaptic plasticity in vivo. Nat Med 11: 556-561.
31. Klein WL, Krafft GA, Finch CE, (2001) Targeting small Abeta oligomers: the solution to an Alzheimer's disease conundrum? Trends Neurosci 24: 219-224.
32. Klein WL, Stine WB Jr, Teplow DB, (2004) Small assemblies of unmodified amyloid beta-protein are the proximate neurotoxin in Alzheimer's disease. Neurobiol Aging 25: 569-580.
33. Brinton RD, (2008) The healthy cell bias of estrogen action: mitochondrial bioenergetics and neurological implications. Trends Neurosci 31: 529-537.
34. Oddo S, Billings L, Kesslak JP, Cribbs DH, LaFerla FM, (2004) Abeta immunotherapy leads to clearance of early, but not late, hyperphosphorylated tau aggregates via the proteasome. Neuron 43: 321-332.
35. Li R, Shen Y, Yang LB, Lue LF, Finch C, et al. (2000) Estrogen enhances uptake of amyloid beta-protein by microglia derived from the human cortex. J Neurochem 75: 1447-1454.
36. Xie Z, Harris-White ME, Wals PA, Frautschy SA, Finch CE, et al. (2005) Apolipoprotein J (clusterin) activates rodent microglia in vivo and in vitro. J Neurochem 93: 1038-1046.
37. Xie Z, Wei M, Morgan TE, Fabrizio P, Han D, et al. (2002) Peroxynitrite mediates neurotoxicity of amyloid beta-peptide1-42- and lipopolysaccharide-activated microglia. J Neurosci 22: 3484-3492.
38. Kuczynski B, Reed B, Mungas D, Weiner M, Chui HC, et al. (2008) Cognitive and anatomic contributions of metabolic decline in Alzheimer disease and cerebrovascular disease. Archives of Neurology 65: 650-655.
39. Repa JJ, Li H, Frank-Cannon TC, Valasek MA, Turley SD, et al. (2007) Liver X receptor activation enhances cholesterol loss from the brain, decreases neuroinflammation, and increases survival of the NPC1 mouse. J Neurosci 27: 14470-14480.
40. Leduc V, Jasmin-Belanger S, Poirier J, (2010) APOE and cholesterol homeostasis in Alzheimer's disease. Trends Mol Med.
41. Whitney KD, Watson MA, Collins JL, Benson WG, Stone TM, et al. (2002) Regulation of cholesterol homeostasis by the liver X receptors in the central nervous system. Mol Endocrinol 16: 1378-1385.
42. Xiong H, Callaghan D, Jones A, Walker DG, Lue LF, 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.
43. Schultz JR, Tu H, Luk A, Repa JJ, Medina JC, et al. (2000) Role of LXRs in control of lipogenesis. Genes Dev 14: 2831-2838.
44. Donkin JJ, Stukas S, Hirsch-Reinshagen V, Namjoshi D, Wilkinson A, et al. (2010) ATP-binding cassette transporter A1 mediates the beneficial effects of the liver-X-receptor agonist GW3965 on object recognition memory and amyloid burden in APP/PS1 mice. J Biol Chem.
45. Jiang Q, Lee CY, Mandrekar S, Wilkinson B, Cramer P, et al. (2008) ApoE promotes the proteolytic degradation of Abeta. Neuron 58: 681-693.
46. Sun Y, Yao J, Kim TW, Tall AR, (2003) Expression of liver X receptor target genes decreases cellular amyloid beta peptide secretion. J Biol Chem 278: 27688-27694.
47. Riddell DR, Zhou H, Comery TA, Kouranova E, Lo CF, et al. (2007) The LXR agonist TO901317 selectively lowers hippocampal Abeta42 and improves memory in the Tg2576 mouse model of Alzheimer's disease. Mol Cell Neurosci 34: 621-628.
48. Shenoy SD, Spencer TA, Mercer-Haines NA, Alipour M, Gargano MD, et al. (2004) CYP3A induction by liver x receptor ligands in primary cultured rat and mouse hepatocytes is mediated by the pregnane X receptor. Drug Metab Dispos 32: 66-71.
49. Sonoda J, Xie W, Rosenfeld JM, Barwick JL, Guzelian PS, et al. (2002) Regulation of a xenobiotic sulfonation cascade by nuclear pregnane X receptor (PXR). Proc Natl Acad Sci U S A 99: 13801-13806.
50. Davidson CD, Ali NF, Micsenyi MC, Stephney G, Renault S, et al. (2009) Chronic cyclodextrin treatment of murine Niemann-Pick C disease ameliorates neuronal cholesterol and glycosphingolipid storage and disease progression. PLoS One 4: e6951.
51. Rosenbaum AI, Zhang G, Warren JD, Maxfield FR, (2010) Endocytosis of beta-cyclodextrins is responsible for cholesterol reduction in Niemann-Pick type C mutant cells. Proc Natl Acad Sci U S A 107: 5477-5482.
52. Griffin LD, Gong W, Verot L, Mellon SH, (2004) Niemann-Pick type C disease involves disrupted neurosteroidogenesis and responds to allopregnanolone. Nat Med 10: 704-711.
53. Mellon S, Gong W, Griffin LD, (2004) Niemann pick type C disease as a model for defects in neurosteroidogenesis. Endocr Res 30: 727-735.
54. Billings LM, Oddo S, Green KN, McGaugh JL, LaFerla FM, (2005) Intraneuronal Abeta causes the onset of early Alzheimer's disease-related cognitive deficits in transgenic mice. Neuron 45: 675-688.
55. Henry S, Bigler S, Wang J, (2009) High throughput analysis of neural progenitor cell proliferation in adult rodent hippocampus. Biosci Trends 3: 233-238.
56. Bilsland JG, Haldon C, Goddard J, Oliver K, Murray F, et al. (2006) A rapid method for the quantification of mouse hippocampal neurogenesis in vivo by flow cytometry. Validation with conventional and enhanced immunohistochemical methods. J Neurosci Methods 157: 54-63.
57. Mika J, Osikowicz M, Rojewska E, Korostynski M, Wawrzczak-Bargiela A, et al. (2009) Differential activation of spinal microglial and astroglial cells in a mouse model of peripheral neuropathic pain. Eur J Pharmacol 623: 65-72.
58. Ahmed Z, Shaw G, Sharma VP, Yang C, McGowan E, et al. (2007) Actin-binding proteins coronin-1a and IBA-1 are effective microglial markers for immunohistochemistry. J Histochem Cytochem 55: 687-700.