Neuropathologic and biochemical changes during disease progression in liver x receptor β-/-mice, a model of adult neuron disease

Journal of Neuropathology and Experimental Neurology

Volumn 69, Issue 6, 2010, Pages 593-605

  Bigini, Paolo ^a   Steffensen, Knut R ^b   Ferrario, Anna ^a   Diomede, Luisa ^a   Ferrara, Giovanni ^a   Barbera, Sara ^a   Salzano, Sonia ^c   Fumagalli, Elena ^a   Ghezzi, Pietro ^c   Mennini, Tiziana ^a   Gustafsson, Jan Åke ^b,d  

^a MARIO NEGRI INSTITUTE FOR PHARMACOLOGICAL RESEARCH   (Italy)

^b KAROLINSKA INSTITUTE   (Sweden)

^c BRIGHTON AND SUSSEX MEDICAL SCHOOL   (United Kingdom)

^d University of Houston   (United States)

Author keywords

Amyotrophic lateral sclerosis; Cholesterol; CNS inflammation; Glial cells; Liver X receptors; Motor neurons; Spinal neurons.

Indexed keywords

CHOLESTEROL; LIVER X RECEPTOR BETA;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHOLESTEROL BLOOD LEVEL; CHOLESTEROL METABOLISM; CONTROLLED STUDY; DISEASE COURSE; GLIOSIS; INFLAMMATION; LIFESPAN; MOTONEURON; MOUSE; NEUROMUSCULAR SYNAPSE; NEUROPATHOLOGY; NONHUMAN; PARALYSIS; PRIORITY JOURNAL; SPINAL CORD NERVE CELL;

AGE FACTORS; AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; BODY WEIGHT; CELL COUNT; CELL DEATH; CHOLESTEROL; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; ENZYME-LINKED IMMUNOSORBENT ASSAY; GLIOSIS; IMMUNOHISTOCHEMISTRY; INFLAMMATION; MICE; MICE, KNOCKOUT; MOTOR NEURONS; NERVE DEGENERATION; NEUROMUSCULAR JUNCTION; ORPHAN NUCLEAR RECEPTORS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; ROTAROD PERFORMANCE TEST;

EID: 77953126604     PISSN: 00223069     EISSN: None     Source Type: Journal    
DOI: 10.1097/NEN.0b013e3181df20e1     Document Type: Article

References (42)

1. Wijesekera LC, Leigh PN. Amyotrophic lateral sclerosis. Orphanet J Rare Dis 2009;4:3
2. Beghi E, Mennini T, Bendotti C, et al. The heterogeneity of amyotrophic lateral sclerosis: A possible explanation of treatment failure. Curr Med Chem 2007;14:3185-200
3. Strong MJ, Hudson AJ, Alvord WG. Familial amyotrophic lateral sclerosis, 1850-1989: A statistical analysis of the world literature. Can J Neurol Sci 1991;18:45-58
4. Beckman JS, Carson M, Smith CD, et al. ALS, SOD and peroxynitrite. Nature 1993;364:584
5. Duchen LW, Strich SJ. An hereditary motor neurone disease with progressive denervation of muscle in the mouse: The mutant Bwobbler.[J Neurol Neurosurg Psychiatry 1968;31:535-42
6. Gurney ME, Pu H, Chiu AY, et al. Motor neuron degeneration in mice that express a human Cu,Zn superoxide dismutase mutation. Science 1994;264:1772-75
7. Schmitt-John T, Drepper C, Mussmann A, et al. Mutation of Vps54 causes motor neuron disease and defective spermiogenesis in the wobbler mouse. Nat Genet 2005;37:1213-15
8. Andersson S, Gustafsson N, Warner M, et al. Inactivation of liver X receptor beta leads to adult-onset motor neuron degeneration in male mice. Proc Natl Acad Sci USA 2005;102:3857-62
9. Hindinger C, Hinton DR, Kirwin SJ, et al. Liver X receptor activation decreases the severity of experimental autoimmune encephalomyelitis. J Neurosci Res 2006;84:1225-34
10. Zelcer N, Tontonoz P. Liver X receptors as integrators of metabolic and inflammatory signaling. J Clin Invest 2006;116:607-14
11. Zhang-Gandhi CX, Drew PD. Liver X receptor and retinoid X receptor agonists inhibit inflammatory responses of microglia and astrocytes. J Neuroimmunol 2007;183:50-59
12. Alberti S, Schuster G, Parini P, et al. Hepatic cholesterol metabolism and resistance to dietary cholesterol in LXRbeta-deficient mice. J Clin Invest 2001;107:565-73
13. Fumagalli E, Bigini P, Barbera S, et al. Riluzole, unlike the AMPA antagonist RPR119990, reduces motor impairment and partially prevents motoneuron death in the wobbler mouse, a model of neurodegenerative disease. Exp Neurol 2006;198:114-28
14. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976;72:248-54
15. Bigini P, Mennini T. Immunohistochemical localization of TNF# and its receptors in the rodent central nervous system. Methods Mol Med 2004; 98:73-80
16. Ravizza T, Noe F, Zardoni D, et al. Interleukin converting enzyme inhibition impairs kindling epileptogenesis in rats by blocking astrocytic IL-1beta production. Neurobiol Dis 2008;31:327-33
17. Houser CR, Barber RP, Crawford GD, et al. Species-specific second antibodies reduce spurious staining in immunocytochemistry. J Histo-chem Cytochem 1984;32:395-402
18. Burgers HF, Schelshorn DW, Wagner W, et al. Acute anoxia stimulates proliferation in adult neural stem cells from the rat brain. Exp Brain Res 2008;188:33-43
19. -/- mouse brain. Am J Pathol 2007;171:962-75
20. Hensley K, Fedynyshyn J, Ferrell S, et al. Message and protein-level elevation of tumor necrosis factor alpha (TNF#) and TNF alphaYmodulating cytokines in spinal cords of the G93A-SOD1 mouse model for amyotrophic lateral sclerosis. Neurobiol Dis 2003;14: 74-80
21. Boillee S, Viala L, Peschanski M, et al. Differential microglial response to progressive neurodegeneration in the murine mutant Wobbler. Glia 2001;33:277-87
22. Alexianu ME, Kozovska M, Appel SH. Immune reactivity in a mouse model of familial ALS correlates with disease progression. Neurology 2001;57:1282-89
23. Veglianese P, Lo Coco D, Bao Cutrona M, et al. Activation of the p38MAPK cascade is associated with upregulation of TNF# receptors in the spinal motor neurons of mouse models of familial ALS. Mol Cell Neurosci 2006;31:218-31
24. Kim HJ, Fan X, Gabbi C, et al. Liver X receptor beta (LXRbeta): A link between beta-sitosterol and amyotrophic lateral sclerosis-Parkinson's dementia. Proc Natl Acad Sci USA 2008;105:2094-99
25. Kiernan JA, Hudson AJ. Changes in sizes of cortical and lower motor neurons in amyotrophic lateral sclerosis. Brain 1991;114: 843-53
26. Jaarsma D, Haasdijk ED, Grashorn JA, et al. Human Cu/Zn superoxide dismutase (SOD1) overexpression in mice causes mito-chondrial vacuolization, axonal degeneration, and premature moto-neuron death and accelerates motoneuron disease in mice expressing a familial amyotrophic lateral sclerosis mutant SOD1. Neurobiol Dis 2000;7:623-43
27. Mitsumoto H, McQuarrie IG, Kurahashi K, et al. Histometric characteristics and regenerative capacity in wobbler mouse motor neuron disease. Brain 1990;113:497-507 (Pubitemid 20136156)
28. Martin LJ, Liu Z, Chen K, et al. Motor neuron degeneration in amyotrophic lateral sclerosis mutant superoxide dismutase-1 transgenic mice: Mechanisms of mitochondriopathy and cell death. J Comp Neurol 2007;500:20-46
29. Morrison BM, Gordon JW, Ripps ME, et al. Quantitative immunocy-tochemical analysis of the spinal cord in G86R superoxide dismutase transgenic mice: Neurochemical correlates of selective vulnerability. J Comp Neurol 1996;373:619-31
30. Hensley K, Floyd RA, Gordon B, et al. Temporal patterns of cytokine and apoptosis-related gene expression in spinal cords of the G93A-SOD1 mouse model of amyotrophic lateral sclerosis. J Neuro-chem 2002;82:365-74
31. Fowler AJ, Sheu MY, Schmuth M, et al. Liver X receptor activators display anti-inflammatory activity in irritant and allergic contact dermatitis models: Liver-X-receptorYspecific inhibition of inflammation and primary cytokine production. J Invest Dermatol 2003;120:246-55
32. Fontaine C, Rigamonti E, Nohara A, et al. Liver X receptor activation potentiates the lipopolysaccharide response in human macrophages. Circ Res 2007;101:40-49
33. Dupuis L, Corcia P, Fergani A, et al. Dyslipidemia is a protective factor in amyotrophic lateral sclerosis. Neurology 2008;70:1004-9
34. Ghisletti S, Huang W, Ogawa S, et al. Parallel SUMOylation-dependent pathways mediate gene-and signal-specific transrepression by LXRs and PPARgamma. Mol Cell 2007;25:57-70
35. Cutler RG, Pedersen WA, Camandola S, et al. Evidence that accumulation of ceramides and cholesterol esters mediates oxidative stressYinduced death of motor neurons in amyotrophic lateral sclerosis. Ann Neurol 2002;52:448-57
36. Quan G, Xie C, Dietschy JM, et al. Ontogenesis and regulation of cholesterol metabolism in the central nervous system of the mouse. Brain Res Dev Brain Res 2003;146:87-98
37. Bjorkhem I, Cedazo-Minguez A, et al. Oxysterols and neurodegenerative diseases. Mol Aspects Med 2009;30:171-79
38. Fu X, Menke JG, Chen Y, et al. 27-hydroxycholesterol is an endogenous ligand for liver X receptor in cholesterol-loaded cells. J Biol Chem 2001; 276:38378-87
39. Kim GH, Park K, Yeom SY, et al. Characterization of ASC-2 as an anti-atherogenic transcriptional coactivator of liver X receptors in macrophages. Mol Endocrinol 2009;23:966-74
40. Liang Y, Lin S, Beyer TP, et al. A liver X receptor and retinoid X receptor heterodimer mediates apolipoprotein E expression, secretion and cholesterol homeostasis in astrocytes. J Neurochem 2004;88: 623-34
41. Pfrieger FW. Cholesterol homeostasis and function in neurons of the central nervous system. Cell Mol Life Sci 2003;60:1158-71
42. Casserly I, Topol E. Convergence of atherosclerosis and Alzheimer's disease: Inflammation, cholesterol, and misfolded proteins. Lancet 2004; 363:1139-46