Brain endogenous liver X receptor ligands selectively promote midbrain neurogenesis

Nature Chemical Biology

Volumn 9, Issue 2, 2013, Pages 126-133

  Theofilopoulos, Spyridon ^a   Wang, Yuqin ^b   Kitambi, Satish Srinivas ^a   Sacchetti, Paola ^a,g   Sousa, Kyle M ^a,g,h   Bodin, Karl ^a   Kirk, Jayne ^c   Saltó, Carmen ^a   Gustafsson, Magnus ^a   Toledo, Enrique M ^a   Karu, Kersti ^d   Gustafsson, Jan Åke ^e   Steffensen, Knut R ^f   Ernfors, Patrik ^a   Sjövall, Jan ^a   Griffiths, William J ^b   Arenas, Ernest ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b SWANSEA UNIVERSITY   (United Kingdom)

^c Waters UK   (United Kingdom)

^d UNIVERSITY OF LONDON   (United Kingdom)

^e UNIVERSITY OF HOUSTON   (United States)

^f Center for Biosciences   (Sweden)

^g MOUNT HOLYOKE COLLEGE   (United States)

^h CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

25 EPOXYCHOLESTEROL; CHOLIC ACID; LIVER X RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL POPULATION; CELL SURVIVAL; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; EMBRYONIC STEM CELL; IN VIVO STUDY; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; MESENCEPHALON; MOUSE; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; RED NUCLEUS; ZEBRA FISH;

ANIMALS; BRAIN MAPPING; CELL DIFFERENTIATION; CELL NUCLEUS; CHOLESTEROL; CHOLIC ACID; DOPAMINE; DOSE-RESPONSE RELATIONSHIP, DRUG; EMBRYONIC STEM CELLS; LIGANDS; MESENCEPHALON; MICE; MODELS, BIOLOGICAL; NEUROGENESIS; ORPHAN NUCLEAR RECEPTORS; TIME FACTORS; TRANSFECTION; ZEBRAFISH;

DANIO RERIO;

EID: 84872677234     PISSN: 15524450     EISSN: 15524469     Source Type: Journal    
DOI: 10.1038/nchembio.1156     Document Type: Article

References (52)

1. Chawla, A., Repa, J.J., Evans, R.M. & Mangelsdorf, D.J. Nuclear receptors and lipid physiology: opening the X-files. Science 294, 1866-1870 (2001).
2. Bensinger, S.J. & Tontonoz, P. Integration of metabolism and inflammation by lipid-activated nuclear receptors. Nature 454, 470-477 (2008).
3. Alberti, S., Steffensen, K.R. & Gustafsson, J.A. Structural characterisation of the mouse nuclear oxysterol receptor genes LXRaand LXRβ. Gene 243, 93-103 (2000).
4. Edwards, P.A., Kennedy, M.A. & Mak, P.A. LXRs: oxysterol-activated nuclear receptors that regulate genes controlling lipid homeostasis. Vascul. Pharmacol. 38, 249-256 (2002).
5. Zelcer, N. & Tontonoz, P. Liver X receptors as integrators of metabolic and inflammatory signaling. J. Clin. Invest. 116, 607-614 (2006).
6. Hu, X., Li, S., Wu, J., Xia, C. & Lala, D.S. Liver X receptors interact with corepressors to regulate gene expression. Mol. Endocrinol. 17, 1019-1026 (2003).
7. Janowski, B.A., Willy, P.J., Devi, T.R., Falck, J.R. & Mangelsdorf, D.J. An oxysterol signalling pathway mediated by the nuclear receptor LXRα. Nature 383, 728-731 (1996).
8. Janowski, B.A. et al. Structural requirements of ligands for the oxysterol liver X receptors LXRaand LXRβ. Proc. Natl. Acad. Sci. USA 96, 266-271 (1999).
9. Viennois, E. et al. Targeting liver X receptors in human health: deadlock or promising trail? Expert Opin. Ther. Targets 15, 219-232 (2011).
10. Björkhem, I. Are side-chain oxidized oxysterols regulators also in vivo? J. Lipid Res. 50, S213-S218 (2009).
11. Lehmann, J.M. et al. Activation of the nuclear receptor LXR by oxysterols defines a new hormone response pathway. J. Biol. Chem. 272, 3137-3140 (1997).
12. Fu, X. et al. 27-hydroxycholesterol is an endogenous ligand for liver X receptor in cholesterol-loaded cells. J. Biol. Chem. 276, 38378-38387 (2001).
13. Zhao, C. & Dahlman-Wright, K. Liver X receptor in cholesterol metabolism. J. Endocrinol. 204, 233-240 (2010).
14. Björkhem, I. & Diczfalusy, U. Oxysterols: friends, foes, or just fellow passengers? Arterioscler. Thromb. Vasc. Biol. 22, 734-742 (2002).
15. Schroepfer, G.J. Oxysterols: modulators of cholesterol metabolism and other processes. Physiol. Rev. 80, 361-554 (2000).
16. Laffitte, B.A. et al. LXRs control lipid-inducible expression of the apolipoprotein E gene in macrophages and adipocytes. Proc. Natl. Acad. Sci. USA 98, 507-512 (2001).
17. Venkateswaran, A. et al. Control of cellular cholesterol efflux by the nuclear oxysterol receptor LXRα. Proc. Natl. Acad. Sci. USA 97, 12097-12102 (2000).
18. Joseph, S.B., Castrillo, A., Laffitte, B.A., Mangelsdorf, D.J. & Tontonoz, P. Reciprocal regulation of inflammation and lipid metabolism by liver X receptors. Nat. Med. 9, 213-219 (2003).
19. Hannedouche, S. et al. Oxysterols direct immune cell migration via EBI2. Nature 475, 524-527 (2011).
20. Valledor, A.F. et al. Activation of liver X receptors and retinoid X receptors prevents bacterial-induced macrophage apoptosis. Proc. Natl. Acad. Sci. USA 101, 17813-17818 (2004).
21. Wang, L. et al. Liver X receptors in the central nervous system: from lipid homeostasis to neuronal degeneration. Proc. Natl. Acad. Sci. USA 99, 13878-13883 (2002).
22. Sacchetti, P. et al. Liver X receptors and oxysterols promote ventral midbrain neurogenesis in vivo and in human embryonic stem cells. Cell Stem Cell 5, 409-419 (2009).
23. Andersson, S., Gustafsson, N., Warner, M. & Gustafsson, J.A. Inactivation of liver X receptor β leads to adult-onset motor neuron degeneration in male mice. Proc. Natl. Acad. Sci. USA 102, 3857-3862 (2005).
24. Zelcer, N. et al. Attenuation of neuroinflammation and Alzheimer's disease pathology by liver x receptors. Proc. Natl. Acad. Sci. USA 104, 10601-10606 (2007).
25. Fitz, N.F. et al. Liver X receptor agonist treatment ameliorates amyloid pathology and memory deficits caused by high-fat diet in APP23 mice. J. Neurosci. 30, 6862-6872 (2010).
26. Kele, J. et al. Neurogenin 2 is required for the development of ventral midbrain dopaminergic neurons. Development 133, 495-505 (2006).
27. Wang, Y. et al. Targeted lipidomic analysis of oxysterols in the embryonic central nervous system. Mol. Biosyst. 5, 529-541 (2009).
28. Mano, N. et al. Presence of protein-bound unconjugated bile acids in the cytoplasmic fraction of rat brain. J. Lipid Res. 45, 295-300 (2004).
29. Gan, X. et al. Dual mechanisms of ABCA1 regulation by geranylgeranyl pyrophosphate. J. Biol. Chem. 276, 48702-48708 (2001).
30. Russek-Blum, N. et al. Dopaminergic neuronal cluster size is determined during early forebrain patterning. Development 135, 3401-3413 (2008).
31. Chen, Y.C., Priyadarshini, M. & Panula, P. Complementary developmental expression of the two tyrosine hydroxylase transcripts in zebrafish. Histochem. Cell Biol. 132, 375-381 (2009).
32. Zetterström, R.H. et al. Dopamine neuron agenesis in Nurr1-deficient mice. Science 276, 248-250 (1997).
33. Bello, E.P. et al. Cocaine supersensitivity and enhanced motivation for reward in mice lacking dopamine D2 autoreceptors. Nat. Neurosci. 14, 1033-1038 (2011).
34. Makishima, M. et al. Identification of a nuclear receptor for bile acids. Science 284, 1362-1365 (1999).
35. Parks, D.J. et al. Bile acids: natural ligands for an orphan nuclear receptor. Science 284, 1365-1368 (1999).
36. Wang, H., Chen, J., Hollister, K., Sowers, L.C. & Forman, B.M. Endogenous bile acids are ligands for the nuclear receptor FXR/BAR. Mol. Cell 3, 543-553 (1999).
37. Song, C., Hiipakka, R.A. & Liao, S. Selective activation of liver X receptor α by 6α-hydroxy bile acids and analogs. Steroids 65, 423-427 (2000).
38. Song, C. & Liao, S. Cholestenoic acid is a naturally occurring ligand for liver X receptor α. Endocrinology 141, 4180-4184 (2000).
39. Goodwin, B.J., Zuercher, W.J. & Collins, J.L. Recent advances in liver X receptor biology and chemistry. Curr. Top. Med. Chem. 8, 781-791 (2008).
40. Gray, P.A. et al. Mouse brain organization revealed through direct genome-scale TF expression analysis. Science 306, 2255-2257 (2004).
41. Makishima, M. et al. Vitamin D receptor as an intestinal bile acid sensor. Science 296, 1313-1316 (2002).
42. Tint, G.S., Yu, H., Shang, Q., Xu, G. & Patel, S.B. The use of the Dhcr7 knockout mouse to accurately determine the origin of fetal sterols. J. Lipid Res. 47, 1535-1541 (2006).
43. Zhang, C.L., Zou, Y., He, W., Gage, F.H. & Evans, R.M. A role for adult TLX-positive neural stem cells in learning and behaviour. Nature 451, 1004-1007 (2008).
44. Lee, S., Lee, B., Lee, J.W. & Lee, S.K. Retinoid signaling and neurogenin2 function are coupled for the specification of spinal motor neurons through a chromatin modifier CBP. Neuron 62, 641-654 (2009).
45. Környei, Z. et al. Astroglia-derived retinoic acid is a key factor in glia-induced neurogenesis. FASEB J. 21, 2496-2509 (2007).
46. Berrodin, T.J. et al. Identification of 5,6-epoxycholesterol as a novel modulator of liver x receptor activity. Mol. Pharmacol. 78, 1046-1058 (2010).
47. Venteclef, N. et al. GPS2-dependent corepressor/SUMO pathways govern anti-inflammatory actions of LRH-1 and LXRβ in the hepatic acute phase response. Genes Dev. 24, 381-395 (2010).
48. Huang, P., Chandra, V. & Rastinejad, F. Structural overview of the nuclear receptor superfamily: insights into physiology and therapeutics. Annu. Rev. Physiol. 72, 247-272 (2010).
49. Clare, K., Hardwick, S.J., Carpenter, K.L., Weeratunge, N. & Mitchinson, M.J. Toxicity of oxysterols to human monocyte-macrophages. Atherosclerosis 118, 67-75 (1995).
50. Jakobsson, T. et al. GPS2 is required for cholesterol efflux by triggering histone demethylation, LXR recruitment, and coregulator assembly at the ABCG1 locus. Mol. Cell 34, 510-518 (2009).
51. Boergesen, M. et al. Genome-wide profiling of liver X receptor, retinoid X receptor, and peroxisome proliferator-activated receptor in mouse liver reveals extensive sharing of binding sites. Mol. Cell. Biol. 32, 852-867 (2012).
52. Archer, A. et al. The Liver X-Receptor (Lxr) governs lipid homeostasis in zebrafish during development. Open J. Endocrine Metab. Diseases. 2, 74-81 (2012).