Treatment of stroke with a synthetic liver X receptor agonist, TO901317, promotes synaptic plasticity and axonal regeneration in mice

Journal of Cerebral Blood Flow and Metabolism

Volumn 30, Issue 1, 2010, Pages 102-109

  Chen, Jieli ^a   Zacharek, Alex ^a   Cui, Xu ^a   Shehadah, Amjad ^a   Jiang, Hao ^a   Roberts, Cynthia ^a   Lu, Mei ^a   Chopp, Michael ^a,b  

^a HENRY FORD HOSPITAL   (United States)

^b OAKLAND UNIVERSITY   (United States)

Author keywords

Axonal regeneration; LXR agonist; Nogo receptor; Phosphatidylinositol 3 kinase; Stroke

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; AMYLOID BETA PROTEIN; AMYLOID BETAA4 PROTEIN; N (2,2,2 TRIFLUOROETHYL) N [4 (2,2,2 TRIFLUORO 1 HYDROXY 1 TRIFLUOROMETHYLETHYL)PHENYL]BENZENESULFONAMIDE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B BETA; PROTEIN NOGO; SYNAPTOPHYSIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; MALE; MIDDLE CEREBRAL ARTERY OCCLUSION; MOUSE; NERVE CELL CULTURE; NERVE CELL PLASTICITY; NERVE FIBER GROWTH; NERVE FIBER REGENERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; STROKE;

1-PHOSPHATIDYLINOSITOL 3-KINASE; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; AXONS; BLOTTING, WESTERN; CELLS, CULTURED; DENDRITES; HYDROCARBONS, FLUORINATED; IMMUNOHISTOCHEMISTRY; LIGATION; MALE; MICE; MICE, INBRED C57BL; MIDDLE CEREBRAL ARTERY; MYELIN PROTEINS; NERVE REGENERATION; NEURONAL PLASTICITY; ONCOGENE PROTEIN V-AKT; ORPHAN NUCLEAR RECEPTORS; RECEPTORS, CELL SURFACE; SILVER STAINING; STROKE; SULFONAMIDES; SYNAPTOPHYSIN;

EID: 73949096756     PISSN: 0271678X     EISSN: None     Source Type: Journal    
DOI: 10.1038/jcbfm.2009.187     Document Type: Article

References (45)

1. Andersson S, Gustafsson N, Warner M, Gustafsson JA (2005) Inactivation of liver X receptor beta leads to adult-onset motor neuron degeneration in male mice. Proc Natl Acad Sci USA 102:3857-3862
2. Bonnet D, Garcia M, Vecino E, Lorentz JG, Sahel J, Hicks D (2004) Brain-derived neurotrophic factor signalling in adult pig retinal ganglion cell neurite regeneration in vitro. Brain Res 1007:142-151
3. Calza L, Giardino L, Giuliani A, Aloe L, Levi-Montalcini R (2001) Nerve growth factor control of neuronal expression of angiogenetic and vasoactive factors. Proc Natl Acad Sci USA 98:4160-4165
4. Chen J, Cui X, Zacharek A, Chopp M (2008) Increasing Ang1/Tie2 expression by simvastatin treatment induces vascular stabilization and neuroblast migration after stroke. J Cell Mol Med 13:1348-1357
5. Chen J, Cui X, Zacharek A, Jiang H, Roberts C, Zhang C, Lu M, Kapke A, Feldkamp CS, Chopp M (2007) Niaspan increases angiogenesis and improves functional recovery after stroke. Ann Neurol 62:49-58 (Pubitemid 47235280)
6. Chen J, Cui X, Zacharek A, Roberts C, Chopp M (2009) eNOS mediates TO90317 treatment-induced angiogen-esis and functional outcome after stroke in mice. Stroke 40:2532-2538
7. Chen J, Zhang ZG, Li Y, Wang Y, Wang L, Jiang H, Zhang C, Lu M, Katakowski M, Feldkamp CS, Chopp M (2003a) Statins induce angiogenesis, neurogenesis, and synap-togenesis after stroke. Ann Neurol 53:743-751
8. Chen J, Zhang ZG, Li Y, Wang L, Xu YX, Gautam SC, Lu M, Zhu Z, Chopp M (2003b) Intravenous administration of human bone marrow stromal cells induces angiogenesis in the ischemic boundary zone after stroke in rats. Circ Res 92:692-699 (Pubitemid 36417705)
9. Ditlevsen DK, Kohler LB, Pedersen MV, Risell M, Kolkova K, Meyer M, Berezin V, Bock E (2003) The role of phosphatidylinositol 3-kinase in neural cell adhesion molecule-mediated neuronal differentiation and survival. J Neurochem 84:546-556
10. Domeniconi M, Cao Z, Spencer T, Sivasankaran R, Wang K, Nikulina E, Kimura N, Cai H, Deng K, Gao Y, He Z, Filbin M (2002) Myelin-associated glycoprotein interacts with the Nogo66 receptor to inhibit neurite outgrowth. Neuron 35:283-290 (Pubitemid 34876731)
11. Fan X, Kim HJ, Bouton D, Warner M, Gustafsson JA (2008) Expression of liver X receptor beta is essential for formation of superficial cortical layers and migration of later-born neurons. Proc Natl Acad Sci USA 105:13445-13450
12. Galtrey CM, Fawcett JW (2007) The role of chondroitin sulfate proteoglycans in regeneration and plasticity in the central nervous system. Brain Res Rev 54:1-18
13. Hou ST, Jiang SX, Smith RA (2008) Permissive and repulsive cues and signalling pathways of axonal outgrowth and regeneration. Int Rev Cell Mol Biol 267:125-181
14. Karnezis T, Mandemakers W, McQualter JL, Zheng B, Ho PP, Jordan KA, Murray BM, Barres B, Tessier-Lavigne M, Bernard CC (2004) The neurite outgrowth inhibitor Nogo A is involved in autoimmune-mediated demyeli-nation. Nat Neurosci 7:736-744
15. Kim HJ, Fan X, Gabbi C, Yakimchuk K, Parini P, Warner M, Gustafsson JA (2008) Liver X receptor beta (LXRbeta): a link between beta-sitosterol and amyotrophic lateral sclerosis-Parkinson's dementia. Proc Natl Acad Sci USA 105:2094-2099
16. Laurino L, Wang XX, de la Houssaye BA, Sosa L, Dupraz S, Caceres A, Pfenninger KH, Quiroga S (2005) PI3K activation by IGF-1 is essential for the regulation of membrane expansion at the nerve growth cone. J Cell Sci 118:3653-3662
17. Leclercq PD, McKenzie JE, Graham DI, Gentleman SM (2001) Axonal injury is accentuated in the caudal corpus callosum of head-injured patients. J Neurotrau-ma 18:1-9
18. Li S, Kim JE, Budel S, Hampton TG, Strittmatter SM (2005) Transgenic inhibition of Nogo-66 receptor function allows axonal sprouting and improved locomotion after spinal injury. Mol Cell Neurosci 29:26-39
19. Li Y, Jiang N, Powers C, Chopp M (1998) Neuronal damage and plasticity identified by microtubule-associated protein 2, growth-associated protein 43, and cyclin D1 immunoreactivity after focal cerebral ischemia in rats. Stroke 29:1972-80; discussion 1980-1981
20. Liu Z, Li Y, Zhang X, Savant-Bhonsale S, Chopp M (2008) Contralesional axonal remodeling of the corticospinal system in adult rats after stroke and bone marrow stromal cell treatment. Stroke 39:2571-2577
21. Mao Y, Yang GY, Zhou LF, Stern JD, Betz AL (1999) Focal cerebral ischemia in the mouse: description of a model and effects of permanent and temporary occlusion. Brain Res Mol Brain Res 63:366-370
22. McKerracher L, Winton MJ (2002) Nogo on the go. Neuron 36:345-348
23. McPhie DL, Golde T, Eckman CB, Yager D, Brant JB, Neve RL (2001) Beta-secretase cleavage of the amyloid precursor protein mediates neuronal apoptosis caused by familial Alzheimer's disease mutations. Brain Res Mol Brain Res 97:103-113
24. Morales JR, Ballesteros I, Deniz JM, Hurtado O, Vivancos J, Nombela F, Lizasoain I, Castrillo A, Moro MA (2008) Activation of liver X receptors promotes neuroprotec-tion and reduces brain inflammation in experimental stroke. Circulation 118:1450-1459
25. Namikawa K, Honma M, Abe K, Takeda M, Mansur K, Obata T, Miwa A, Okado H, Kiyama H (2000) Akt/ protein kinase B prevents injury-induced motoneuron death and accelerates axonal regeneration. J Neurosci 20:2875-2886
26. Nourhaghighi N, Teichert-Kuliszewska K, Davis J, Stewart DJ, Nag S (2003) Altered expression of angiopoietins during blood-brain barrier breakdown and angiogenesis. Lab Invest 83:1211-1222
27. Pan J, Kao YL, Joshi S, Jeetendran S, Dipette D, Singh US (2005) Activation of Rac1 by phosphatidylinositol 3-kinase in vivo: role in activation of mitogen-activated protein kinase (MAPK) pathways and retinoic acid-induced neuronal differentiation of SH-SY5Y cells. J Neurochem 93:571-583
28. Papadopoulos CM, Tsai SY, Cheatwood JL, Bollnow MR, Kolb BE, Schwab ME, Kartje GL (2006) Dendritic plasticity in the adult rat following middle cerebral artery occlusion and Nogo-a neutralization. Cereb Cortex 16:529-536
29. Pluchino S, Quattrini A, Brambilla E, Gritti A, Salani G, Dina G, Galli R, Del Carro U, Amadio S, Bergami A, Furlan R, Comi G, Vescovi AL, Martino G (2003) Injection of adult neurospheres induces recovery in a chronic model of multiple sclerosis. Nature 422: 688-694
30. Ransome MI, Turnley AM (2008) Erythropoietin promotes axonal growth in a model of neuronal polarization. Mol Cell Neurosci 38:537-547
31. Reddy PH (2009) Amyloid beta, mitochondrial structural and functional dynamics in Alzheimer's disease. Exp Neurol 218:286-292
32. Riddell DR, Zhou H, Comery TA, Kouranova E, Lo CF, Warwick HK, Ring RH, Kirksey Y, Aschmies S, Xu J, Kubek K, Hirst WD, Gonzales C, Chen Y, Murphy E, Leonard S, Vasylyev D, Oganesian A, Martone RL, Pangalos MN, Reinhart PH, Jacobsen JS (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
33. Sanchez S, Jimenez C, Carrera AC, Diaz-Nido J, Avila J, Wandosell F (2004) A cAMP-activated pathway, including PKA and PI3K, regulates neuronal differentiation. Neurochem Int 44:231-242
34. Sandhu R, Teichert-Kuliszewska K, Nag S, Proteau G, Robb MJ, Campbell AI, Kuliszewski MA, Kutryk MJ, Stewart DJ (2004) Reciprocal regulation of angiopoietin-1 and angiopoietin-2 following myocardial infarction in the rat. Cardiovasc Res 64:115-124
35. Schmidt A, Vogel R, Holloway MK, Rutledge SJ, Friedman O, Yang Z, Rodan GA, Friedman E (1999) Transcription control and neuronal differentiation by agents that activate the LXR nuclear receptor family. Mol Cell Endocrinol 155:51-60
36. Sherriff FE, Bridges LR, Sivaloganathan S (1994) Early detection of axonal injury after human head trauma using immunocytochemistry for beta-amyloid precursor protein. Acta Neuropathol 87:55-62
37. Sironi L, Mitro N, Cimino M, Gelosa P, Guerrini U, Tremoli E, Saez E (2008) Treatment with LXR agonists after focal cerebral ischemia prevents brain damage. FEBS Lett 582:3396-3400
38. Ujike H, Takaki M, Kodama M, Kuroda S (2002) Gene expression related to synaptogenesis, neuritogenesis, and MAP kinase in behavioral sensitization to psychos-timulants. Ann NYAcad Sci 965:55-67
39. Walmsley AR, Mir AK (2007) Targeting the Nogo-A signalling pathway to promote recovery following acute CNS injury. Curr Pharm Des 13:2470-2484
40. Wang F, Liang Z, Hou Q, Xing S, Ling L, He M, Pei Z, Zeng J (2007) Nogo-A is involved in secondary axonal degeneration of thalamus in hypertensive rats with focal cortical infarction. Neurosci Lett 417:255-260 (Pubitemid 46589790)
41. Wang KC, Koprivica V, Kim JA, Sivasankaran R, Guo Y, Neve RL, He Z (2002a) Oligodendrocyte-myelin glyco-protein is a Nogo receptor ligand that inhibits neurite outgrowth. Nature 417:941-944
42. Wang L, Schuster GU, Hultenby K, Zhang Q, Andersson S, Gustafsson JA (2002b) Liver X receptors in the central nervous system: from lipid homeostasis to neuronal degeneration. Proc Natl Acad Sci USA 99:13878-13883
43. Zacharek A, Chen J, Zhang C, Cui X, Roberts C, Jiang H, Teng H, Chopp M (2006) Nitric oxide regulates Angio-poietin1/Tie2 expression after stroke. Neurosci Lett 404:28-32
44. Zhang S, Zhang Q, Zhang JH, Qin X (2008) Electro-stimulation of cerebellar fastigial nucleus (FNS) improves axonal regeneration. Front Biosci 13:6999-7007
45. Zhou FQ, Snider WD (2006) Intracellular control of developmental and regenerative axon growth. Philos Trans R Soc Lond B Biol Sci 361:1575-1592