Fingolimod increases brain-derived neurotrophic factor levels and ameliorates amyloid β-induced memory impairment

Behavioural Brain Research

Volumn 268, Issue , 2014, Pages 88-93

  Fukumoto, Kazuya ^a   Mizoguchi, Hiroyuki ^a   Takeuchi, Hideyuki ^a   Horiuchi, Hiroshi ^a   Kawanokuchi, Jun ^a   Jin, Shijie ^a   Mizuno, Tetsuya ^a   Suzumura, Akio ^a  

^a NAGOYA UNIVERSITY   (Japan)

Author keywords

Alzheimer's disease; Amyloid ; Brain derived neurotrophic factor; Fingolimod

Indexed keywords

AMYLOID BETA PROTEIN; BRAIN DERIVED NEUROTROPHIC FACTOR; FINGOLIMOD; AMYLOID BETA-PROTEIN (1-42); NEUROPROTECTIVE AGENT; PEPTIDE FRAGMENT; PROPANEDIOL DERIVATIVE; SPHINGOSINE;

ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CONTROLLED STUDY; DRUG EFFICACY; HIPPOCAMPUS; LEARNING DISORDER; MALE; MEMORY CONSOLIDATION; MEMORY DISORDER; MOUSE; NEUROANATOMY; NEUROPROTECTION; NONHUMAN; NOVEL OBJECT RECOGNITION TEST; OUTCOME ASSESSMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; STATE DEPENDENT LEARNING; UPREGULATION; ANALOGS AND DERIVATIVES; ANIMAL; BRAIN; C57BL MOUSE; DRUG EFFECTS; EXPLORATORY BEHAVIOR; LEARNING; MEMORY DISORDERS; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY; RECOGNITION; TOXICITY;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; ASSOCIATION LEARNING; BRAIN; BRAIN-DERIVED NEUROTROPHIC FACTOR; CEREBRAL CORTEX; EXPLORATORY BEHAVIOR; HIPPOCAMPUS; MALE; MEMORY DISORDERS; MICE, INBRED C57BL; NEUROPROTECTIVE AGENTS; PEPTIDE FRAGMENTS; PROPYLENE GLYCOLS; RECOGNITION (PSYCHOLOGY); SPHINGOSINE; UP-REGULATION;

EID: 84898987283     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2014.03.046     Document Type: Article

References (50)

1. Selkoe D.J., Schenk D. Alzheimer's disease: molecular understanding predicts amyloid-based therapeutics. Annu Rev Pharmacol Toxicol 2003, 43:545-584.
2. Yamada K., Nabeshima T. Animal models of Alzheimer's disease and evaluation of anti-dementia drugs. Pharmacol Ther 2000, 88:93-113.
3. Deshpande A., Mina E., Glabe C., Busciglio J. Different conformations of amyloid beta induce neurotoxicity by distinct mechanisms in human cortical neurons. J Neurosci 2006, 26:6011-6018.
4. Doi Y., Mizuno T., Maki Y., Jin S., Mizoguchi H., Ikeyama M. Microglia activated with the toll-like receptor 9 ligand CpG attenuate oligomeric amyloid β neurotoxicity in in vitro and in vivo models of Alzheimer's disease. Am J Pathol 2009, 175:2121-2132.
5. De Felice F.G., Velasco P.T., Lambert M.P., Viola K., Fernandez S.J., Ferreira S.T. Abeta oligomers induce neuronal oxidative stress through an N-methyl-d-aspartate receptor-dependent mechanism that is blocked by the Alzheimer drug memantine. J Biol Chem 2007, 282:11590-11601.
6. Mizoguchi H., Takuma K., Fukuzaki E., Ibi D., Someya E., Akazawa K.H., et al. Matrix metalloprotease-9 inhibition improves amyloid beta-mediated cognitive impairment and neurotoxicity in mice. J Pharmacol Exp Ther 2009, 331:14-22.
7. Yamada K., Tanaka T., Han D., Senzaki K., Kameyama T., Nabeshima T. Protective effects of idebenone and alpha-tocopherol on beta-amyloid-(1-42)-induced learning and memory deficits in rats: implication of oxidative stress in beta-amyloid-induced neurotoxicity in vivo. Eur J Neurosci 1999, 11:83-90.
8. Takuma K., Hoshina Y., Arai S., Himeno Y., Matsuo A., Funatsu Y., et al. Ginkgo biloba extract EGb 761 attenuates hippocampal neuronal loss and cognitive dysfunction resulting from chronic restraint stress in ovariectomized rats. Neuroscience 2007, 149:256-262.
9. Brinkmann V., Billich A., Baumruker T., Heining P., Schmouder R., Francis G., et al. Fingolimod (FTY720): discovery and development of an oral drug to treat multiple sclerosis. Nat Rev Drug Discov 2010, 9:883-897.
10. Chun J., Hartung H.P. Mechanism of action of oral fingolimod (FTY720) in multiple sclerosis. Clin Neuropharmacol 2010, 33:91-101.
11. Cohen J.A., Chun J. Mechanisms of fingolimod's efficacy and adverse effects in multiple sclerosis. Ann Neurol 2011, 69:759-777.
12. Pelletier D., Hafler D.A. Fingolimod for multiple sclerosis. N Engl J Med 2012, 366:339-347.
13. Foster C.A., Howard L.M., Schweitzer A., Persohn E., Hiestand P.C., Balatoni B., et al. Brain penetration of the oral immunomodulatory drug FTY720 and its phosphorylation in the central nervous system during experimental autoimmune encephalomyelitis: consequences for mode of action in multiple sclerosis. J Pharmacol Exp Ther 2007, 323:469-475.
14. Adachi K., Kohara T., Nakao N., Arita M., Chiba K., Mishina T., et al. Design, synthesis, and structure-activity relationships of 2-substituted-2-amino-1, 3-propanediols: discovery of a novel immunosuppressant, FTY720. Bioorg Med Chem 1995, 5:853-856.
15. Mandala S., Hajdu R., Bergstrom J., Quackenbush E., Xie J., Milligan J. Alteration of lymphocyte trafficking by sphingosine-1-phosphate receptor agonists. Science 2002, 296:346-349.
16. Matloubian M., Lo C.G., Cinamon G., Lesneski M.J., Xu Y., Brinkmann V. Lymphocyte egress from thymus and peripheral lymphoid organs is dependent on S1P receptor 1. Nature 2004, 427:355-360.
17. Pinschewer D.D., Ochsenbein A.F., Odermatt B., Brinkmann V., Hengartner H., Zinkernagel R.M. FTY720 immunosuppression impairs effector T cell peripheral homing without affecting induction, expansion, and memory. J Immunol 2000, 164:5761-5770.
18. Brinkmann V. Sphingosine 1-phosphate receptors in health and disease: mechanistic insight from gene deletion studies and reverse pharmacology. Pharmacol Ther 2007, 115:84-105.
19. Brinkmann V., Davis M.D., Heise C.E., Albert R., Cottens S., Hof R., et al. The immune modulator FTY720 targets sphingosine 1-phosphate receptors. J Biol Chem 2002, 277:21453-21457.
20. Dev K.K., Mullershausen F., Mattes H., Kuhn R.R., Bilbe G., Hoyer D. Brain sphingosine-1-phosphate receptors: implication for FTY720 in the treatment of multiple sclerosis. Pharmacol Ther 2008, 117:77-93.
21. Miron V.E., Ludwin S.K., Darlington P.J., Jarjour A.A., Soliven B., Kennedy T.E., Fingolimod (FTY720) enhances remyelination following demyelination of organotypic cerebellar slices. Am J Pathol 2010, 176:2682-2694.
22. Choi J.W., Gardell S.E., Herr D.R., Rivera R., Lee C.W., Noguchi K., et al. FTY720 (fingolimod) efficacy in an animal model of multiple sclerosis requires astrocyte sphingosine 1-phosphate receptor 1 (S1P1) modulation. Proc Natl Acad Sci 2011, 108:751-756.
23. Noda H., Takeuchi H., Mizuno T., Suzumura A. Fingolimod phosphate promotes the neuroprotective effects of microglia. J Neuroimmunol 2013, 256:13-18.
24. Doi Y., Takeuchi H., Horiuchi H., Hanyu T., Kawanokuchi J., Jin S., et al. Fingolimod phosphate attenuates oligomeric amyloid β-induced neurotoxicity via increased brain-derived neurotrophic factor expression in neurons. PLoS ONE 2013, 8:e61988.
25. Dahlgren K.N., Manelli A.M., Stine W.B., Baker L.K., Krafft G.A., LaDu M.J. Oligomeric and fibrillar species of amyloid-beta peptides differentially affect neuronal viability. J Biol Chem 2002, 277:32046-32053.
26. Mizuno T., Doi Y., Mizoguchi H., Jin S., Noda M., Sonobe Y., et al. Interleukin-34 selectively enhances the neuroprotective effects of microglia to attenuate oligomeric amyloid-beta neurotoxicity. Am J Pathol 2011, 179:2016-2027.
27. Mizoguchi H., Takuma K., Fukakusa A., Ito Y., Nakatani A., Ibi D., et al. Improvement by minocycline of methamphetamine-induced impairment of recognition memory in mice. Psychopharmacology (Berl) 2008, 196:233-241.
28. Takeuchi H., Mizoguchi H., Doi Y., Jin S., Noda M., Liang J., et al. Blockade of gap junction hemichannel suppresses disease progression in mouse models of amyotrophic lateral sclerosis and Alzheimer's disease. PLoS ONE 2011, 6:e21108.
29. Mizoguchi H., Ibi D., Takuma K., Toth E., Sato J., Itohara S., et al. Alterations of emotional and cognitive behaviors in matrix metalloproteinase-2 and -9-deficient mice. Open Behav Sci J 2010, 4:19-25.
30. Mizoguchi H., Yamada K., Nabeshima T. Matrix metalloproteinases contribute to neuronal dysfunction in animal models of drug dependence, Alzheimer's disease, and epilepsy. Biochem Res Int 2011, 2011:681385.
31. Franklin K.B.J., Paxinos G. The mouse brain in stereotaxic coordinates 1997, Academic, San Diego.
32. Tran M.H., Yamada K., Olariu A., Mizuno M., Ren X.H., Nabeshima T. Amyloid β-peptide induces nitric oxide production in rat hippocampus: association with cholinergic dysfunction and amelioration by inducible nitric oxide synthase inhibitors. FASEB J 2001, 15:1407-1409.
33. Conner J.M., Lauterborn J.C., Yan Q., Gall C.M., Varon S. Distribution of brain-derived neurotrophic factor (BDNF) protein and mRNA in the normal adult rat CNS: evidence for anterograde axonal transport. J Neurosci 1997, 17:2295-2313.
34. Yan Q., Radeke M.J., Matheson C.R., Talvenheimo J., Welcher A.A., Feinstein S.C. Immunocytochemical localization of TrkB in the central nervous system of the adult rat. J Comp Neurol 1997, 378:135-157.
35. Asle-Rousta M., Kolahdooz Z., Oryan S., Ahmadiani A., Dargahi L. FTY720 (Fingolimod) attenuates beta-amyloid peptide (Aβ42)-induced impairment of spatial learning and memory in rats. J Mol Neurosci 2013, 4:1-9.
36. Hemmati F., Dargahi L., Nasoohi S., Omidbakhsh R., Mohamed Z., Naidu M., et al. Neurorestorative effect of FTY720 in a rat model of Alzheimer's disease: comparison with Memantine. Behav Brain Res 2013, 252:415-421.
37. Drake C.T., Milner T.A., Patterson S.L. Ultrastructural localization of full-length trkB immunoreactivity in rat hippocampus suggests multiple roles in modulating activity-dependent synaptic plasticity. J Neurosci 1999, 19:8009-8026.
38. Huang E.J., Reichardt L.F. Neurotrophins: roles in neuronal development and function. Annu Rev Neurosci 2001, 24:677-736.
39. Yoshii A., Constantine-Paton M. Postsynaptic BDNF-TrkB signaling in synapse maturation, plasticity, and disease. Dev Neurobiol 2010, 70:304-322.
40. Minichiello L. TrkB signalling pathways in LTP and learning. Nat Rev Neurosci 2009, 10:850-860.
41. Zhang F., Kang Z., Li W., Xiao Z., Zhou X. Roles of brain-derived neurotrophic factor/tropomyosin-related kinase B (BDNF/TrkB) signalling in Alzheimer's disease. J Clin Neurosci 2012, 19:946-949.
42. Koponen E., Voikar V., Riekki R., Saarelainen T., Rauramaa T., Rauramaa T. Transgenic mice overexpressing the full-length neurotrophin receptor trkB exhibit increased activation of the trkB-PLCgamma pathway, reduced anxiety, and facilitated learning. Mol Cell Neurosci 2004, 26:166-181.
43. Ferrer I., Marin C., Rey M.J., Ribalta T., Goutan E., Blanco R. BDNF and full-length and truncated TrkB expression in Alzheimer disease. Implications in therapeutic strategies. J Neuropathol Exp Neurol 1999, 58:729-739.
44. Phillips H.S., Hains J.M., Armanini M., Laramee G.R., Johnson S.A., Winslow J.W. BDNF mRNA is decreased in the hippocampus of individuals with Alzheimer's disease. Neuron 1991, 7:695-702.
45. Weinstein G., Beiser A.S., Choi S.H., Preis S.R., Chen T.C., Vorgas D., et al. Serum brain-derived neurotrophic factor and the risk for dementia: the Framingham Heart Study. JAMA Neurol 2014, 71:55-61.
46. Nagata T., Kobayashi N., Shinagawa S., Yamada H., Kondo K., Nakayama K. Plasma BDNF levels are correlated with aggressiveness in patients with amnestic mild cognitive impairment or Alzheimer disease. J Neural Transm 2014, 121:433-441.
47. Norimatsu Y., Ohmori T., Kimura A., Madoiwa S., Mimuro J., Seichi A. FTY720 improves functional recovery after spinal cord injury by primarily nonimmunomodulatory mechanisms. Am J Pathol 2012, 180:1625-1635.
48. Deogracias R., Yazdani M., Dekkers M.P., Guy J., Ionescu M.C., Vogt K.E., Fingolimod a sphingosine-1 phosphate receptor modulator, increases BDNF levels and improves symptoms of a mouse model of Rett syndrome. Proc Natl Acad Sci USA 2012, 109:14230-14235.
49. Gómez-Muñoz A., Kong J., Salh B., Steinbrecher U.P. Sphingosine-1-phosphate inhibits acid sphingomyelinase and blocks apoptosis in macrophages. FEBS Lett 2003, 539:56-60.
50. Takasugi N., Sasaki T., Ebinuma I., Osawa S., Isshiki H., Takeo K., et al. FTY720/fingolimod, a sphingosine analogue, reduces amyloid-β production in neurons. PLoS ONE 2013, 8:e64050.