FTY720 attenuates excitotoxicity and neuroinflammation

Journal of Neuroinflammation

Volumn 12, Issue 1, 2015, Pages

  Cipriani, Raffaela ^a,b   Chara, Juan Carlos ^a,b   Rodríguez Antigüedad, Alfredo ^c   Matute, Carlos ^a,b  

^a CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED SOBRE ENFERMEDADES NEURODEGENERATIVAS CIBERNED   (Spain)

^b UNIVERSITY OF THE BASQUE COUNTRY UPV EHU   (Spain)

^c HOSPITAL DE BASURTO   (Spain)

Author keywords

FTY720; Kainic acid; LPS; Microglia; Neuroinflammation; Neurons; NMDA

Indexed keywords

DIZOCILPINE; FINGOLIMOD; KAINIC ACID; LACTATE DEHYDROGENASE; LIPOPOLYSACCHARIDE; MITOGEN ACTIVATED PROTEIN KINASE P38; N METHYL DEXTRO ASPARTIC ACID; NEUROPROTECTIVE AGENT; PROPIDIUM IODIDE; STRESS ACTIVATED PROTEIN KINASE; AMINO ACID RECEPTOR STIMULATING AGENT; ANTIINFLAMMATORY AGENT; LACTATE DEHYDROGENASE (CYTOCHROME); N METHYLASPARTIC ACID;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CELL CULTURE; CELL SURVIVAL; CELLULAR STRESS SIGNAL; DRUG EFFICACY; DRUG MECHANISM; EMBRYO; ENZYME ACTIVATION; EXCITOTOXICITY; HIPPOCAMPAL CA3 REGION; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; MICROGLIA; MICROGLIAL CELL CULTURE; NERVE CELL CULTURE; NERVE CELL NECROSIS; NERVE DEGENERATION; NERVOUS SYSTEM INFLAMMATION; NEUROPROTECTION; NONHUMAN; PRIMARY CELL CULTURE; RAT; SPRAGUE DAWLEY RAT; WESTERN BLOTTING; ANIMAL; BRAIN CORTEX; BRAIN DISEASES; CELL CULTURE; CELL DEATH; CEREBELLUM; CHEMICALLY INDUCED; CYTOLOGY; DISEASE MODEL; DOSE RESPONSE; DRUG EFFECTS; MALE; METABOLISM; NERVE CELL; NEWBORN; ORGAN CULTURE TECHNIQUE; PHOSPHORYLATION; TIME FACTOR;

ANIMALS; ANIMALS, NEWBORN; ANTI-INFLAMMATORY AGENTS; BRAIN DISEASES; CELL DEATH; CELLS, CULTURED; CEREBELLUM; CEREBRAL CORTEX; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; EXCITATORY AMINO ACID AGONISTS; FINGOLIMOD HYDROCHLORIDE; IN VITRO TECHNIQUES; KAINIC ACID; L-LACTATE DEHYDROGENASE (CYTOCHROME); MALE; N-METHYLASPARTATE; NEURONS; ORGAN CULTURE TECHNIQUES; PHOSPHORYLATION; RATS; RATS, SPRAGUE-DAWLEY; TIME FACTORS;

EID: 84929326941     PISSN: None     EISSN: 17422094     Source Type: Journal    
DOI: 10.1186/s12974-015-0308-6     Document Type: Article

References (56)

1. Kappos L, Radue E-W, O'Connor P, Polman C, Hohlfeld R, Calabresi P, et al. A placebo-controlled trial of oral fingolimod in relapsing multiple sclerosis. N Engl J Med. 2010;362:387-401.
2. Cohen JA, Barkhof F, Comi G, Hartung H-P, Khatri BO, Montalban X, et al. Oral fingolimod or intramuscular interferon for relapsing multiple sclerosis. N Engl J Med. 2010;362:402-15.
3. Brinkmann V, Davis MD, Heise CE, Albert R, Cottens S, Hof R, et al. The immune modulator FTY720 targets sphingosine 1-phosphate receptors. J Biol Chem. 2002;277:21453-7.
4. Mandala S, Hajdu R, Bergstrom J, Quackenbush E, Xie J, Milligan J, et al. Alteration of lymphocyte trafficking by sphingosine-1-phosphate receptor agonists. Science. 2002;296:346-9.
5. Mullershausen F, Zecri F, Cetin C, Billich A, Guerini D, Seuwen K. Persistent signaling induced by FTY720-phosphate is mediated by internalized S1P1 receptors. Nat Chem Biol. 2009;5:428-34.
6. Kataoka H, Sugahara K, Shimano K, Teshima K, Koyama M, Fukunari A, et al. FTY720, sphingosine 1-phosphate receptor modulator, ameliorates experimental autoimmune encephalomyelitis by inhibition of T cell infiltration. Cell Mol Immunol. 2005;2:439-48.
7. Balatoni B, Storch MK, Swoboda E-M, Schönborn V, Koziel A, Lambrou GN, et al. FTY720 sustains and restores neuronal function in the DA rat model of MOG-induced experimental autoimmune encephalomyelitis. Brain Res Bull. 2007;74:307-16.
8. Foster CA, Mechtcheriakova D, Storch MK, Balatoni B, Howard LM, Bornancin F, et al. FTY720 rescue therapy in the dark agouti rat model of experimental autoimmune encephalomyelitis: expression of central nervous system genes and reversal of blood-brain-barrier damage. Brain Pathol. 2009;19:254-66.
9. Rossi S, Lo Giudice T, De Chiara V, Musella A, Studer V, Motta C, et al. Oral fingolimod rescues the functional deficits of synapses in experimental autoimmune encephalomyelitis. Br J Pharmacol. 2012;165:861-9.
10. Kim HJ, Miron VE, Dukala D, Proia RL, Ludwin SK, Traka M, et al. Neurobiological effects of sphingosine 1-phosphate receptor modulation in the cuprizone model. FASEB J. 2011;25:1509-18.
11. Miron VE, Ludwin SK, Darlington PJ, Jarjour AA, Soliven B, Kennedy TE, et al. Fingolimod (FTY720) enhances remyelination following demyelination of organotypic cerebellar slices. Am J Pathol. 2010;176:2682-94.
12. Foster CA, Howard LM, Schweitzer A, Persohn E, Hiestand PC, 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;323:469-75.
13. Billich A, Bornancin F, Dévay P, Mechtcheriakova D, Urtz N, Baumruker T. Phosphorylation of the immunomodulatory drug FTY720 by sphingosine kinases. J Biol Chem. 2003;278:47408-15.
14. Miron VE, Schubart A, Antel JP. Central nervous system-directed effects of FTY720 (fingolimod). J Neurol Sci. 2008;274:13-7.
15. Wei Y, Yemisci M, Kim H-H, Yung LM, Shin HK, Hwang S-K, et al. Fingolimod provides long-term protection in rodent models of cerebral ischemia. Ann Neurol. 2011;69:119-29.
16. Kraft P, Göb E, Schuhmann MK, Göbel K, Deppermann C, Thielmann I, et al. FTY720 ameliorates acute ischemic stroke in mice by reducing thrombo-inflammation but not by direct neuroprotection. Stroke. 2013;44:3202-10.
17. Hasegawa Y, Suzuki H, Sozen T, Rolland W, Zhang JH. Activation of sphingosine 1-phosphate receptor-1 by FTY720 is neuroprotective after ischemic stroke in rats. Stroke. 2010;41:368-74.
18. Lu L, Barfejani AH, Qin T, Dong Q, Ayata C, Waeber C. Fingolimod exerts neuroprotective effects in a mouse model of intracerebral hemorrhage. Brain Res. 2014;1555:89-96.
19. Rolland WB, Lekic T, Krafft PR, Hasegawa Y, Altay O, Hartman R, et al. Fingolimod reduces cerebral lymphocyte infiltration in experimental models of rodent intracerebral hemorrhage. Exp Neurol. 2013;241:45-55.
20. Lee KD, Chow WN, Sato-Bigbee C, Graf MR, Graham RS, Colello RJ, et al. FTY720 reduces inflammation and promotes functional recovery after spinal cord injury. J Neurotrauma. 2009;26:2335-44.
21. 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.
22. 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.
23. Fukumoto K, Mizoguchi H, Takeuchi H, Horiuchi H, Kawanokuchi J, Jin S, et al. Fingolimod increases brain-derived neurotrophic factor levels and ameliorates amyloid β-induced memory impairment. Behav Brain Res. 2014;268:88-93.
24. Hemmati F, Dargahi L, Nasoohi S, Omidbakhsh R, Mohamed Z, Chik Z, et al. Neurorestorative effect of FTY720 in a rat model of Alzheimer's disease: comparison with memantine. Behav Brain Res. 2013;252:415-21.
25. Estrada-Bernal A, Palanichamy K, Ray Chaudhury A, Van Brocklyn JR. Induction of brain tumor stem cell apoptosis by FTY720: a potential therapeutic agent for glioblastoma. Neuro Oncol. 2012;14:405-15.
26. Gao F, Liu Y, Li X, Wang Y, Wei D, Jiang W. Fingolimod (FTY720) inhibits neuroinflammation and attenuates spontaneous convulsions in lithium-pilocarpine induced status epilepticus in rat model. Pharmacol Biochem Behav. 2012;103:187-96.
27. Noda H, Takeuchi H, Mizuno T, Suzumura A. Fingolimod phosphate promotes the neuroprotective effects of microglia. J Neuroimmunol. 2013;146:1-6.
28. Jackson SJ, Giovannoni G, Baker D. Fingolimod modulates microglial activation to augment markers of remyelination. J Neuroinflammation. 2011;8:76.
29. Deogracias R, Yazdani M, Dekkers MPJ, Guy J, Ionescu MCS, Vogt KE, et al. Fingolimod, a sphingosine-1 phosphate receptor modulator, increases BDNF levels and improves symptoms of a mouse model of Rett syndrome. Proc Natl Acad Sci U S A. 2012;109:14230-5.
30. Di Menna L, Molinaro G, Di Nuzzo L, Riozzi B, Zappulla C, Pozzilli C, et al. Fingolimod protects cultured cortical neurons against excitotoxic death. Pharmacol Res. 2013;67:1-9.
31. Mulle C, Sailer A, Pérez-Otaño I, Dickinson-Anson H, Castillo PE, Bureau I, et al. Altered synaptic physiology and reduced susceptibility to kainate-induced seizures in GluR6-deficient mice. Nature. 1998;392:601-5.
32. Ben-Ari Y. Limbic seizure and brain damage produced by kainic acid: Mechanisms and relevance to human temporal lobe epilepsy. Neuroscience. 1985;14:375-403.
33. Andersson PB, Perry VH, Gordon S. The kinetics and morphological characteristics of the macrophage-microglial response to kainic acid-induced neuronal degeneration. Neuroscience. 1991;42:201-14.
34. Ravizza T, Rizzi M, Perego C, Richichi C, Velísková J, Moshé SL, et al. Inflammatory response and glia activation in developing rat hippocampus after status epilepticus. Epilepsia. 2005;46 Suppl 5:113-7.
35. Mitchell J, Sundstrom LE, Wheal HV. Microglial and astrocytic cell responses in the rat hippocampus after an intracerebroventricular kainic acid injection. Exp Neurol. 1993;121:224-30.
36. Ruiz A, Matute C, Alberdi E. Endoplasmic reticulum Ca(2+) release through ryanodine and IP(3) receptors contributes to neuronal excitotoxicity. Cell Calcium. 2009;46:273-81.
37. Plenz D, Kitai ST. Organotypic cortex-striatum-mesencephalon cultures: the nigrostriatal pathway. Neurosci Lett. 1996;209:177-80.
38. Cavaliere F, Dinkel K, Reymann K. The subventricular zone releases factors which can be protective in oxygen/glucose deprivation-induced cortical damage: an organotypic study. Exp Neurol. 2006;201:66-74.
39. Zimmer J, Kristensen BW, Jakobsen B, Noraberg J. Excitatory amino acid neurotoxicity and modulation of glutamate receptor expression in organotypic brain slice cultures. Amino Acids. 2000;19:7-21.
40. Paxinos G, Watson C. The Rat Brain in stereotaxic coordinates: hard cover edition, vol. 1. London, UK: Elsevier Academic Press; 2013.
41. Racine RJ, Method G. Modification of seizure activity by electrical stimulation: II. Motor seizure. Electroencephalogr Clin Neurophysiol. 1972;32:281-94.
42. Schmued LC, Stowers CC, Scallet AC, Xu L. Fluoro-Jade C results in ultra high resolution and contrast labeling of degenerating neurons. Brain Res. 2005;1035:24-31.
43. Yoshino T, Tabunoki H, Sugiyama S, Ishii K, Kim SU, Satoh J-I. Non-phosphorylated FTY720 induces apoptosis of human microglia by activating SREBP2. Cell Mol Neurobiol. 2011;31:1009-20.
44. Koistinaho M, Koistinaho J. Role of p38 and p44/42 mitogen-activated protein kinases in microglia. Glia. 2002;40:175-83.
45. Waetzig V, Czeloth K, Hidding U, Mielke K, Kanzow M, Brecht S, et al. c-Jun N-terminal kinases (JNKs) mediate pro-inflammatory actions of microglia. Glia. 2005;50:235-46.
46. Wang Q, Yu S, Simonyi A, Sun GY, Sun AY. Kainic acid-mediated excitotoxicity as a model for neurodegeneration. Mol Neurobiol. 2005;31:3-16.
47. Brunkhorst R, Kanaan N, Koch A, Ferreirós N, Mirceska A, Zeiner P, et al. FTY720 treatment in the convalescence period improves functional recovery and reduces reactive astrogliosis in photothrombotic stroke. PLoS One. 2013;8:e70124.
48. Choi JW, Gardell SE, Herr DR, Rivera R, Lee C, 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 U S A. 2011;108:751-6.
49. Choi JW, Chun J. Lysophospholipids and their receptors in the central nervous system. Biochim Biophys Acta. 2013;1831:20-32.
50. Coelho RP, Payne SG, Bittman R, Spiegel S, Sato-Bigbee C. The immunomodulator FTY720 has a direct cytoprotective effect in oligodendrocyte progenitors. J Pharmacol Exp Ther. 2007;323:626-35.
51. Blondeau N, Lai Y, Tyndall S, Popolo M, Topalkara K, Pru JK, et al. Distribution of sphingosine kinase activity and mRNA in rodent brain. J Neurochem. 2007;103:509-17.
52. Hait NC, Wise LE, Allegood JC, O'Brien M, Avni D, Reeves TM, et al. Active, phosphorylated fingolimod inhibits histone deacetylases and facilitates fear extinction memory. Nat Neurosci. 2014;17:971-80.
53. Brandt C, Potschka H, Löscher W, Ebert U. N-methyl-d-aspartate receptor blockade after status epilepticus protects against limbic brain damage but not against epilepsy in the kainate model of temporal lobe epilepsy. Neuroscience. 2003;118:727-40.
54. Van Doorn R, Nijland PG, Dekker N, Witte ME, Lopes-Pinheiro MA, van het Hof B, et al. Fingolimod attenuates ceramide-induced blood-brain barrier dysfunction in multiple sclerosis by targeting reactive astrocytes. Acta Neuropathol. 2012;124:397-410.
55. Tham C-S, Lin F-F, Rao TS, Yu N, Webb M. Microglial activation state and lysophospholipid acid receptor expression. Int J Dev Neurosci. 2003;21:431-43.
56. Kobayashi K, Imagama S, Ohgomori T, Hirano K, Uchimura K, Sakamoto K, et al. Minocycline selectively inhibits M1 polarization of microglia. Cell Death Dis. 2013;4:e525.