Fingolimod induces neuroprotective factors in human astrocytes

Journal of Neuroinflammation

Volumn 12, Issue 1, 2015, Pages

  Hoffmann, Franziska S ^a   Hofereiter, Johann ^a   Rübsamen, Heike ^a   Melms, Johannes ^b   Schwarz, Sigrid ^b   Faber, Hans ^c   Weber, Peter ^c   Pütz, Benno ^c   Loleit, Verena ^a   Weber, Frank ^c   Hohlfeld, Reinhard ^a,e   Meinl, Edgar ^a   Krumbholz, Markus ^a,d  

^a UNIVERSITY OF MUNICH   (Germany)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^c MAX PLANCK INSTITUTE OF PSYCHIATRY   (Germany)

^d UNIVERSITY OF TÜBINGEN   (Germany)

^e Munich Cluster for Systems Neurology ^*  (Germany)

Author keywords

Astrocyte; B cell activating factor of the TNF family TNFSF13b; CXCL10 IP10; Fingolimod; Heparin binding EGF like growth factor; Interleukin 11; Leukemia inhibitory factor; MX1; Neuroprotection; OAS2

Indexed keywords

B CELL ACTIVATING FACTOR; CYTOKINE; FINGOLIMOD; GAMMA INTERFERON INDUCIBLE PROTEIN 10; HEPARIN BINDING EPIDERMAL GROWTH FACTOR; INTERLEUKIN 11; LEUKEMIA INHIBITORY FACTOR; MESSENGER RNA; NEUROTROPHIC FACTOR; SPHINGOSINE 1 PHOSPHATE; SPHINGOSINE 1 PHOSPHATE RECEPTOR; SPHINGOSINE 1 PHOSPHATE RECEPTOR 1; SPHINGOSINE 1 PHOSPHATE RECEPTOR 3; TRANSCRIPTION FACTOR EMX1; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; HBEGF PROTEIN, HUMAN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LYSOPHOSPHOLIPID; NEUROPROTECTIVE AGENT; SMALL INTERFERING RNA; SPHINGOSINE; SPHINGOSINE 1-PHOSPHATE;

ARTICLE; ASTROCYTE; ASTROCYTOMA CELL; B LYMPHOCYTE; BAFF GENE; CELL MEMBRANE PERMEABILITY; CONTROLLED STUDY; CXCL10 GENE; FETUS; GENE; GENE EXPRESSION; GENE SILENCING; GENOME ANALYSIS; HBEGF GENE; HUMAN; HUMAN CELL; HUMAN GENOME; HUMAN TISSUE; IL11 GENE; LIF GENE; MICROARRAY ANALYSIS; MULTIPLE SCLEROSIS; MX1 GENE; NERVE CELL STIMULATION; NEUROPROTECTION; OAS2 GENE; PROTEIN SECRETION; RNA INTERFERENCE; VALIDATION STUDY; ANALOGS AND DERIVATIVES; CORPUS STRIATUM; CYTOLOGY; DOSE RESPONSE; DRUG EFFECTS; ENZYME LINKED IMMUNOSORBENT ASSAY; GENETICS; METABOLISM; NEURAL STEM CELL; TIME FACTOR;

ASTROCYTES; CHEMOKINE CXCL10; CORPUS STRIATUM; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME-LINKED IMMUNOSORBENT ASSAY; FETUS; FINGOLIMOD HYDROCHLORIDE; HEPARIN-BINDING EGF-LIKE GROWTH FACTOR; HUMANS; INTERLEUKIN-11; LYSOPHOSPHOLIPIDS; MICROARRAY ANALYSIS; NEURAL STEM CELLS; NEUROPROTECTIVE AGENTS; NF-KAPPA B; RNA, MESSENGER; RNA, SMALL INTERFERING; SPHINGOSINE; TIME FACTORS;

EID: 84942607562     PISSN: None     EISSN: 17422094     Source Type: Journal    
DOI: 10.1186/s12974-015-0393-6     Document Type: Article

References (62)

1. Kappos L, Radue EW, 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 HP, Khatri BO, Montalban X, et al. Oral fingolimod or intramuscular interferon for relapsing multiple sclerosis. N Engl J Med. 2010;362:402-15.
3. Strub GM, Maceyka M, Hait NC, Milstien S, Spiegel S. Extracellular and intracellular actions of sphingosine-1-phosphate. Adv Exp Med Biol. 2010;688:141-55.
4. Alvarez SE, Harikumar KB, Hait NC, Allegood J, Strub GM, Kim EY, et al. Sphingosine-1-phosphate is a missing cofactor for the E3 ubiquitin ligase TRAF2. Nature. 2010;465:1084-8.
5. 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.
6. Jo E, Sanna MG, Gonzalez-Cabrera PJ, Thangada S, Tigyi G, Osborne DA, et al. S1P1-selective in vivo-active agonists from high- throughput screening: off-the-shelf chemical probes of receptor interactions, signaling, and fate. Chem Biol. 2005;12:703-15.
7. 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.
8. 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;9:883-97.
9. Mullershausen F, Craveiro LM, Shin Y, Cortes-Cros M, Bassilana F, Osinde M, et al. Phosphorylated FTY720 promotes astrocyte migration through sphingosine-1-phosphate receptors. J Neurochem. 2007;102:1151-61.
10. Singer II, Tian M, Wickham LA, Lin J, Matheravidathu SS, Forrest MJ, et al. Sphingosine-1-phosphate agonists increase macrophage homing, lymphocyte contacts, and endothelial junctional complex formation in murine lymph nodes. J Immunol. 2005;175:7151-61.
11. Rosen H, Goetzl EJ. Sphingosine 1-phosphate and its receptors: an autocrine and paracrine network. Nat Rev Immunol. 2005;5:560-70.
12. Foster CA, Howard LM, Schweitzer A, Persohn E, Hiestand PC, Balatoni BZ, 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. Dev KK, Mullershausen F, Mattes H, Kuhn RR, Bilbe G, Hoyer D, et al. Brain sphingosine-1-phosphate receptors: implication for FTY720 in the treatment of multiple sclerosis. Pharmacol Ther. 2008;117:77-93.
14. Seifert G, Schilling K, Steinhauser C. Astrocyte dysfunction in neurological disorders: a molecular perspective. Nat Rev Neurosci. 2006;7:194-206.
15. Stadelmann C, Kerschensteiner M, Misgeld T, Bruck W, Hohlfeld R, Lassmann H. BDNF and gp145trkB in multiple sclerosis brain lesions: neuroprotective interactions between immune and neuronal cells? Brain. 2002;125:75-85.
16. Farina C, Aloisi F, Meinl E. Astrocytes are active players in cerebral innate immunity. Trends Immunol. 2007;28:138-45.
17. Sorensen TL, Tani M, Jensen J, Pierce V, Lucchinetti C, Folcik VA, et al. Expression of specific chemokines and chemokine receptors in the central nervous system of multiple sclerosis patients. J Clin Invest. 1999;103:807-15.
18. Krumbholz M, Theil D, Derfuss T, Rosenwald A, Schrader F, Monoranu CM, et al. BAFF is produced by astrocytes and up-regulated in multiple sclerosis lesions and primary central nervous system lymphoma. J Exp Med. 2005;201:195-200.
19. Trapp BD, Nave KA. Multiple sclerosis: an immune or neurodegenerative disorder? Annu Rev Neurosci. 2008;31:247-69.
20. Radue EW, Barkhof F, Kappos L, Sprenger T, Haring DA, de Vera A, et al. Correlation between brain volume loss and clinical and MRI outcomes in multiple sclerosis. Neurology. 2015;84(8):784-93.
21. Sormani M, De Stefano N, Francis G, Sprenger T, Chin P, Radue E, et al. Fingolimod effect on brain volume loss independently contributes to its effect on disability. Mult Scler. 2015;21(7):916-24.
22. Calabresi PA, Radue EW, Goodin D, Jeffery D, Rammohan KW, Reder AT, et al. Safety and efficacy of fingolimod in patients with relapsing-remitting multiple sclerosis (FREEDOMS II): a double-blind, randomised, placebo-controlled, phase 3 trial. Lancet Neurol. 2014;13:545-56.
23. Choi JW, Gardell SE, Herr DR, Rivera R, Lee CW, 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;108:751-6.
24. Colombo E, Dario MD, Capitolo E, Chaabane L, Newcombe J, Martino G, et al. Fingolimod may support neuroprotection via blockade of astrocyte nitric oxide. Ann Neurol. 2014;76(3):325-37.
25. Aloisi F, Borsellino G, Samoggia P, Testa U, Chelucci C, Russo G, et al. Astrocyte cultures from human embryonic brain: characterization and modulation of surface molecules by inflammatory cytokines. J Neurosci Res. 1992;32:494-506.
26. Krumbholz M, Faber H, Steinmeyer F, Hoffmann LA, Kümpfel T, Pellkofer H, et al. Interferon-{beta} increases BAFF levels in multiple sclerosis: implications for B cell autoimmunity. Brain. 2008;131:1415-63.
27. Theil D, Derfuss T, Paripovic I, Herberger S, Meinl E, Schueler O, et al. Latent herpesvirus infection in human trigeminal ganglia causes chronic immune response. Am J Pathol. 2003;163:2179-84.
28. R Core Team. R: a language and environment for statistical computing. 3.0.1 edition. Vienna, Austria: R Foundation for Statistical Computing; 2013.
29. Huber W, Carey VJ, Gentleman R, Anders S, Carlson M, Carvalho BS, et al. Orchestrating high-throughput genomic analysis with Bioconductor. Nat Methods. 2015;12:115-21.
30. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, et al. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol. 2004;5:R80.
31. Huber W, von Heydebreck A, Sultmann H, Poustka A, Vingron M. Variance stabilization applied to microarray data calibration and to the quantification of differential expression. Bioinformatics. 2002;18 Suppl 1:S96-104.
32. Blom T, Bergelin N, Meinander A, Lof C, Slotte JP, Eriksson JE, et al. An autocrine sphingosine-1-phosphate signaling loop enhances NF-kappaB-activation and survival. BMC Cell Biol. 2010;11:45.
33. Rosen H, Sanna MG, Cahalan SM, Gonzalez-Cabrera PJ. Tipping the gatekeeper: S1P regulation of endothelial barrier function. Trends Immunol. 2007;28:102-7.
34. Suomalainen L, Pentikäinen V, Dunkel L. Sphingosine-1-phosphate inhibits nuclear factor ΚB activation and germ cell apoptosis in the human testis independently of its receptors. Am J Surg Pathol. 2005;166:773-81.
35. Van Brocklyn JR, Lee M-J, Menzeleev R, Olivera A, Edsall L, Cuvillier O, et al. Dual actions of sphingosine-1-phosphate: extracellular through the Gi-coupled receptor Edg-1 and intracellular to regulate proliferation and survival. J Cell Biol. 1998;142:229-40.
36. Liu Y, Peng M, Zang D, Zhang B. Leukemia inhibitory factor promotes nestin-positive cells, and increases gp130 levels in the Parkinson disease mouse model of 6-hydroxydopamine. Neurosciences (Riyadh). 2013;18:363-70.
37. Chollangi S, Wang J, Martin A, Quinn J, Ash JD. Preconditioning-induced protection from oxidative injury is mediated by leukemia inhibitory factor receptor (LIFR) and its ligands in the retina. Neurobiol Dis. 2009;34:535-44.
38. Park SK, Solomon D, Vartanian T. Growth factor control of CNS myelination. Dev Neurosci. 2001;23:327-37.
39. Ishibashi T, Dakin KA, Stevens B, Lee PR, Kozlov SV, Stewart CL, et al. Astrocytes promote myelination in response to electrical impulses. Neuron. 2006;49:823-32.
40. Putoczki T, Ernst M. More than a sidekick: the IL-6 family cytokine IL-11 links inflammation to cancer. J Leukoc Biol. 2010;88:1109-17.
41. Zhang PL, Izrael M, Ainbinder E, Ben-Simchon L, Chebath J, Revel M. Increased myelinating capacity of embryonic stem cell derived oligodendrocyte precursors after treatment by interleukin-6/soluble interleukin-6 receptor fusion protein. Mol Cell Neurosci. 2006;31:387-98.
42. Gurfein BT, Zhang Y, López CB, Argaw AT, Zameer A, Moran TM, et al. IL-11 regulates autoimmune demyelination. J Immunol. 2009;183:4229-40.
43. Jin K, Mao XO, Sun Y, Xie L, Jin L, Nishi E, et al. Heparin-binding epidermal growth factor-like growth factor: hypoxia-inducible expression in vitro and stimulation of neurogenesis in vitro and in vivo. J Neurosci. 2002;22:5365-73.
44. Farkas LM, Krieglstein K. Heparin-binding epidermal growth factor-like growth factor (HB-EGF) regulates survival of midbrain dopaminergic neurons. J Neural Transm. 2002;109:267-77.
45. Krumbholz M, Derfuss T, Hohlfeld R, Meinl E. B cells and antibodies in multiple sclerosis pathogenesis and therapy. Nat Rev Neurol. 2012;8:613-23.
46. Tada S, Yasui T, Nakatsuji Y, Okuno T, Koda T, Mochizuki H, et al. BAFF controls neural cell survival through BAFF receptor. PLoS One. 2013;8, e70924.
47. Zhang L, Zheng S, Wu H, Wu Y, Liu S, Fan M, et al. Identification of BLyS (B lymphocyte stimulator), a non-myelin-associated protein, as a functional ligand for nogo-66 receptor. J Neurosci. 2009;29:6348-52.
48. Fife BT, Kennedy KJ, Paniagua MC, Lukacs NW, Kunkel SL, Luster AD, et al. CXCL10 (IFN-γ-inducible protein-10) control of encephalitogenic CD4+ T cell accumulation in the central nervous system during experimental autoimmune encephalomyelitis. J Immunol. 2001;166:7617-24.
49. Hofman FM, Hinton DR, Johnson K, Merrill JE. Tumor necrosis factor identified in multiple sclerosis brain. J Exp Med. 1989;170:607-12.
50. Sharief MK, Hentges R. Association between tumor necrosis factor-aα and disease progression in patients with multiple sclerosis. N Engl J Med. 1991;325:467-72.
51. Selmaj KW, Raine CS. Tumor necrosis factor mediates myelin and oligodendrocyte damage in vitro. Ann Neurol. 1988;23:339-46.
52. Rossi S, Motta C, Studer V, Barbieri F, Buttari F, Bergami A, et al. Tumor necrosis factor is elevated in progressive multiple sclerosis and causes excitotoxic neurodegeneration. Mult Scler. 2014;20(3):304-12. doi: 10.1177/1352458513498128
53. Bosch X, Saiz A, Ramos-Casals M. Monoclonal antibody therapy-associated neurological disorders. Nat Rev Neurol. 2011;7:165-72.
54. Kaltsonoudis E, Voulgari PV, Konitsiotis S, Drosos AA. Demyelination and other neurological adverse events after anti-TNF therapy. Autoimmun Rev. 2014;13:54-8.
55. Brambilla R, Ashbaugh JJ, Magliozzi R, Dellarole A, Karmally S, Szymkowski DE, et al. Inhibition of soluble tumour necrosis factor is therapeutic in experimental autoimmune encephalomyelitis and promotes axon preservation and remyelination. Brain. 2011;134:2736-54.
56. Van Hauwermeiren F, Vandenbroucke RE, Libert C. Treatment of TNF mediated diseases by selective inhibition of soluble TNF or TNFR1. Cytokine Growth Factor Rev. 2011;22:311-9.
57. Wu C, Leong S, Moore C, Cui Q, Gris P, Bernier L-P, et al. Dual effects of daily FTY720 on human astrocytes in vitro: relevance for neuroinflammation. J Neuroinflammation. 2013;10:41.
58. Haller O, Kochs G. Human MxA protein: an interferon-induced dynamin-like GTPase with broad antiviral activity. J Interferon Cytokine Res. 2011;31:79-87.
59. Hovanessian AG. On the discovery of interferon-inducible, double-stranded RNA activated enzymes: the 2-5oligoadenylate synthetases and the protein kinase PKR. Cytokine Growth Factor Rev. 2007;18:351-61.
60. Floyd-Smith G, Slattery E, Lengyel P. Interferon action: RNA cleavage pattern of a (2-5)oligoadenylate-dependent endonuclease. Science. 1981;212:1030-2.
61. Cinamon G, Zachariah MA, Lam OM, Foss Jr FW, Cyster JG. Follicular shuttling of marginal zone B cells facilitates antigen transport. Nat Immunol. 2008;9:54-62.
62. Garris CS, Wu L, Acharya S, Arac A, Blaho VA, Huang Y, et al. Defective sphingosine 1-phosphate receptor 1 (S1P1) phosphorylation exacerbates TH17-mediated autoimmune neuroinflammation. Nat Immunol. 2013;14:1166-72.