Sphingosine 1 phosphate at the blood brain barrier: Can the modulation of S1P receptor 1 influence the response of endothelial cells and astrocytes to inflammatory stimuli?

PLoS ONE

Volumn 10, Issue 7, 2015, Pages

  Spampinato, Simona F ^c   Obermeier, Birgit ^d   Cotleur, Anne ^d   Love, Anna ^a   Takeshita, Yukio ^e   Sano, Yasuteru ^b   Kanda, Takashi ^b   Ransohoff, Richard M ^d  

^a LERNER RESEARCH INSTITUTE   (United States)

^b YAMAGUCHI UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c UNIVERSITY OF CATANIA   (Italy)

^d BIOGEN   (United States)

^e YAMAGUCHI UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

FINGOLIMOD; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; SPHINGOSINE 1 PHOSPHATE; SPHINGOSINE 1 PHOSPHATE RECEPTOR; CYTOKINE; LYSOPHOSPHOLIPID; SPHINGOLIPID; SPHINGOSINE; SPHINGOSINE 1-PHOSPHATE;

ARTICLE; ASTROCYTE; BLOOD BRAIN BARRIER; CELL DEATH; CELL INTERACTION; CELL LOSS; CELL STIMULATION; CELL SURVIVAL; CELL VIABILITY; COCULTURE; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOKINE RELEASE; CYTOKINE RESPONSE; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; INFLAMMATION; INTRACELLULAR SIGNALING; LEUKOCYTE MIGRATION; MULTIPLE SCLEROSIS; NEUROPROTECTION; PERIPHERAL BLOOD MONONUCLEAR CELL; REGULATORY MECHANISM; SHEAR STRESS; ADULT; ANALOGS AND DERIVATIVES; CELL MOTION; CHEMISTRY; CYTOLOGY; IMMUNOLOGY; LEUKOCYTE; MECHANICAL STRESS; METABOLISM; MICROCIRCULATION; MIDDLE AGED; NORMAL HUMAN; SIGNAL TRANSDUCTION; YOUNG ADULT;

ADULT; ASTROCYTES; BLOOD-BRAIN BARRIER; CELL MOVEMENT; CELL SURVIVAL; CYTOKINES; ENDOTHELIAL CELLS; FINGOLIMOD HYDROCHLORIDE; GRANULOCYTE-MACROPHAGE COLONY-STIMULATING FACTOR; HEALTHY VOLUNTEERS; HUMANS; INFLAMMATION; LEUKOCYTES; LYSOPHOSPHOLIPIDS; MICROCIRCULATION; MIDDLE AGED; MULTIPLE SCLEROSIS; RECEPTORS, LYSOSPHINGOLIPID; SIGNAL TRANSDUCTION; SPHINGOLIPIDS; SPHINGOSINE; STRESS, MECHANICAL; YOUNG ADULT;

EID: 84941248949     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0133392     Document Type: Article

References (64)

1. Ransohoff RM, Engelhardt B. The anatomical and cellular basis of immune surveillance in the central nervous system. Nature reviews Immunology. 2012; 12(9):623-35. doi:10.1038/nri3265 PMID: 22903150.
2. Obermeier B, Daneman R, Ransohoff RM. Development, maintenance and disruption of the bloodbrain barrier. Nature medicine. 2013; 19(12):1584-96. doi:10.1038/nm.3407 PMID: 24309662.
3. Abbott NJ, Ronnback L, Hansson E. Astrocyte-endothelial interactions at the blood-brain barrier. Nature reviews Neuroscience. 2006; 7(1):41-53. doi:10.1038/nrn1824PMID: 16371949.
4. Lassmann H, van Horssen J, Mahad D. Progressive multiple sclerosis: pathology and pathogenesis. Nature reviews Neurology. 2012; 8(11):647-56. doi:10.1038/nrneurol.2012.168 PMID: 23007702.
5. Engelhardt B, Ransohoff RM. Capture, crawl, cross: The T cell code to breach the blood-brain barriers. Trends in immunology. 2012; 33(12):579-89. doi:10.1016/j.it.2012.07.004 PMID: 22926201.
6. 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. Nature reviews Drug discovery. 2010; 9(11):883-97. PMID: 21031003.
7. Rosen H, Germana Sanna M, Gonzalez-Cabrera PJ, Roberts E. The organization of the sphingosine 1- phosphate signaling system. Current topics in microbiology and immunology. 2014; 378:1-21. doi:10.1007/978-3-319-05879-5-1PMID: 24728591.
8. Cohen JA, Chun J. Mechanisms of fingolimod's efficacy and adverse effects in multiple sclerosis. Annals of neurology. 2011; 69(5):759-77. doi:10.1002/ana.22426 PMID: 21520239.
9. Maceyka M, Harikumar KB, Milstien S, Spiegel S. Sphingosine-1-phosphate signaling and its role in disease. Trends in cell biology. 2012; 22(1):50-60. doi:10.1016/j.tcb.2011.09.003 PMID: 22001186; PubMed Central PMCID: PMC3253987.
10. Abbasi T, Garcia JG. Sphingolipids in lung endothelial biology and regulation of vascular integrity. Handbook of experimental pharmacology. 2013;(216: ):201-26. doi:10.1007/978-3-7091-1511-4-10 PMID: 23563658.
11. McVerry BJ, Garcia JG. Endothelial cell barrier regulation by sphingosine 1-phosphate. Journal of cellular biochemistry. 2004; 92(6):1075-85. doi:10.1002/jcb.20088 PMID: 15258893.
12. Pebay A, Toutant M, Premont J, Calvo CF, Venance L, Cordier J, et al. Sphingosine-1-phosphate induces proliferation of astrocytes: regulation by intracellular signalling cascades. The European journal of neuroscience. 2001; 13(12):2067-76. PMID: 11467306.
13. Furukawa A, Kita K, Toyomoto M, Fujii S, Inoue S, Hayashi K, et al. Production of nerve growth factor enhanced in cultured mouse astrocytes by glycerophospholipids, sphingolipids, and their related compounds. Molecular and cellular biochemistry. 2007; 305(1-2):27-34. doi:10.1007/s11010-007-9524-4 PMID: 17577630.
14. Sato K, Ishikawa K, Ui M, Okajima F. Sphingosine 1-phosphate induces expression of early growth response-1 and fibroblast growth factor-2 through mechanism involving extracellular signal-regulated kinase in astroglial cells. Brain research Molecular brain research. 1999; 74(1-2):182-9. PMID: 10640689.
15. Fischer I, Alliod C, Martinier N, Newcombe J, Brana C, Pouly S. Sphingosine kinase 1 and sphingosine 1-phosphate receptor 3 are functionally upregulated on astrocytes under pro-inflammatory conditions. PLoS One. 2011; 6(8):e23905. doi:10.1371/journal.pone.0023905 PMID: 21887342; PubMed Central PMCID: PMC3161076.
16. Kimura A, Ohmori T, Ohkawa R, Madoiwa S, Mimuro J, Murakami T, et al. Essential roles of sphingosine 1-phosphate/S1P1 receptor axis in the migration of neural stem cells toward a site of spinal cord injury. Stem cells. 2007; 25(1):115-24. doi:10.1634/stemcells.2006-0223 PMID: 16990586.
17. 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 neuropathologica. 2012; 124(3):397-410. doi:10.1007/s00401-012-1014-4 PMID: 22810490.
18. Takeshita Y, Obermeier B, Cotleur A, Sano Y, Kanda T, Ransohoff RM. An in vitro blood-brain barrier model combining shear stress and endothelial cell/astrocyte co-culture. Journal of neuroscience methods. 2014; 232:165-72. PMID: 24858797.
19. Sano Y, Shimizu F, Abe M, Maeda T, Kashiwamura Y, Ohtsuki S, et al. Establishment of a new conditionally immortalized human brain microvascular endothelial cell line retaining an in vivo blood-brain barrier function. Journal of cellular physiology. 2010; 225(2):519-28. doi:10.1002/jcp.22232 PMID: 20458752.
20. Haruki H, Sano Y, Shimizu F, Omoto M, Tasaki A, Oishi M, et al. NMO sera down-regulate AQP4 in human astrocyte and induce cytotoxicity independent of complement. Journal of the neurological sciences. 2013; 331(1-2):136-44. doi:10.1016/j.jns.2013.05.035 PMID: 23809190.
21. Mahad D, Callahan MK, Williams KA, Ubogu EE, Kivisakk P, Tucky B, et al. Modulating CCR2 and CCL2 at the blood-brain barrier: relevance for multiple sclerosis pathogenesis. Brain: A journal of neurology. 2006; 129(Pt 1):212-23. doi:10.1093/brain/awh655 PMID: 16230319.
22. Teitelbaum D, Fridkis-Hareli M, Arnon R, Sela M. Copolymer 1 inhibits chronic relapsing experimental allergic encephalomyelitis induced by proteolipid protein (PLP) peptides in mice and interferes with PLP-specific T cell responses. Journal of neuroimmunology. 1996; 64(2):209-17. PMID: 8632064.
23. Yednock TA, Cannon C, Fritz LC, Sanchez-Madrid F, Steinman L, Karin N. Prevention of experimental autoimmune encephalomyelitis by antibodies against alpha 4 beta 1 integrin. Nature. 1992; 356 (6364):63-6. doi:10.1038/356063a0 PMID: 1538783.
24. Webb M, Tham CS, Lin FF, Lariosa-Willingham K, Yu N, Hale J, et al. Sphingosine 1-phosphate receptor agonists attenuate relapsing-remitting experimental autoimmune encephalitis in SJL mice. Journal of neuroimmunology. 2004; 153(1-2):108-21. doi:10.1016/j.jneuroim.2004.04.015 PMID: 15265669.
25. Brinkmann V, Davis MD, Heise CE, Albert R, Cottens S, Hof R, et al. The immune modulator FTY720 targets sphingosine 1-phosphate receptors. The Journal of biological chemistry. 2002; 277(24):21453- 7. doi:10.1074/jbc.C200176200 PMID: 11967257.
26. 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 pathology. 2009; 19 (2):254-66. doi:10.1111/j.1750-3639.2008.00182.x PMID: 18540945.
27. Gaengel K, Niaudet C, Hagikura K, Lavina B, Muhl L, Hofmann JJ, et al. The sphingosine-1-phosphate receptor S1PR1 restricts sprouting angiogenesis by regulating the interplay between VE-cadherin and VEGFR2. Developmental cell. 2012; 23(3):587-99. doi:10.1016/j.devcel.2012.08.005 PMID: 22975327.
28. Garcia JG, Liu F, Verin AD, Birukova A, Dechert MA, Gerthoffer WT, et al. Sphingosine 1-phosphate promotes endothelial cell barrier integrity by Edg-dependent cytoskeletal rearrangement. The Journal of clinical investigation. 2001; 108(5):689-701. doi:10.1172/JCI12450PMID: 11544274; PubMed Central PMCID: PMC209379.
29. Lee MJ, T S, Claffey KP, Ancellin N, Liu CH, Kluk M, Volpi M, Sha'afi RI, Hla T. Vascular Endothelial Cell Adherens Junction Assembly and Morphogenesis Induced by Sphingosine-1-Phosphate. Cell press. 1999; 99:301-12.
30. Sanchez T, Skoura A, Wu MT, Casserly B, Harrington EO, Hla T. Induction of vascular permeability by the sphingosine-1-phosphate receptor-2 (S1P2R) and its downstream effectors ROCK and PTEN. Arteriosclerosis, thrombosis, and vascular biology. 2007; 27(6):1312-8. doi:10.1161/ATVBAHA.107. 143735 PMID: 17431187.
31. Zhang W, An J, Jawadi H, Siow DL, Lee JF, Zhao J, et al. Sphingosine-1-phosphate receptor-2 mediated NFkappaB activation contributes to tumor necrosis factor-alpha induced VCAM-1 and ICAM-1 expression in endothelial cells. Prostaglandins & other lipid mediators. 2013; 106:62-71. PMID: 23770055; PubMed Central PMCID: PMC3844125.
32. Rutherford C, Childs S, Ohotski J, McGlynn L, Riddick M, MacFarlane S, et al. Regulation of cell survival by sphingosine-1-phosphate receptor S1P1 via reciprocal ERK-dependent suppression of Bim and PI-3-kinase/protein kinase C-mediated upregulation of Mcl-1. Cell death & disease. 2013; 4:e927. doi:10.1038/cddis.2013.455PMID: 24263101; PubMed Central PMCID: PMC3847331.
33. Kono M, Mi Y, Liu Y, Sasaki T, Allende ML, Wu YP, et al. The sphingosine-1-phosphate receptors S1P1, S1P2, and S1P3 function coordinately during embryonic angiogenesis. The Journal of biological chemistry. 2004; 279(28):29367-73. doi:10.1074/jbc.M403937200 PMID: 15138255.
34. Singleton PA, Dudek SM, Chiang ET, Garcia JG. Regulation of sphingosine 1-phosphate-induced endothelial cytoskeletal rearrangement and barrier enhancement by S1P1 receptor, PI3 kinase, Tiam1/Rac1, and alpha-actinin. FASEB journal: official publication of the Federation of American Societies for Experimental Biology. 2005; 19(12):1646-56. doi:10.1096/fj.05-3928com PMID: 16195373.
35. Bigaud M, Guerini D, Billich A, Bassilana F, Brinkmann V. Second generation S1P pathway modulators: Research strategies and clinical developments. Biochimica et biophysica acta. 2013. doi:10.1016/j.bbalip.2013.11.001 PMID: 24239768.
36. Bazzoni G, Dejana E. Endothelial cell-to-cell junctions: molecular organization and role in vascular homeostasis. Physiological reviews. 2004; 84(3):869-901. doi:10.1152/physrev.00035.2003 PMID: 15269339.
37. Cruz-Orengo L, Daniels BP, Dorsey D, Basak SA, Grajales-Reyes JG, McCandless EE, et al. Enhanced sphingosine-1-phosphate receptor 2 expression underlies female CNS autoimmunity susceptibility. The Journal of clinical investigation. 2014; 124(6):2571-84. doi:10.1172/JCI73408 PMID: 24812668; PubMed Central PMCID: PMC4089451.
38. Du J, Zeng C, Li Q, Chen B, Liu H, Huang X, et al. LPS and TNF-alpha induce expression of sphingosine- 1-phosphate receptor-2 in human microvascular endothelial cells. Pathology, research and practice. 2012; 208(2):82-8. PMID: 22244964.
39. Prager B, Spampinato SF, Ransohoff RM. Sphingosine 1-phosphate signaling at the blood-brain barrier. Trends in molecular medicine. 2015; 21(6):354-63. doi:10.1016/j.molmed.2015.03.006 PMID: 25939882.
40. Coomber BL, Stewart PA. Three-dimensional reconstruction of vesicles in endothelium of blood-brain barrier versus highly permeable microvessels. The Anatomical record. 1986; 215(3):256-61. doi:10.1002/ar.1092150308 PMID: 3740465.
41. Fujino M, Funeshima N, Kitazawa Y, Kimura H, Amemiya H, Suzuki S, et al. Amelioration of experimental autoimmune encephalomyelitis in Lewis rats by FTY720 treatment. The Journal of pharmacology and experimental therapeutics. 2003; 305(1):70-7. doi:10.1124/jpet.102.045658 PMID: 12649354.
42. Murata N, Sato K, Kon J, Tomura H, Yanagita M, Kuwabara A, et al. Interaction of sphingosine 1-phosphate with plasma components, including lipoproteins, regulates the lipid receptor-mediated actions. The Biochemical journal. 2000; 352 Pt 3:809-15. PMID: 11104690; PubMed Central PMCID: PMC1221521.
43. Galicia-Rosas G, Pikor N, Schwartz JA, Rojas O, Jian A, Summers-Deluca L, et al. A sphingosine-1- phosphate receptor 1-directed agonist reduces central nervous system inflammation in a plasmacytoid dendritic cell-dependent manner. Journal of immunology. 2012; 189(7):3700-6. doi:10.4049/jimmunol.1102261 PMID: 22933630.
44. Brinkmann V, Cyster JG, Hla T. FTY720: sphingosine 1-phosphate receptor-1 in the control of lymphocyte egress and endothelial barrier function. American journal of transplantation: official journal of the American Society of Transplantation and the American Society of Transplant Surgeons. 2004; 4 (7):1019-25. doi:10.1111/j.1600-6143.2004.00476.x PMID: 15196057.
45. Mullershausen F, Zecri F, Cetin C, Billich A, Guerini D, Seuwen K. Persistent signaling induced by FTY720-phosphate is mediated by internalized S1P1 receptors. Nature chemical biology. 2009; 5 (6):428-34. doi:10.1038/nchembio.173 PMID: 19430484.
46. Oo ML, Thangada S, Wu MT, Liu CH, Macdonald TL, Lynch KR, et al. Immunosuppressive and antiangiogenic sphingosine 1-phosphate receptor-1 agonists induce ubiquitinylation and proteasomal degradation of the receptor. The Journal of biological chemistry. 2007; 282(12):9082-9. doi:10.1074/jbc.M610318200 PMID: 17237497.
47. Quancard J, Bollbuck B, Janser P, Angst D, Berst F, Buehlmayer P, et al. A potent and selective S1P (1) antagonist with efficacy in experimental autoimmune encephalomyelitis. Chemistry & biology. 2012; 19(9):1142-51. doi:10.1016/j.chembiol.2012.07.016 PMID: 22999882.
48. Alvarez JI, Katayama T, Prat A. Glial influence on the blood brain barrier. Glia. 2013; 61(12):1939-58. doi:10.1002/glia.22575 PMID: 24123158; PubMed Central PMCID: PMC4068281.
49. Nair A, Frederick TJ, Miller SD. Astrocytes in multiple sclerosis: A product of their environment. Cellular and molecular life sciences: CMLS. 2008; 65(17):2702-20. doi:10.1007/s00018-008-8059-5 PMID: 18516496; PubMed Central PMCID: PMC2858316.
50. Kooij G, Mizee MR, van Horssen J, Reijerkerk A, Witte ME, Drexhage JA, et al. Adenosine triphosphate- binding cassette transporters mediate chemokine (C-C motif) ligand 2 secretion from reactive astrocytes: relevance to multiple sclerosis pathogenesis. Brain: A journal of neurology. 2011; 134(Pt 2):555-70. doi:10.1093/brain/awq330 PMID: 21183485.
51. Mizee MR, Nijland PG, vanderPol SM, Drexhage JA, van Het Hof B, Mebius R, et al. Astrocyte-derived retinoic acid: A novel regulator of blood-brain barrier function in multiple sclerosis. Acta neuropathologica. 2014; 128(5):691-703. doi:10.1007/s00401-014-1335-6 PMID: 25149081.
52. Brana C, Frossard MJ, Pescini Gobert R, Martinier N, Boschert U, Seabrook TJ. Immunohistochemical detection of sphingosine-1-phosphate receptor 1 and 5 in human multiple sclerosis lesions. Neuropathology and applied neurobiology. 2014; 40(5):564-78. doi:10.1111/nan.12048 PMID: 23551178.
53. Van Doorn R, Van Horssen J, Verzijl D, Witte M, Ronken E, Van Het Hof B, et al. Sphingosine 1-phosphate receptor 1 and 3 are upregulated in multiple sclerosis lesions. Glia. 2010; 58(12):1465-76. doi:10.1002/glia.21021 PMID: 20648639.
54. 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. Proceedings of the National Academy of Sciences of the United States of America. 2011; 108 (2):751-6. doi:10.1073/pnas.1014154108 PMID: 21177428; PubMed Central PMCID: PMC3021041.
55. Colombo E, Di Dario M, Capitolo E, Chaabane L, Newcombe J, Martino G, et al. Fingolimod may support neuroprotection via blockade of astrocyte nitric oxide. Annals of neurology. 2014; 76(3):325-37. doi:10.1002/ana.24217 PMID: 25043204.
56. Hla T, Maciag T. An abundant transcript induced in differentiating human endothelial cells encodes a polypeptide with structural similarities to G-protein-coupled receptors. The Journal of biological chemistry. 1990; 265(16):9308-13. PMID: 2160972.
57. Nishihara H, Shimizu F, Sano Y, Takeshita Y, Maeda T, Abe M, et al. Fingolimod prevents blood-brain barrier disruption induced by the sera from patients with multiple sclerosis. PLoS One. 2015; 10(3): e0121488. doi:10.1371/journal.pone.0121488 PMID: 25774903; PubMed Central PMCID: PMC4361641.
58. Zhan Y, Xu Y, Lew AM. The regulation of the development and function of dendritic cell subsets by GMCSF: more than a hematopoietic growth factor. Molecular immunology. 2012; 52(1):30-7. PMID: 22580403.
59. Codarri L, Gyulveszi G, Tosevski V, Hesske L, Fontana A, Magnenat L, et al. RORgammat drives production of the cytokine GM-CSF in helper T cells, which is essential for the effector phase of autoimmune neuroinflammation. Nature immunology. 2011; 12(6):560-7. doi:10.1038/ni.2027 PMID: 21516112.
60. McGeachy MJ. GM-CSF: The secret weapon in the T(H)17 arsenal. Nature immunology. 2011; 12 (6):521-2. doi:10.1038/ni.2044 PMID: 21587311.
61. Mortha A, Chudnovskiy A, Hashimoto D, Bogunovic M, Spencer SP, Belkaid Y, et al. Microbiota-dependent crosstalk between macrophages and ILC3 promotes intestinal homeostasis. Science. 2014; 343 (6178):1249288. doi:10.1126/science.1249288 PMID: 24625929.
62. Schabitz WR, Kruger C, Pitzer C, Weber D, Laage R, Gassler N, et al. A neuroprotective function for the hematopoietic protein granulocyte-macrophage colony stimulating factor (GM-CSF). Journal of cerebral blood flow and metabolism: official journal of the International Society of Cerebral Blood Flow and Metabolism. 2008; 28(1):29-43. doi:10.1038/sj.jcbfm.9600496 PMID: 17457367.
63. Tisato V, Secchiero P, Rimondi E, Gianesini S, Menegatti E, Casciano F, et al. GM-CSF exhibits antiinflammatory activity on endothelial cells derived from chronic venous disease patients. Mediators of inflammation. 2013; 2013:561689. doi:10.1155/2013/561689 PMID: 24327798; PubMed Central PMCID: PMC3845402.
64. Sanna MG, Wang SK, Gonzalez-Cabrera PJ, Don A, Marsolais D, Matheu MP, et al. Enhancement of capillary leakage and restoration of lymphocyte egress by a chiral S1P1 antagonist in vivo. Nature chemical biology. 2006; 2(8):434-41. doi:10.1038/nchembio804 PMID: 16829954.