Vascular biology: The role of sphingosine 1-phosphate in both the resting state and inflammation

Journal of Cellular and Molecular Medicine

Volumn 14, Issue 9, 2010, Pages 2211-2222

  Swan, David J ^a   Kirby, John A ^a   Ali, Simi ^a  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

Endothelial cell; Inflammation; Lymphocyte; Sphingosine 1 phosphate

Indexed keywords

DRUG DERIVATIVE; LYSOPHOSPHOLIPID; SPHINGOSINE; SPHINGOSINE 1 PHOSPHATE; SPHINGOSINE 1 PHOSPHATE RECEPTOR; SPHINGOSINE 1-PHOSPHATE;

ANIMAL; BLOOD VESSEL; CHEMISTRY; HUMAN; INFLAMMATION; METABOLISM; PATHOLOGY; REST; REVIEW; VASCULAR ENDOTHELIUM;

ANIMALS; BLOOD VESSELS; ENDOTHELIUM, VASCULAR; HUMANS; INFLAMMATION; LYSOPHOSPHOLIPIDS; RECEPTORS, LYSOSPHINGOLIPID; REST; SPHINGOSINE;

MAMMALIA;

EID: 78649350463     PISSN: 15821838     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1582-4934.2010.01136.x     Document Type: Review

References (109)

1. Takuwa Y, Okamoto Y, Yoshioka K, et al. Sphingosine-1-phosphate signaling and biological activities in the cardiovascular system. Biochim Biophys Acta. 2008; 1781: 483-8.
2. Limaye V. The role of sphingosine kinase and sphingosine-1-phosphate in the regulation of endothelial cell biology. Endothelium. 2008; 15: 101-12.
3. Takabe K, Paugh SW, Milstien S, et al. "Inside-out" signaling of sphingosine-1-phosphate: therapeutic targets. Pharmacol Rev. 2008; 60: 181-95.
4. Lynch KR, Macdonald TL. Sphingosine 1-phosphate chemical biology. Biochim Biophys Acta. 2008; 1781: 508-12.
5. Kihara A, Mitsutake S, Mizutani Y, et al. Metabolism and biological functions of two phosphorylated sphingolipids, sphingosine 1-phosphate and ceramide 1-phosphate. Prog Lipid Res. 2007; 46: 126-44.
6. Hannun YA, Obeid LM. Principles of bioactive lipid signalling: lessons from sphingolipids. Nat Rev Mol Cell Biol. 2008; 9: 139-50.
7. Alvarez SE, Milstien S, Spiegel S. Autocrine and paracrine roles of sphingosine-1-phosphate. Trends Endocrinol Metab. 2007; 18: 300-7.
8. Hait NC, Oskeritzian CA, Paugh SW, et al. Sphingosine kinases, sphingosine 1-phosphate, apoptosis and diseases. Biochim Biophys Acta. 2006; 1758: 2016-26.
9. Taha TA, Hannun YA, Obeid LM. Sphingosine kinase: biochemical and cellular regulation and role in disease. J Biochem Mol Biol. 2006; 39: 113-31.
10. Xia P, Wang L, Moretti PA, et al. Sphingosine kinase interacts with TRAF2 and dissects tumor necrosis factor-alpha signaling. J Biol Chem. 2002; 277: 7996-8003.
11. Sarkar S, Maceyka M, Hait NC, et al. Sphingosine kinase 1 is required for migration, proliferation and survival of MCF-7 human breast cancer cells. FEBS Lett. 2005; 579: 5313-7.
12. Brindley DN, English D, Pilquil C, et al. Lipid phosphate phosphatases regulate signal transduction through glycerolipids and sphingolipids. Biochim Biophys Acta. 2002; 1582: 33-44.
13. Sigal YJ, McDermott MI, Morris AJ. Integral membrane lipid phosphatases/phosphotransferases: common structure and diverse functions. Biochem J. 2005; 387: 281-93.
14. Ikeda M, Kihara A, Igarashi Y. Sphingosine-1-phosphate lyase SPL is an endoplasmic reticulum-resident, integral membrane protein with the pyridoxal 5'-phosphate binding domain exposed to the cytosol. Biochem Biophys Res Commun. 2004; 325: 338-43.
15. Bandhuvula P, Saba JD. Sphingosine-1-phosphate lyase in immunity and cancer: silencing the siren. Trends Mol Med. 2007; 13: 210-7.
16. Yatomi Y, Yamamura S, Ruan F, et al. Sphingosine 1-phosphate induces platelet activation through an extracellular action and shares a platelet surface receptor with lysophosphatidic acid. J Biol Chem. 1997; 272: 5291-7.
17. Hanel P, Andreani P, Graler MH. Erythrocytes store and release sphingosine 1-phosphate in blood. FASEB J. 2007; 21: 1202-9.
18. Schwab SR, Pereira JP, Matloubian M, et al. Lymphocyte sequestration through S1P lyase inhibition and disruption of S1P gradients. Science. 2005; 309: 1735-9.
19. Sciorra VA, Morris AJ. Roles for lipid phosphate phosphatases in regulation of cellular signaling. Biochim Biophys Acta. 2002; 1582: 45-51.
20. Sato K, Malchinkhuu E, Horiuchi Y, et al. Critical role of ABCA1 transporter in sphingosine 1-phosphate release from astrocytes. J Neurochem. 2007; 103: 2610-9.
21. Mitra P, Oskeritzian CA, Payne SG, et al. Role of ABCC1 in export of sphingosine-1-phosphate from mast cells. Proc Natl Acad Sci USA. 2006; 103: 16394-9.
22. Kobayashi N, Yamaguchi A, Nishi T. Characterization of the ATP-dependent sphingosine 1-phosphate transporter in rat erythrocytes. J Biol Chem. 2009; 284: 21192-200.
23. Nieuwenhuis B, Luth A, Chun J, et al. Involvement of the ABC-transporter ABCC1 and the sphingosine 1-phosphate receptor subtype S1P(3) in the cytoprotection of human fibroblasts by the glucocorticoid dexamethasone. J Mol Med. 2009; 87: 645-57.
24. Boujaoude LC, Bradshaw-Wilder C, Mao C, et al. Cystic fibrosis transmembrane regulator regulates uptake of sphingoid base phosphates and lysophosphatidic acid: modulation of cellular activity of sphingosine 1-phosphate. J Biol Chem. 2001; 276: 35258-64.
25. Hobson JP, Rosenfeldt HM, Barak LS, et al. Role of the sphingosine-1-phosphate receptor EDG-1 in PDGFinduced cell motility. Science. 2001; 291: 1800-3.
26. Rosen H, Goetzl EJ. Sphingosine 1-phosphate and its receptors: an autocrine and paracrine network. Nat Rev Immunol. 2005; 5: 560-70.
27. Wang W, Graeler MH, Goetzl EJ. Type 4 sphingosine 1-phosphate G protein-coupled receptor (S1P4) transduces S1P effects on T cell proliferation and cytokine secretion without signaling migration. FASEB J. 2005; 19: 1731-3.
28. Jenne CN, Enders A, Rivera R, et al. T-bet-dependent S1P5 expression in NK cells promotes egress from lymph nodes and bone marrow. J Exp Med. 2009; 206: 2469-81.
29. Rosen H, Gonzalez-Cabrera P, Marsolais D, et al. Modulating tone: the overture of S1P receptor immunotherapeutics. Immunol Rev. 2008; 223: 221-35.
30. Mandala S, Hajdu R, Bergstrom J, et al. Alteration of lymphocyte trafficking by sphingosine-1-phosphate receptor agonists. Science. 2002; 296: 346-9.
31. Brinkmann V, Davis MD, Heise CE, et al. The immune modulator FTY720 targets sphingosine 1-phosphate receptors. J Biol Chem. 2002; 277: 21453-7.
32. Sanna MG, Liao J, Jo E, et al. Sphingosine 1-phosphate (S1P) receptor subtypes S1P1 and S1P3, respectively, regulate lymphocyte recirculation and heart rate. J Biol Chem. 2004; 279: 13839-48.
33. Ishii I, Fukushima N, Ye X, et al. Lysophospholipid receptors: signaling and biology. Annu Rev Biochem. 2004; 73: 321-54.
34. Rosen H, Liao J. Sphingosine 1-phosphate pathway therapeutics: a lipid ligandreceptor paradigm. Curr Opin Chem Biol. 2003; 7: 461-8.
35. Gonzalez-Cabrera PJ, Hla T, et al. Mapping pathways downstream of sphingosine 1-phosphate subtype 1 by differential chemical perturbation and proteomics. J Biol Chem. 2007; 282: 7254-64.
36. Spiegel S, Milstien S. Functions of a new family of sphingosine-1-phosphate receptors. Biochim Biophys Acta. 2000; 1484: 107-16.
37. Pyne S, Pyne NJ. Sphingosine 1-phosphate signalling in mammalian cells. Biochem J. 2000; 349: 385-402.
38. Hait NC, Allegood J, Maceyka M, et al. Regulation of histone acetylation in the nucleus by sphingosine-1-phosphate. Science. 2009; 325: 1254-7.
39. Liu Y, Wada R, Yamashita T, et al. Edg-1, the G protein-coupled receptor for sphingosine-1-phosphate, is essential for vascular maturation. J Clin Invest. 2000; 106: 951-61.
40. Matloubian M, Lo CG, Cinamon G, et al. Lymphocyte egress from thymus and peripheral lymphoid organs is dependent on S1P receptor 1. Nature. 2004; 427: 355-60.
41. Singleton PA, Dudek SM, Chiang ET, et al. Regulation of sphingosine 1-phosphate-induced endothelial cytoskeletal rearrangement and barrier enhancement by S1P1 receptor, PI3 kinase, Tiam1/Rac1, and alpha-actinin. FASEB J. 2005; 19: 1646-56.
42. Sanna MG, Wang SK, Gonzalez-Cabrera PJ, et al. Enhancement of capillary leakage and restoration of lymphocyte egress by a chiral S1P1 antagonist in vivo. Nat Chem Biol. 2006; 2: 434-41.
43. Lee MJ, Evans M, Hla T. The inducible G protein-coupled receptor edg-1 signals via the G(i)/mitogen-activated protein kinase pathway. J Biol Chem. 1996; 271: 11272-9.
44. Mullershausen F, Zecri F, Cetin C, et al. Persistent signaling induced by FTY720-phosphate is mediated by internalized S1P1 receptors. Nat Chem Biol. 2009; 5: 428-34.
45. Watterson KR, Johnston E, Chalmers C, et al. Dual regulation of EDG1/S1P(1) receptor phosphorylation and internalization by protein kinase C and G-proteincoupled receptor kinase 2. J Biol Chem. 2002; 277: 5767-77.
46. Oo ML, Thangada S, Wu MT, et al. Immunosuppressive and anti-angiogenic sphingosine 1-phosphate receptor-1 agonists induce ubiquitinylation and proteasomal degradation of the receptor. J Biol Chem. 2007; 282: 9082-9.
47. Liao JJ, Huang MC, Graler M, et al. Distinctive T cell-suppressive signals from nuclearized type 1 sphingosine 1-phosphate G protein-coupled receptors. J Biol Chem. 2007; 282: 1964-72.
48. Brinkmann V, Cyster JG, Hla T. FTY720: sphingosine 1-phosphate receptor-1 in the control of lymphocyte egress and endothelial barrier function. Am J Transplant. 2004; 4: 1019-25.
49. Rosen H, Sanna MG, Cahalan SM, et al. Tipping the gatekeeper: S1P regulation of endothelial barrier function. Trends Immunol. 2007; 28: 102-7.
50. Ishii I, Friedman B, Ye X, et al. Selective loss of sphingosine 1-phosphate signaling with no obvious phenotypic abnormality in mice lacking its G protein-coupled receptor, LP(B3)/EDG-3. J Biol Chem. 2001; 276: 33697-704.
51. Takuwa Y, Okamoto Y, Yoshioka K, et al. Sphingosine-1-phosphate signaling and biological activities in the cardiovascular system. Biochim Biophys Acta. 2008; 1781: 483-8.
52. Hla T, Venkataraman K, Michaud J. The vascular S1P gradient-Cellular sources and biological significance. Biochim Biophys Acta. 2008; 1781: 477-82.
53. Murata N, Sato K, Kon J, et al. Interaction of sphingosine 1-phosphate with plasma components, including lipoproteins, regulates the lipid receptor-mediated actions. Biochem J. 2000; 352: 809-15.
54. Pappu R, Schwab SR, Cornelissen I, et al. Promotion of lymphocyte egress into blood and lymph by distinct sources of sphingosine-1-phosphate. Science. 2007; 316: 295-8.
55. Bode C, Sensken SC, Peest U, et al. Erythrocytes serve as a reservoir for cellular and extracellular sphingosine 1-phosphate. J Cell Biochem. 2010; 109: 1232-43.
56. Venkataraman K, Lee YM, Michaud J, et al. Vascular endothelium as a contributor of plasma sphingosine 1-phosphate. Circ Res. 2008; 102: 669-76.
57. Pham TH, Baluk P, Xu Y, et al. Lymphatic endothelial cell sphingosine kinase activity is required for lymphocyte egress and lymphatic patterning. J Exp Med. 2010; 207: 17-27, S1-4.
58. Schwab SR, Cyster JG. Finding a way out: lymphocyte egress from lymphoid organs. Nat Immunol. 2007; 8: 1295-301.
59. Lo CG, Xu Y, Proia RL, et al. Cyclical modulation of sphingosine-1-phosphate receptor 1 surface expression during lymphocyte recirculation and relationship to lymphoid organ transit. J Exp Med. 2005; 201: 291-301.
60. Dustin ML, Chakraborty AK. Tug of war at the exit door. Immunity. 2008; 28: 15-7.
61. Grigorova IL, Schwab SR, Phan TG, et al. Cortical sinus probing, S1P1-dependent entry and flow-based capture of egressing T cells. Nat Immunol. 2009; 10: 58-65.
62. Shiow LR, Rosen DB, Brdickova N, et al. CD69 acts downstream of interferonalpha/beta to inhibit S1P1 and lymphocyte egress from lymphoid organs. Nature. 2006; 440: 540-4.
63. Ledgerwood LG, Lal G, Zhang N, et al. The sphingosine 1-phosphate receptor 1 causes tissue retention by inhibiting the entry of peripheral tissue T lymphocytes into afferent lymphatics. Nat Immunol. 2008; 9: 42-53.
64. Predescu SA, Predescu DN, Malik AB. Molecular determinants of endothelial transcytosis and their role in endothelial permeability. Am J Physiol Lung Cell Mol Physiol. 2007; 293: L823-42.
65. Bazzoni G, Dejana E. Endothelial cell-to-cell junctions: molecular organization and role in vascular homeostasis. Physiol Rev. 2004; 84: 869-901.
66. Garcia JG, Liu F, Verin AD, et al. Sphingosine 1-phosphate promotes endothelial cell barrier integrity by Edg-dependent cytoskeletal rearrangement. J Clin Invest. 2001; 108: 689-701.
67. Mehta D, Konstantoulaki M, Ahmmed GU, et al. Sphingosine 1-phosphateinduced mobilization of intracellular Ca2+ mediates rac activation and adherens junction assembly in endothelial cells. J Biol Chem. 2005; 280: 17320-8.
68. Sun X, Shikata Y, Wang L, et al. Enhanced interaction between focal adhesion and adherens junction proteins: involvement in sphingosine 1-phosphateinduced endothelial barrier enhancement. Microvasc Res. 2009; 77: 304-13.
69. Lee JF, Zeng Q, Ozaki H, et al. Dual roles of tight junction-associated protein, zonula occludens-1, in sphingosine 1-phosphate-mediated endothelial chemotaxis and barrier integrity. J Biol Chem. 2006; 281: 29190-200.
70. van Nieuw Amerongen GP, Natarajan K, Yin G, et al. GIT1 mediates thrombin signaling in endothelial cells: role in turnover of RhoA-type focal adhesions. Circ Res. 2004; 94: 1041-9.
71. Sanchez T, Skoura A, Wu MT, et al. Induction of vascular permeability by the sphingosine-1-phosphate receptor-2 (S1P2R) and its downstream effectors ROCK and PTEN. Arterioscler Thromb Vasc Biol. 2007; 27: 1312-8.
72. Olsson AK, Dimberg A, Kreuger J, et al. VEGF receptor signalling - in control of vascular function. Nat Rev Mol Cell Biol. 2006; 7: 359-71.
73. Walshe TE, Saint-Geniez M, Maharaj AS, et al. TGF-beta is required for vascular barrier function, endothelial survival and homeostasis of the adult microvasculature. PLoS One. 2009; 4: e5149. doi:10.1371/journal.pone.0005149.
74. Letterio JJ, Roberts AB. Regulation of immune responses by TGF-beta. Annu Rev Immunol. 1998; 16: 137-61.
75. Tanimoto T, Jin ZG, Berk BC. Transactivation of vascular endothelial growth factor (VEGF) receptor Flk-1/KDR is involved in sphingosine 1-phosphate-stimulated phosphorylation of Akt and endothelial nitric-oxide synthase (eNOS). J Biol Chem. 2002; 277: 42997-3001.
76. Igarashi J, Erwin PA, Dantas AP, et al. VEGF induces S1P1 receptors in endothelial cells: implications for cross-talk between sphingolipid and growth factor receptors. Proc Natl Acad Sci USA. 2003; 100: 10664-9.
77. Sauer B, Vogler R, von Wenckstern H, et al. Involvement of Smad signaling in sphingosine 1-phosphate-mediated biological responses of keratinocytes. J Biol Chem. 2004; 279: 38471-9.
78. Xin C, Ren S, Kleuser B, et al. Sphingosine 1-phosphate cross-activates the Smad signaling cascade and mimics transforming growth factor-beta-induced cell responses. J Biol Chem. 2004; 279: 35255-62.
79. Pham TH, Okada T, Matloubian M, et al. S1P1 receptor signaling overrides retention mediated by G alpha i-coupled receptors to promote T cell egress. Immunity. 2008; 28: 122-33.
80. Graeler M, Shankar G, Goetzl EJ. Cutting edge: suppression of T cell chemotaxis by sphingosine 1-phosphate. J Immunol. 2002; 169: 4084-7.
81. Ali S, Robertson H, Wain JH, et al. A non-glycosaminoglycan-binding variant of CC chemokine ligand 7 (monocyte chemoattractant protein-3) antagonizes chemokine-mediated inflammation. J Immunol. 2005; 175: 1257-66.
82. Ryser MF, Ugarte F, Lehmann R, et al. S1P(1) overexpression stimulates S1Pdependent chemotaxis of human CD34+ hematopoietic progenitor cells but strongly inhibits SDF-1/CXCR4-dependent migration and in vivo homing. Mol Immunol. 2008; 46: 166-71.
83. Whetton AD, Lu Y, Pierce A, et al. Lysophospholipids synergistically promote primitive hematopoietic cell chemotaxis via a mechanism involving Vav 1. Blood. 2003; 102: 2798-802.
84. Suzuki S, Li XK, Enosawa S, Shinomiya T. A new immunosuppressant, FTY720, induces bcl-2-associated apoptotic cell death in human lymphocytes. Immunology. 1996; 89: 518-23.
85. Graler MH, Goetzl EJ. The immunosuppressant FTY720 down-regulates sphingosine 1-phosphate G-protein-coupled receptors. FASEB J. 2004; 18: 551-3.
86. Wei SH, Rosen H, Matheu MP, et al. Sphingosine 1-phosphate type 1 receptor agonism inhibits transendothelial migration of medullary T cells to lymphatic sinuses. Nat Immunol. 2005; 6: 1228-35.
87. Sanchez T, Estrada-Hernandez T, Paik JH, et al. Phosphorylation and action of the immunomodulator FTY720 inhibits vascular endothelial cell growth factorinduced vascular permeability. J Biol Chem. 2003; 278: 47281-90.
88. Budde K, R LS, Nashan B, et al. Pharmacodynamics of single doses of the novel immunosuppressant FTY720 in stable renal transplant patients. Am J Transplant. 2003; 3: 846-54.
89. Kahan BD, Karlix JL, Ferguson RM, et al. Pharmacodynamics, pharmacokinetics, and safety of multiple doses of FTY720 in stable renal transplant patients: a multicenter, randomized, placebo-controlled, phase I study. Transplantation. 2003; 76: 1079-84.
90. Brinkmann V, Lynch KR. FTY720: targeting G-protein-coupled receptors for sphingosine 1-phosphate in transplantation and autoimmunity. Curr Opin Immunol. 2002; 14: 569-75.
91. Mulgaonkar S, Tedesco H, Oppenheimer F, et al. FTY720/cyclosporine regimens in de novo renal transplantation: a 1-year dose-finding study. Am J Transplant. 2006; 6: 1848-57.
92. Tedesco-Silva H, Mourad G, Kahan BD, et al. FTY720, a novel immunomodulator: efficacy and safety results from the first phase 2A study in de novo renal transplantation. Transplantation. 2005; 79: 1553-60.
93. Salvadori M, Budde K, Charpentier B, et al. FTY720 versus MMF with cyclosporine in de novo renal transplantation: a 1-year, randomized controlled trial in Europe and Australasia. Am J Transplant. 2006; 6: 2912-21.
94. Tedesco-Silva H, Pescovitz MD, Cibrik D, et al. Randomized controlled trial of FTY720 versus MMF in de novo renal transplantation. Transplantation. 2006; 82: 1689-97.
95. Brinkmann V. Sphingosine 1-phosphate receptors in health and disease: mechanistic insights from gene deletion studies and reverse pharmacology. Pharmacol Ther. 2007; 115: 84-105.
96. Koyrakh L, Roman MI, Brinkmann V, et al. The heart rate decrease caused by acute FTY720 administration is mediated by the G protein-gated potassium channel I. Am J Transplant. 2005; 5: 529-36.
97. DeAngelis T, Lublin F. Multiple sclerosis: new treatment trials and emerging therapeutic targets. Curr Opin Neurol. 2008; 21: 261-71.
98. Miron VE, Schubart A, Antel JP. Central nervous system-directed effects of FTY720 (fingolimod). J Neurol Sci. 2008; 274: 13-7.
99. Foster CA, Howard LM, Schweitzer A, 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.
100. Kappos L, Antel J, Comi G, et al. Oral fingolimod (FTY720) for relapsing multiple sclerosis. N Engl J Med. 2006; 355: 1124-40.
101. O'Connor P, Comi G, Montalban X, et al. Oral fingolimod (FTY720) in multiple sclerosis: two-year results of a phase II extension study. Neurology. 2009; 72: 73-9.
102. Kappos L, Radue EW, O'Connor P, et al. A placebo-controlled trial of oral fingolimod in relapsing multiple sclerosis. N Engl J Med. 2010; 362: 387-401.
103. Kebir H, Kreymborg K, Ifergan I, et al. Human TH17 lymphocytes promote bloodbrain barrier disruption and central nervous system inflammation. Nat Med. 2007; 13: 1173-5.
104. Tzartos JS, Friese MA, Craner MJ, et al. Interleukin-17 production in central nervous system-infiltrating T cells and glial cells is associated with active disease in multiple sclerosis. Am J Pathol. 2008; 172: 146-55.
105. Massberg S, von Andrian UH. Fingolimod and sphingosine-1-phosphate-modifiers of lymphocyte migration. N Engl J Med. 2006; 355: 1088-91.
106. Dev KK, Mullershausen F, Mattes H, et al. Brain sphingosine-1-phosphate receptors: implication for FTY720 in the treatment of multiple sclerosis. Pharmacol Ther. 2008; 117: 77-93.
107. Brinkmann V. FTY720 (fingolimod) in Multiple Sclerosis: therapeutic effects in the immune and the central nervous system. Br J Pharmacol. 2009; 158: 1173-82.
108. Visentin B, Vekich JA, Sibbald BJ, et al. Validation of an anti-sphingosine-1-phosphate antibody as a potential therapeutic in reducing growth, invasion, and angiogenesis in multiple tumor lineages. Cancer Cell. 2006; 9: 225-38.
109. Billich A, Urtz N, Reuschel R, et al. Sphingosine kinase 1 is essential for proteinase-activated receptor-1 signalling in epithelial and endothelial cells. Int J Biochem Cell Biol. 2009; 41: 1547-55.