Advertisement

S1P Control of Endothelial Integrity

  • Yuquan Xiong
  • Timothy HlaEmail author
Chapter
Part of the Current Topics in Microbiology and Immunology book series (CT MICROBIOLOGY, volume 378)

Abstract

Sphingosine 1-phosphate (S1P), a lipid mediator produced by sphingolipid metabolism, promotes endothelial cell spreading, vascular maturation/stabilization, and barrier function. S1P is present at high concentrations in the circulatory system, whereas in tissues its levels are low. This so-called vascular S1P gradient is essential for S1P to regulate much physiological and pathophysiological progress such as the modulation of vascular permeability. Cellular sources of S1P in blood has only recently begun to be identified. In this review, we summarize the current understanding of S1P in regulating vascular integrity. In particular, we discuss the recent discovery of the endothelium-protective functions of HDL-bound S1P which is chaperoned by apolipoprotein M.

Keywords

Acute Lung Injury Myosin Light Chain Kinase Dengue Hemorrhagic Fever Myosin Light Chain Phosphorylation Vascular Barrier 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Abbreviations

AJ

Adherens junctions

AKI

Acute kidney injury

ALI

Acute lung injury

ApoM

Apolipoprotein M

BAL

Bronchoalveolar lavage

EC

Endothelial cells

eNOS

Endothelial nitric oxide synthase

GEFs

Guanine nucleotide exchange factors

GJ

Gap junctions

HDL

High-density lipoprotein

HUVEC

Human umbilical vein endothelial cells

I/R

Ischemia-reperfusion

JAM

Junctional adhesion molecules

LDL

Low-density lipoprotein

LPP3

Lysophospholipid phosphatase 3

LPs

Lysophospholipids

LPS

Lipopolysaccharide

MLC

Myosin light chain

MLCK

Myosin light chain kinase

PAF

Platelet-activating factor

PE

Phosphatidylethanolamine

PECAM-1

Platelet-endothelial cell adhesion molecule-1

RBC

Red blood cells

S1P

Sphingosine 1-phosphate

SM

Sphingomyelin

Spns2

Spinster 2

SPP

S1P phosphatases

TER

Transmonolayer electrical resistance

TJ

Tight junctions

VE-cadherin

Vascular endothelial cadherin

VLDL

Very low-density lipoprotein

ZO

Zona occludens proteins

References

  1. Allende ML, Sasaki T, Kawai H, Olivera A, Mi Y, van Echten-Deckert G, Hajdu R, Rosenbach M, Keohane CA, Mandala S, Spiegel S, Proia RL (2004) Mice deficient in sphingosine kinase 1 are rendered lymphopenic by FTY720. J Biol Chem 279(50):52487–52492. doi: 10.1074/jbc.M406512200, M406512200 [pii]Google Scholar
  2. Ancellin N, Colmont C, Su J, Li Q, Mittereder N, Chae SS, Stefansson S, Liau G, Hla T (2002) Extracellular export of sphingosine kinase-1 enzyme. Sphingosine 1-phosphate generation and the induction of angiogenic vascular maturation. J Biol Chem 277(8):6667–6675. doi: 10.1074/jbc.M102841200, M102841200 [pii]Google Scholar
  3. Anelli V, Bassi R, Tettamanti G, Viani P, Riboni L (2005) Extracellular release of newly synthesized sphingosine-1-phosphate by cerebellar granule cells and astrocytes. J Neurochem 92(5):1204–1215. doi: 10.1111/j.1471-4159.2004.02955.x, JNC2955 [pii]Google Scholar
  4. Arce FT, Whitlock JL, Birukova AA, Birukov KG, Arnsdorf MF, Lal R, Garcia JG, Dudek SM (2008) Regulation of the micromechanical properties of pulmonary endothelium by S1P and thrombin: role of cortactin. Biophys J 95(2):886–894. doi: 10.1529/biophysj.107.127167, S0006-3495(08)70263-7 [pii]Google Scholar
  5. Argraves KM, Gazzolo PJ, Groh EM, Wilkerson BA, Matsuura BS, Twal WO, Hammad SM, Argraves WS (2008) High density lipoprotein-associated sphingosine 1-phosphate promotes endothelial barrier function. J Biol Chem 283(36):25074–25081. doi: 10.1074/jbc.M801214200, M801214200 [pii]Google Scholar
  6. Argraves KM, Sethi AA, Gazzolo PJ, Wilkerson BA, Remaley AT, Tybjaerg-Hansen A, Nordestgaard BG, Yeatts SD, Nicholas KS, Barth JL, Argraves WS (2011) S1P, dihydro-S1P and C24:1-ceramide levels in the HDL-containing fraction of serum inversely correlate with occurrence of ischemic heart disease. Lipids Health Dis 10:70. doi: 10.1186/1476-511X-10-70, 1476-511X-10-70 [pii]
  7. Bandhuvula P, Saba JD (2007) Sphingosine-1-phosphate lyase in immunity and cancer: silencing the siren. Trends Mol Med 13(5):210–217. doi: 10.1016/j.molmed.2007.03.005, S1471-4914(07)00060-3 [pii]Google Scholar
  8. Bassi R, Anelli V, Giussani P, Tettamanti G, Viani P, Riboni L (2006) Sphingosine-1-phosphate is released by cerebellar astrocytes in response to bFGF and induces astrocyte proliferation through Gi-protein-coupled receptors. Glia 53(6):621–630. doi: 10.1002/glia.20324 Google Scholar
  9. Bazzoni G, Dejana E (2004) Endothelial cell-to-cell junctions: molecular organization and role in vascular homeostasis. Physiol Rev 84(3):869–901. doi: 10.1152/physrev.00035.2003, 84/3/869 [pii]Google Scholar
  10. Belvitch P, Dudek SM (2012) Role of FAK in S1P-regulated endothelial permeability. Microvasc Res 83(1):22–30. doi: 10.1016/j.mvr.2011.08.012, S0026-2862(11)00158-0 [pii] Google Scholar
  11. Berdyshev EV, Gorshkova I, Skobeleva A, Bittman R, Lu X, Dudek SM, Mirzapoiazova T, Garcia JG, Natarajan V (2009) FTY720 inhibits ceramide synthases and up-regulates dihydrosphingosine 1-phosphate formation in human lung endothelial cells. J Biol Chem 284(9):5467–5477. doi: 10.1074/jbc.M805186200, M805186200 [pii]Google Scholar
  12. Berdyshev EV, Gorshkova IA, Garcia JG, Natarajan V, Hubbard WC (2005) Quantitative analysis of sphingoid base-1-phosphates as bisacetylated derivatives by liquid chromatography-tandem mass spectrometry. Anal Biochem 339(1):129–136. doi: 10.1016/j.ab.2004.12.006, S0003-2697(04)00975-3 [pii]Google Scholar
  13. Blaho VA, Hla T (2011) Regulation of mammalian physiology, development, and disease by the sphingosine 1-phosphate and lysophosphatidic acid receptors. Chem Rev 111(10):6299–6320. doi: 10.1021/cr200273u Google Scholar
  14. Blondeau N, Lai Y, Tyndall S, Popolo M, Topalkara K, Pru JK, Zhang L, Kim H, Liao JK, Ding K, Waeber C (2007) Distribution of sphingosine kinase activity and mRNA in rodent brain. J Neurochem 103(2):509–517. doi: 10.1111/j.1471-4159.2007.04755.x, JNC4755 [pii]Google Scholar
  15. Bode C, Sensken SC, Peest U, Beutel G, Thol F, Levkau B, Li Z, Bittman R, Huang T, Tolle M, van der Giet M, Graler MH (2010) Erythrocytes serve as a reservoir for cellular and extracellular sphingosine 1-phosphate. J Cell Biochem 109(6):1232–1243. doi: 10.1002/jcb.22507 Google Scholar
  16. Bogatcheva NV, Verin AD (2008) The role of cytoskeleton in the regulation of vascular endothelial barrier function. Microvasc Res 76(3):202–207. doi: 10.1016/j.mvr.2008.06.003, S0026-2862(08)00095-2 [pii]Google Scholar
  17. Caligan TB, Peters K, Ou J, Wang E, Saba J, Merrill AH, Jr. (2000) A high-performance liquid chromatographic method to measure sphingosine 1-phosphate and related compounds from sphingosine kinase assays and other biological samples. Anal Biochem 281(1):36–44. doi: 10.1006/abio.2000.4555, S0003-2697(00)94555-X [pii]Google Scholar
  18. Camerer E, Regard JB, Cornelissen I, Srinivasan Y, Duong DN, Palmer D, Pham TH, Wong JS, Pappu R, Coughlin SR (2009) Sphingosine-1-phosphate in the plasma compartment regulates basal and inflammation-induced vascular leak in mice. J Clin Invest 119(7):1871–1879Google Scholar
  19. Carmeliet P, Lampugnani MG, Moons L, Breviario F, Compernolle V, Bono F, Balconi G, Spagnuolo R, Oosthuyse B, Dewerchin M, Zanetti A, Angellilo A, Mattot V, Nuyens D, Lutgens E, Clotman F, de Ruiter MC, Gittenberger-de Groot A, Poelmann R, Lupu F, Herbert JM, Collen D, Dejana E (1999) Targeted deficiency or cytosolic truncation of the VE-cadherin gene in mice impairs VEGF-mediated endothelial survival and angiogenesis. Cell 98(2):147–157. doi:S0092-8674(00)81010-7 [pii]Google Scholar
  20. Cattelino A, Liebner S, Gallini R, Zanetti A, Balconi G, Corsi A, Bianco P, Wolburg H, Moore R, Oreda B, Kemler R, Dejana E (2003) The conditional inactivation of the beta-catenin gene in endothelial cells causes a defective vascular pattern and increased vascular fragility. J Cell Biol 162(6):1111–1122. doi: 10.1083/jcb.200212157, jcb.200212157 [pii]Google Scholar
  21. Christoffersen C, Ahnstrom J, Axler O, Christensen EI, Dahlback B, Nielsen LB (2008) The signal peptide anchors apolipoprotein M in plasma lipoproteins and prevents rapid clearance of apolipoprotein M from plasma. J Biol Chem 283(27):18765–18772. doi: 10.1074/jbc.M800695200, M800695200 [pii]Google Scholar
  22. Christoffersen C, Nielsen LB, Axler O, Andersson A, Johnsen AH, Dahlback B (2006) Isolation and characterization of human apolipoprotein M-containing lipoproteins. J Lipid Res 47(8):1833–1843. doi: 10.1194/jlr.M600055-JLR200, M600055-JLR200 [pii]Google Scholar
  23. Christoffersen C, Obinata H, Kumaraswamy SB, Galvani S, Ahnstrom J, Sevvana M, Egerer-Sieber C, Muller YA, Hla T, Nielsen LB, Dahlback B (2011) Endothelium-protective sphingosine-1-phosphate provided by HDL-associated apolipoprotein M. Proc Natl Acad Sci USA 108(23):9613–9618. doi: 10.1073/pnas.1103187108, 1103187108 [pii] Google Scholar
  24. Chun J, Goetzl EJ, Hla T, Igarashi Y, Lynch KR, Moolenaar W, Pyne S, Tigyi G (2002) International Union of Pharmacology. XXXIV. Lysophospholipid receptor nomenclature. Pharmacol Rev 54(2):265–269Google Scholar
  25. Chun J, Hla T, Lynch KR, Spiegel S, Moolenaar WH (2010) International Union of Basic and Clinical Pharmacology. LXXVIII. Lysophospholipid receptor nomenclature. Pharmacol Rev 62(4):579–587. doi: 10.1124/pr.110.003111 Google Scholar
  26. Corada M, Mariotti M, Thurston G, Smith K, Kunkel R, Brockhaus M, Lampugnani MG, Martin-Padura I, Stoppacciaro A, Ruco L, McDonald DM, Ward PA, Dejana E (1999) Vascular endothelial-cadherin is an important determinant of microvascular integrity in vivo. Proc Natl Acad Sci USA 96(17):9815–9820Google Scholar
  27. Cui H, Okamoto Y, Yoshioka K, Du W, Takuwa N, Zhang W, Asano M, Shibamoto T, Takuwa Y (2013) Sphingosine-1-phosphate receptor 2 protects against anaphylactic shock through suppression of endothelial nitric oxide synthase in mice. J Allergy Clin Immunol. doi: 10.1016/j.jaci.2013.07.026, S0091-6749(13)01151-2 [pii]
  28. de Bisschop MB, Bellou A (2012) Anaphylaxis. Curr Opin Crit Care 18(4):308–317. doi: 10.1097/MCC.0b013e3283557a63
  29. Dejana E (2004) Endothelial cell-cell junctions: happy together. Nat Rev Mol Cell Biol 5(4):261–270. doi: 10.1038/nrm1357, nrm1357 [pii]Google Scholar
  30. Dudek SM, Camp SM, Chiang ET, Singleton PA, Usatyuk PV, Zhao Y, Natarajan V, Garcia JG (2007) Pulmonary endothelial cell barrier enhancement by FTY720 does not require the S1P1 receptor. Cell Sig 19(8):1754–1764. doi: 10.1016/j.cellsig.2007.03.011, S0898-6568(07)00098-8 [pii]Google Scholar
  31. Dudek SM, Jacobson JR, Chiang ET, Birukov KG, Wang P, Zhan X, Garcia JG (2004) Pulmonary endothelial cell barrier enhancement by sphingosine 1-phosphate: roles for cortactin and myosin light chain kinase. J Biol Chem 279(23):24692–24700. doi: 10.1074/jbc.M313969200, M313969200 [pii]Google Scholar
  32. Edsall LC, Spiegel S (1999) Enzymatic measurement of sphingosine 1-phosphate. Anal Biochem 272(1):80–86. doi: 10.1006/abio.1999.4157, S0003-2697(99)94157-X [pii]Google Scholar
  33. Egom EE (2013) Sphingosine-1-phosphate signalling as a therapeutic target for patients with abnormal glucose metabolism and ischaemic heart disease. J Cardiovasc Med (Hagerstown). (in press). doi: 10.2459/JCM.0b013e3283639755
  34. English D, Welch Z, Kovala AT, Harvey K, Volpert OV, Brindley DN, Garcia JG (2000) Sphingosine 1-phosphate released from platelets during clotting accounts for the potent endothelial cell chemotactic activity of blood serum and provides a novel link between hemostasis and angiogenesis. FASEB J 14(14):2255–2265. doi: 10.1096/fj.00-0134com, 14/14/2255 [pii]Google Scholar
  35. Fukuhara S, Simmons S, Kawamura S, Inoue A, Orba Y, Tokudome T, Sunden Y, Arai Y, Moriwaki K, Ishida J, Uemura A, Kiyonari H, Abe T, Fukamizu A, Hirashima M, Sawa H, Aoki J, Ishii M, Mochizuki N (2012) The sphingosine-1-phosphate transporter Spns2 expressed on endothelial cells regulates lymphocyte trafficking in mice. J Clin Invest 122(4):1416–1426. doi: 10.1172/JCI60746, 60746 [pii]Google Scholar
  36. Gaengel K, Niaudet C, Hagikura K, Lavina B, Muhl L, Hofmann JJ, Ebarasi L, Nystrom S, Rymo S, Chen LL, Pang MF, Jin Y, Raschperger E, Roswall P, Schulte D, Benedito R, Larsson J, Hellstrom M, Fuxe J, Uhlen P, Adams R, Jakobsson L, Majumdar A, Vestweber D, Uv A, Betsholtz C (2012) The sphingosine-1-phosphate receptor S1PR1 restricts sprouting angiogenesis by regulating the interplay between VE-cadherin and VEGFR2. Dev Cell 23(3):587–599. doi: 10.1016/j.devcel.2012.08.005, S1534-5807(12)00373-5 [pii]Google Scholar
  37. Garcia JG, Liu F, Verin AD, Birukova A, Dechert MA, Gerthoffer WT, Bamberg JR, English D (2001) Sphingosine 1-phosphate promotes endothelial cell barrier integrity by Edg-dependent cytoskeletal rearrangement. J Clin Invest 108(5):689–701. doi: 10.1172/JCI12450 Google Scholar
  38. Hait NC, Oskeritzian CA, Paugh SW, Milstien S, Spiegel S (2006) Sphingosine kinases, sphingosine 1-phosphate, apoptosis and diseases. Biochim Biophys Acta 1758(12):2016–2026. doi: 10.1016/j.bbamem.2006.08.007, S0005-2736(06)00313-0 [pii]
  39. Hanel P, Andreani P, Graler MH (2007) Erythrocytes store and release sphingosine 1-phosphate in blood. FASEB J 21(4):1202–1209. doi: 10.1096/fj.06-7433com, fj.06-7433com [pii]Google Scholar
  40. Hannun YA, Obeid LM (2008) Principles of bioactive lipid signalling: lessons from sphingolipids. Nat Rev Mol Cell Biol 9(2):139–150. doi: 10.1038/nrm2329, nrm2329 [pii]Google Scholar
  41. Hanson MA, Roth CB, Jo E, Griffith MT, Scott FL, Reinhart G, Desale H, Clemons B, Cahalan SM, Schuerer SC, Sanna MG, Han GW, Kuhn P, Rosen H, Stevens RC (2012) Crystal structure of a lipid G protein-coupled receptor. Science 335(6070):851–855. doi: 10.1126/science.1215904, 335/6070/851 [pii]Google Scholar
  42. Herzog BH, Fu J, Wilson SJ, Hess PR, Sen A, McDaniel JM, Pan Y, Sheng M, Yago T, Silasi-Mansat R, McGee S, May F, Nieswandt B, Morris AJ, Lupu F, Coughlin SR, McEver RP, Chen H, Kahn ML, Xia L (2013) Podoplanin maintains high endothelial venule integrity by interacting with platelet CLEC-2. Nature 502 (7469):105--109. doi: 10.1038/nature12501
  43. Hisano Y, Kobayashi N, Yamaguchi A, Nishi T (2012) Mouse SPNS2 functions as a sphingosine-1-phosphate transporter in vascular endothelial cells. PLoS One 7(6):e38941. doi: 10.1371/journal.pone.0038941, PONE-D-12-07568 [pii]
  44. Hla T (2003) Signaling and biological actions of sphingosine 1-phosphate. Pharmacol Res 47(5):401–407. doi:S104366180300046X [pii]Google Scholar
  45. Hla T, Lee MJ, Ancellin N, Paik JH, Kluk MJ (2001) Lysophospholipids–receptor revelations. Science 294(5548):1875–1878. doi: 10.1126/science.1065323, 294/5548/1875 [pii]Google Scholar
  46. Hla T, Venkataraman K, Michaud J (2008) The vascular S1P gradient-cellular sources and biological significance. Biochim Biophys Acta 1781(9):477–482. doi: 10.1016/j.bbalip.2008.07.003, S1388-1981(08)00132-7 [pii]Google Scholar
  47. Igarashi N, Okada T, Hayashi S, Fujita T, Jahangeer S, Nakamura S (2003) Sphingosine kinase 2 is a nuclear protein and inhibits DNA synthesis. J Biol Chem 278(47):46832–46839. doi: 10.1074/jbc.M306577200, M306577200 [pii]Google Scholar
  48. Ito K, Anada Y, Tani M, Ikeda M, Sano T, Kihara A, Igarashi Y (2007) Lack of sphingosine 1-phosphate-degrading enzymes in erythrocytes. Biochem Biophys Res Commun 357(1):212–217. doi: 10.1016/j.bbrc.2007.03.123, S0006-291X(07)00607-9 [pii]Google Scholar
  49. Jessup W (2008) Lipid metabolism: sources and stability of plasma sphingosine-1-phosphate. Curr Opin Lipidol 19(5):543–544. doi: 10.1097/MOL.0b013e32830f4a90, 00041433-200810000-00017 [pii]Google Scholar
  50. Jiang X, Han X (2006) Characterization and direct quantitation of sphingoid base-1-phosphates from lipid extracts: a shotgun lipidomics approach. J Lipid Res 47(8):1865–1873. doi: 10.1194/jlr.D600012-JLR200, D600012-JLR200 [pii]Google Scholar
  51. Jung B, Obinata H, Galvani S, Mendelson K, Ding BS, Skoura A, Kinzel B, Brinkmann V, Rafii S, Evans T, Hla T (2012) Flow-regulated endothelial S1P receptor-1 signaling sustains vascular development. Dev Cell 23(3):600–610. doi: 10.1016/j.devcel.2012.07.015, S1534-5807(12)00334-6 [pii]Google Scholar
  52. Karuna R, Park R, Othman A, Holleboom AG, Motazacker MM, Sutter I, Kuivenhoven JA, Rohrer L, Matile H, Hornemann T, Stoffel M, Rentsch KM, von Eckardstein A (2011) Plasma levels of sphingosine-1-phosphate and apolipoprotein M in patients with monogenic disorders of HDL metabolism. Atherosclerosis 219(2):855–863. doi: 10.1016/j.atherosclerosis.2011.08.049, S0021-9150(11)00853-7 [pii]Google Scholar
  53. Kawahara A, Nishi T, Hisano Y, Fukui H, Yamaguchi A, Mochizuki N (2009) The sphingolipid transporter spns2 functions in migration of zebrafish myocardial precursors. Science 323(5913):524–527. doi: 10.1126/science.1167449, 1167449 [pii]Google Scholar
  54. Krump-Konvalinkova V, Chwalla I, Siess W (2008) FTY720 inhibits S1P-mediated endothelial healing: relationship to S1P1-receptor surface expression. Biochem Biophys Res Commun 370(4):603–608. doi: 10.1016/j.bbrc.2008.03.144, S0006-291X(08)00637-2 [pii]Google Scholar
  55. Krump-Konvalinkova V, Yasuda S, Rubic T, Makarova N, Mages J, Erl W, Vosseler C, Kirkpatrick CJ, Tigyi G, Siess W (2005) Stable knock-down of the sphingosine 1-phosphate receptor S1P1 influences multiple functions of human endothelial cells. Arterioscler Thromb Vasc Biol 25(3):546–552. doi: 10.1161/01.ATV.0000154360.36106.d9, 01.ATV.0000154360.36106.d9 [pii]Google Scholar
  56. Kuhn R, Schwenk F, Aguet M, Rajewsky K (1995) Inducible gene targeting in mice. Science 269(5229):1427–1429Google Scholar
  57. Kurano M, Tsukamoto K, Ohkawa R, Hara M, Iino J, Kageyama Y, Ikeda H, Yatomi Y (2013) Liver involvement in sphingosine 1-phosphate dynamism revealed by adenoviral hepatic overexpression of apolipoprotein M. Atherosclerosis 229(1):102–109. doi: 10.1016/j.atherosclerosis.2013.04.024, S0021-9150(13)00266-9 [pii]Google Scholar
  58. Le Stunff H, Peterson C, Thornton R, Milstien S, Mandala SM, Spiegel S (2002) Characterization of murine sphingosine-1-phosphate phosphohydrolase. J Biol Chem 277(11):8920–8927. doi: 10.1074/jbc.M109968200, M109968200 [pii]Google Scholar
  59. Lee JF, Gordon S, Estrada R, Wang L, Siow DL, Wattenberg BW, Lominadze D, Lee MJ (2009) Balance of S1P1 and S1P2 signaling regulates peripheral microvascular permeability in rat cremaster muscle vasculature. Am J Physiol Heart Circ Physiol 296(1):H33–42. doi: 10.1152/ajpheart.00097.2008, 00097.2008 [pii]Google Scholar
  60. Lee JF, Zeng Q, Ozaki H, Wang L, Hand AR, Hla T, Wang E, Lee MJ (2006) Dual roles of tight junction-associated protein, zonula occludens-1, in sphingosine 1-phosphate-mediated endothelial chemotaxis and barrier integrity. J Biol Chem 281(39):29190–29200. doi: 10.1074/jbc.M604310200, M604310200 [pii]Google Scholar
  61. Lee MJ, Thangada S, Claffey KP, Ancellin N, Liu CH, Kluk M, Volpi M, Sha’afi RI, Hla T (1999) Vascular endothelial cell adherens junction assembly and morphogenesis induced by sphingosine-1-phosphate. Cell 99(3):301–312. doi:S0092-8674(00)81661-X [pii]Google Scholar
  62. Lee MJ, Van Brocklyn JR, Thangada S, Liu CH, Hand AR, Menzeleev R, Spiegel S, Hla T (1998) Sphingosine-1-phosphate as a ligand for the G protein-coupled receptor EDG-1. Science 279(5356):1552–1555Google Scholar
  63. Lee SY, Kim DH, Sung SA, Kim MG, Cho WY, Kim HK, Jo SK (2011) Sphingosine-1-phosphate reduces hepatic ischaemia/reperfusion-induced acute kidney injury through attenuation of endothelial injury in mice. Nephrology (Carlton) 16(2):163–173. doi: 10.1111/j.1440-1797.2010.01386.x
  64. Matthay MA, Ware LB, Zimmerman GA (2012) The acute respiratory distress syndrome. J Clin Invest 122(8):2731–2740. doi: 10.1172/JCI60331, 60331 [pii]Google Scholar
  65. McVerry BJ, Peng X, Hassoun PM, Sammani S, Simon BA, Garcia JG (2004) Sphingosine 1-phosphate reduces vascular leak in murine and canine models of acute lung injury. Am J Respir Crit Care Med 170(9):987–993. doi: 10.1164/rccm.200405-684OC, 200405-684OC [pii]Google Scholar
  66. Mendoza A, Breart B, Ramos-Perez WD, Pitt LA, Gobert M, Sunkara M, Lafaille JJ, Morris AJ, Schwab SR (2012) The transporter Spns2 is required for secretion of lymph but not plasma sphingosine-1-phosphate. Cell Rep 2(5):1104–1110. doi: 10.1016/j.celrep.2012.09.021, S2211-1247(12)00325-7 [pii]Google Scholar
  67. Michel CC, Curry FE (1999) Microvascular permeability. Physiol Rev 79 (3):703-761Google Scholar
  68. Min JK, Yoo HS, Lee EY, Lee WJ, Lee YM (2002) Simultaneous quantitative analysis of sphingoid base 1-phosphates in biological samples by o-phthalaldehyde precolumn derivatization after dephosphorylation with alkaline phosphatase. Anal Biochem 303(2):167–175. doi: 10.1006/abio.2002.5579 S000326970295579X [pii]Google Scholar
  69. Moolenaar WH, Hla T (2012) SnapShot: bioactive lysophospholipids. Cell 148(1–2):378–378 e372. doi: 10.1016/j.cell.2012.01.013 Google Scholar
  70. Moreno-Vinasco L, Jacobson JR, Bonde P, Sammani S, Mirzapoiazova T, Vigneswaran WT, Garcia JGN (2008) Attenuation of rodent lung ischemia-reperfusion injury by sphingosine 1-phosphate. J Organ Dysfunction 4(2):106–114. doi: 10.1080/17471060701505289 Google Scholar
  71. Muller HC, Hocke AC, Hellwig K, Gutbier B, Peters H, Schonrock SM, Tschernig T, Schmiedl A, Hippenstiel S, N’Guessan PD, Rosseau S, Suttorp N, Witzenrath M (2011) The Sphingosine-1 Phosphate receptor agonist FTY720 dose dependently affected endothelial integrity in vitro and aggravated ventilator-induced lung injury in mice. Pulm Pharmacol Ther 24(4):377–385. doi: 10.1016/j.pupt.2011.01.017, S1094-5539(11)00039-3 [pii]
  72. Mullin JM, Agostino N, Rendon-Huerta E, Thornton JJ (2005) Keynote review: epithelial and endothelial barriers in human disease. Drug Discov Today 10(6):395–408. doi: 10.1016/S1359-6446(05)03379-9, S1359644605033799 [pii]
  73. Murata N, Sato K, Kon J, Tomura H, Okajima F (2000a) Quantitative measurement of sphingosine 1-phosphate by radioreceptor-binding assay. Anal Biochem 282 (1):115-120. doi: 10.1006/abio.2000.4580 S0003-2697(00)94580-9 [pii]Google Scholar
  74. Murata N, Sato K, Kon J, Tomura H, Yanagita M, Kuwabara A, Ui M, Okajima F (2000b) Interaction of sphingosine 1-phosphate with plasma components, including lipoproteins, regulates the lipid receptor-mediated actions. Biochem J 352(Pt 3):809–815Google Scholar
  75. Nofer JR, van der Giet M, Tolle M, Wolinska I, von Wnuck Lipinski K, Baba HA, Tietge UJ, Godecke A, Ishii I, Kleuser B, Schafers M, Fobker M, Zidek W, Assmann G, Chun J, Levkau B (2004) HDL induces NO-dependent vasorelaxation via the lysophospholipid receptor S1P3. J Clin Invest 113(4):569–581. doi: 10.1172/JCI18004 Google Scholar
  76. Ogawa C, Kihara A, Gokoh M, Igarashi Y (2003) Identification and characterization of a novel human sphingosine-1-phosphate phosphohydrolase, hSPP2. J Biol Chem 278(2):1268–1272. doi: 10.1074/jbc.M209514200, M209514200 [pii]Google Scholar
  77. Okazaki M, Kreisel F, Richardson SB, Kreisel D, Krupnick AS, Patterson GA, Gelman AE (2007) Sphingosine 1-phosphate inhibits ischemia reperfusion injury following experimental lung transplantation. Am J Transplant 7(4):751–758. doi: 10.1111/j.1600-6143.2006.01710.x, AJT1710 [pii]Google Scholar
  78. Olivera A, Mizugishi K, Tikhonova A, Ciaccia L, Odom S, Proia RL, Rivera J (2007) The sphingosine kinase-sphingosine-1-phosphate axis is a determinant of mast cell function and anaphylaxis. Immunity 26(3):287–297. doi: 10.1016/j.immuni.2007.02.008, S1074-7613(07)00174-4 [pii]Google Scholar
  79. Olivera A, Spiegel S (1993) Sphingosine-1-phosphate as second messenger in cell proliferation induced by PDGF and FCS mitogens. Nature 365(6446):557–560. doi: 10.1038/365557a0 Google Scholar
  80. Oo ML, Chang SH, Thangada S, Wu MT, Rezaul K, Blaho V, Hwang SI, Han DK, Hla T (2011) Engagement of S1P(1)-degradative mechanisms leads to vascular leak in mice. J Clin Invest 121(6):2290–2300. doi: 10.1172/JCI45403, 45403 [pii]Google Scholar
  81. Oskeritzian CA, Price MM, Hait NC, Kapitonov D, Falanga YT, Morales JK, Ryan JJ, Milstien S, Spiegel S (2010) Essential roles of sphingosine-1-phosphate receptor 2 in human mast cell activation, anaphylaxis, and pulmonary edema. J Exp Med 207(3):465–474. doi: 10.1084/jem.20091513, jem.20091513 [pii]Google Scholar
  82. Owen KA, Pixley FJ, Thomas KS, Vicente-Manzanares M, Ray BJ, Horwitz AF, Parsons JT, Beggs HE, Stanley ER, Bouton AH (2007) Regulation of lamellipodial persistence, adhesion turnover, and motility in macrophages by focal adhesion kinase. J Cell Biol 179(6):1275–1287. doi: 10.1083/jcb.200708093, jcb.200708093 [pii]Google Scholar
  83. Oyama O, Sugimoto N, Qi X, Takuwa N, Mizugishi K, Koizumi J, Takuwa Y (2008) The lysophospholipid mediator sphingosine-1-phosphate promotes angiogenesis in vivo in ischaemic hindlimbs of mice. Cardiovasc Res 78(2):301–307. doi: 10.1093/cvr/cvn002, cvn002 [pii]Google Scholar
  84. Paik JH, Chae S, Lee MJ, Thangada S, Hla T (2001) Sphingosine 1-phosphate-induced endothelial cell migration requires the expression of EDG-1 and EDG-3 receptors and Rho-dependent activation of alpha vbeta3- and beta1-containing integrins. J Biol Chem 276(15):11830–11837. doi: 10.1074/jbc.M009422200, M009422200 [pii]Google Scholar
  85. Pappu R, Schwab SR, Cornelissen I, Pereira JP, Regard JB, Xu Y, Camerer E, Zheng YW, Huang Y, Cyster JG, Coughlin SR (2007) Promotion of lymphocyte egress into blood and lymph by distinct sources of sphingosine-1-phosphate. Science 316(5822):295–298. doi: 10.1126/science.1139221, 1139221 [pii]Google Scholar
  86. Peng X, Hassoun PM, Sammani S, McVerry BJ, Burne MJ, Rabb H, Pearse D, Tuder RM, Garcia JG (2004) Protective effects of sphingosine 1-phosphate in murine endotoxin-induced inflammatory lung injury. Am J Respir Crit Care Med 169(11):1245–1251. doi: 10.1164/rccm.200309-1258OC, 200309-1258OC [pii]Google Scholar
  87. Pitman MR, Woodcock JM, Lopez AF, Pitson SM (2012) Molecular targets of FTY720 (fingolimod). Curr Mol Med 12(10):1207–1219. doi:CMM-EPUB-20120723-1 [pii]Google Scholar
  88. Predescu SA, Predescu DN, Malik AB (2007) Molecular determinants of endothelial transcytosis and their role in endothelial permeability. Am J Physiol Lung Cell Mol Physiol 293(4):L823–842. doi: 10.1152/ajplung.00436.2006, 00436.2006 [pii]Google Scholar
  89. Sammani S, Moreno-Vinasco L, Mirzapoiazova T, Singleton PA, Chiang ET, Evenoski CL, Wang T, Mathew B, Husain A, Moitra J, Sun X, Nunez L, Jacobson JR, Dudek SM, Natarajan V, Garcia JG (2010) Differential effects of sphingosine 1-phosphate receptors on airway and vascular barrier function in the murine lung. Am J Respir Cell Mol Biol 43(4):394–402. doi: 10.1165/rcmb.2009-0223OC, 2009-0223OC [pii]Google Scholar
  90. Sanchez T, Estrada-Hernandez T, Paik JH, Wu MT, Venkataraman K, Brinkmann V, Claffey K, Hla T (2003) Phosphorylation and action of the immunomodulator FTY720 inhibits vascular endothelial cell growth factor-induced vascular permeability. J Biol Chem 278(47):47281–47290. doi: 10.1074/jbc.M306896200, M306896200 [pii]Google Scholar
  91. Sanchez T, Skoura A, Wu MT, Casserly B, Harrington EO, Hla T (2007) Induction of vascular permeability by the sphingosine-1-phosphate receptor-2 (S1P2R) and its downstream effectors ROCK and PTEN. Arterioscler Thromb Vasc Biol 27(6):1312–1318. doi: 10.1161/ATVBAHA.107.143735, ATVBAHA.107.143735 [pii]
  92. Seal JB, Gewertz BL (2005) Vascular dysfunction in ischemia-reperfusion injury. Ann Vasc Surg 19(4):572–584. doi: 10.1007/s10016-005-4616-7 Google Scholar
  93. Shea BS, Brooks SF, Fontaine BA, Chun J, Luster AD, Tager AM (2010) Prolonged exposure to sphingosine 1-phosphate receptor-1 agonists exacerbates vascular leak, fibrosis, and mortality after lung injury. Am J Respir Cell Mol Biol 43(6):662–673. doi: 10.1165/rcmb.2009-0345OC, 2009-0345OC [pii]Google Scholar
  94. Shikata Y, Birukov KG, Garcia JG (2003) S1P induces FA remodeling in human pulmonary endothelial cells: role of Rac, GIT1, FAK, and paxillin. J Appl Physiol 94(3):1193–1203. doi: 10.1152/japplphysiol.00690.2002, 00690.2002 [pii]Google Scholar
  95. Shivdasani RA, Rosenblatt MF, Zucker-Franklin D, Jackson CW, Hunt P, Saris CJ, Orkin SH (1995) Transcription factor NF-E2 is required for platelet formation independent of the actions of thrombopoietin/MGDF in megakaryocyte development. Cell 81(5):695–704. doi:0092-8674(95)90531-6 [pii]Google Scholar
  96. Spiering D, Hodgson L (2011) Dynamics of the Rho-family small GTPases in actin regulation and motility. Cell Adh Migr 5(2):170–180. doi:14403 [pii]Google Scholar
  97. Szczepaniak WS, Zhang Y, Hagerty S, Crow MT, Kesari P, Garcia JG, Choi AM, Simon BA, McVerry BJ (2008) Sphingosine 1-phosphate rescues canine LPS-induced acute lung injury and alters systemic inflammatory cytokine production in vivo. Transl Res 152(5):213–224. doi: 10.1016/j.trsl.2008.09.002, S1931-5244(08)00225-9 [pii]
  98. Takashima S (2009) Phosphorylation of myosin regulatory light chain by myosin light chain kinase, and muscle contraction. Circ J 73(2):208–213. doi:JST.JSTAGE/circj/CJ-08-1041 [pii]Google Scholar
  99. Tani M, Sano T, Ito M, Igarashi Y (2005) Mechanisms of sphingosine and sphingosine 1-phosphate generation in human platelets. J Lipid Res 46(11):2458–2467. doi: 10.1194/jlr.M500268-JLR200, M500268-JLR200 [pii]Google Scholar
  100. Venkataraman K, Lee YM, Michaud J, Thangada S, Ai Y, Bonkovsky HL, Parikh NS, Habrukowich C, Hla T (2008) Vascular endothelium as a contributor of plasma sphingosine 1-phosphate. Circ Res 102(6):669–676. doi: 10.1161/CIRCRESAHA.107.165845, CIRCRESAHA.107.165845 [pii]Google Scholar
  101. Venkataraman K, Thangada S, Michaud J, Oo ML, Ai Y, Lee YM, Wu M, Parikh NS, Khan F, Proia RL, Hla T (2006) Extracellular export of sphingosine kinase-1a contributes to the vascular S1P gradient. Biochem J 397(3):461–471. doi: 10.1042/BJ20060251 Google Scholar
  102. Venkiteswaran K, Xiao K, Summers S, Calkins CC, Vincent PA, Pumiglia K, Kowalczyk AP (2002) Regulation of endothelial barrier function and growth by VE-cadherin, plakoglobin, and beta-catenin. Am J Physiol Cell Physiol 283(3):C811–821. doi: 10.1152/ajpcell.00417.2001 Google Scholar
  103. Waeber C (2013) Sphingosine 1-Phosphate (S1P) signaling and the vasculature. In: Lysophospholipid receptors. John Wiley & Sons, Inc., New York, pp 313–347. doi: 10.1002/9781118531426.ch15
  104. Wilkerson BA, Grass GD, Wing SB, Argraves WS, Argraves KM (2012) Sphingosine 1-phosphate (S1P) carrier-dependent regulation of endothelial barrier: high density lipoprotein (HDL)-S1P prolongs endothelial barrier enhancement as compared with albumin-S1P via effects on levels, trafficking, and signaling of S1P1. J Biol Chem 287(53):44645–44653. doi: 10.1074/jbc.M112.423426, M112.423426 [pii]Google Scholar
  105. Wojciak-Stothard B, Potempa S, Eichholtz T, Ridley AJ (2001) Rho and Rac but not Cdc42 regulate endothelial cell permeability. J Cell Sci 114 (Pt 7):1343–1355Google Scholar
  106. Xu M, Waters CL, Hu C, Wysolmerski RB, Vincent PA, Minnear FL (2007) Sphingosine 1-phosphate rapidly increases endothelial barrier function independently of VE-cadherin but requires cell spreading and Rho kinase. Am J Physiol Cell Physiol 293(4):C1309–1318. doi: 10.1152/ajpcell.00014.2007, 00014.2007 [pii]Google Scholar
  107. Yatomi Y, Igarashi Y, Yang L, Hisano N, Qi R, Asazuma N, Satoh K, Ozaki Y, Kume S (1997a) Sphingosine 1-phosphate, a bioactive sphingolipid abundantly stored in platelets, is a normal constituent of human plasma and serum. J Biochem 121(5):969–973Google Scholar
  108. Yatomi Y, Ozaki Y, Ohmori T, Igarashi Y (2001) Sphingosine 1-phosphate: synthesis and release. Prostaglandins Other Lipid Mediat 64(1–4):107–122Google Scholar
  109. Yatomi Y, Welch RJ, Igarashi Y (1997b) Distribution of sphingosine 1-phosphate, a bioactive sphingolipid, in rat tissues. FEBS Lett 404(2–3):173–174. doi:S0014-5793(97)00121-X [pii]Google Scholar
  110. Zhang G, Yang L, Kim GS, Ryan K, Lu S, O’Donnell RK, Spokes K, Shapiro N, Aird WC, Kluk MJ, Yano K, Sanchez T (2013) Critical role of sphingosine-1-phosphate receptor 2 (S1PR2) in acute vascular inflammation. Blood 122(3):443–455. doi: 10.1182/blood-2012-11-467191, blood-2012-11-467191 [pii]Google Scholar
  111. Zhao Y, Gorshkova IA, Berdyshev E, He D, Fu P, Ma W, Su Y, Usatyuk PV, Pendyala S, Oskouian B, Saba JD, Garcia JG, Natarajan V (2011) Protection of LPS-induced murine acute lung injury by sphingosine-1-phosphate lyase suppression. Am J Respir Cell Mol Biol 45(2):426–435. doi: 10.1165/rcmb.2010-0422OC, 2010-0422OC [pii]Google Scholar

Copyright information

© Springer International Publishing Switzerland 2014

Authors and Affiliations

  1. 1.Center for Vascular Biology, Department of Pathology and Laboratory MedicineWeill Cornell Medical College, Cornell UniversityNew YorkUSA

Personalised recommendations