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Annual Review of Physiology

Volume 79, 2017

Vascular and Immunobiology of the Circulatory Sphingosine 1-Phosphate Gradient

Abstract

Vertebrates are endowed with a closed circulatory system, the evolution of which required novel structural and regulatory changes. Furthermore, immune cell trafficking paradigms adapted to the barriers imposed by the closed circulatory system. How did such changes occur mechanistically? We propose that spatial compartmentalization of the lipid mediator sphingosine 1-phosphate (S1P) may be one such mechanism. In vertebrates, S1P is spatially compartmentalized in the blood and lymphatic circulation, thus comprising a sharp S1P gradient across the endothelial barrier. Circulatory S1P has critical roles in maturation and homeostasis of the vascular system as well as in immune cell trafficking. Physiological functions of S1P are tightly linked to shear stress, the key biophysical stimulus from blood flow. Thus, circulatory S1P confinement could be a primordial strategy of vertebrates in the development of a closed circulatory system. This review discusses the cellular and molecular basis of the S1P gradients and aims to interpret its physiological significance as a key feature of the closed circulatory system.

Keyword(s): angiogenesis, G protein-coupled receptor, HDL, immune cell trafficking, lipid chaperones, lipid mediators, sphingolipid, vascular biology
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/content/journals/10.1146/annurev-physiol-021014-071635
2017-02-10
2024-04-23
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Literature Cited

  1. Armulik A, Genove G, Betsholtz C. 1.  2011. Pericytes: developmental, physiological, and pathological perspectives, problems, and promises. Dev. Cell 21:193–215 [Google Scholar]
  2. Kihara A. 2.  2014. Sphingosine 1-phosphate is a key metabolite linking sphingolipids to glycerophospholipids. Biochim. Biophys. Acta 1841:766–72 [Google Scholar]
  3. Hla T. 3.  2005. Genomic insights into mediator lipidomics. Prostaglandins Other Lipid Mediat 77:197–209 [Google Scholar]
  4. Schwab SR, Pereira JP, Matloubian M, Xu Y, Huang Y, Cyster JG. 4.  2005. Lymphocyte sequestration through S1P lyase inhibition and disruption of S1P gradients. Science 309:1735–39 [Google Scholar]
  5. Hla T, Venkataraman K, Michaud J. 5.  2008. The vascular S1P gradient-cellular sources and biological significance. Biochim. Biophys. Acta 1781:477–82 [Google Scholar]
  6. Givens C, Tzima E. 6.  2012. S1P1 bridges mechanotransduction and angiogenesis during vascular development. Dev. Cell 23:451–52 [Google Scholar]
  7. Tarbell JM, Simon SI, Curry FR. 7.  2014. Mechanosensing at the vascular interface. Annu. Rev. Biomed. Eng 16505–32 [Google Scholar]
  8. Schwab SR, Cyster JG. 8.  2007. Finding a way out: lymphocyte egress from lymphoid organs. Nat. Immunol. 8:1295–301 [Google Scholar]
  9. Pappu R, Schwab SR, Cornelissen I, Pereira JP, Regard JB. 9.  et al. 2007. Promotion of lymphocyte egress into blood and lymph by distinct sources of sphingosine-1-phosphate. Science 316:295–98 [Google Scholar]
  10. Xiong Y, Yang P, Proia RL, Hla T. 10.  2014. Erythrocyte-derived sphingosine 1-phosphate is essential for vascular development. J. Clin. Investig. 124:4823–28 [Google Scholar]
  11. Lee YM, Venkataraman K, Hwang SI, Han DK, Hla T. 11.  2007. A novel method to quantify sphingosine 1-phosphate by immobilized metal affinity chromatography (IMAC). Prostaglandins Other Lipid Mediat 84:154–62 [Google Scholar]
  12. Venkataraman K, Lee YM, Michaud J, Thangada S, Ai Y. 12.  et al. 2008. Vascular endothelium as a contributor of plasma sphingosine 1-phosphate. Circ. Res. 102:669–76 [Google Scholar]
  13. Yatomi Y, Igarashi Y, Yang L, Hisano N, Qi R. 13.  et al. 1997. Sphingosine 1-phosphate, a bioactive sphingolipid abundantly stored in platelets, is a normal constituent of human plasma and serum. J. Biochem. 121:969–73 [Google Scholar]
  14. Yatomi Y, Ruan F, Hakomori S, Igarashi Y. 14.  1995. Sphingosine-1-phosphate: a platelet-activating sphingolipid released from agonist-stimulated human platelets. Blood 86:193–202 [Google Scholar]
  15. Yatomi Y, Yamamura S, Ruan F, Igarashi Y. 15.  1997. Sphingosine 1-phosphate induces platelet activation through an extracellular action and shares a platelet surface receptor with lysophosphatidic acid. J. Biol. Chem. 272:5291–97 [Google Scholar]
  16. Ikeda M, Kihara A, Igarashi Y. 16.  2004. 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. 325:338–43 [Google Scholar]
  17. Jonnalagadda D, Sunkara M, Morris AJ, Whiteheart SW. 17.  2014. Granule-mediated release of sphingosine-1-phosphate by activated platelets. Biochim. Biophys. Acta 1841:1581–89 [Google Scholar]
  18. Urtz N, Gaertner F, von Bruehl ML, Chandraratne S, Rahimi F. 18.  et al. 2015. Sphingosine 1-phosphate produced by sphingosine kinase 2 intrinsically controls platelet aggregation in vitro and in vivo. Circ. Res. 117:376–87 [Google Scholar]
  19. Allende ML, Sasaki T, Kawai H, Olivera A, Mi Y. 19.  et al. 2004. Mice deficient in sphingosine kinase 1 are rendered lymphopenic by FTY720. J. Biol. Chem. 279:52487–92 [Google Scholar]
  20. Zemann B, Kinzel B, Müller M, Reuschel R, Mechtcheriakova D. 20.  et al. 2006. Sphingosine kinase type 2 is essential for lymphopenia induced by the immunomodulatory drug FTY720. Blood 107:1454–58 [Google Scholar]
  21. Olivera A, Mizugishi K, Tikhonova A, Ciaccia L, Odom S. 21.  et al. 2007. The sphingosine kinase-sphingosine-1-phosphate axis is a determinant of mast cell function and anaphylaxis. Immunity 26:287–97 [Google Scholar]
  22. Kharel Y, Mathews TP, Gellett AM, Tomsig JL, Kennedy PC. 22.  et al. 2011. Sphingosine kinase type 1 inhibition reveals rapid turnover of circulating sphingosine 1-phosphate. Biochem. J. 440:345–53 [Google Scholar]
  23. Kharel Y, Raje M, Gao M, Gellett AM, Tomsig JL. 23.  et al. 2012. Sphingosine kinase type 2 inhibition elevates circulating sphingosine 1-phosphate. Biochem. J. 447:149–57 [Google Scholar]
  24. Sensken SC, Bode C, Nagarajan M, Peest U, Pabst O, Gräler MH. 24.  2010. Redistribution of sphingosine 1-phosphate by sphingosine kinase 2 contributes to lymphopenia. J. Immunol. 184:4133–42 [Google Scholar]
  25. Olivera A, Eisner C, Kitamura Y, Dillahunt S, Allende L. 25.  et al. 2010. Sphingosine kinase 1 and sphingosine-1-phosphate receptor 2 are vital to recovery from anaphylactic shock in mice. J. Clin. Investig. 120:1429–40 [Google Scholar]
  26. Liang J, Nagahashi M, Kim EY, Harikumar KB, Yamada A. 26.  et al. 2013. Sphingosine-1-phosphate links persistent STAT3 activation, chronic intestinal inflammation, and development of colitis-associated cancer. Cancer Cell 23:107–20 [Google Scholar]
  27. Kharel Y, Morris EA, Congdon MD, Thorpe SB, Tomsig JL. 27.  et al. 2015. Sphingosine kinase 2 inhibition and blood sphingosine 1-phosphate levels. J. Pharmacol. Exp. Ther. 355:23–31 [Google Scholar]
  28. Takuwa N, Ohkura S, Takashima S, Ohtani K, Okamoto Y. 28.  et al. 2010. S1P3-mediated cardiac fibrosis in sphingosine kinase 1 transgenic mice involves reactive oxygen species. Cardiovasc. Res. 85:484–93 [Google Scholar]
  29. Kawahara A, Nishi T, Hisano Y, Fukui H, Yamaguchi A, Mochizuki N. 29.  2009. The sphingolipid transporter Spns2 functions in migration of zebrafish myocardial precursors. Science 323:524–27 [Google Scholar]
  30. Osborne N, Brand-Arzamendi K, Ober EA, Jin SW, Verkade H. 30.  et al. 2008. The spinster homolog, two of hearts, is required for sphingosine 1-phosphate signaling in zebrafish. Curr. Biol. 18:1882–88 [Google Scholar]
  31. Fukuhara S, Simmons S, Kawamura S, Inoue A, Orba Y. 31.  et al. 2012. The sphingosine-1-phosphate transporter Spns2 expressed on endothelial cells regulates lymphocyte trafficking in mice. J. Clin. Investig. 122:1416–26 [Google Scholar]
  32. Hisano Y, Kobayashi N, Yamaguchi A, Nishi T. 32.  2012. Mouse SPNS2 functions as a sphingosine-1-phosphate transporter in vascular endothelial cells. PLOS ONE 7:e38941 [Google Scholar]
  33. Mendoza A, Bréart B, Ramos-Perez WD, Pitt LA, Gobert M. 33.  et al. 2012. The transporter Spns2 is required for secretion of lymph but not plasma sphingosine-1-phosphate. Cell Rep 2:1104–10 [Google Scholar]
  34. Nagahashi M, Kim EY, Yamada A, Ramachandran S, Allegood JC. 34.  et al. 2013. Spns2, a transporter of phosphorylated sphingoid bases, regulates their blood and lymph levels, and the lymphatic network. FASEB J 27:1001–11 [Google Scholar]
  35. Honig SM, Fu S, Mao X, Yopp A, Gunn MD. 35.  et al. 2003. FTY720 stimulates multidrug transporter- and cysteinyl leukotriene-dependent T cell chemotaxis to lymph nodes. J. Clin. Investig. 111:627–37 [Google Scholar]
  36. Mitra P, Oskeritzian CA, Payne SG, Beaven MA, Milstien S, Spiegel S. 36.  2006. Role of ABCC1 in export of sphingosine-1-phosphate from mast cells. PNAS 103:16394–99 [Google Scholar]
  37. Kobayashi N, Nishi T, Hirata T, Kihara A, Sano T. 37.  et al. 2006. Sphingosine 1-phosphate is released from the cytosol of rat platelets in a carrier-mediated manner. J. Lipid Res. 47:614–21 [Google Scholar]
  38. Sato K, Malchinkhuu E, Horiuchi Y, Mogi C, Tomura H. 38.  et al. 2007. Critical role of ABCA1 transporter in sphingosine 1-phosphate release from astrocytes. J. Neurochem. 103:2610–19 [Google Scholar]
  39. Takabe K, Kim RH, Allegood JC, Mitra P, Ramachandran S. 39.  et al. 2010. Estradiol induces export of sphingosine 1-phosphate from breast cancer cells via ABCC1 and ABCG2. J. Biol. Chem. 285:10477–86 [Google Scholar]
  40. Hisano Y, Kobayashi N, Kawahara A, Yamaguchi A, Nishi T. 40.  2011. The sphingosine 1-phosphate transporter, SPNS2, functions as a transporter of the phosphorylated form of the immunomodulating agent FTY720. J. Biol. Chem. 286:1758–66 [Google Scholar]
  41. Bode C, Sensken SC, Peest U, Beutel G, Thol F. 41.  et al. 2010. Erythrocytes serve as a reservoir for cellular and extracellular sphingosine 1-phosphate. J. Cell. Biochem. 109:1232–43 [Google Scholar]
  42. Kimura T, Tomura H, Mogi C, Kuwabara A, Damirin A. 42.  et al. 2006. Role of scavenger receptor class B type I and sphingosine 1-phosphate receptors in high density lipoprotein-induced inhibition of adhesion molecule expression in endothelial cells. J. Biol. Chem. 281:37457–67 [Google Scholar]
  43. Argraves KM, Gazzolo PJ, Groh EM, Wilkerson BA, Matsuura BS. 43.  et al. 2008. High density lipoprotein-associated sphingosine 1-phosphate promotes endothelial barrier function. J. Biol. Chem. 283:25074–81 [Google Scholar]
  44. Wilkerson BA, Grass GD, Wing SB, Argraves WS, Argraves KM. 44.  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. 287:44645–53 [Google Scholar]
  45. Blaho VA, Galvani S, Engelbrecht E, Liu C, Swendeman SL. 45.  et al. 2015. HDL-bound sphingosine-1-phosphate restrains lymphopoiesis and neuroinflammation. Nature 523:342–46 [Google Scholar]
  46. Galvani S, Sanson M, Blaho VA, Swendeman SL, Obinata H. 46.  et al. 2015. HDL-bound sphingosine 1-phosphate acts as a biased agonist for the endothelial cell receptor S1P1 to limit vascular inflammation. Sci. Signal. 8:ra79 [Google Scholar]
  47. Murata N, Sato K, Kon J, Tomura H, Yanagita M. 47.  et al. 2000. Interaction of sphingosine 1-phosphate with plasma components, including lipoproteins, regulates the lipid receptor-mediated actions. Biochem. J. 352:Pt. 3809–15 [Google Scholar]
  48. Christoffersen C, Obinata H, Kumaraswamy SB, Galvani S, Ahnström J. 48.  et al. 2011. Endothelium-protective sphingosine-1-phosphate provided by HDL-associated apolipoprotein M. PNAS 108:9613–18 [Google Scholar]
  49. Christoffersen C, Nielsen LB, Axler O, Andersson A, Johnsen AH, Dahlbäck B. 49.  2006. Isolation and characterization of human apolipoprotein M-containing lipoproteins. J. Lipid Res. 47:1833–43 [Google Scholar]
  50. Kurano M, Tsukamoto K, Ohkawa R, Hara M, Iino J. 50.  et al. 2013. Liver involvement in sphingosine 1-phosphate dynamism revealed by adenoviral hepatic overexpression of apolipoprotein M. Atherosclerosis 229:102–9 [Google Scholar]
  51. Sevvana M, Ahnström J, Egerer-Sieber C, Lange HA, Dahlbäck B, Muller YA. 51.  2009. Serendipitous fatty acid binding reveals the structural determinants for ligand recognition in apolipoprotein M. J. Mol. Biol. 393:920–36 [Google Scholar]
  52. Yatomi Y, Ohmori T, Rile G, Kazama F, Okamoto H. 52.  et al. 2000. Sphingosine 1-phosphate as a major bioactive lysophospholipid that is released from platelets and interacts with endothelial cells. Blood 96:3431–38 [Google Scholar]
  53. Weber C, Krueger A, Munk A, Bode C, Van Veldhoven PP, Gräler MH. 53.  2009. Discontinued postnatal thymocyte development in sphingosine 1-phosphate-lyase-deficient mice. J. Immunol. 183:4292–301 [Google Scholar]
  54. Vogel P, Donoviel MS, Read R, Hansen GM, Hazlewood J. 54.  et al. 2009. Incomplete inhibition of sphingosine 1-phosphate lyase modulates immune system function yet prevents early lethality and non-lymphoid lesions. PLOS ONE 4:e4112 [Google Scholar]
  55. Bektas M, Allende ML, Lee BG, Chen W, Amar MJ. 55.  et al. 2010. Sphingosine 1-phosphate lyase deficiency disrupts lipid homeostasis in liver. J. Biol. Chem. 285:10880–89 [Google Scholar]
  56. Ito K, Anada Y, Tani M, Ikeda M, Sano T. 56.  et al. 2007. Lack of sphingosine 1-phosphate-degrading enzymes in erythrocytes. Biochem. Biophys. Res. Commun. 357:212–17 [Google Scholar]
  57. Mandala SM. 57.  2001. Sphingosine-1-phosphate phosphatases. Prostaglandins Other Lipid Mediat 64:143–56 [Google Scholar]
  58. Pyne S, Long JS, Ktistakis NT, Pyne NJ. 58.  2005. Lipid phosphate phosphatases and lipid phosphate signalling. Biochem. Soc. Trans. 33:1370–74 [Google Scholar]
  59. Bréart B, Ramos-Perez WD, Mendoza A, Salous AK, Gobert M. 59.  et al. 2011. Lipid phosphate phosphatase 3 enables efficient thymic egress. J. Exp. Med. 208:1267–78 [Google Scholar]
  60. Eilken HM, Adams RH. 60.  2010. Dynamics of endothelial cell behavior in sprouting angiogenesis. Curr. Opin. Cell Biol. 22:617–25 [Google Scholar]
  61. Bergstrand CG, Czar B. 61.  1956. Demonstration of a new protein fraction in serum from the human fetus. Scand. J. Clin. Lab. Investig. 8:174 [Google Scholar]
  62. Tilghman SM, Belayew A. 62.  1982. Transcriptional control of the murine albumin/alpha-fetoprotein locus during development. PNAS 79:5254–57 [Google Scholar]
  63. Zhang XY, Jiao GQ, Hurtig M, Dong X, Zheng L. 63.  et al. 2004. Expression pattern of apolipoprotein M during mouse and human embryogenesis. Acta Histochem 106:123–28 [Google Scholar]
  64. Gabant P, Forrester L, Nichols J, Van Reeth T, De Mees C. 64.  et al. 2002. Alpha-fetoprotein, the major fetal serum protein, is not essential for embryonic development but is required for female fertility. PNAS 99:12865–70 [Google Scholar]
  65. Mizugishi K, Yamashita T, Olivera A, Miller GF, Spiegel S, Proia RL. 65.  2005. Essential role for sphingosine kinases in neural and vascular development. Mol. Cell. Biol. 25:11113–21 [Google Scholar]
  66. Liu Y, Wada R, Yamashita T, Mi Y, Deng CX. 66.  et al. 2000. Edg-1, the G protein-coupled receptor for sphingosine-1-phosphate, is essential for vascular maturation. J. Clin. Investig. 106:951–61 [Google Scholar]
  67. Allende ML, Yamashita T, Proia RL. 67.  2003. G-protein-coupled receptor S1P1 acts within endothelial cells to regulate vascular maturation. Blood 102:3665–67 [Google Scholar]
  68. Ishii I, Ye X, Friedman B, Kawamura S, Contos JJ. 68.  et al. 2002. Marked perinatal lethality and cellular signaling deficits in mice null for the two sphingosine 1-phosphate (S1P) receptors, S1P(2)/LP(B2)/EDG-5 and S1P(3)/LP(B3)/EDG-3. J. Biol. Chem. 277:25152–59 [Google Scholar]
  69. Kono M, Mi Y, Liu Y, Sasaki T, Allende ML. 69.  et al. 2004. The sphingosine-1-phosphate receptors S1P1, S1P2, and S1P3 function coordinately during embryonic angiogenesis. J. Biol. Chem. 279:29367–73 [Google Scholar]
  70. Pham TH, Baluk P, Xu Y, Grigorova I, Bankovich AJ. 70.  et al. 2010. Lymphatic endothelial cell sphingosine kinase activity is required for lymphocyte egress and lymphatic patterning. J. Exp. Med. 207:17–27 [Google Scholar]
  71. Sloop CH, Dory L, Roheim PS. 71.  1987. Interstitial fluid lipoproteins. J. Lipid Res. 28:225–37 [Google Scholar]
  72. Blaho VA, Hla T. 72.  2011. Regulation of mammalian physiology, development, and disease by the sphingosine 1-phosphate and lysophosphatidic acid receptors. Chem. Rev. 111:6299–320 [Google Scholar]
  73. Obinata H, Hla T. 73.  2012. Sphingosine 1-phosphate in coagulation and inflammation. Semin. Immunopathol. 34:73–91 [Google Scholar]
  74. Blaho VA, Hla T. 74.  2014. An update on the biology of sphingosine 1-phosphate receptors. J. Lipid Res. 55:1596–608 [Google Scholar]
  75. Proia RL, Hla T. 75.  2015. Emerging biology of sphingosine-1-phosphate: its role in pathogenesis and therapy. J. Clin. Investig. 125:1379–87 [Google Scholar]
  76. Du W, Takuwa N, Yoshioka K, Okamoto Y, Gonda K. 76.  et al. 2010. S1P(2), the G protein-coupled receptor for sphingosine-1-phosphate, negatively regulates tumor angiogenesis and tumor growth in vivo in mice. Cancer Res 70:772–81 [Google Scholar]
  77. Liu CH, Thangada S, Lee MJ, Van Brocklyn JR, Spiegel S, Hla T. 77.  1999. Ligand-induced trafficking of the sphingosine-1-phosphate receptor EDG-1. Mol. Biol. Cell 10:1179–90 [Google Scholar]
  78. Watterson KR, Johnston E, Chalmers C, Pronin A, Cook SJ. 78.  et al. 2002. Dual regulation of EDG1/S1P(1) receptor phosphorylation and internalization by protein kinase C and G-protein-coupled receptor kinase 2. J. Biol. Chem. 277:5767–77 [Google Scholar]
  79. Oo ML, Thangada S, Wu MT, Liu CH, Macdonald TL. 79.  et al. 2007. Immunosuppressive and anti-angiogenic sphingosine 1-phosphate receptor-1 agonists induce ubiquitinylation and proteasomal degradation of the receptor. J. Biol. Chem. 282:9082–89 [Google Scholar]
  80. Zachariah MA, Cyster JG. 80.  2010. Neural crest-derived pericytes promote egress of mature thymocytes at the corticomedullary junction. Science 328:1129–35 [Google Scholar]
  81. Sanchez T, Estrada-Hernandez T, Paik JH, Wu MT, Venkataraman K. 81.  et al. 2003. Phosphorylation and action of the immunomodulator FTY720 inhibits vascular endothelial cell growth factor-induced vascular permeability. J. Biol. Chem. 278:47281–90 [Google Scholar]
  82. Kharel Y, Lee S, Snyder AH, Sheasley-O'Neill SL, Morris MA. 82.  et al. 2005. Sphingosine kinase 2 is required for modulation of lymphocyte traffic by FTY720. J. Biol. Chem. 280:36865–72 [Google Scholar]
  83. Cohen JA, Barkhof F, Comi G, Hartung H-P, Khatri BO. 83.  et al. 2010. Oral fingolimod or intramuscular interferon for relapsing multiple sclerosis. N. Engl. J. Med. 362:402–15 [Google Scholar]
  84. Kappos L, Radue EW, O'Connor P, Polman C, Hohlfeld R. 84.  et al. 2010. A placebo-controlled trial of oral fingolimod in relapsing multiple sclerosis. N. Engl. J. Med. 362:387–401 [Google Scholar]
  85. Mandala S, Hajdu R, Bergstrom J, Quackenbush E, Xie J. 85.  et al. 2002. Alteration of lymphocyte trafficking by sphingosine-1-phosphate receptor agonists. Science 296:346–49 [Google Scholar]
  86. Brinkmann V, Davis MD, Heise CE, Albert R, Cottens S. 86.  et al. 2002. The immune modulator FTY720 targets sphingosine 1-phosphate receptors. J. Biol. Chem. 277:21453–57 [Google Scholar]
  87. Gräler MH, Goetzl EJ. 87.  2004. The immunosuppressant FTY720 down-regulates sphingosine 1-phosphate G-protein-coupled receptors. FASEB J 18:551–53 [Google Scholar]
  88. Oo ML, Chang SH, Thangada S, Wu MT, Rezaul K. 88.  et al. 2011. Engagement of S1P(1)-degradative mechanisms leads to vascular leak in mice. J. Clin. Investig. 121:2290–300 [Google Scholar]
  89. Matloubian M, Lo CG, Cinamon G, Lesneski MJ, Xu Y. 89.  et al. 2004. Lymphocyte egress from thymus and peripheral lymphoid organs is dependent on S1P receptor 1. Nature 427:355–60 [Google Scholar]
  90. Barnea G, Strapps W, Herrada G, Berman Y, Ong J. 90.  et al. 2008. The genetic design of signaling cascades to record receptor activation. PNAS 105:64–69 [Google Scholar]
  91. Kono M, Tucker AE, Tran J, Bergner JB, Turner EM, Proia RL. 91.  2014. Sphingosine-1-phosphate receptor 1 reporter mice reveal receptor activation sites in vivo. J. Clin. Investig. 124:2076–86 [Google Scholar]
  92. Ramos-Perez WD, Fang V, Escalante-Alcalde D, Cammer M, Schwab SR. 92.  2015. A map of the distribution of sphingosine 1-phosphate in the spleen. Nat. Immunol. 16:1245–52 [Google Scholar]
  93. Christensen PM, Liu CH, Swendeman SL, Obinata H, Qvortrup K. 93.  et al. 2016. Impaired endothelial barrier function in apolipoprotein M-deficient mice is dependent on sphingosine-1-phosphate receptor 1. FASEB J 30:2351–59 [Google Scholar]
  94. Shenoy SK, Lefkowitz RJ. 94.  2011. β-Arrestin-mediated receptor trafficking and signal transduction. Trends Pharmacol. Sci. 32:521–33 [Google Scholar]
  95. Tatematsu S, Francis SA, Natarajan P, Rader DJ, Saghatelian A. 95.  et al. 2013. Endothelial lipase is a critical determinant of high-density lipoprotein-stimulated sphingosine 1-phosphate-dependent signaling in vascular endothelium. Arterioscler. Thromb. Vasc. Biol. 33:1788–94 [Google Scholar]
  96. Takada Y, Kato C, Kondo S, Korenaga R, Ando J. 96.  1997. Cloning of cDNAs encoding G protein-coupled receptor expressed in human endothelial cells exposed to fluid shear stress. Biochem. Biophys. Res. Commun. 240:737–41 [Google Scholar]
  97. Hughes SK, Wacker BK, Kaneda MM, Elbert DL. 97.  2005. Fluid shear stress modulates cell migration induced by sphingosine 1-phosphate and vascular endothelial growth factor. Ann. Biomed. Eng 331003–14 [Google Scholar]
  98. Aoki S, Osada M, Kaneko M, Ozaki Y, Yatomi Y. 98.  2007. Fluid shear stress enhances the sphingosine 1-phosphate responses in cell-cell interactions between platelets and endothelial cells. Biochem. Biophys. Res. Commun. 358:1054–57 [Google Scholar]
  99. Jung B, Obinata H, Galvani S, Mendelson K, Ding BS. 99.  et al. 2012. Flow-regulated endothelial S1P receptor-1 signaling sustains vascular development. Dev. Cell 23:600–10 [Google Scholar]
  100. Carlson CM, Endrizzi BT, Wu J, Ding X, Weinreich MA. 100.  et al. 2006. Krüppel-like factor 2 regulates thymocyte and T-cell migration. Nature 442:299–302 [Google Scholar]
  101. Bai A, Hu H, Yeung M, Chen J. 101.  2007. Krüppel-like factor 2 controls T cell trafficking by activating L-selectin (CD62L) and sphingosine-1-phosphate receptor 1 transcription. J. Immunol. 178:7632–39 [Google Scholar]
  102. Weinreich MA, Takada K, Skon C, Reiner SL, Jameson SC, Hogquist KA. 102.  2009. KLF2 transcription-factor deficiency in T cells results in unrestrained cytokine production and upregulation of bystander chemokine receptors. Immunity 31:122–30 [Google Scholar]
  103. Dekker RJ, Boon RA, Rondaij MG, Kragt A, Volger OL. 103.  et al. 2006. KLF2 provokes a gene expression pattern that establishes functional quiescent differentiation of the endothelium. Blood 107:4354–63 [Google Scholar]
  104. Parmar KM, Larman HB, Dai G, Zhang Y, Wang ET. 104.  et al. 2006. Integration of flow-dependent endothelial phenotypes by Kruppel-like factor 2. J. Clin. Investig. 116:49–58 [Google Scholar]
  105. Kuo CT, Veselits ML, Barton KP, Lu MM, Clendenin C, Leiden JM. 105.  1997. The LKLF transcription factor is required for normal tunica media formation and blood vessel stabilization during murine embryogenesis. Genes Dev 11:2996–3006 [Google Scholar]
  106. Hahn C, Schwartz MA. 106.  2009. Mechanotransduction in vascular physiology and atherogenesis. Nat. Rev. Mol. Cell Biol. 10:53–62 [Google Scholar]
  107. Ishii I, Friedman B, Ye X, Kawamura S, McGiffert C. 107.  et al. 2001. 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. 276:33697–704 [Google Scholar]
  108. Gaengel K, Niaudet C, Hagikura K, Laviña B, Muhl L. 108.  et al. 2012. The sphingosine-1-phosphate receptor S1PR1 restricts sprouting angiogenesis by regulating the interplay between VE-cadherin and VEGFR2. Dev. Cell 23:587–99 [Google Scholar]
  109. Chae SS, Paik JH, Allende ML, Proia RL, Hla T. 109.  2004. Regulation of limb development by the sphingosine 1-phosphate receptor S1p1/EDG-1 occurs via the hypoxia/VEGF axis. Dev. Biol. 268:441–47 [Google Scholar]
  110. Ben Shoham A, Malkinson G, Krief S, Shwartz Y, Ely Y. 110.  et al. 2012. S1P1 inhibits sprouting angiogenesis during vascular development. Development 139:3859–69 [Google Scholar]
  111. Phng LK, Gerhardt H. 111.  2009. Angiogenesis: a team effort coordinated by notch. Dev. Cell 16:196–208 [Google Scholar]
  112. Paik JH, Skoura A, Chae SS, Cowan AE, Han DK. 112.  et al. 2004. Sphingosine 1-phosphate receptor regulation of N-cadherin mediates vascular stabilization. Genes Dev 18:2392–403 [Google Scholar]
  113. Lindahl P, Johansson BR, Leveen P, Betsholtz C. 113.  1997. Pericyte loss and microaneurysm formation in PDGF-B-deficient mice. Science 277:242–45 [Google Scholar]
  114. Hellström M, Kalén M, Lindahl P, Abramsson A, Betsholtz C. 114.  1999. Role of PDGF-B and PDGFR-β in recruitment of vascular smooth muscle cells and pericytes during embryonic blood vessel formation in the mouse. Development 126:3047–55 [Google Scholar]
  115. Lee MJ, Thangada S, Claffey KP, Ancellin N, Liu CH. 115.  et al. 1999. Vascular endothelial cell adherens junction assembly and morphogenesis induced by sphingosine-1-phosphate. Cell 99:301–12 [Google Scholar]
  116. Xiong Y, Hla T. 116.  2014. S1P control of endothelial integrity. Curr. Top. Microbiol. Immunol. 378:85–105 [Google Scholar]
  117. Li X, Stankovic M, Bonder CS, Hahn CN, Parsons M. 117.  et al. 2008. Basal and angiopoietin-1-mediated endothelial permeability is regulated by sphingosine kinase-1. Blood 111:3489–97 [Google Scholar]
  118. Camerer E, Regard JB, Cornelissen I, Srinivasan Y, Duong DN. 118.  et al. 2009. Sphingosine-1-phosphate in the plasma compartment regulates basal and inflammation-induced vascular leak in mice. J. Clin. Investig. 119:1871–79 [Google Scholar]
  119. Sanna MG, Wang SK, Gonzalez-Cabrera PJ, Don A, Marsolais D. 119.  et al. 2006. Enhancement of capillary leakage and restoration of lymphocyte egress by a chiral S1P1 antagonist in vivo. Nat. Chem. Biol. 2:434–41 [Google Scholar]
  120. Montrose DC, Scherl EJ, Bosworth BP, Zhou XK, Jung B. 120.  et al. 2013. S1P(1) localizes to the colonic vasculature in ulcerative colitis and maintains blood vessel integrity. J. Lipid Res. 54:843–51 [Google Scholar]
  121. Oskeritzian CA, Price MM, Hait NC, Kapitonov D, Falanga YT. 121.  et al. 2010. Essential roles of sphingosine-1-phosphate receptor 2 in human mast cell activation, anaphylaxis, and pulmonary edema. J. Exp. Med. 207:465–74 [Google Scholar]
  122. Olivera A, Dillahunt SE, Rivera J. 122.  2013. Interrogation of sphingosine-1-phosphate receptor 2 function in vivo reveals a prominent role in the recovery from IgE and IgG-mediated anaphylaxis with minimal effect on its onset. Immunol. Lett. 150:89–96 [Google Scholar]
  123. Cui H, Okamoto Y, Yoshioka K, Du W, Takuwa N. 123.  et al. 2013. Sphingosine-1-phosphate receptor 2 protects against anaphylactic shock through suppression of endothelial nitric oxide synthase in mice. J. Allergy Clin. Immunol. 132:1205–14.e9 [Google Scholar]
  124. Cruz-Orengo L, Daniels BP, Dorsey D, Basak SA, Grajales-Reyes JG. 124.  et al. 2014. Enhanced sphingosine-1-phosphate receptor 2 expression underlies female CNS autoimmunity susceptibility. J. Clin. Investig. 124:2571–84 [Google Scholar]
  125. Kim GS, Yang L, Zhang G, Zhao H, Selim M. 125.  et al. 2015. Critical role of sphingosine-1-phosphate receptor-2 in the disruption of cerebrovascular integrity in experimental stroke. Nat. Commun. 6:7893 [Google Scholar]
  126. Kappos L, Antel J, Comi G, Montalban X, O'Connor P. 126.  et al. 2006. Oral fingolimod (FTY720) for relapsing multiple sclerosis. N. Engl. J. Med. 355:1124–40 [Google Scholar]
  127. van Doorn R, Lopes Pinheiro MA, Kooij G, Lakeman K, van het Hof B. 127.  et al. 2012. Sphingosine 1-phosphate receptor 5 mediates the immune quiescence of the human brain endothelial barrier. J. Neuroinflamm. 9:133 [Google Scholar]
  128. Cannon RE, Peart JC, Hawkins BT, Campos CR, Miller DS. 128.  2012. Targeting blood-brain barrier sphingolipid signaling reduces basal P-glycoprotein activity and improves drug delivery to the brain. PNAS 109:15930–35 [Google Scholar]
  129. Cartwright TA, Campos CR, Cannon RE, Miller DS. 129.  2013. Mrp1 is essential for sphingolipid signaling to p-glycoprotein in mouse blood-brain and blood-spinal cord barriers. J. Cereb. Blood Flow Metab. 33:381–88 [Google Scholar]
  130. Herzog BH, Fu J, Wilson SJ, Hess PR, Sen A. 130.  et al. 2013. Podoplanin maintains high endothelial venule integrity by interacting with platelet CLEC-2. Nature 502:105–9 [Google Scholar]
  131. Lorenz JN, Arend LJ, Robitz R, Paul RJ, MacLennan AJ. 131.  2007. Vascular dysfunction in S1P2 sphingosine 1-phosphate receptor knockout mice. Am. J. Physiol. Regul. Integr. Comp. Physiol. 292:R440–46 [Google Scholar]
  132. Igarashi J, Michel T. 132.  2009. Sphingosine-1-phosphate and modulation of vascular tone. Cardiovasc. Res. 82:212–20 [Google Scholar]
  133. Igarashi J, Bernier SG, Michel T. 133.  2001. Sphingosine 1-phosphate and activation of endothelial nitric-oxide synthase. differential regulation of Akt and MAP kinase pathways by EDG and bradykinin receptors in vascular endothelial cells. J. Biol. Chem. 276:12420–26 [Google Scholar]
  134. Morales-Ruiz M, Lee MJ, Zöllner S, Gratton JP, Scotland R. 134.  et al. 2001. Sphingosine 1-phosphate activates Akt, nitric oxide production, and chemotaxis through a Giprotein/phosphoinositide 3-kinase pathway in endothelial cells. J. Biol. Chem. 276:19672–77 [Google Scholar]
  135. Kimura T, Sato K, Kuwabara A, Tomura H, Ishiwara M. 135.  et al. 2001. Sphingosine 1-phosphate may be a major component of plasma lipoproteins responsible for the cytoprotective actions in human umbilical vein endothelial cells. J. Biol. Chem. 276:31780–85 [Google Scholar]
  136. Dantas AP, Igarashi J, Michel T. 136.  2003. Sphingosine 1-phosphate and control of vascular tone. Am. J. Physiol. Heart Circ. Physiol. 284:H2045–52 [Google Scholar]
  137. Igarashi J, Miyoshi M, Hashimoto T, Kubota Y, Kosaka H. 137.  2007. Statins induce S1P1 receptors and enhance endothelial nitric oxide production in response to high-density lipoproteins. Br. J. Pharmacol. 150:470–79 [Google Scholar]
  138. Cantalupo A, Zhang Y, Kothiya M, Galvani S, Obinata H. 138.  et al. 2015. Nogo-B regulates endothelial sphingolipid homeostasis to control vascular function and blood pressure. Nat. Med. 21:1028–37 [Google Scholar]
  139. Szczepaniak WS, Pitt BR, McVerry BJ. 139.  2010. S1P2 receptor-dependent Rho-kinase activation mediates vasoconstriction in the murine pulmonary circulation induced by sphingosine 1-phosphate. Am. J. Physiol. Lung Cell. Mol. Physiol. 299:L137–45 [Google Scholar]
  140. Salomone S, Potts EM, Tyndall S, Ip PC, Chun J. 140.  et al. 2008. Analysis of sphingosine 1-phosphate receptors involved in constriction of isolated cerebral arteries with receptor null mice and pharmacological tools. Br. J. Pharmacol. 153:140–47 [Google Scholar]
  141. Guan Z, Singletary ST, Cook AK, Hobbs JL, Pollock JS, Inscho EW. 141.  2014. Sphingosine-1-phosphate evokes unique segment-specific vasoconstriction of the renal microvasculature. J. Am. Soc. Nephrol. 25:1774–85 [Google Scholar]
  142. MacLennan AJ, Benner SJ, Andringa A, Chaves AH, Rosing JL. 142.  et al. 2006. The S1P2 sphingosine 1-phosphate receptor is essential for auditory and vestibular function. Hear. Res. 220:38–48 [Google Scholar]
  143. Herr DR, Grillet N, Schwander M, Rivera R, Müller U, Chun J. 143.  2007. Sphingosine 1-phosphate (S1P) signaling is required for maintenance of hair cells mainly via activation of S1P2. J. Neurosci. 27:1474–78 [Google Scholar]
  144. Kono M, Belyantseva IA, Skoura A, Frolenkov GI, Starost MF. 144.  et al. 2007. Deafness and stria vascularis defects in S1P2 receptor-null mice. J. Biol. Chem. 282:10690–96 [Google Scholar]
  145. Scherer EQ, Lidington D, Oestreicher E, Arnold W, Pohl U, Bolz SS. 145.  2006. Sphingosine-1-phosphate modulates spiral modiolar artery tone: A potential role in vascular-based inner ear pathologies?. Cardiovasc. Res. 70:79–87 [Google Scholar]
  146. Chen J, Ingham N, Kelly J, Jadeja S, Goulding D. 146.  et al. 2014. Spinster homolog 2 (Spns2) deficiency causes early onset progressive hearing loss. PLOS Genet 10:e1004688 [Google Scholar]
  147. Santos-Cortez RL, Faridi R, Rehman AU, Lee K, Ansar M. 147.  et al. 2016. Autosomal-recessive hearing impairment due to rare missense variants within S1PR2. Am. J. Hum. Genet. 98:331–38 [Google Scholar]
  148. Nofer JR, van der Giet M, Tölle M, Wolinska I, von Wnuck Lipinski K. 148.  et al. 2004. HDL induces NO-dependent vasorelaxation via the lysophospholipid receptor S1P3. J. Clin. Investig. 113:569–81 [Google Scholar]
  149. Salomone S, Yoshimura S, Reuter U, Foley M, Thomas SS. 149.  et al. 2003. S1P3 receptors mediate the potent constriction of cerebral arteries by sphingosine-1-phosphate. Eur. J. Pharmacol. 469:125–34 [Google Scholar]
  150. Gergely P, Nuesslein-Hildesheim B, Guerini D, Brinkmann V, Traebert M. 150.  et al. 2012. The selective sphingosine 1-phosphate receptor modulator BAF312 redirects lymphocyte distribution and has species-specific effects on heart rate. Br. J. Pharmacol. 167:1035–47 [Google Scholar]
  151. Legangneux E, Gardin A, Johns D. 151.  2013. Dose titration of BAF312 attenuates the initial heart rate reducing effect in healthy subjects. Br. J. Clin. Pharmacol. 75:831–41 [Google Scholar]
  152. Pham TH, Okada T, Matloubian M, Lo CG, Cyster JG. 152.  2008. S1P1 receptor signaling overrides retention mediated by G alpha i-coupled receptors to promote T cell egress. Immunity 28:122–33 [Google Scholar]
  153. Lo CG, Xu Y, Proia RL, Cyster JG. 153.  2005. Cyclical modulation of sphingosine-1-phosphate receptor 1 surface expression during lymphocyte recirculation and relationship to lymphoid organ transit. J. Exp. Med. 201:291–301 [Google Scholar]
  154. Arnon TI, Xu Y, Lo C, Pham T, An J. 154.  et al. 2011. GRK2-dependent S1PR1 desensitization is required for lymphocytes to overcome their attraction to blood. Science 333:1898–903 [Google Scholar]
  155. Green JA, Suzuki K, Cho B, Willison LD, Palmer D. 155.  et al. 2011. The sphingosine 1-phosphate receptor S1P(2) maintains the homeostasis of germinal center B cells and promotes niche confinement. Nat. Immunol. 12:672–80 [Google Scholar]
  156. Czeloth N, Bernhardt G, Hofmann F, Genth H, Förster R. 156.  2005. Sphingosine-1-phosphate mediates migration of mature dendritic cells. J. Immunol. 175:2960–67 [Google Scholar]
  157. Walzer T, Chiossone L, Chaix J, Calver A, Carozzo C. 157.  et al. 2007. Natural killer cell trafficking in vivo requires a dedicated sphingosine 1-phosphate receptor. Nat. Immunol. 8:1337–44 [Google Scholar]
  158. Jenne CN, Enders A, Rivera R, Watson SR, Bankovich AJ. 158.  et al. 2009. T-bet-dependent S1P5 expression in NK cells promotes egress from lymph nodes and bone marrow. J. Exp. Med. 206:2469–81 [Google Scholar]
  159. Massberg S, Schaerli P, Knezevic-Maramica I, Köllnberger M, Tubo N. 159.  et al. 2007. Immunosurveillance by hematopoietic progenitor cells trafficking through blood, lymph, and peripheral tissues. Cell 131:994–1008 [Google Scholar]
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Vascular and Immunobiology of the Circulatory Sphingosine 1-Phosphate Gradient
Annual Review of Physiology 79, 67 (2017); https://doi.org/10.1146/annurev-physiol-021014-071635
/content/journals/10.1146/annurev-physiol-021014-071635
/content/journals/10.1146/annurev-physiol-021014-071635
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