Sphingosine-I-phosphate: A bioactive lipid that confers high-density lipoprotein with vasculoprotection mediated by nitric oxide and prostacyclin

Thrombosis and Haemostasis

Volumn 101, Issue 4, 2009, Pages 665-673

  Rodríguez, Cristina ^a   González Díez, María ^a   Badimon, Lina ^a   Martínez González, José ^a  

^a HOSPITAL DE LA SANTA CREU I SANT PAU   (Spain)

Author keywords

High density lipoproteins; Nitric oxide; Prostacyclin; Sphingosine I phosphate; Vascular function

Indexed keywords

FINGOLIMOD; G PROTEIN COUPLED RECEPTOR; HIGH DENSITY LIPOPROTEIN; NITRIC OXIDE; PROSTACYCLIN; SIMVASTATIN; SPHINGOSINE 1 PHOSPHATE; SPHINGOSINE 1 PHOSPHATE RECEPTOR; DRUG DERIVATIVE; LYSOPHOSPHOLIPID; SPHINGOSINE; SPHINGOSINE 1-PHOSPHATE;

APOPTOSIS; ATHEROSCLEROSIS; CELL FUNCTION; CELL SURVIVAL; ENDOTHELIUM CELL; HEART PROTECTION; HUMAN; MACROPHAGE; MONOCYTE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; REVIEW; SMOOTH MUSCLE FIBER; UPREGULATION; ANGIOGENESIS; ANIMAL; BLOOD; CELL ADHESION; CELL MOTION; CELL PROLIFERATION; METABOLISM; PATHOPHYSIOLOGY; SIGNAL TRANSDUCTION; VASCULAR DISEASE; VASCULAR ENDOTHELIUM; VASCULAR SMOOTH MUSCLE; VASODILATATION;

ANIMALS; CELL ADHESION; CELL MOVEMENT; CELL PROLIFERATION; CELL SURVIVAL; ENDOTHELIUM, VASCULAR; EPOPROSTENOL; HUMANS; LIPOPROTEINS, HDL; LYSOPHOSPHOLIPIDS; MACROPHAGES; MONOCYTES; MUSCLE, SMOOTH, VASCULAR; NEOVASCULARIZATION, PHYSIOLOGIC; NITRIC OXIDE; RECEPTORS, LYSOSPHINGOLIPID; SIGNAL TRANSDUCTION; SPHINGOSINE; VASCULAR DISEASES; VASODILATION;

EID: 64849106325     PISSN: 03406245     EISSN: None     Source Type: Journal    
DOI: 10.1160/TH08-10-0675     Document Type: Review

References (95)

1. Yatomi Y, Ozaki Y, Ohmori T, et al. Sphingosine 1-phosphate: synthesis and release. Prostaglandins Other Lipid Mediat 2001; 64: 107-122.
2. Hänel P, Andréani P, Gräler MH. Erythrocytes store and release sphingosine 1-phosphate in blood. FASEB J 2007; 21: 1202-1209.
3. Venkataraman K, Lee YM, Michaud J, et al. Vascular endothelium as a contributor of plasma sphingosine 1-phosphate. Circ Res 2008; 102: 669-676.
4. 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: 16394-16399.
5. Okajima F. Plasma lipoproteins behave as carriers of extracellular sphingosine 1-phosphate: is this an atherogenic mediator or an anti-atherogenic mediator? Biochim Biophys Acta 2002; 1582: 132-137.
6. Rhoads GG, Gulbrandsen CL, Kagan A. Serum lipoproteins and coronary heart disease in a population study of Hawaii Japanese men. N Engl J Med 1976; 294: 293-298.
7. Badimon JJ, Badimon L, Galvez A, et al. High density lipoprotein plasma fractions inhibit aortic fatty streaks in cholesterol-fed rabbits. Lab Invest 1989; 60: 455-461.
8. Badimon JJ, Badimon L, Fuster V. Regression of atherosclerotic lesions by high density lipoprotein plasma fraction in the cholesterol-fed rabbit. J Clin Invest 1990; 85: 1234-1241.
9. Ibanez B, Vilahur G, Cimmino G, et al. Rapid change in plaque size, composition, and molecular footprint after recombinant apolipoprotein A-I Milano (ETC-216) administration: magnetic resonance imaging study in an experimental model of atherosclerosis. J Am Coll Cardiol 2008; 51: 1104-1109.
10. Assmann G, Nofer JR. Atheroprotective effects of high-density lipoproteins. Annu Rev Med 2003; 54: 321-341.
11. Mineo C, Deguchi H, Griffin JH, Shaul PW. Endothelial and antithrombotic actions of HDL. Circ Res 2006; 98: 1352-1364.
12. Barter PJ, Puranik R, Rye KA. New insights into the role of HDL as an anti-inflammatory agent in the prevention of cardiovascular disease. Curr Cardiol Rep 2007; 9: 493-498.
13. Spiegel S, Milstien S. Sphingosine-1-phosphate: an enigmatic signalling lipid. Nat Rev Mol Cell Biol 2003; 4: 397-407.
14. Nofer JR, van der Giet M, Tölle M, et al. HDL induces NO-dependent vasorelaxation via the lysophospholipid receptor S1P3. J Clin Invest 2004; 113: 569-581.
15. Miura S, Fujino M, Matsuo Y, et al. High density lipoprotein-induced angiogenesis requires the activation of Ras/MAP kinase in human coronary artery endothelial cells. Arterioscler Thromb Vasc Biol 2003; 23: 802-808.
16. von Otte S, Paletta JR, Becker S, et al. Follicular fluid high density lipoprotein-associated sphingosine 1-phosphate is a novel mediator of ovarian angiogenesis. J Biol Chem 2006; 281: 5398-5405.
17. Nofer JR, Bot M, Brodde M, et al. FTY720, a synthetic sphingosine 1 phosphate analogue, inhibits development of atherosclerosis in low-density lipoprotein receptor-deficient mice. Circulation 2007; 115: 501-508.
18. Theilmeier G, Schmidt C, Herrmann J, et al. Highdensity lipoproteins and their constituent, sphingosine- 1-phosphate, directly protect the heart against ischemia/reperfusion injury in vivo via the S1P3 lysophospholipid receptor. Circulation 2006; 114: 1403-1409.
19. Alewijnse AE, Peters SL. Sphingolipid signalling in the cardiovascular system: good, bad or both? Eur J Pharmacol 2008; 585: 292-302.
20. Yatomi Y. Sphingosine 1-phosphate in vascular biology: possible therapeutic strategies to control vascular diseases. Curr Pharm Des 2006; 12: 575-587.
21. Keul P, Tölle M, Lucke S, et al. The sphingosine- 1-phosphate analogue FTY720 reduces atherosclerosis in apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol 2007; 27: 607-613.
22. Martínez-González J, Badimon L. Influence of statin use on endothelial function: from bench to clinics. Curr Pharm Des 2007; 13: 1771-1786.
23. Igarashi J, Miyoshi M, Hashimoto T, et al. Statins induce S1P1 receptors and enhance endothelial nitric oxide production in response to high-density lipoproteins. Br J Pharmacol 2007; 150: 470-479.
24. González-Díez M, Rodríguez C, Badimon L, Martínez-González J. Prostacyclin induction by high-density lipoprotein (HDL) in vascular smooth muscle cells depends on sphingosine 1-phosphate receptors: effect of simvastatin. Thromb Haemost 2008; 100: 119-126.
25. 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: 295-298.
26. Ohkawa R, Nakamura K, Okubo S, et al. Plasma sphingosine-1-phosphate measurement in healthy subjects: close correlation with red blood cell parameters. Ann Clin Biochem 2008; 45: 356-363.
27. Hla T, Venkataraman K, Michaud J. The vascular S1P gradient-Cellular sources and biological significance. Biochim Biophys Acta 2008; 1781: 477-482.
28. Waeber C, Blondeau N, Salomone S. Vascular sphingosine-1-phosphate S1P1 and S1P3 receptors. Drug News Perspect 2004; 17: 365-382.
29. Kimura T, Watanabe T, Sato K, et al. Sphingosine 1-phosphate stimulates proliferation and migration of human endothelial cells possibly through the lipid receptors, Edg-1 and Edg-3. Biochem J 2000; 348: 71-76.
30. Tamama K, Kon J, Sato K, et al. Extracellular mechanism through the Edg family of receptors might be responsible for sphingosine-1-phosphate-induced regulation of DNA synthesis and migration of rat aortic smooth-muscle cells. Biochem J 2001; 353: 139-146.
31. Mazurais D, Robert P, Gout B, et al. Cell type-specific localization of human cardiac S1P receptors. J Histochem Cytochem 2002; 50: 661-670.
32. Ryu Y, Takuwa N, Sugimoto N, et al. Sphingosine- 1-phosphate, a platelet-derived lysophospholipid mediator, negatively regulates cellular Rac activity and cell migration in vascular smooth muscle cells. Circ Res 2002; 90: 325-332.
33. Damirin A, Tomura H, Komachi M, et al. Sphingosine 1-phosphate receptors mediate the lipid-induced cAMP accumulation through cyclooxygenase-2/ prostaglandin I2 pathway in human coronary artery smooth muscle cells. Mol Pharmacol 2005; 67: 1177-1185.
34. Michel MC, Mulders AC, Jongsma M, et al. Vascular effects of sphingolipids. Acta Paediatr Suppl 2007; 96: 44-48.
35. Sensken SC, Stäubert C, Keul P, et al. Selective activation of G alpha i mediated signalling of S1P3 by FTY720-phosphate. Cell Signal 2008; 20: 1125-1133.
36. Yuhanna IS, Zhu Y, Cox BE, et al. High-density lipoprotein binding to scavenger receptor-BI activates endothelial nitric oxide synthase. Nat Med 2001; 7: 853-857.
37. Mineo C, Yuhanna IS, Quon MJ, Shaul P W. High density lipoprotein-induced endothelial nitric-oxide synthase activation is mediated by Akt and MAP kinases. J Biol Chem 2003; 278: 9142-9149.
38. Rämet ME, Rämet M, Lu Q, et al. High-density lipoprotein increases the abundance of eNOS protein in human vascular endothelial cells by increasing its halflife. J Am Coll Cardiol 2003; 41: 2288-2297.
39. Tölle M, Levkau B, Keul P, et al. Immunomodulator FTY720 Induces eNOS-dependent arterial vasodilatation via the lysophospholipid receptor S1P3. Circ Res 2005; 96: 913-920.
40. Igarashi J, Michel T. Agonist-modulated targeting of the EDG-1 receptor to plasmalemmal caveolae. eNOS activation by sphingosine 1-phosphate and the role of caveolin-1 in sphingolipid signal transduction. J Biol Chem 2000; 275: 32363-32370.
41. Roviezzo F, Bucci M, Delisle C, et al. Essential requirement for sphingosine kinase activity in eNOS- dependent NO release and vasorelaxation. FASEB J 2006; 20: 340-342.
42. Viñals M, Martinez-Gonzalez J, Badimon JJ, et al. HDL-induced prostacyclin release in smooth muscle cells is dependent on cyclooxygenase-2 (Cox-2). Arterioscler Thromb Vasc Biol 1997; 17: 3481-3488.
43. Viñals M, Martinez-Gonzalez J, Badimon L. Regulatory effects of HDL on smooth muscle cell prostacyclin release. Arterioscler Thromb Vasc Biol 1999; 19: 2405-2411.
44. Cockerill G W, Saklatvala J, Ridley SH, et al. Highdensity lipoproteins differentially modulate cytokineinduced expression of E-selectin and cyclooxygenase-2. Arterioscler Thromb Vasc Biol 1999; 19: 910-917.
45. Norata GD, Callegari E, Inoue H, Catapano AL. HDL3 induces cyclooxygenase-2 expression and prostacyclin release in human endothelial cells via a p38 MAPK/CRE-dependent pathway: effects on COX- 2/PGI-synthase coupling. Arterioscler Thromb Vasc Biol 2004; 24: 871-877.
46. Escudero I, Martínez-González J, Alonso R, et al. Experimental and interventional dietary study in humans on the role of HDL fatty acid composition in PGI2 release and Cox-2 expression by VSMC. Eur J Clin Invest 2003; 33: 779-786.
47. Martínez-González J, Badimon L. Mechanisms underlying the cardiovascular effects of COX-inhibition: benefits and risks. Curr Pharm Des 2007; 13: 2215-2227.
48. Topper JN, Cai J, Falb D, Gimbrone MA Jr. Identification of vascular endothelial genes differentially responsive to fluid mechanical stimuli. Proc Natl Acad Sci USA 1996; 93: 10417-10422.
49. 2 release induced by HDL in human VSMC: effect on Cox-2 up-regulation and MAPK signalling pathways activated by HDL. Atherosclerosis 2004; 174: 305-313.
50. Ohmori T, Yatomi Y, Osada M, et al. Sphingosine 1-phosphate induces contraction of coronary artery smooth muscle cells via S1P2. Cardiovasc Res 2003; 58: 170-177.
51. Salomone S, Potts EM, Tyndall S, et al. Analysis of sphingosine 1-phosphate receptors involved in constriction of isolated cerebral arteries with receptor null mice and pharmacological tools. Br J Pharmacol 2008; 153: 140-147.
52. Cockerill GW, Rye KA, Gamble JR, et al. Highdensity lipoproteins inhibit cytokine-induced expression of endothelial cell adhesion molecules. Arterioscler Thromb Vasc Biol 1995; 15: 1987-1994.
53. Schmidt A, Geigenmüller S, Völker W, Buddecke E. The antiatherogenic and antiinflammatory effect of HDL-associated lysosphingolipids operates via Akt ->NF-kappaB signalling pathways in human vascular endothelial cells. Basic Res Cardiol 2006; 101: 109-116.
54. Kimura T, Tomura H, Mogi C, et al. 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 2006; 281: 37457-37467.
55. Lee H, Lin CI, Liao JJ, et al. Lysophospholipids increase ICAM-1 expression in HUVEC through a Giand NF-kappaB-dependent mechanism. Am J Physiol Cell Physiol 2004; 287: C1657-1666.
56. Xia P, Vadas MA, Rye KA, et al. High density lipoproteins (HDL) interrupt the sphingosine kinase signalling pathway. A possible mechanism for protection against atherosclerosis by HDL. J Biol Chem 1999; 274: 33143-33147.
57. Kase H, Hattori Y, Jojima T, et al. Globular adiponectin induces adhesion molecule expression through the sphingosine kinase pathway in vascular endothelial cells. Life Sci 2007; 81: 939-943.
58. Kimura T, Tomura H, Mogi C, et al. Sphingosine 1-phosphate receptors mediate stimulatory and inhibitory signalings for expression of adhesion molecules in endothelial cells. Cell Signal 2006; 18: 841-850.
59. Whetzel AM, Bolick D T, Srinivasan S, et al. Sphingosine-1 phosphate prevents monocyte/endothelial interactions in type 1 diabetic NOD mice through activation of the S1P1 receptor. Circ Res 2006; 99: 731-739.
60. Tani M, Kawakami A, Nagai M, et al. Sphingosine 1-phosphate (S1P) inhibits monocyte-endothelial cell interaction by regulating of RhoA activity. FEBS Lett 2007; 581: 4621-4626.
61. Aoki S, Yatomi Y, Shimosawa T, et al. The suppressive effect of sphingosine 1-phosphate on monocyte-endothelium adhesion may be mediated by the rearrangement of the endothelial integrins alpha(5)beta(1) and alpha(v)beta(3). J Thromb Haemost 2007; 5: 1292-1301.
62. Nofer JR, Levkau B, Wolinska I, et al. Suppression of endothelial cell apoptosis by high density lipoproteins (HDL) and HDL-associated lysosphingolipids. J Biol Chem 2001; 276: 34480-34485.
63. Kwon YG, Min JK, Kim KM, et al. Sphingosine 1-phosphate protects human umbilical vein endothelial cells from serum-deprived apoptosis by nitric oxide production. J Biol Chem 2001; 276: 10627-10633.
64. Kimura T, Sato K, Kuwabara A, et al. 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 2001; 276: 31780-31785.
65. Kontush A, Therond P, Zerrad A, et al. Preferential sphingosine-1- phosphate enrichment and sphingomyelin depletion are key features of small dense HDL3 particles: relevance to antiapoptotic and antioxidative activities. Arterioscler Thromb Vasc Biol 2007; 27: 1843-1849.
66. Mihovilovic M, Robinette JB, DeKroon RM, et al. High-fat/high-cholesterol diet promotes a S1P receptor-mediated antiapoptotic activity for VLDL. J Lipid Res 2007; 48: 806-815.
67. Lee OH, Kim YM, Lee YM, et al. Sphingosine 1-phosphate induces angiogenesis: its angiogenic action and signalling mechanism in human umbilical vein endothelial cells. Biochem Biophys Res Commun 1999; 264: 743-750.
68. English D, Welch Z, Kovala AT, et al. 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 2000; 14: 2255-2265.
69. Rikitake Y, Hirata K, Kawashima S, et al. Involvement of endothelial nitric oxide in sphingosine-1-phosphate-induced angiogenesis. Arterioscler Thromb Vasc Biol 2002; 22: 108-114.
70. Igarashi J, Erwin PA , Dantas A P, 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: 10664-10669.
71. Kimura T, Sato K, Malchinkhuu E, et al. High-density lipoprotein stimulates endothelial cell migration and survival through sphingosine 1-phosphate and its receptors. Arterioscler Thromb Vasc Biol 2003; 23: 1283-1288.
72. Miura S, Tanigawa H, Matsuo Y, et al. Ras/Raf1-dependent signal in sphingosine-1-phosphate-induced tube formation in human coronary artery endothelial cells. Biochem Biophys Res Commun 2003; 306: 924-929.
73. Matsuo Y, Miura S, Kawamura A, et al. Newly developed reconstituted high-density lipoprotein containing sphingosine-1-phosphate induces endothelial tube formation. Atherosclerosis 2007; 194: 159-168.
74. McVerry BJ, Garcia JG. In vitro and in vivo modulation of vascular barrier integrity by sphingosine 1-phosphate: mechanistic insights. Cell Signal 2005; 17: 131-139.
75. Lee J F, 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: 29190-29200.
76. Xu M, Waters CL, Hu C, et al. Sphingosine 1-phosphate rapidly increases endothelial barrier function independently of VE-cadherin but requires cell spreading and Rho kinase. Am J Physiol Cell Physiol 2007; 293: C1309-1318.
77. Argraves KM, Gazzolo PJ, Groh EM, et al. HDL- associated sphingosine-1-phosphate promotes endothelial barrier function. J Biol Chem 2008; 25074-25081.
78. Noor R, Shuaib U, Wang CX, et al. High-density lipoprotein cholesterol regulates endothelial progenitor cells by increasing eNOS and preventing apoptosis. Atherosclerosis 2007; 192: 92-99.
79. Tso C, Martinic G, Fan WH, et al. High-density lipoproteins enhance progenitor-mediated endothelium repair in mice. Arterioscler Thromb Vasc Biol 2006; 26: 1144-1149.
80. Petoumenos V, Nickenig G, Werner N. High density lipoprotein exerts vasculoprotection via endothelial progenitor cells. J Cell Mol Med 2008 Aug 14; epub ahead of print.
81. Kimura T, Boehmler AM, Seitz G, et al. The sphingosine 1-phosphate receptor agonist FTY720 supports CXCR4-dependent migration and bone marrow homing of human CD34+ progenitor cells. Blood 2004; 103: 4478-4486.
82. Walter DH, Rochwalsky U, Reinhold J, et al. Sphingosine-1-phosphate stimulates the functional capacity of progenitor cells by activation of the CXCR4-dependent signaling pathway via the S1P3 receptor. Arterioscler Thromb Vasc Biol 2007; 27: 275-282.
83. Tamama K, Tomura H, Sato K, et al. High-density lipoprotein inhibits migration of vascular smooth muscle cells through its sphingosine 1-phosphate component. Atherosclerosis 2005; 178: 19-23.
84. Damirin A, Tomura H, Komachi M, et al. Role of lipoprotein-associated lysophospholipids in migratory activity of coronary artery smooth muscle cells. Am J Physiol Heart Circ Physiol 2007; 292: H2513-2522.
85. Hobson J P, Rosenfeldt HM, Barak LS, et al. Role of the sphingosine-1-phosphate receptor EDG-1 in PDGF-induced cell motility. Science 2001; 291: 1800-1803.
86. Lockman K, Hinson JS, Medlin MD, et al. Sphingosine 1-phosphate stimulates smooth muscle cell differentiation and proliferation by activating separate serum response factor co-factors. J Biol Chem 2004; 279: 42422-42430.
87. Kluk MJ, Hla T. Role of the sphingosine 1-phosphate receptor EDG-1 in vascular smooth muscle cell proliferation and migration. Circ Res 2001; 89: 496-502.
88. Takuwa Y. Subtype-specific differential regulation of Rho family G proteins and cell migration by the Edg family sphingosine-1-phosphate receptors. Biochim Biophys Acta 2002; 1582: 112-120.
89. Tölle M, Pawlak A, Schuchardt M, et al. HDL-associated lysosphingolipids inhibit NAD(P)H oxidasedependent monocyte chemoattractant protein-1 production. Arterioscler Thromb Vasc Biol 2008; 28: 1542-1548.
90. Kothapalli D, Fuki I, Ali K, et al. Antimitogenic effects of HDL and APOE mediated by Cox-2-dependent IP activation. J Clin Invest 2004; 113: 609-618.
91. Duong CQ, Bared SM, Abu-Khader A, et al. Expression of the lysophospholipid receptor family and investigation of lysophospholipid-mediated responses in human macrophages. Biochim Biophys Acta 2004; 1682: 112-119.
92. Peng X, Hassoun PM, Sammani S, et al. Protective effects of sphingosine 1-phosphate in murine endotoxin-induced inflammatory lung injury. Am J Respir Crit Care Med 2004; 169: 1245-1251.
93. Dueñas AI, Aceves M, Fernández-Pisonero I, et al. Selective attenuation of Toll-like receptor 2 signalling may explain the atheroprotective effect of sphingosine 1-phosphate. Cardiovasc Res 2008; 79: 537-544.
94. Hughes JE, Srinivasan S, Lynch KR, et al. Sphingosine-1-phosphate induces an antiinflammatory phenotype in macrophages. Circ Res 2008; 102: 950-958.
95. Nissen SE, Tardif JC, Nicholls SJ, et al. Effect of torcetrapib on the progression of coronary atherosclerosis. N Engl J Med 2007; 356: 1304-1316.