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Sphingosine-1-phosphate transport and its role in immunology

  • Received: 25 July 2014 Accepted: 02 December 2014 Published: 10 December 2014
  • Sphingosine-1-phosphate (S1P) is a sphingolipid metabolite with many important functions in cellular and systemic physiology, including the immune system. As it cannot traverse the membrane, it is exported from cells by transporters. Several members of the ATP-binding cassette (ABC) transporter family, ABCA1, ABCC1, ABCG2 and potentially ABCA7 have been identified as S1P transporters. In addition spinster 2 (SPNS2), a protein from the major facilitator superfamily (MFS), was identified as a S1P transporter. Here we review the current knowledge on S1P transport and discuss how this process creates S1P gradients in the body that are important in various functions of the immune system.

    Citation: Vera Reitsema, Hjalmar Bouma, Jan Willem Kok. Sphingosine-1-phosphate transport and its role in immunology[J]. AIMS Molecular Science, 2014, 1(4): 183-201. doi: 10.3934/molsci.2014.4.183

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  • Sphingosine-1-phosphate (S1P) is a sphingolipid metabolite with many important functions in cellular and systemic physiology, including the immune system. As it cannot traverse the membrane, it is exported from cells by transporters. Several members of the ATP-binding cassette (ABC) transporter family, ABCA1, ABCC1, ABCG2 and potentially ABCA7 have been identified as S1P transporters. In addition spinster 2 (SPNS2), a protein from the major facilitator superfamily (MFS), was identified as a S1P transporter. Here we review the current knowledge on S1P transport and discuss how this process creates S1P gradients in the body that are important in various functions of the immune system.


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    [1] Schwab SR, Pereira JP, Matloubian M, et al. (2005) Lymphocyte sequestration through S1P lyase inhibition and disruption of S1P gradients. Science 309: 1735-1739. doi: 10.1126/science.1113640
    [2] Matloubian M, Lo CG, Cinamon G, et al. (2004) Lymphocyte egress from thymus and peripheral lymphoid organs is dependent on S1P receptor 1. Nature 427: 355-360. doi: 10.1038/nature02284
    [3] Tarling EJ, de Aguiar Vallim TQ, Edwards PA (2013) Role of ABC transporters in lipid transport and human disease. Trends Endocrinol Metab 4: 342-350.
    [4] Takabe K, Spiegel S (2014) Export of sphingosine-1-phosphate and cancer progression. J Lipid Res 55: 1839-1846. doi: 10.1194/jlr.R046656
    [5] Kornhuber J, Müller CP, Becker KA, et al. (2014) The ceramide system as a novel antidepressant target. Trends Pharmacol Sci 35: 293-304. doi: 10.1016/j.tips.2014.04.003
    [6] Ito M, Okino N, Tani M. (2014) New insight into the structure, reaction mechanism, and biological functions of neutral ceramidase. Biochim Biophys Acta 1841: 682-691. doi: 10.1016/j.bbalip.2013.09.008
    [7] Kumar A, Saba JD (2009) Lyase to live by: sphingosine phosphate lyase as a therapeutic target. Expert Opin Ther Targets 13: 1013-1025. doi: 10.1517/14728220903039722
    [8] Pyne S, Kong K-C, Darroch PI (2004) Lysophosphatidic acid and sphingosine 1-phosphate biology: the role of lipid phosphate phosphatases. Semin Cell Dev Biol 15: 491-501. doi: 10.1016/j.semcdb.2004.05.007
    [9] Blaho VA, Hla T (2014) An update on the biology of sphingosine 1-phosphate receptors. J Lipid Res 55: 1596-1608. doi: 10.1194/jlr.R046300
    [10] Nishi T, Kobayashi N, Hisano Y, et al. (2014) Molecular and physiological functions of sphingosine 1-phosphate transporters. Biochim Biophys Acta 1841: 759-765. doi: 10.1016/j.bbalip.2013.07.012
    [11] Hisano Y, Nishi T, Kawahara A (2012) The functional roles of S1P in immunity. J Biochem 152: 305-311. doi: 10.1093/jb/mvs090
    [12] Mitra P, Oskeritzian CA, Payne SG, et al. (2006) Role of ABCC1 in export of sphingosine-1-phosphate from mast cells. Proc Natl Acad Sci USA 103: 16394-16399. doi: 10.1073/pnas.0603734103
    [13] Tanfin Z, Serrano-Sanchez M, Leiber D (2011) ATP-binding cassette ABCC1 is involved in the release of sphingosine 1-phosphate from rat uterine leiomyoma ELT3 cells and late pregnant rat myometrium. Cell Signal 23: 1997-2004. doi: 10.1016/j.cellsig.2011.07.010
    [14] Nieuwenhuis B, Lüth A, Chun J, et al. (2009) 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 (Berl) 87: 645-657. doi: 10.1007/s00109-009-0468-x
    [15] Cartwright TA, Campos CR, Cannon RE, et al. (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: 381-388. doi: 10.1038/jcbfm.2012.174
    [16] Takabe K, Kim RH, Allegood JC, et al. (2010) Estradiol induces export of sphingosine 1-phosphate from breast cancer cells via ABCC1 and ABCG2. J Biol Chem 285: 10477-10486. doi: 10.1074/jbc.M109.064162
    [17] Sato K, Malchinkhuu E, HoriuchiY, et al. (2007) Critical role of ABCA1 transporter in sphingosine 1-phosphate release from astrocytes. J Neurochem 103: 2610-2619.
    [18] Lee Y-M, Venkataraman K, Hwang S-I, et al. (2007) A novel method to quantify sphingosine 1-phosphate by immobilized metal affinity chromatography (IMAC). Prostaglandins Other Lipid Mediat 84: 154-162. doi: 10.1016/j.prostaglandins.2007.08.001
    [19] Hisano Y, Kobayashi N, Kawahara A, et al. (2011) The sphingosine 1-phosphate transporter, SPNS2, functions as a transporter of the phosphorylated form of the immunomodulating agent FTY720. J Biol Chem 286: 1758-1766. doi: 10.1074/jbc.M110.171116
    [20] Hänel P, Andréani P, Gräler MH (2007) Erythrocytes store and release sphingosine 1-phosphate in blood. FASEB J 21: 1202-1209. doi: 10.1096/fj.06-7433com
    [21] Venkataraman K, Lee Y-M, Michaud J, et al. (2008) Vascular endothelium as a contributor of plasma sphingosine 1-phosphate. Circ Res 102: 669-676. doi: 10.1161/CIRCRESAHA.107.165845
    [22] Yatomi Y, Igarashi Y, Yang L, 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: 969-973. doi: 10.1093/oxfordjournals.jbchem.a021681
    [23] Yatomi Y, Ruan F, Hakomori S, et al. (1995) Sphingosine-1-phosphate: a platelet-activating sphingolipid released from agonist-stimulated human platelets. Blood 86: 193-202.
    [24] Maceyka M, Milstien S, Spiegel S. (2009) Sphingosine-1-phosphate: the Swiss army knife of sphingolipid signaling. J Lipid Res 50: S272-S276.
    [25] Bode C, Sensken S-C, Peest U, et al. (2010) Erythrocytes serve as a reservoir for cellular and extracellular sphingosine 1-phosphate. J Cell Biochem 109: 1232-1243.
    [26] Pappu R, Schwab SR, Cornelissen I, et al. (2007) Promotion of lymphocyte egress into blood and lymph by distinct sources of sphingosine-1-phosphate. Science 316: 295-298. doi: 10.1126/science.1139221
    [27] Kobayashi N, Nishi T, Hirata T, et al. (2006) Sphingosine 1-phosphate is released from the cytosol of rat platelets in a carrier-mediated manner. J Lipid Res 47: 614-621.
    [28] Kobayashi N, Kobayashi N, Yamaguchi A, et al. (2009) Characterization of the ATP-dependent sphingosine 1-phosphate transporter in rat erythrocytes. J Biol Chem 284: 21192-21200. doi: 10.1074/jbc.M109.006163
    [29] Bouma HR, Kroese FGM, Kok JW, et al. (2011) Low body temperature governs the decline of circulating lymphocytes during hibernation through sphingosine-1-phosphate. Proc Natl Acad Sci USA 108: 2052-2057. doi: 10.1073/pnas.1008823108
    [30] Lamkanfi M, Mueller JL, Vitari AC, et al. (2009) Glyburide inhibits the cryopyrin/Nalp3 inflammasome. J Cell Biol 187: 61-70. doi: 10.1083/jcb.200903124
    [31] Ancellin N, Colmont C, Su J, et al. (2002) Extracellular export of sphingosine kinase-1 enzyme. Sphingosine 1-phosphate generation and the induction of angiogenic vascular maturation. J Biol Chem 277: 6667-6675.
    [32] Venkataraman K, Thangada S, Michaud J, et al. (2006) Extracellular export of sphingosine kinase-1a contributes to the vascular S1P gradient. Biochem J 397: 461-471. doi: 10.1042/BJ20060251
    [33] Rosen H, Stevens RC, Hanson M, et al. (2013) Sphingosine-1-phosphate and its receptors: structure, signaling, and influence. Annu Rev Biochem 82: 637-662. doi: 10.1146/annurev-biochem-062411-130916
    [34] Osborne N, Brand-Arzamendi K, Ober EA, et al. (2008) The spinster homolog, two of hearts, is required for sphingosine 1-phosphate signaling in zebrafish. Curr Biol 18: 1882-1888. doi: 10.1016/j.cub.2008.10.061
    [35] Kawahara A, Nishi T, Hisano Y, et al. (2009) The sphingolipid transporter spns2 functions in migration of zebrafish myocardial precursors. Science 323: 524-527. doi: 10.1126/science.1167449
    [36] Mandala S, Hajdu R, Bergstrom J, et al. (2002) Alteration of lymphocyte trafficking by sphingosine-1-phosphate receptor agonists. Science 296: 346-349. doi: 10.1126/science.1070238
    [37] Nagahashi M, Kim EY, Yamada A, et al. (2013) Spns2, a transporter of phosphorylated sphingoid bases, regulates their blood and lymph levels, and the lymphatic network. FASEB J 27: 1001-1011. doi: 10.1096/fj.12-219618
    [38] Fukuhara S, Simmons S, Kawamura S, et al. (2012) The sphingosine-1-phosphate transporter Spns2 expressed on endothelial cells regulates lymphocyte trafficking in mice. J Clin Invest 122 : 1416-1426.
    [39] Hisano Y, Kobayashi N, Yamaguchi A, et al. (2012) Mouse SPNS2 functions as a sphingosine-1-phosphate transporter in vascular endothelial cells. PLoS One 7: e38941.
    [40] Mendoza A, Bréart B, Ramos-Perez WD, et al. (2012) The transporter Spns2 is required for secretion of lymph but not plasma sphingosine-1-phosphate. Cell Rep 2: 1104-1110. doi: 10.1016/j.celrep.2012.09.021
    [41] Nijnik A, Clare S, Hale C, et al. (2012) The role of sphingosine-1-phosphate transporter Spns2 in immune system function. J Immunol 189: 102-111. doi: 10.4049/jimmunol.1200282
    [42] Brizuela L, Martin C, Jeannot P, et al. (2014) Osteoblast-derived sphingosine 1-phosphate to induce proliferation and confer resistance to therapeutics to bone metastasis-derived prostate cancer cells. Mol Oncol 8: 1181-1195. doi: 10.1016/j.molonc.2014.04.001
    [43] Zachariah MA, Cyster JG (2010) Neural crest-derived pericytes promote egress of mature thymocytes at the corticomedullary junction. Science 328: 1129-1135. doi: 10.1126/science.1188222
    [44] Ansel KM, Cyster JG (2001) Chemokines in lymphopoiesis and lymphoid organ development. Current Opinion in Immunology 13: 172-179. doi: 10.1016/S0952-7915(00)00201-6
    [45] Luo ZJ, Tanaka T, Kimura F, et al. (1999) Analysis of the mode of action of a novel immunosuppressant FTY720 in mice. Immunopharmacology 41: 199-207. doi: 10.1016/S0162-3109(99)00004-1
    [46] Chiba K, Yanagawa Y, Masubuchi Y, et al. (1998) FTY720, a novel immunosuppressant, induces sequestration of circulating mature lymphocytes by acceleration of lymphocyte homing in rats. I. FTY720 selectively decreases the number of circulating mature lymphocytes by acceleration of lymphocyte homing. J Immunol 160: 5037-5044.
    [47] Schwab SR, Cyster JG (2007) Finding a way out: lymphocyte egress from lymphoid organs. Nat Immunol 8: 1295-1301. doi: 10.1038/ni1545
    [48] Ito K, Anada Y, Tani M, et al. (2007) Lack of sphingosine 1-phosphate-degrading enzymes in erythrocytes. Biochem Biophys Res Commun 357: 212-217. doi: 10.1016/j.bbrc.2007.03.123
    [49] Murata N, Sato K, Kon J, et al. (2000) Interaction of sphingosine 1-phosphate with plasma components, including lipoproteins, regulates the lipid receptor-mediated actions. Biochem J 352: 809-815. doi: 10.1042/0264-6021:3520809
    [50] Allende ML, Sasaki T, Kawai H, et al. (2004) Mice deficient in sphingosine kinase 1 are rendered lymphopenic by FTY720. J Biol Chem 279: 52487-52492. doi: 10.1074/jbc.M406512200
    [51] Bréart B, Ramos-Perez WD, Mendoza A, et al. (2011) Lipid phosphate phosphatase 3 enables efficient thymic egress. J Exp Med 208: 1267-1278. doi: 10.1084/jem.20102551
    [52] Pham THM, Baluk P, Xu Y, et al. (2010) Lymphatic endothelial cell sphingosine kinase activity is required for lymphocyte egress and lymphatic patterning. J Exp. Med 207: 17-27. doi: 10.1084/jem.20091619
    [53] Mildner A, Yona S, Jung S (2013) A close encounter of the third kind: monocyte-derived cells. Adv Immunol 120: 69-103. doi: 10.1016/B978-0-12-417028-5.00003-X
    [54] Kolaczkowska E, Kubes P (2013) Neutrophil recruitment and function in health and inflammation. Nat Rev Immunol 13: 159-175. doi: 10.1038/nri3399
    [55] Roviezzo F, Brancaleone V, De Gruttola L, et al. (2011) Sphingosine-1-phosphate modulates vascular permeability and cell recruitment in acute inflammation in vivo. J Pharmacol Exp Ther 337: 830-837. doi: 10.1124/jpet.111.179168
    [56] Olivera A, Rivera J (2011) An emerging role for the lipid mediator sphingosine-1-phosphate in mast cell effector function and allergic disease. Ad Exp Med Biol 716: 123-142. doi: 10.1007/978-1-4419-9533-9_8
    [57] Finley A, Chen Z, Esposito E, et al. (2013) Sphingosine 1-phosphate mediates hyperalgesia via a neutrophil-dependent mechanism. PLoS One 8: e55255.
    [58] Florey O, Haskard DO (2009) Sphingosine 1-phosphate enhances Fc gamma receptor-mediated neutrophil activation and recruitment under flow conditions. J Immunol 183: 2330-2336. doi: 10.4049/jimmunol.0901019
    [59] Sun WY, Abeynaike LD, Escarbe S, et al. (2012) Rapid histamine-induced neutrophil recruitment is sphingosine kinase-1 dependent. Am J Pathol 180: 1740-1750. doi: 10.1016/j.ajpath.2011.12.024
    [60] Lewis ND, Haxhinasto SA, Anderson SM, et al. (2013) Circulating monocytes are reduced by sphingosine-1-phosphate receptor modulators independently of S1P3. J Immunol 190: 3533-3540. doi: 10.4049/jimmunol.1201810
    [61] Zemann B, Urtz N, Reuschel R, et al. (2007) Normal neutrophil functions in sphingosine kinase type 1 and 2 knockout mice. Immunol Lett 109: 56-63. doi: 10.1016/j.imlet.2007.01.001
    [62] Linke B, Schreiber Y, Zhang DD, et al. (2012) Analysis of sphingolipid and prostaglandin synthesis during zymosan-induced inflammation. Prostaglandins Other Lipid Mediat. 99: 15-23. doi: 10.1016/j.prostaglandins.2012.06.002
    [63] Gräler MH (2012) The role of sphingosine 1-phosphate in immunity and sepsis. Am J Clin Exp Immunol 1: 90-100.
    [64] Ogle ME, Sefcik LS, Awojoodu AO, et al. (2014) Engineering in vivo gradients of sphingosine-1-phosphate receptor ligands for localized microvascular remodeling and inflammatory cell positioning. Acta Biomater 10: 4704-4714. doi: 10.1016/j.actbio.2014.08.007
    [65] Allende ML, Bektas M, Lee BG, et al. (2011) Sphingosine-1-phosphate lyase deficiency produces a pro-inflammatory response while impairing neutrophil trafficking. J Biol Chem 286: 7348-7358. doi: 10.1074/jbc.M110.171819
    [66] Belz GT, Heath WR, Carbone FR (2002) The role of dendritic cell subsets in selection between tolerance and immunity. Immunol Cell Biol 80: 463-468. doi: 10.1046/j.1440-1711.2002.01116.x
    [67] Singer II, Tian M, Wickham LA, et al. (2005) Sphingosine-1-phosphate agonists increase macrophage homing, lymphocyte contacts, and endothelial junctional complex formation in murine lymph nodes. J Immunol 175: 7151-7161. doi: 10.4049/jimmunol.175.11.7151
    [68] Lan YY, De Creus A, Colvin BL, et al. (2005). The sphingosine-1-phosphate receptor agonist FTY720 modulates dendritic cell trafficking in vivo. Am J Transplant 2649-2659.
    [69] Idzko M, Panther E, Corinti S, et al. (2002) Sphingosine 1-phosphate induces chemotaxis of immature and modulates cytokine-release in mature human dendritic cells for emergence of Th2 immune responses. FASEB J 16: 625-627.
    [70] Czeloth N, Bernhardt G, Hofmann F, et al. (2005) Sphingosine-1-phosphate mediates migration of mature dendritic cells. J Immunol 175: 2960-2967. doi: 10.4049/jimmunol.175.5.2960
    [71] Oskeritzian CA (2015) Mast cell plasticity and sphingosine-1-phosphate in immunity, inflammation and cancer. Mol Immunol 63:104-112. doi: 10.1016/j.molimm.2014.03.018
    [72] Jolly PS, Bektas M, Olivera A, et al. (2004) Transactivation of sphingosine-1-phosphate receptors by FcepsilonRI triggering is required for normal mast cell degranulation and chemotaxis. J Exp Med 199: 959-970. doi: 10.1084/jem.20030680
    [73] Olivera A, Mizugishi K, Tikhonova A, et al. (2007) The sphingosine kinase-sphingosine-1-phosphate axis is a determinant of mast cell function and anaphylaxis. Immunity 26: 287-297. doi: 10.1016/j.immuni.2007.02.008
    [74] Oskeritzian CA, Price MM, Hait NC, et al. (2010) Essential roles of sphingosine-1-phosphate receptor 2 in human mast cell activation, anaphylaxis, and pulmonary edema. J Exp Med 207: 465-474. doi: 10.1084/jem.20091513
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