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Blood lymphocyte numbers, essential for the development of
efficient immune responses, are maintained by recirculation throughsecondary lymphoid organs. We show that lymphocyte traffickingis
altered by the lysophospholipid sphingosine-1-phosphate (S1P)and
by a phosphoryl metabolite of the immunosuppressive agentFTY720. Both
species were high-affinity agonists of at least fourof the five S1P
receptors. These agonists produce lymphopeniain blood and thoracic
duct lymph by sequestration of lymphocytesin lymph nodes, but not
spleen. S1P receptor agonists inducedemptying of lymphoid sinuses by
retention of lymphocytes on theabluminal side of sinus-lining
endothelium and inhibition of egressinto lymph. Inhibition of
lymphocyte recirculation by activationof S1P receptors may result in
therapeutically useful immunosuppression.
Departments of
1 Immunology and Rheumatology,
2 zaff;2>Pharmacology, and
3 zaff;3>Medicinal Chemistry, Merck
Research Laboratories, Post Office Box 2000, Rahway, NJ 07065, USA.
*
To whom correspondence should be addressed. E-mail:
hugh_rosen{at}merck.com
Targeted Disruption of the S1P2 Sphingosine 1-Phosphate Receptor Gene Leads to Diffuse Large B-Cell Lymphoma Formation.
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Cancer Res.
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T-bet-dependent S1P5 expression in NK cells promotes egress from lymph nodes and bone marrow.
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Synthetic Analogs of FTY720 [2-Amino-2-(2-[4-octylphenyl]ethyl)-1,3-propanediol] Differentially Regulate Pulmonary Vascular Permeability in Vivo and in Vitro.
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Blood
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Genes Cells
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Ceramide Synthesis Is Modulated by the Sphingosine Analog FTY720 via a Mixture of Uncompetitive and Noncompetitive Inhibition in an Acyl-CoA Chain Length-de pend ent Manner.
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FASEB J
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Targeting Protein Serine/Threonine Phosphatases for Drug Development.
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328, 963-969
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Inhibition of CCR6 Function Reduces the Severity of Experimental Autoimmune Encephalomyelitis via Effects on the Priming Phase of the Immune Response.
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A critical role for the sphingosine analog AAL-R in dampening the cytokine response during influenza virus infection.
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PNAS
106, 1560-1565
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Oral fingolimod (FTY720) in multiple sclerosis: Two-year results of a phase II extension study.
P. O'Connor, G. Comi, X. Montalban, J. Antel, E. W. Radue, A. de Vera, H. Pohlmann, L. Kappos, and For the FTY720 D2201 Study Group (2009)
Neurology
72, 73-79
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Use of an Exposure-Response Model to Aid Early Drug Development of an Oral Sphingosine 1-Phosphate Receptor Modulator.
S. Rohatagi, H. Zahir, J. B. Moberly, K. E. Truitt, S.-i. Inaba, T. Shimozato, and T. J. Carrothers (2009)
J. Clin. Pharmacol.
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Deactivation of Sphingosine Kinase 1 by Protein Phosphatase 2A.
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{beta}-Arrestin Recruitment Assay for the Identification of Agonists of the Sphingosine 1-Phosphate Receptor EDG1.
M. M.C. van Der Lee, M. Bras, C. J. van Koppen, and G. J.R. Zaman (2008)
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Am. J. Respir. Crit. Care Med.
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Cutting Edge: Contact with Secondary Lymphoid Organs Drives Postthymic T Cell Maturation.
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J. Immunol.
181, 5213-5217
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Induction of Antiproliferative Connective Tissue Growth Factor Expression in Wilms' Tumor Cells by Sphingosine-1-Phosphate Receptor 2.
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Mol. Cancer Res.
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Fingolimod (FTY720) as an Acute Rescue Therapy for Intraocular Inflammatory Disease.
B. J. E. Raveney, D. A. Copland, L. B. Nicholson, and A. D. Dick (2008)
Arch Ophthalmol
126, 1390-1395
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Cyclical and Dose-Dependent Responses of Adult Human Mature Oligodendrocytes to Fingolimod.
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Am. J. Pathol.
173, 1143-1152
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Local Not Systemic Modulation of Dendritic Cell S1P Receptors in Lung Blunts Virus-Specific Immune Responses to Influenza.
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Thymic Emigration: When and How T Cells Leave Home.
Sphingosine kinase 1/S1P receptor signaling axis controls glial proliferation in mice with Sandhoff disease.
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Hum. Mol. Genet.
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Sphingosine-1-phosphate receptor type-1 agonism impairs blood dendritic cell chemotaxis and skin dendritic cell migration to lymph nodes under inflammatory conditions.
G. Gollmann, H. Neuwirt, C. H. Tripp, H. Mueller, G. Konwalinka, C. Heufler, N. Romani, and M. Tiefenthaler (2008)
Int. Immunol.
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Attenuation of cell motility observed with high doses of sphingosine 1-phosphate or phosphorylated FTY720 involves RGS2 through its interactions with the receptor S1P..
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Sphingosine 1-phosphate-dependent trafficking of peritoneal B cells requires functional NF{kappa}B-inducing kinase in stromal cells.
J. Kunisawa, M. Gohda, Y. Kurashima, I. Ishikawa, M. Higuchi, and H. Kiyono (2008)
Blood
111, 4646-4652
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The Apoptotic Pathway Contributing to the Deletion of Naive CD8 T Cells during the Induction of Peripheral Tolerance to a Cross-Presented Self-Antigen.
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J. Immunol.
180, 5275-5282
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Proliferative Expansion and Acquisition of Effector Activity by Memory CD4+ T Cells in the Lungs following Pulmonary Virus Infection.
E. L. Wissinger, W. W. Stevens, S. M. Varga, and T. J. Braciale (2008)
J. Immunol.
180, 2957-2966
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S1P1 receptor expression regulates emergence of NKT cells in peripheral tissues.
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FASEB J
22, 307-315
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Isoflurane mediates protection from renal ischemia-reperfusion injury via sphingosine kinase and sphingosine-1-phosphate-dependent pathways.
M. Kim, M. Kim, N. Kim, V. D. D'Agati, C. W. Emala Sr, and H. T. Lee (2007)
Am J Physiol Renal Physiol
293, F1827-F1835
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Transcriptional Profiling of Antigen-Dependent Murine B Cell Differentiation and Memory Formation.
D. Bhattacharya, M. T. Cheah, C. B. Franco, N. Hosen, C. L. Pin, W. C. Sha, and I. L. Weissman (2007)
J. Immunol.
179, 6808-6819
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Brain Penetration of the Oral Immunomodulatory Drug FTY720 and Its Phosphorylation in the Central Nervous System during Experimental Autoimmune Encephalomyelitis: Consequences for Mode of Action in Multiple Sclerosis.
C. A. Foster, L. M. Howard, A. Schweitzer, E. Persohn, P. C. Hiestand, B. Balatoni, R. Reuschel, C. Beerli, M. Schwartz, and A. Billich (2007)
J. Pharmacol. Exp. Ther.
323, 469-475
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The Immunomodulator FTY720 Has a Direct Cytoprotective Effect in Oligodendrocyte Progenitors.
R. P. Coelho, S. G. Payne, R. Bittman, S. Spiegel, and C. Sato-Bigbee (2007)
J. Pharmacol. Exp. Ther.
323, 626-635
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Sphingosine-1-Phosphate Analogue FTY720 Causes Lymphocyte Redistribution and Hypercholesterolemia in ApoE-Deficient Mice.
R. Klingenberg, J.-R. Nofer, M. Rudling, F. Bea, E. Blessing, M. Preusch, H. J. Grone, H. A. Katus, G. K. Hansson, and T. J. Dengler (2007)
Arterioscler Thromb Vasc Biol
27, 2392-2399
|Abstract »|Full Text »|PDF »
Sphingosine 1-phosphate dependence in the regulation of lymphocyte trafficking to the gut epithelium.
J. Kunisawa, Y. Kurashima, M. Higuchi, M. Gohda, I. Ishikawa, I. Ogahara, N. Kim, M. Shimizu, and H. Kiyono (2007)
J. Exp. Med.
204, 2335-2348
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Maternal and Embryonic Control of Uterine Sphingolipid-Metabolizing Enzymes During Murine Embryo Implantation.
T. Kaneko-Tarui, L. Zhang, K. J Austin, L. E Henkes, J. Johnson, T. R Hansen, and J. K Pru (2007)
Biol Reprod
77, 658-665
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Fingolimod: A Novel Immunosuppressant for Multiple Sclerosis.
B. A Brown, P. P Kantesaria, and L. M McDevitt (2007)
Ann. Pharmacother.
41, 1660-1668
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Sphingosylphosphorylcholine acts in an anti-inflammatory manner in renal mesangial cells by reducing interleukin-1{beta}-induced prostaglandin E2 formation.
C. Xin, S. Ren, W. Eberhardt, J. Pfeilschifter, and A. Huwiler (2007)
J. Lipid Res.
48, 1985-1996
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Sphingosine 1-Phosphate-Mediated Trafficking of Pathogenic Th2 and Mast Cells for the Control of Food Allergy.
Y. Kurashima, J. Kunisawa, M. Higuchi, M. Gohda, I. Ishikawa, N. Takayama, M. Shimizu, and H. Kiyono (2007)
J. Immunol.
179, 1577-1585
|Abstract »|Full Text »|PDF »
Kruppel-Like Factor 2 Controls T Cell Trafficking by Activating L-Selectin (CD62L) and Sphingosine-1-Phosphate Receptor 1 Transcription.
Induction of Vascular Permeability by the Sphingosine-1-Phosphate Receptor-2 (S1P2R) and its Downstream Effectors ROCK and PTEN.
T. Sanchez, A. Skoura, M. T. Wu, B. Casserly, E. O. Harrington, and T. Hla (2007)
Arterioscler Thromb Vasc Biol
27, 1312-1318
|Abstract »|Full Text »|PDF »
Essential Requirement for Sphingosine Kinase 2 in a Sphingolipid Apoptosis Pathway Activated by FTY720 Analogues.
A. S. Don, C. Martinez-Lamenca, W. R. Webb, R. L. Proia, E. Roberts, and H. Rosen (2007)
J. Biol. Chem.
282, 15833-15842
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Cutting Edge: Alternative Signaling of Th17 Cell Development by Sphingosine 1-Phosphate.
J.-J. Liao, M.-C. Huang, and E. J. Goetzl (2007)
J. Immunol.
178, 5425-5428
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Activation of sphingosine-1-phosphate receptor S1P5 inhibits oligodendrocyte progenitor migration.
A. S. Novgorodov, M. El-Alwani, J. Bielawski, L. M. Obeid, and T. I. Gudz (2007)
FASEB J
21, 1503-1514
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Sphingosine 1-phosphate regulates peritoneal B-cell trafficking for subsequent intestinal IgA production.
J. Kunisawa, Y. Kurashima, M. Gohda, M. Higuchi, I. Ishikawa, F. Miura, I. Ogahara, and H. Kiyono (2007)
Blood
109, 3749-3756
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Use of a cAMP BRET Sensor to Characterize a Novel Regulation of cAMP by the Sphingosine 1-Phosphate/G13 Pathway.
L. I. Jiang, J. Collins, R. Davis, K.-M. Lin, D. DeCamp, T. Roach, R. Hsueh, R. A. Rebres, E. M. Ross, R. Taussig, et al. (2007)
J. Biol. Chem.
282, 10576-10584
|Abstract »|Full Text »|PDF »
Erythrocytes store and release sphingosine 1-phosphate in blood.
Immunosuppressive and Anti-angiogenic Sphingosine 1-Phosphate Receptor-1 Agonists Induce Ubiquitinylation and Proteasomal Degradation of the Receptor.
M. L. Oo, S. Thangada, M.-T. Wu, C. H. Liu, T. L. Macdonald, K. R. Lynch, C.-Y. Lin, and T. Hla (2007)
J. Biol. Chem.
282, 9082-9089
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A central role for DOCK2 during interstitial lymphocyte motility and sphingosine-1-phosphate-mediated egress.
C. Nombela-Arrieta, T. R. Mempel, S. F. Soriano, I. Mazo, M. P. Wymann, E. Hirsch, C. Martinez-A., Y. Fukui, U. H. von Andrian, and J. V. Stein (2007)
J. Exp. Med.
204, 497-510
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Migration of CD4 T Cells and Dendritic Cells toward Sphingosine 1-Phosphate (S1P) Is Mediated by Different Receptor Subtypes: S1P Regulates the Functions of Murine Mature Dendritic Cells via S1P Receptor Type 3.
Y. Maeda, H. Matsuyuki, K. Shimano, H. Kataoka, K. Sugahara, and K. Chiba (2007)
J. Immunol.
178, 3437-3446
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Mapping Pathways Downstream of Sphingosine 1-Phosphate Subtype 1 by Differential Chemical Perturbation and Proteomics.
P. J. Gonzalez-Cabrera, T. Hla, and H. Rosen (2007)
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282, 7254-7264
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The Sphingosine-1-Phosphate Analogue FTY720 Reduces Atherosclerosis in Apolipoprotein E-Deficient Mice.
P. Keul, M. Tolle, S. Lucke, K. von Wnuck Lipinski, G. Heusch, M. Schuchardt, M. van der Giet, and B. Levkau (2007)
Arterioscler Thromb Vasc Biol
27, 607-613
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Identification of Leu276 of the S1P1 Receptor and Phe263 of the S1P3 Receptor in Interaction with Receptor Specific Agonists by Molecular Modeling, Site-Directed Mutagenesis, and Affinity Studies.
Q. Deng, J. A. Clemas, G. Chrebet, P. Fischer, J. J. Hale, Z. Li, S. G. Mills, J. Bergstrom, S. Mandala, R. Mosley, et al. (2007)
Mol. Pharmacol.
71, 724-735
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Sphingosine-1-Phosphate Stimulates the Functional Capacity of Progenitor Cells by Activation of the CXCR4-Dependent Signaling Pathway via the S1P3 Receptor.
D. H. Walter, U. Rochwalsky, J. Reinhold, F. Seeger, A. Aicher, C. Urbich, I. Spyridopoulos, J. Chun, V. Brinkmann, P. Keul, et al. (2007)
Arterioscler Thromb Vasc Biol
27, 275-282
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The immunosuppressant drug FTY720 inhibits cytosolic phospholipase A2 independently of sphingosine-1-phosphate receptors.
S. G. Payne, C. A. Oskeritzian, R. Griffiths, P. Subramanian, S. E. Barbour, C. E. Chalfant, S. Milstien, and S. Spiegel (2007)
Blood
109, 1077-1085
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Identification of the Hydrophobic Ligand Binding Pocket of the S1P1 Receptor.
Y. Fujiwara, D. A. Osborne, M. D. Walker, D.-a. Wang, D. A. Bautista, K. Liliom, J. R. Van Brocklyn, A. L. Parrill, and G. Tigyi (2007)
J. Biol. Chem.
282, 2374-2385
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Lipids in dendritic cell biology: messengers, effectors, and antigens.
Immunomodulator FTY720 Induces Myofibroblast Differentiation via the Lysophospholipid Receptor S1P3 and Smad3 Signaling.
C. D. Keller, P. Rivera Gil, M. Tolle, M. van der Giet, J. Chun, H. H. Radeke, M. Schafer-Korting, and B. Kleuser (2007)
Am. J. Pathol.
170, 281-292
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Exogenous sphingosine 1-phosphate and sphingosine kinase activated by endothelin-1 induced myometrial contraction through differential mechanisms.
D. Leiber, Y. Banno, and Z. Tanfin (2007)
Am J Physiol Cell Physiol
292, C240-C250
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Plasma cell S1P1 expression determines secondary lymphoid organ retention versus bone marrow tropism.
K. Kabashima, N. M. Haynes, Y. Xu, S. L. Nutt, M. L. Allende, R. L. Proia, and J. G. Cyster (2006)
J. Exp. Med.
203, 2683-2690
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Type I interferons directly regulate lymphocyte recirculation and cause transient blood lymphopenia.
E. Kamphuis, T. Junt, Z. Waibler, R. Forster, and U. Kalinke (2006)
Blood
108, 3253-3261
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Sphingosine-1 Phosphate Prevents Monocyte/Endothelial Interactions in Type 1 Diabetic NOD Mice Through Activation of the S1P1 Receptor.
A. M. Whetzel, D. T. Bolick, S. Srinivasan, T. L. Macdonald, M. A. Morris, K. Ley, and C. C. Hedrick (2006)
Circ. Res.
99, 731-739
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Oral Fingolimod (FTY720) for Relapsing Multiple Sclerosis.
L. Kappos, J. Antel, G. Comi, X. Montalban, P. O'Connor, C. H. Polman, T. Haas, A. A. Korn, G. Karlsson, E. W. Radue, et al. (2006)
N. Engl. J. Med.
355, 1124-1140
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FHL2/SLIM3 Decreases Cardiomyocyte Survival by Inhibitory Interaction With Sphingosine Kinase-1.
J. Sun, G. Yan, A. Ren, B. You, and J. K. Liao (2006)
Circ. Res.
99, 468-476
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SPECIES DIFFERENCES IN METABOLISM AND PHARMACOKINETICS OF A SPHINGOSINE-1-PHOSPHATE RECEPTOR AGONIST IN RATS AND DOGS: FORMATION OF A UNIQUE GLUTATHIONE ADDUCT IN THE RAT.
M. R. Anari, M. D. Creighton, J. S. Ngui, R. A. Tschirret-Guth, Y. Teffera, G. A. Doss, W. Tang, N. X. Yu, S. L. Ciccotto, D. F. Hobra Jr., et al. (2006)
Drug Metab. Dispos.
34, 1367-1375
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Antitumor Activity of Sphingosine Kinase Inhibitors.
K. J. French, J. J. Upson, S. N. Keller, Y. Zhuang, J. K. Yun, and C. D. Smith (2006)
J. Pharmacol. Exp. Ther.
318, 596-603
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FTY720 suppresses CD4+CD44highCD62L- effector memory T cell-mediated colitis.
R. Fujii, T. Kanai, Y. Nemoto, S. Makita, S. Oshima, R. Okamoto, K. Tsuchiya, T. Totsuka, and M. Watanabe (2006)
Am J Physiol Gastrointest Liver Physiol
291, G267-G274
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Sphingosine and Its Analog, the Immunosuppressant 2-Amino-2-(2-[4-octylphenyl]ethyl)-1,3-propanediol, Interact with the CB1 Cannabinoid Receptor.
S. W. Paugh, M. P. Cassidy, H. He, S. Milstien, L. J. Sim-Selley, S. Spiegel, and D. E. Selley (2006)
Mol. Pharmacol.
70, 41-50
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A. S. Awad, H. Ye, L. Huang, L. Li, F. W. Foss Jr., T. L. Macdonald, K. R. Lynch, and M. D. Okusa (2006)
Am J Physiol Renal Physiol
290, F1516-F1524
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Mouse Sphingosine Kinase Isoforms SPHK1a and SPHK1b Differ in Enzymatic Traits Including Stability, Localization, Modification, and Oligomerization.
Sphingosine kinase type 2 is essential for lymphopenia induced by the immunomodulatory drug FTY720.
B. Zemann, B. Kinzel, M. Muller, R. Reuschel, D. Mechtcheriakova, N. Urtz, F. Bornancin, T. Baumruker, and A. Billich (2006)
Blood
107, 1454-1458
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Further characterization of mammalian ceramide kinase: substrate delivery and (stereo)specificity, tissue distribution, and subcellular localization studies.
H. Van Overloop, S. Gijsbers,, and P. P. Van Veldhoven (2006)
J. Lipid Res.
47, 268-283
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Neutrophil Sphingosine 1-Phosphate and Lysophosphatidic Acid Receptors in Pneumonia.
M. Rahaman, R. W. Costello, K. E. Belmonte, S. S. Gendy, and M.-T. Walsh (2006)
Am. J. Respir. Cell Mol. Biol.
34, 233-241
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Enhanced FTY720-Mediated Lymphocyte Homing Requires G{alpha}i Signaling and Depends on beta2 and beta7 Integrin.
O. Pabst, H. Herbrand, S. Willenzon, T. Worbs, A. Schippers, W. Muller, G. Bernhardt, and R. Forster (2006)
J. Immunol.
176, 1474-1480
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Lymphoid Sequestration of Alloreactive Memory CD4 T Cells Promotes Cardiac Allograft Survival.
Q. Zhang, Y. Chen, R. L. Fairchild, P. S. Heeger, and A. Valujskikh (2006)
J. Immunol.
176, 770-777
|Abstract »|Full Text »|PDF »
The Sphingosine 1-Phosphate Receptor Agonist FTY720 Differentially Affects the Sequestration of CD4+/CD25+ T-Regulatory Cells and Enhances Their Functional Activity.
E. Sawicka, G. Dubois, G. Jarai, M. Edwards, M. Thomas, A. Nicholls, R. Albert, C. Newson, V. Brinkmann, and C. Walker (2005)
J. Immunol.
175, 7973-7980
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Sphingosine-1-Phosphate Agonists Increase Macrophage Homing, Lymphocyte Contacts, and Endothelial Junctional Complex Formation in Murine Lymph Nodes.
I. I. Singer, M. Tian, L. A. Wickham, J. Lin, S. S. Matheravidathu, M. J. Forrest, S. Mandala, and E. J. Quackenbush (2005)
J. Immunol.
175, 7151-7161
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Sphingosine Kinase 1 Is a Negative Regulator of CD4+ Th1 Cells.
J. Yang, B. E. Castle, A. Hanidu, L. Stevens, Y. Yu, X. Li, C. Stearns, V. Papov, D. Rajotte, and J. Li (2005)
J. Immunol.
175, 6580-6588
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Sphingosine Kinase 2 Is Required for Modulation of Lymphocyte Traffic by FTY720.
Y. Kharel, S. Lee, A. H. Snyder, S. L. Sheasley-O'Neill, M. A. Morris, Y. Setiady, R. Zhu, M. A. Zigler, T. L. Burcin, K. Ley, et al. (2005)
J. Biol. Chem.
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|Abstract »|Full Text »|PDF »
Sphingosine 1-phosphate and ceramide 1-phosphate: expanding roles in cell signaling.
