Sphingosine kinase and sphingosine-1-phosphate: Regulators in autoimmune and inflammatory disease

International Journal of Clinical Rheumatology

Volumn 8, Issue 4, 2013, Pages 453-463

  Snider, Ashley J ^a,b  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b STONY BROOK UNIVERSITY   (United States)

Author keywords

autoimmune; inflammation; sphingosine kinase; sphingosine 1 phosphate; TNF

Indexed keywords

1 [2 (ISOXAZOL 3 YL) 1H IMIDAZOL 4 YL]BUTANE 1,2,3,4 TETRAOL; 1 [4 (1,2,3,4 TETRAHYDROXYBUTYL) 1H IMIDAZOL 2 YL]ETHANONE OXIME; 2 AMINO 2 [2 [4 (3 BENZYLOXYPHENYLTHIO) 2 CHLOROPHENYL]ETHYL] 1,3 PROPANEDIOL; ABC 294640; ANTIRHEUMATIC AGENT; CERAMIDE; CYCLOOXYGENASE 2; CYCLOPHOSPHAMIDE; DIMETHYLSPHINGOSINE; FINGOLIMOD; IMMUNOMODULATING AGENT; INTERLEUKIN 1BETA; LX 2931; LX 2932; LYASE INHIBITOR; PHOSPHOTRANSFERASE INHIBITOR; PONESIMOD; SMALL INTERFERING RNA; SPHINGOSINE; SPHINGOSINE 1 PHOSPHATE; SPHINGOSINE 1 PHOSPHATE RECEPTOR; SPHINGOSINE KINASE; SPHINGOSINE KINASE 1; SPHINGOSINE KINASE 2; TASP 0277308; TRANSFERASE INHIBITOR; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; W 061;

ARTHRITIS; AUTOIMMUNE DISEASE; BRADYCARDIA; CELL FUNCTION; CELL MIGRATION; CELLULAR DISTRIBUTION; COLITIS; CROHN DISEASE; DISEASE SEVERITY; DOSE RESPONSE; DRUG EFFICACY; DRUG MECHANISM; DRUG TARGETING; DRUG TOLERABILITY; ENTERITIS; ENZYME INHIBITION; ENZYME SPECIFICITY; GENE DELETION; HUMAN; IMMUNOCOMPETENT CELL; IMMUNOMODULATION; INFLAMMATORY DISEASE; INTRACELLULAR SIGNALING; LIPID METABOLISM; LUPUS ERYTHEMATOSUS NEPHRITIS; MOLECULAR DYNAMICS; MULTIPLE SCLEROSIS; NONHUMAN; PRIORITY JOURNAL; RECEPTOR BINDING; REVIEW; RHEUMATOID ARTHRITIS; SYSTEMIC LUPUS ERYTHEMATOSUS; TREATMENT RESPONSE;

EID: 84883099881     PISSN: 17584272     EISSN: 17584280     Source Type: Journal    
DOI: 10.2217/ijr.13.40     Document Type: Review

References (88)

1. Hannun YA, Obeid LM. Principles of bioactive lipid signalling: lessons from sphingolipids. Nat. Rev. Mol. Cell Biol. 9(2), 139-150 (2008).
2. Sun WY, Pitson SM, Bonder CS. Tumor necrosis factor-induced neutrophil adhesion occurs via sphingosine kinase-1-dependent activation of endothelial {alpha}5{beta}1 integrin. Am. J. Pathol. 177(1), 436-446 (2010).
3. Baker DA, Barth J, Chang R, Obeid LM, Gilkeson GS. Genetic sphingosine kinase 1 deficiency significantly decreases synovial inflammation and joint erosions in murine TNF-Alpha-induced arthritis. J. Immunol. 185(4), 2570-2579 (2010).
4. Maines LW, Fitzpatrick LR, French KJ et al. Suppression of ulcerative colitis in mice by orally available inhibitors of sphingosine kinase. Dig. Dis. Sci. 53(4), 997-1012 (2008).
5. Ishimaru N, Yamada A, Nitta T et al. CCR7 with S1P1 signaling through AP-1 for migration of Foxp3+ regulatory T-cells controls autoimmune exocrinopathy. Am. J. Pathol. 180(1), 199-208 (2012).
6. Bode C, Graler MH. Immune regulation by sphingosine 1-phosphate and its receptors. Arch. Immunol. Ther. Exp. (Warsz) 60(1), 3-12 (2012).
7. Chi H. Sphingosine-1-phosphate and immune regulation: trafficking and beyond. Trends Pharmacol. Sci. 32(1), 16-24 (2011).
8. Weigert A, Weis N, Brune B. Regulation of macrophage function by sphingosine-1- phosphate. Immunobiology 214(9-10), 748-760 (2009).
9. Brinkmann V. FTY720 (fingolimod) in multiple sclerosis: therapeutic effects in the immune and the central nervous system. Br. J. Pharmacol. 158(5), 1173-1182 (2009).
10. Pappu R, Schwab SR, Cornelissen I et al. Promotion of lymphocyte egress into blood and lymph by distinct sources of sphingosine- 1-phosphate. Science 316(5822), 295-298 (2007).
11. Venable ME, Lee JY, Smyth MJ, Bielawska A, Obeid LM. Role of ceramide in cellular senescence. J. Biol. Chem. 270(51), 30701-30708 (1995).
12. Obeid LM, Linardic CM, Karolak LA, Hannun YA. Programmed cell death induced by ceramide. Science 259(5102), 1769-1771 (1993).
13. Johnson KR, Becker KP, Facchinetti MM, Hannun YA, Obeid LM. PKC-dependent activation of sphingosine kinase 1 and translocation to the plasma membrane. Extracellular release of sphingosine-1- phosphate induced by phorbol 12-myristate 13-Acetate (PMA). J. Biol. Chem. 277(38), 35257-35262 (2002).
14. Seufferlein T, Rozengurt E. Sphingosine induces p125FAK and paxillin tyrosine phosphorylation, actin stress fiber formation, and focal contact assembly in Swiss 3T3 cells. J. Biol. Chem. 269(44), 27610-27617 (1994).
15. Kluk MJ, Hla T. Signaling of sphingosine-1- phosphate via the S1P/EDG-family of G-protein-coupled receptors. Biochim. Biophys. Acta 1582(1-3), 72-80 (2002).
16. Taha TA, Argraves KM, Obeid LM. Sphingosine-1-phosphate receptors: receptor specificity versus functional redundancy. Biochim. Biophys. Acta 1682(1-3), 48-55 (2004).
17. Jolly PS, Bektas M, Olivera A et al. Transactivation of sphingosine-1-phosphate receptors by FcepsilonRI triggering is required for normal mast cell degranulation and chemotaxis. J. Exp. Med. 199(7), 959-970 (2004).
18. Pham TH, Baluk P, Xu Y et al. Lymphatic endothelial cell sphingosine kinase activity is required for lymphocyte egress and lymphatic patterning. J. Exp. Med. 207(1), 17-27 (2010).
19. Alemany R, van Koppen CJ, Danneberg K, Ter Braak M, Meyer Zu Heringdorf D. Regulation and functional roles of sphingosine kinases. Naunyn Schmiedebergs Arch. Pharmacol. 374(5-6), 413-428 (2007).
20. Okada T, Ding G, Sonoda H et al. Involvement of N-terminal-extended form of sphingosine kinase 2 in serum-dependent regulation of cell proliferation and apoptosis. J. Biol. Chem. 280(43), 36318-36325 (2005).
21. Liu H, Sugiura M, Nava VE et al. Molecular cloning and functional characterization of a novel mammalian sphingosine kinase type 2 isoform. J. Biol. Chem. 275, 19513-19520 (2000).
22. Igarashi N, Okada T, Hayashi S, Fujita T, Jahangeer S, Nakamura S. Sphingosine kinase 2 is a nuclear protein and inhibits DNA synthesis. J. Biol. Chem. 278(47), 46832-46839 (2003).
23. Liu H, Toman RE, Goparaju SK et al. Sphingosine kinase type 2 is a putative BH3-only protein that induces apoptosis. J. Biol. Chem. 278(41), 40330-40336 (2003).
24. Hait NC, Allegood J, Maceyka M et al. Regulation of histone acetylation in the nucleus by sphingosine-1-phosphate. Science 325(5945), 1254-1257 (2009).
25. Pitson SM, Xia P, Leclercq TM et al. Phosphorylation-dependent translocation of sphingosine kinase to the plasma membrane drives its oncogenic signalling. J. Exp. Med. 201(1), 49-54 (2005).
26. Jarman KE, Moretti PA, Zebol JR, Pitson SM. Translocation of sphingosine kinase 1 to the plasma membrane is mediated by calcium and integrin binding protein 1. J. Biol. Chem. 285(1), 483-492 (2009).
27. Sutherland CM, Moretti PA, Hewitt NM, Bagley CJ, Vadas MA, Pitson SM. The calmodulin-binding site of sphingosine kinase and its role in agonist-dependent translocation of sphingosine kinase 1 to the plasma membrane. J. Biol. Chem. 281(17), 11693-11701 (2006).
28. Xia P, Wang L, Moretti PA et al. Sphingosine kinase interacts with TRAF2 and dissects tumor necrosis factor-Alpha signaling. J. Biol. Chem. 277(10), 7996-8003 (2002).
29. Alvarez SE, Harikumar KB, Hait NC et al. Sphingosine-1-phosphate is a missing cofactor for the E3 ubiquitin ligase TRAF2. Nature 465(7301), 1084-1088 (2010).
30. Pitson SM, Moretti PA, Zebol JR et al. Activation of sphingosine kinase 1 by ERK1/2-mediated phosphorylation. EMBO J. 22(20), 5491-5500 (2003).
31. Stahelin RV, Hwang JH, Kim JH et al. The mechanism of membrane targeting of human sphingosine kinase 1. J. Biol. Chem. 280(52), 43030-43038 (2005).
32. Sethu S, Mendez-Corao G, Melendez AJ. Phospholipase D1 plays a key role in TNF-Alpha signaling. J. Immunol. 180(9), 6027-6034 (2008).
33. Snider AJ, Orr Gandy KA, Obeid LM. Sphingosine kinase: role in regulation of bioactive sphingolipid mediators in inflammation. Biochimie 92(6), 707-715 (2010).
34. Billich A, Bornancin F, Mechtcheriakova D, Natt F, Huesken D, Baumruker T. Basal and induced sphingosine kinase 1 activity in A549 carcinoma cells: function in cell survival and IL-1beta and TNF-Alpha induced production of inflammatory mediators. Cell. Signal. 17(10), 1203-1217 (2005).
35. Pettus BJ, Bielawski J, Porcelli AM et al. The sphingosine kinase 1/sphingosine-1- phosphate pathway mediates COX-2 induction and PGE2 production in response to TNF-Alpha. FASEB J. 17(11), 1411-1421 (2003).
36. Melendez AJ, Ibrahim FB. Antisense knockdown of sphingosine kinase 1 in human macrophages inhibits C5a receptor-dependent signal transduction, Ca2+ signals, enzyme release, cytokine production, and chemotaxis. J. Immunol. 173(3), 1596-1603 (2004).
37. Hammad SM, Crellin HG, Wu BX, Melton J, Anelli V, Obeid LM. Dual and distinct roles for sphingosine kinase 1 and sphingosine 1 phosphate in the response to inflammatory stimuli in RAW macrophages. Prostaglandins Other Lipid Mediat. 85(3-4), 107-114 (2007).
38. Michaud J, Kohno M, Proia RL, Hla T. Normal acute and chronic inflammatory responses in sphingosine kinase 1 knockout mice. FEBS Lett. 580(19), 4607-4612 (2006).
39. Mizugishi K, Yamashita T, Olivera A, Miller GF, Spiegel S, Proia RL. Essential role for sphingosine kinases in neural and vascular development. Mol. Cell. Biol. 25(24), 11113-11121 (2005).
40. Allende ML, Sasaki T, Kawai H et al. Mice deficient in sphingosine kinase 1 are rendered lymphopenic by FTY720. J. Biol. Chem. 279(50), 52487-52492 (2004).
41. Zemann B, Urtz N, Reuschel R et al. Normal neutrophil functions in sphingosine kinase type 1 and 2 knockout mice. Immunol. Lett. 109(1), 56-63 (2007).
42. Kharel Y, Raje M, Gao M et al. Sphingosine kinase type 2 inhibition elevates circulating sphingosine 1-phosphate. Biochem. J. 447(1), 149-157 (2012).
43. Spiegel S, Milstien S. Sphingosine-1- phosphate: an enigmatic signalling lipid. Nat. Rev. Mol. Cell Biol. 4(5), 397-407 (2003).
44. Hla T. Physiological and pathological actions of sphingosine 1-phosphate. Semin. Cell Dev. Biol. 15(5), 513-520 (2004).
45. Tanfin Z, Serrano-Sanchez M, Leiber D. 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(12), 1997-2004 (2011).
46. Mitra P, Oskeritzian CA, Payne SG, Beaven MA, Milstien S, Spiegel S. Role of ABCC1 in export of sphingosine-1-phosphate from mast cells. Proc. Natl Acad. Sci. USA 103(44), 16394-16399 (2006).
47. Hammad SM, Taha TA, Nareika A, Johnson KR, Lopes-Virella MF, Obeid LM. Oxidized LDL immune complexes induce release of sphingosine kinase in human U937 monocytic cells. Prostaglandins Other Lipid Mediat. 79(1-2), 126-140 (2006).
48. Venkataraman K, Thangada S, Michaud J et al. Extracellular export of sphingosine kinase-1a contributes to the vascular S1P gradient. Biochem. J. 397(3), 461-471 (2006).
49. Xia P, Wang L, Gamble JR, Vadas MA. Activation of sphingosine kinase by tumor necrosis factor-Alpha inhibits apoptosis in human endothelial cells. J. Biol. Chem. 274(48), 34499-34505. (1999).
50. Xia P, Gamble JR, Rye KA et al. Tumor necrosis factor-Alpha induces adhesion molecule expression through the sphingosine kinase pathway. Proc. Natl Acad. Sci. USA 95(24), 14196-14201 (1998).
51. Kharel Y, Lee S, Snyder AH et al. Sphingosine kinase 2 is required for modulation of lymphocyte traffic by FTY720. J. Biol. Chem. 280(44), 36865-36872 (2005).
52. Liang J, Nagahashi M, Kim EY et al. Sphingosine-1-phosphate links persistent STAT3 activation, chronic intestinal inflammation, and development of colitis-Associated cancer. Cancer Cell 23(1), 107-120 (2013).
53. Oo ML, Thangada S, Wu MT et al. Immunosuppressive and anti-Angiogenic sphingosine 1-phosphate receptor-1 agonists induce ubiquitinylation and proteasomal degradation of the receptor. J. Biol. Chem. 282(12), 9082-9089 (2007).
54. Lim KG, Tonelli F, Li Z et al. FTY720 analogues as sphingosine kinase 1 inhibitors: enzyme inhibition kinetics, allosterism, proteasomal degradation, and actin rearrangement in MCF-7 breast cancer cells. J. Biol. Chem. 286(21), 18633-18640 (2011).
55. Tonelli F, Lim KG, Loveridge C et al. FTY720 and (S)-FTY720 vinylphosphonate inhibit sphingosine kinase 1 and promote its proteasomal degradation in human pulmonary artery smooth muscle, breast cancer and androgen-independent prostate cancer cells. Cell. Signal. 22(10), 1536-1542 (2010).
56. Song J, Matsuda C, Kai Y et al. A novel sphingosine 1-phosphate receptor agonist, 2-Amino-2-propanediol hydrochloride (KRP- 203), regulates chronic colitis in interleukin-10 gene-deficient mice. J. Pharmacol. Exp. Ther. 324(1), 276-283 (2008).
57. Wenderfer SE, Stepkowski SM, Braun MC. Increased survival and reduced renal injury in MRL/lpr mice treated with a novel sphingosine-1-phosphate receptor agonist. Kidney Int. 74(10), 1319-1326 (2008).
58. Sanada Y, Mizushima T, Kai Y et al. Therapeutic effects of novel sphingosine-1- phosphate receptor agonist W-061 in murine DSS colitis. PLoS ONE 6(9), e23933 (2011).
59. Piali L, Froidevaux S, Hess P et al. The selective sphingosine 1-phosphate receptor 1 agonist ponesimod protects against lymphocyte-mediated tissue inflammation. J. Pharmacol. Exp. Ther. 337(2), 547-556 (2011).
60. Watson L, Tullus K, Marks SD, Holt RC, Pilkington C, Beresford MW. Increased serum concentration of sphingosine-1- phosphate in juvenile-onset systemic lupus erythematosus. J. Clin. Immunol. 32(5), 1019-1025 (2012).
61. Snider AJ, Ruiz P, Obeid LM, Oates JC. Inhibition of sphingosine kinase-2 in a murine model of lupus nephritis. PLoS ONE 8(1), e53521 (2013).
62. Okazaki H, Hirata D, Kamimura T et al. Effects of FTY720 in MRL-lpr/lpr mice: therapeutic potential in systemic lupus erythematosus. J. Rheumatol. 29(4), 707-716 (2002).
63. Alperovich G, Rama I, Lloberas N et al. New immunosuppresor strategies in the treatment of murine lupus nephritis. Lupus 16(1), 18-24 (2007).
64. Ando S, Amano H, Amano E et al. FTY720 exerts a survival advantage through the prevention of end-stage glomerular inflammation in lupus-prone BXSB mice. Biochem. Biophys. Res. Commun. 394(3), 804-810 (2010).
65. Limaye V, Xia P, Hahn C et al. Chronic increases in sphingosine kinase-1 activity induce a pro-inflammatory, pro-Angiogenic phenotype in endothelial cells. Cell Mol. Biol. Lett. 14(3), 424-441 (2009).
66. Lai WQ, Irwan AW, Goh HH et al. Anti-inflammatory effects of sphingosine kinase modulation in inflammatory arthritis. J. Immunol. 181(11), 8010-8017 (2008).
67. Kamada K, Arita N, Tsubaki T et al. Expression of sphingosine kinase 2 in synovial fibroblasts of rheumatoid arthritis contributing to apoptosis by a sphingosine analogue, FTY720. Pathol. Int. 59(6), 382-389 (2009).
68. Kitano M, Hla T, Sekiguchi M et al. Sphingosine 1-phosphate/sphingosine 1-phosphate receptor 1 signaling in rheumatoid synovium: regulation of synovial proliferation and inflammatory gene expression. Arthritis. Rheum. 54(3), 742-753 (2006).
69. Lai WQ, Irwan AW, Goh HH, Melendez AJ, Mcinnes IB, Leung BP. Distinct roles of sphingosine kinase 1 and 2 in murine collagen-induced arthritis. J. Immunol. 183(3), 2097-2103 (2009).
70. Baker DA, Eudaly J, Smith CD, Obeid LM, Gilkeson GS. Impact of sphingosine kinase 2 deficiency on the development of TNF-Alpha-induced inflammatory arthritis. Rheumatol. Int. doi:10.1007/s00296-012-2493-2 (2012) (Epub ahead of print).
71. Fitzpatrick LR, Green C, Maines LW, Smith CD. Experimental osteoarthritis in rats is attenuated by ABC294640, a selective inhibitor of sphingosine kinase-2. Pharmacology 87(3-4), 135-143 (2011).
72. Antoon JW, White MD, Meacham WD et al. Antiestrogenic effects of the novel sphingosine kinase-2 inhibitor ABC294640. Endocrinology 151(11), 5124-5135 (2010).
73. Bagdanoff JT, Donoviel MS, Nouraldeen A et al. Inhibition of sphingosine 1-phosphate lyase for the treatment of rheumatoid arthritis: discovery of (E)-1-(4-((1R,2S,3R)- 1,2,3,4-tetrahydroxybutyl)-1H-imidazol-2-yl) ethanone oxime (LX2931) and (1R,2S,3R)-1- (2-(isoxazol-3-yl)-1H-imidazol-4-yl)butane- 1,2,3,4-tetraol (LX2932). J. Med. Chem. 53(24), 8650-8662 (2010).
74. Matsuura M, Imayoshi T, Okumoto T. Effect of FTY720, a novel immunosuppressant, on adjuvant- and collagen-induced arthritis in rats. Int. J. Immunopharmacol. 22(4), 323-331 (2000).
75. Wang F, Tan W, Guo D, He S. Reduction of CD4 positive T cells and improvement of pathological changes of collagen-induced arthritis by FTY720. Eur. J. Pharmacol. 573(1-3), 230-240 (2007).
76. Tsunemi S, Iwasaki T, Kitano S, Imado T, Miyazawa K, Sano H. Effects of the novel immunosuppressant FTY720 in a murine rheumatoid arthritis model. Clin. Immunol. 136(2), 197-204 (2010).
77. Fujii Y, Hirayama T, Ohtake H et al. Amelioration of collagen-induced arthritis by a novel S1P1 antagonist with immunomodulatory activities. J. Immunol. 188(1), 206-215 (2012).
78. Brossard P, Derendorf H, Xu J, Maatouk H, Halabi A, Dingemanse J. Pharmacokinetics and pharmacodynamics of ponesimod, a selective S1P receptor modulator, in the First-in-Human Study. Br. J. Clin. Pharmacol. doi:10.1111/bcp.12129 (2013) (Epub ahead of print).
79. Kawamori T, Osta W, Johnson KR et al. Sphingosine kinase 1 is up-regulated in colon carcinogenesis. FASEB J. 20(2), 386-388 (2006).
80. Snider AJ, Kawamori T, Bradshaw SG et al. A role for sphingosine kinase 1 in dextran sulfate sodium-induced colitis. FASEB J. 23(1), 143-152 (2009).
81. Maines LW, Fitzpatrick LR, Green CL, Zhuang Y, Smith CD. Efficacy of a novel sphingosine kinase inhibitor in experimental Crohn's disease. Inflammopharmacology 18(2), 73-85 (2013).
82. Daniel C, Sartory NA, Zahn N et al. FTY720 ameliorates oxazolone colitis in mice by directly affecting T helper type 2 functions. Mol. Immunol. 44(13), 3305-3316 (2007).
83. Radi ZA, Heuvelman DM, Masferrer JL, Benson EL. Pharmacologic evaluation of sulfasalazine, FTY720, and anti-IL-12/23p40 in a TNBS-induced Crohn's disease model. Dig. Dis. Sci. 56(8), 2283-2291 (2011).
84. Murphy CT, Hall LJ, Hurley G et al. The sphingosine-1-phosphate analogue FTY720 impairs mucosal immunity and clearance of the enteric pathogen Citrobacter rodentium. Infect. Immun. 80(8), 2712-2723 (2012).
85. Schulze T, GolfS, Tabeling C et al. Sphingosine-1-phospate receptor 4 (S1P(4)) deficiency profoundly affects dendritic cell function and TH17-cell differentiation in a murine model. FASEB J. 25(11), 4024-4036 (2011).
86. Wang Z, Min X, Xiao SH et al. Molecular basis of sphingosine kinase 1 substrate recognition and catalysis. Structure 21(5), 798-809 (2013).
87. Fujii T, Tomita T, Kanai T et al. FTY720 suppresses the development of colitis in lymphoid-null mice by modulating the trafficking of colitogenic CD4+ T cells in bone marrow. Eur. J. Immunol. 38(12), 3290-3303 (2008).
88. Montrose DC, Scherl EJ, Bosworth BP et al. S1P(1) localizes to the colonic vasculature in ulcerative colitis and maintains blood vessel integrity. J. Lipid Res. 54(3), 843-851 (2013).