Sphingosine-1-phosphate modulates dendritic cell function: Focus on non-migratory effects in vitro and in vivo

Cellular Physiology and Biochemistry

Volumn 34, Issue 1, 2014, Pages 27-44

  Arlt, Olga ^a   Schwiebs, Anja ^a   Japtok, Lukasz ^b   Rüger, Katja ^a   Katzy, Elisabeth ^a   Kleuser, Burkhard ^b   Radeke, Heinfried H ^a  

^a GOETHE UNIVERSITY   (Germany)

^b UNIVERSITY OF POTSDAM   (Germany)

Author keywords

Dendritic cells; Fingolimod; IL 12; Inflammation; Sphingosine 1 phosphate

Indexed keywords

CYTOKINE; SPHINGOLIPID; SPHINGOSINE 1 PHOSPHATE; ANTIGEN; LYSOPHOSPHOLIPID; SPHINGOSINE; SPHINGOSINE 1-PHOSPHATE; TOLL LIKE RECEPTOR; TRANSCRIPTOME; FINGOLIMOD;

ADAPTIVE IMMUNITY; ANTIGEN PRESENTATION; ANTIGEN PRESENTING CELL; CELL FUNCTION; DENDRITIC CELL; ENDOSOME; HOMEOSTASIS; HUMAN; IMMUNOLOGICAL TOLERANCE; IMMUNOMODULATION; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATORY DISEASE; INNATE IMMUNITY; LIPID METABOLISM; LYMPHOID ORGAN; NONHUMAN; PRIORITY JOURNAL; REVIEW; T LYMPHOCYTE; ANALOGS AND DERIVATIVES; ANIMAL; IMMUNOLOGY; METABOLISM; PATHOLOGY; SKIN DISEASE; CELL EXPANSION; CELL MATURATION; CYTOLOGY; DERMATITIS; DRUG DISTRIBUTION; DRUG METABOLISM; ENZYME ACTIVITY; IMMUNOCOMPETENT CELL; INFLAMMATION; MIGRATION INHIBITION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN METABOLISM; SPHINGOLIPID METABOLISM; STEM CELL;

ADAPTIVE IMMUNITY; ANIMALS; ANTIGENS; CYTOKINES; DENDRITIC CELLS; HUMANS; IMMUNITY, INNATE; LYSOPHOSPHOLIPIDS; SKIN DISEASES; SPHINGOSINE; TOLL-LIKE RECEPTORS; TRANSCRIPTOME;

EID: 84903983388     PISSN: 10158987     EISSN: 14219778     Source Type: Journal    
DOI: 10.1159/000362982     Document Type: Review

References (91)

1. Kappos L, Radue EW, O'Connor P, Polman C, Hohlfeld R, Calabresi P, Selmaj K, Agoropoulou C, Leyk M, Zhang-Auberson L, Burtin P, Group FS: A placebo-controlled trial of oral fingolimod in relapsing multiple sclerosis. N Engl J Med 2010;362:387-401.
2. Radeke HH, von Wenckstern H, Stoidtner K, Sauer B, Hammer S, Kleuser B: Overlapping signaling pathways of sphingosine 1-phosphate and TGF-beta in the murine Langerhans cell line XS52. J Immunol 2005;174:2778-2786. (Pubitemid 40279694)
3. Massberg S, Schaerli P, Knezevic-Maramica I, Köllnberger M, Tubo N, Moseman EA, Huff IV, Junt T, Wagers AJ, Mazo IB, von Andrian UH: Immunosurveillance by hematopoietic progenitor cells trafficking through blood, lymph, and peripheral tissues. Cell 2007;131:994-1008. (Pubitemid 350138089)
4. Martino A: Sphingosine 1-phosphate as a novel immune regulator of dendritic cells. J Biosci 2007;32:1207-1212. (Pubitemid 47583881)
5. von Wenckstern H, Zimmermann K, Kleuser B: The role of the lysophospholipid sphingosine 1-phosphate in immune cell biology. Arch Immunol Ther Exp (Warsz) 2006;54:239-251. (Pubitemid 44231830)
6. Rivera J, Proia RL, Olivera A: The alliance of sphingosine-1-phosphate and its receptors in immunity. Nat Rev Immunol 2008;8:753-763.
7. Idzko M, Panther E, Corinti S, Morelli A, Ferrari D, Herouy Y, Dichmann S, Mockenhaupt M, Gebicke-Haerter P, Di Virgilio F, Girolomoni G, Norgauer J: Sphingosine 1-phosphate induces chemotaxis of immature and modulates cytokine-release in mature human dendritic cells for emergence of Th2 immune responses. FASEB J 2002;16:625-627.
8. Satpathy AT, Wu X, Albring JC, Murphy KM: Re(de)fining the dendritic cell lineage. Nat Immunol 2012;13:1145-1154.
9. Steinman RM: Some active areas of DC research and their medical potential. Eur J Immunol 2010;40:2085-2088.
10. Miller JC, Brown BD, Shay T, Gautier EL, Jojic V, Cohain A, Pandey G, Leboeuf M, Elpek KG, Helft J, Hashimoto D, Chow A, Price J, Greter M, Bogunovic M, Bellemare-Pelletier A, Frenette PS, Randolph GJ, Turley SJ, Merad M, Consortium IG: Deciphering the transcriptional network of the dendritic cell lineage. Nat Immunol 2012;13:888-899.
11. Kang SJ: The bloodline of CD8a(+) dendritic cells. Mol Cells 2012;34:219-229.
12. Hölzel M, Bovier A, Tüting T: Plasticity of tumour and immune cells: A source of heterogeneity and a cause for therapy resistance? Nat Rev Cancer 2013;13:365-376.
13. Vacchelli E, Vitale I, Eggermont A, Fridman WH, Fucíková J, Cremer I, Galon J, Tartour E, Zitvogel L, Kroemer G, Galluzzi L: Trial watch: Dendritic cell-based interventions for cancer therapy. Oncoimmunology 2013;2:e25771.
14. Frankenberger B, Schendel DJ: Third generation dendritic cell vaccines for tumor immunotherapy. Eur J Cell Biol 2012;91:53-58.
15. Murphy KM: Transcriptional control of dendritic cell development. Adv Immunol 2013;120:239-267.
16. Gautier EL, Shay T, Miller J, Greter M, Jakubzick C, Ivanov S, Helft J, Chow A, Elpek KG, Gordonov S, Mazloom AR, Ma'ayan A, Chua WJ, Hansen TH, Turley SJ, Merad M, Randolph GJ, Consortium IG: Gene-expression profiles and transcriptional regulatory pathways that underlie the identity and diversity of mouse tissue macrophages. Nat Immunol 2012;13:1118-1128.
17. Cyster JG, Schwab SR: Sphingosine-1-phosphate and lymphocyte egress from lymphoid organs. Annu Rev Immunol 2012;30:69-94.
18. Bode C, Sensken SC, Peest U, Beutel G, Thol F, Levkau B, Li Z, Bittman R, Huang T, Tölle M, van der Giet M, Gräler MH: Erythrocytes serve as a reservoir for cellular and extracellular sphingosine 1-phosphate. J Cell Biochem 2010;109:1232-1243.
19. English D, Welch Z, Kovala AT, Harvey K, Volpert OV, Brindley DN, Garcia JG: 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.
20. Ulrych T, Böhm A, Polzin A, Daum G, Nüsing RM, Geisslinger G, Hohlfeld T, Schrör K, Rauch BH: Release of sphingosine-1-phosphate from human platelets is dependent on thromboxane formation. J Thromb Haemost 2011;9:790-798.
21. Venkataraman K, Lee YM, Michaud J, Thangada S, Ai Y, Bonkovsky HL, Parikh NS, Habrukowich C, Hla T: Vascular endothelium as a contributor of plasma sphingosine 1-phosphate. Circ Res 2008;102:669-676. (Pubitemid 351457860)
22. Ruwisch L, Schäfer-Korting M, Kleuser B: An improved high-performance liquid chromatographic method for the determination of sphingosine-1-phosphate in complex biological materials. Naunyn Schmiedebergs Arch Pharmacol 2001;363:358-363. (Pubitemid 32186536)
23. Olivera A, Allende ML, Proia RL: Shaping the landscape: Metabolic regulation of S1P gradients. Biochim Biophys Acta 2013;1831:193-202.
24. Rathinasamy A, Czeloth N, Pabst O, Förster R, Bernhardt G: The origin and maturity of dendritic cells determine the pattern of sphingosine 1-phosphate receptors expressed and required for efficient migration. J Immunol 2010;185:4072-4081.
25. Idzko M, Hammad H, van Nimwegen M, Kool M, Müller T, Soullié T, Willart MA, Hijdra D, Hoogsteden HC, Lambrecht BN: Local application of FTY720 to the lung abrogates experimental asthma by altering dendritic cell function. J Clin Invest 2006;116:2935-2944. (Pubitemid 44684478)
26. Blaho VA, Hla T: An update on the biology of sphingosine 1-phosphate receptors. J Lipid Res 2014
27. Japtok L, Schaper K, Bäumer W, Radeke HH, Jeong SK, Kleuser B: Sphingosine 1-phosphate modulates antigen capture by murine Langerhans cells via the S1P2 receptor subtype. PLoS One 2012;7:e49427.
28. Fukuhara S, Simmons S, Kawamura S, Inoue A, Orba Y, Tokudome T, Sunden Y, Arai Y, Moriwaki K, Ishida J, Uemura A, Kiyonari H, Abe T, Fukamizu A, Hirashima M, Sawa H, Aoki J, Ishii M, Mochizuki N: The sphingosine-1-phosphate transporter spns2 expressed on endothelial cells regulates lymphocyte trafficking in mice. J Clin Invest 2012;122:1416-1426.
29. Hait NC, Allegood J, Maceyka M, Strub GM, Harikumar KB, Singh SK, Luo C, Marmorstein R, Kordula T, Milstien S, Spiegel S: Regulation of histone acetylation in the nucleus by sphingosine-1-phosphate. Science 2009;325:1254-1257.
30. Ferreirós N, Labocha S, Schröder M, Radeke HH, Geisslinger G: LC-MS/MS determination of FTY720 and FTY720-phosphate in murine intracellular compartments and human plasma. J Chromatogr B Analyt Technol Biomed Life Sci 2012;887-888:122-127.
31. Saddoughi SA, Gencer S, Peterson YK, Ward KE, Mukhopadhyay A, Oaks J, Bielawski J, Szulc ZM, Thomas RJ, Selvam SP, Senkal CE, Garrett-Mayer E, De Palma RM, Fedarovich D, Liu A, Habib AA, Stahelin RV, Perrotti D, Ogretmen B: Sphingosine analogue drug FYT720 targets i2PP2a/set and mediates lung tumour suppression via activation of PP2a-RIPK1-dependent necroptosis. EMBO Mol Med 2013;5:105-121.
32. Alvarez SE, Harikumar KB, Hait NC, Allegood J, Strub GM, Kim EY, Maceyka M, Jiang H, Luo C, Kordula T, Milstien S, Spiegel S: Sphingosine-1-phosphate is a missing cofactor for the E3 ubiquitin ligase TRAF2. Nature 2010;465:1084-1088.
33. Richter K: Influence of sphingosine kinases type 1 and 2 on the immune response of murine dendritic spleen cells and bone-marrow derived cells: Diploma Thesis, 2009
34. Schröder M, Richter C, Juan MH, Maltusch K, Giegold O, Quintini G, Pfeilschifter JM, Huwiler A, Radeke HH: The sphingosine kinase 1 and S1P1 axis specifically counteracts LPS-induced IL-12p70 production in immune cells of the spleen. Mol Immunol 2011;48:1139-1148.
35. Lüth A, Neuber C, Kleuser B: Novel methods for the quantification of (2e)-hexadecenal by liquid chromatography with detection by either ESI qTOF tandem mass spectrometry or fluorescence measurement. Anal Chim Acta 2012;722:70-79.
36. Satpathy AT, KC W, Albring JC, Edelson BT, Kretzer NM, Bhattacharya D, Murphy TL, Murphy KM:Zbtb46 expression distinguishes classical dendritic cells and their committed progenitors from other immune lineages. J Exp Med 2012;209:1135-1152.
37. Greter M, Helft J, Chow A, Hashimoto D, Mortha A, Agudo-Cantero J, Bogunovic M, Gautier EL,Miller J, Leboeuf M, Lu G, Aloman C, Brown BD, Pollard JW, Xiong H, Randolph GJ, Chipuk JE, Frenette PS, Merad M: GM-CSF controls nonlymphoid tissue dendritic cell homeostasis but is dispensable for the differentiation of inflammatory dendritic cells. Immunity 2012;36:1031-1046.
38. Zeng X, Wang T, Zhu C, Xing X, Ye Y, Lai X, Song B, Zeng Y: Topographical and biological evidence revealed FTY720-mediated anergy-polarization of mouse bone marrow-derived dendritic cells in vitro. PloS one 2012;7:e34830.
39. Alemany R, van Koppen CJ, Danneberg K, Ter Braak M, Meyer zu Heringdorf D: Regulation and functional roles of sphingosine kinases. Naunyn Schmiedeberg Arch Pharmacol 2007;374:413-428. (Pubitemid 46215289)
40. Martino A, Volpe E, Auricchio G, Izzi V, Poccia F, Mariani F, Colizzi V, Baldini PM: Sphingosine 1-phosphate interferes on the differentiation of human monocytes into competent dendritic cells. Scand J Immunol 2007;65:84-91. (Pubitemid 44968076)
41. Renkl A, Berod L, Mockenhaupt M, Idzko M, Panther E, Termeer C, Elsner P, Huber M, Norgauer J: Distinct effects of sphingosine-1-phosphate, lysophosphatidic acid and histamine in human and mouse dendritic cells. Int J Mol Med 2004;13:203-209.
42. Oo ML, Chang SH, Thangada S, Wu MT, Rezaul K, Blaho V, Hwang SI, Han DK, Hla T: Engagement of S1P(1)-degradative mechanisms leads to vascular leak in mice. J Clin Invest 2011;121:2290-2300.
43. Graler MH, Goetzl EJ: The immunosuppressant FTY720 down-regulates sphingosine 1-phosphate G-protein-coupled receptors. FASEB J 2004;18:551-553.
44. Franchi L, Malisan F, Tomassini B, Testi R: Ceramide catabolism critically controls survival of human dendritic cells. J Leukoc Biol 2006;79:166-172. (Pubitemid 43054262)
45. Lee H, Deng J, Kujawski M, Yang C, Liu Y, Herrmann A, Kortylewski M, Horne D, Somlo G, Forman S, Jove R, Yu H: STAT3-induced S1PR1 expression is crucial for persistent STAT3 activation in tumors. Nat Med 2010;16:1421-1428.
46. Liao JJ, Huang MC, Goetzl EJ: Cutting edge: Alternative signaling of Th17 cell development by sphingosine 1-phosphate. J Immunol 2007;178:5425-5428. (Pubitemid 46674335)
47. Huang MC, Watson SR, Liao JJ, Goetzl EJ: Th17 augmentation in OTII TCR plus T cell-selective type 1 sphingosine 1-phosphate receptor double transgenic mice. J Immunol 2007;178:6806-6813. (Pubitemid 46847405)
48. Akira S: Mammalian toll-like receptors. Current opinion in immunology 2003;15:5-11. (Pubitemid 35454185)
49. Nishi T, Kobayashi N, Hisano Y, Kawahara A, Yamaguchi A: Molecular and physiological functions of sphingosine 1-phosphate transporters. Biochim Biophys Acta;1841:759-765.
50. Kim RH, Takabe K, Milstien S, Spiegel S: Export and functions of sphingosine-1-phosphate. Biochim Biophys Acta 2009;1791:692-696.
51. Sato K, Malchinkhuu E, Horiuchi Y, Mogi C, Tomura H, Tosaka M, Yoshimoto Y, Kuwabara A, Okajima F: Critical role of ABCa1 transporter in sphingosine 1-phosphate release from astrocytes. J Neurochem 2007;103:2610-2619.
52. Kobayashi N, Yamaguchi A, Nishi T: Characterization of the ATP-dependent sphingosine 1-phosphate transporter in rat erythrocytes. J Biol Chem 2009;284:21192-21200.
53. Osborne N, Brand-Arzamendi K, Ober EA, Jin SW, Verkade H, Holtzman NG, Yelon D, Stainier DY: The spinster homolog, two of hearts, is required for sphingosine 1-phosphate signaling in zebrafish. Curr Biol 2008;18:1882-1888.
54. Kawahara A, Nishi T, Hisano Y, Fukui H, Yamaguchi A, Mochizuki N: The sphingolipid transporter spns2 functions in migration of zebrafish myocardial precursors. Science 2009;323:524-527.
55. 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 U S A 2006;103:16394-16399. (Pubitemid 44715207)
56. Nieuwenhuis B, Luth A, Chun J, Huwiler A, Pfeilschifter J, Schafer-Korting M, Kleuser B: 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) 2009;87:645-657.
57. van de Ven R, de Jong MC, Reurs AW, Schoonderwoerd AJ, Jansen G, Hooijberg JH, Scheffer GL, de Gruijl TD, Scheper RJ: Dendritic cells require multidrug resistance protein 1 (ABCc1) transporter activity for differentiation. J Immunol 2006;176:5191-5198.
58. Ocaña-Morgner C, Reichardt P, Chopin M, Braungart S, Wahren C, Gunzer M, Jessberger R: Sphingosine 1-phosphate-induced motility and endocytosis of dendritic cells is regulated by SWAP-70 through RhoA. J Immunol 2011;186:5345-5355.
59. Inaba K, Turley S, Iyoda T, Yamaide F, Shimoyama S, Reis e Sousa C, Germain RN, Mellman I, Steinman RM: The formation of immunogenic major histocompatibility complex class II-peptide ligands in lysosomal compartments of dendritic cells is regulated by inflammatory stimuli. J Exp Med 2000;191:927-936.
60. Reis e Sousa C: Toll-like receptors and dendritic cells: For whom the bug tolls. Sem Immunol 2004;16:27-34. (Pubitemid 38147431)
61. Schaper K, Kietzmann M, Baumer W: Sphingosine-1-phosphate differently regulates the cytokine production of IL-12, IL-23 and IL-27 in activated murine bone marrow derived dendritic cells. Mol Immunol 2014;59:10-18
62. Yamanaka M, Shegogue D, Pei H, Bu S, Bielawska A, Bielawski J, Pettus B, Hannun YA, Obeid L, Trojanowska M: Sphingosine kinase 1 (SphK1) is induced by transforming growth factor-beta and mediates TIMP-1 up-regulation. J Biol Chem 2004;279:53994-54001. (Pubitemid 40053131)
63. Wadgaonkar R, Patel V, Grinkina N, Romano C, Liu J, Zhao Y, Sammani S, Garcia JG, Natarajan V: Differential regulation of sphingosine kinases 1 and 2 in lung injury. Am J Physiol Lung Cell Mol Physiol 2009;296:L603-613.
64. Yoshimoto T, Furuhata M, Kamiya S, Hisada M, Miyaji H, Magami Y, Yamamoto K, Fujiwara H, Mizuguchi J: Positive modulation of IL-12 signaling by sphingosine kinase 2 associating with the IL-12 receptor beta 1 cytoplasmic region. J Immunol 2003;171:1352-1359. (Pubitemid 36900067)
65. Jung ID, Lee JS, Kim YJ, Jeong YI, Lee CM, Baumruker T, Billlich A, Banno Y, Lee MG, Ahn SC, Park WS, Han J, Park YM: Sphingosine kinase inhibitor suppresses a Th1 polarization via the inhibition of immunostimulatory activity in murine bone marrow-derived dendritic cells. Int Immunol 2007;19:411-426. (Pubitemid 46523389)
66. Ceballos A, Sabatté J, Nahmod K, Martínez D, Salamone G, Vermeulen M, Maggini J, Salomón H, Geffner J: Sphingosylphosphorylcholine activates dendritic cells, stimulating the production of interleukin-12. Immunology 2007;121:328-336. (Pubitemid 46817354)
67. Müller H, Hofer S, Kaneider N, Neuwirt H, Mosheimer B, Mayer G, Konwalinka G, Heufler C, Tiefenthaler M: The immunomodulator FTY720 interferes with effector functions of human monocyte-derived dendritic cells. Eur J Immunol 2005;35:533-545. (Pubitemid 40331330)
68. Rolin J, Sand KL, Knudsen E, Maghazachi AA: FTY720 and SEW2871 reverse the inhibitory effect of S1P on natural killer cell mediated lysis of K562 tumor cells and dendritic cells but not on cytokine release. Cancer Immunol Immunother 2010;59:575-586.
69. Seo YJ, Pritzl CJ, Vijayan M, Blake CR, McClain ME, Hahm B: Sphingosine analogue AAL-R increases TLR7-mediated dendritic cell responses via p38 and type I IFN signaling pathways. J Immunol 2012;188:4759-4768.
70. Rüger K, Ottenlinger F, Schröder M, Zivkovic A, Stark H, Pfeilschifter JM, Radeke HH: Modulation of IL-33/ ST2-TIR and TLR signaling pathway by fingolimod and analogs in immune cells Cell Mol Immunol 2014, in revision
71. Sekar D, Hahn C, Brüne B, Roberts E, Weigert A: Apoptotic tumor cells induce IL-27 release from human DCs to activate Treg cells that express CD69 and attenuate cytotoxicity. Eur J Immunol 2012;42:1585-1598.
72. Guerrero M, Urbano M, Zhao J, Crisp M, Chase P, Hodder P, Schaeffer MT, Brown S, Rosen H, Roberts E: Discovery, design and synthesis of novel potent and selective sphingosine-1-phosphate 4 receptor (S1P4-R) agonists. Bioorg Med Chem Lett 2012;22:537-542.
73. Schulze T, Golfier S, Tabeling C, Räbel K, Gräler MH, Witzenrath M, Lipp M: Sphingosine-1-phospate receptor 4 (S1P4) deficiency profoundly affects dendritic cell function and Th17 cell differentiation in a murine model. FASEB J 2011;25:4024-4036.
74. Daniel C, Sartory NA, Zahn N, Schmidt R, Geisslinger G, Radeke HH, Stein JM: FTY720 ameliorates oxazolone colitis in mice by directly affecting T helper type 2 functions. Mol Immunol 2007;44:3305-3316. (Pubitemid 46678202)
75. Daniel C, Sartory N, Zahn N, Geisslinger G, Radeke HH, Stein JM: FTY720 ameliorates Th1-mediated colitis in mice by directly affecting the functional activity of CD4+CD25+ regulatory T cells. J Immunol 2007;178:2458-2468. (Pubitemid 46233446)
76. Marsolais D, Hahm B, Edelmann KH, Walsh KB, Guerrero M, Hatta Y, Kawaoka Y, Roberts E, Oldstone MB, Rosen H: Local not systemic modulation of dendritic cell S1P receptors in lung blunts virus-specific immune responses to influenza. Mol Pharmacol 2008;74:896-903.
77. Marsolais D, Hahm B, Walsh KB, Edelmann KH, McGavern D, Hatta Y, Kawaoka Y, Rosen H, Oldstone MB: A critical role for the sphingosine analog AAL-R in dampening the cytokine response during influenza virus infection. Proc Natl Acad Sci U S A 2009;106:1560-1565.
78. Marsolais D, Yagi S, Kago T, Leaf N, Rosen H: Modulation of chemokines and allergic airway inflammation by selective local sphingosine-1-phosphate receptor 1 agonism in lungs. Mol Pharmacol 2011;79:61-68.
79. Reines I, Kietzmann M, Mischke R, Tschernig T, Lüth A, Kleuser B, Bäumer W: Topical application of sphingosine-1-phosphate and FTY720 attenuate allergic contact dermatitis reaction through inhibition of dendritic cell migration. J Invest Dermatol 2009;129:1954-1962.
80. Baumer W, Rossbach K, Mischke R, Reines I, Langbein-Detsch I, Luth A, Kleuser B: Decreased concentration and enhanced metabolism of sphingosine-1-phosphate in lesional skin of dogs with atopic dermatitis: Disturbed sphingosine-1-phosphate homeostasis in atopic dermatitis. J Invest Dermatol 2011;131:266-268.
81. Seo EY, Park GT, Lee KM, Kim JA, Lee JH, Yang JM: Identification of the target genes of atopic dermatitis by real-time PCR. J Invest Dermatol 2006;126:1187-1189.
82. Wood SH, Clements DN, Ollier WE, Nuttall T, McEwan NA, Carter SD: Gene expression in canine atopic dermatitis and correlation with clinical severity scores. J Dermatol Sci 2009;55:27-33.
83. Nickoloff BJ, Qin JZ, Nestle FO: Immunopathogenesis of psoriasis. Clin Rev Allergy Immunol 2007;33:45-56. (Pubitemid 351514147)
84. Lowes MA, Bowcock AM, Krueger JG: Pathogenesis and therapy of psoriasis. Nature 2007;445:866-873.
85. Leonardi CL, Kimball AB, Papp KA, Yeilding N, Guzzo C, Wang Y, Li S, Dooley LT, Gordon KB: Efficacy and safety of ustekinumab, a human interleukin-12/23 monoclonal antibody, in patients with psoriasis: 76-week results from a randomised, double-blind, placebo-controlled trial (PHOENIX 1). Lancet 2008;371:1665-1674. (Pubitemid 351671883)
86. Leonardi C, Matheson R, Zachariae C, Cameron G, Li L, Edson-Heredia E, Braun D, Banerjee S: Anti-interleukin-17 monoclonal antibody ixekizumab in chronic plaque psoriasis. N Engl J Med 2012;366:1190-1199.
87. Schaper K, Dickhaut J, Japtok L, Kietzmann M, Mischke R, Kleuser B, Bäumer W: Sphingosine-1-phosphate exhibits anti-proliferative and anti-inflammatory effects in mouse models of psoriasis. J Dermatol Sci 2013;71:29-36.
88. van der Fits L, Mourits S, Voerman JS, Kant M, Boon L, Laman JD, Cornelissen F, Mus AM, Florencia E, Prens EP, Lubberts E: Imiquimod-induced psoriasis-like skin inflammation in mice is mediated via the IL-23/IL-17 axis. J Immunol 2009;182:5836-5845.
89. Mechtcheriakova D, Wlachos A, Sobanov J, Kopp T, Reuschel R, Bornancin F, Cai R, Zemann B, Urtz N, Stingl G, Zlabinger G, Woisetschlager M, Baumruker T, Billich A: Sphingosine 1-phosphate phosphatase 2 is induced during inflammatory responses. Cell Signal 2007;19:748-760. (Pubitemid 46275367)
90. Huwiler A, Bourquin F, Kotelevets N, Pastukhov O, Capitani G, Grütter MG, Zangemeister-Wittke U: A prokaryotic S1P lyase degrades extracellular S1P in vitro and in vivo: Implication for treating hyperproliferative disorders. PLoS One 2011;6:e22436.
91. Cristobal I, Manso R, Rincon R, Carames C, Senin C, Borrero A, Martinez-Useros J, Rodriguez M, Zazo S, Martinez-Aguilera O, Madoz-Gurpide J, Rojo F, Garcia-Foncillas J: PP2a inhibition is a common event in colorectal cancer and its restoration using FTY720 shows promising therapeutic potential. Mol Cancer Ther 2014;13:938-947.