S1 pping fire: Sphingosine-1-phosphate signaling as an emerging target in inflammatory bowel disease and colitis-associated cancer

Clinical and Experimental Gastroenterology

Volumn 7, Issue 1, 2014, Pages 205-214

  Degagné, Emilie ^a   Saba, Julie D ^a  

^a CHILDREN S HOSPITAL OAKLAND RESEARCH INSTITUTE   (United States)

Author keywords

S1PR; Sphingadienes; Sphingolipids; Sphingosine kinase; Sphingosine phosphate lyase; STAT3

Indexed keywords

FINGOLIMOD; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LIPID KINASE; PHOSPHOTRANSFERASE; SPHINGOSINE 1 PHOSPHATE; SPHINGOSINE KINASE 1; SPHINGOSINE KINASE 2; STAT3 PROTEIN; UNCLASSIFIED DRUG;

AUTOIMMUNE DISEASE; COLITIS; COLITIS ASOCIATED CANCER; CROHN DISEASE; DEGRADATION KINETICS; DISEASE ASSOCIATION; DOWN REGULATION; HUMAN; IMMUNOCOMPETENT CELL; INFLAMMATORY BOWEL DISEASE; INTESTINE CELL; LIPID DIET; LYMPHOCYTE MIGRATION; LYMPHOCYTE PROLIFERATION; NEOPLASM; NONHUMAN; PROTEIN EXPRESSION; PROTEIN TARGETING; REVIEW; RISK ASSESSMENT; RISK FACTOR; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION; ULCERATIVE COLITIS; UPREGULATION;

EID: 84903632868     PISSN: None     EISSN: 11787023     Source Type: Journal    
DOI: 10.2147/CEG.S43453     Document Type: Review

References (100)

1. Odze R. Diagnostic problems and advances in inflammatory bowel disease. Mod Pathol. 2003;16(4):347-358.
2. Ullman TA, Itzkowitz SH. Intestinal inflammation and cancer. Gastroenterology. 2011;140(6):1807-1816.
3. Bosani M, Ardizzone S, Porro GB. Biologic targeting in the treatment of inflammatory bowel diseases. Biologics. 2009;3:77-97.
4. Neurath MF. Cytokines in inflammatory bowel disease. Nat Rev Immunol. 2014;14(5):329-342.
5. Sylvester FA, Gordon CM, Thayu M, et al. Report of the CCFA pediatric bone, growth and muscle health workshop, New York City, November 11-12, 2011, with updates. Infamm Bowel Dis. 2013;19(13):2919-2926.
6. Baumgart DC, Sandborn WJ. Crohn's disease. Lancet. 2012;380(9853): 1590-1605.
7. Ordás I, Eckmann L, Talamini M, Baumgart DC, Sandborn WJ. Ulcer-ative colitis. Lancet. 2012;380(9853):1606-1619.
8. Blumberg RS. Inflammation in the intestinal tract: pathogenesis and treatment. Dig Dis. 2009;27(4):455-464.
9. Abraham C, Medzhitov R. Interactions between the host innate immune system and microbes in inflammatory bowel disease. Gastroenterology. 2011;140(6):1729-1737.
10. Kaser A, Blumberg RS. Adaptive immunity in inflammatory bowel disease: state of the art. Curr Opin Gastroenterol. 2008;24(4):455-461.
11. Iskandar HN, Ciorba MA. Biomarkers in inflammatory bowel disease: current practices and recent advances. Transl Res. 2012;159(4): 313-325.
12. Christophi G P, Rong R, Holtzapple PG, Massa PT, Landas SK. Immune markers and differential signaling networks in ulcerative colitis and Crohn's disease. Infamm Bowel Dis. 2012;18(12):2342-2356.
13. Biswas A, Petnicki-Ocwieja T, Kobayashi KS. Nod2: a key regulator linking microbiota to intestinal mucosal immunity. J Mol Med (Berl). 2012;90(1):15-24.
14. Boniface K, Blom B, Liu YJ, de Waal Malefyt R. From interleukin-23 to T-helper 1 7 cells: human T-helper cell differentiation revisited. Immunol Rev. 2008;226:132-146.
15. Dubinsky MC, Wang D, Picornell Y, et al; Western Regional Research Alliance for Pediatric IBD. IL-23 receptor (IL-23R) gene protects against pediatric Crohn's disease. Infamm Bowel Dis. 2007;13(5):511-515.
16. Naser SA, Arce M, Khaja A, et al. Role of ATG16L, NOD2 and IL23R in Crohn's disease pathogenesis. World J Gastroenterol. 2012;18(5): 412-424.
17. Maloy KJ, Kullberg MC. IL-23 and Th17 cytokines in intestinal homeo-stasis. Mucosal Immunol. 2008;1(5):339-349.
18. Noble CL, Abbas AR, Lees C W, et al. Characterization of intestinal gene expression profles in Crohn's disease by genome-wide microarray analysis. Infamm Bowel Dis. 2010;16(10):1717-1728.
19. McGovern D P, Gardet A, Törkvist L, et al; NIDDK IBD Genetics Consortium. Genome-wide association identifes multiple ulcerative colitis susceptibility loci. Nat Genet. 2010;42(4):332-337.
20. Grivennikov S, Karin E, Terzic J, et al. IL-6 and Stat3 are required for survival of intestinal epithelial cells and development of colitis-associated cancer. Cancer Cell. 2009;15(2):103-113.
21. Festen EA, Szperl AM, Weersma RK, Wijmenga C, Wapenaar MC. Inflammatory bowel disease and celiac disease: overlaps in the pathology and genetics, and their potential drug targets. Endocr Metab Immune Disord Drug Targets. 2009;9(2):199-218.
22. Erdman SE, Poutahidis T. Roles for inflammation and regulatory T cells in colon cancer. Toxicol Pathol. 2010;38(1):76-87.
23. Hayakawa Y, Maeda S, Nakagawa H, et al. Effectiveness of IkappaB kinase inhibitors in murine colitis-associated tumorigenesis. J Gastroenterol. 2009;44(9):935-943.
24. Bromberg J, Wang TC. Inflammation and cancer: IL-6 and STAT3 complete the link. Cancer Cell. 2009;15(2):79-80.
25. Aaronson DS, Horvath CM. A road map for those who don't know JAK-STAT. Science. 2002;296(5573):1653-1655.
26. Grivennikov SI, Karin M. Dangerous liaisons: STAT3 and NF-kappaB collaboration and crosstalk in cancer. Cytokine Growth Factor Rev. 2010;21(1):11-19.
27. Scaldaferri F, Correale C, Gasbarrini A, Danese S. Molecular signaling blockade as a new approach to inhibit leukocyte-endothelial interactions for inflammatory bowel disease treatment. Cell Adh Migr. 2009;3(3):296-299.
28. Danese S. Role of the vascular and lymphatic endothelium in the pathogenesis of inflammatory bowel disease: 'brothers in arms'. Gut. 2011;60(7):998-1008.
29. Fyrst H, Saba JD. An update on sphingosine-1-phosphate and other sphingolipid mediators. Nat Chem Biol. 2010;6(7):489-497.
30. Spiegel S, Milstien S. The outs and ins of sphingosine-1-phosphate in immunity. Nat Rev Immunol. 2011;11(6):403-415.
31. Rivera J, Proia RL, Olivera A. The alliance of sphingosine-1-phosphate and its receptors in immunity. Nat Rev Immunol. 2008;8(10):753-763.
32. Lee H, Deng J, Kujawski M, et al. STAT3-induced S1PR1 expression is crucial for persistent STAT3 activation in tumors. Nat Med. 2010;16(12):1421-1428.
33. Slattery ML, Lundgreen A, Kadlubar SA, Bondurant KL, Wolff RK. JAK/STAT/SOCS-signaling pathway and colon and rectal cancer. Mol Carcinog. 2013;52(2):155-166.
34. Corvinus FM, Orth C, Moriggl R, et al. Persistent STAT3 activation in colon cancer is associated with enhanced cell proliferation and tumor growth. Neoplasia. 2005;7(6):545-555.
35. Lin Q, Lai R, Chirieac LR, et al. Constitutive activation of JAK3/STAT3 in colon carcinoma tumors and cell lines: inhibition of JAK3/STAT3 signaling induces apoptosis and cell cycle arrest of colon carcinoma cells. Am J Pathol. 2005;167(4):969-980.
36. Santandreu FM, Valle A, Oliver J, Roca P. Resveratrol potentiates the cytotoxic oxidative stress induced by chemotherapy in human colon cancer cells. Cell Physiol Biochem. 2011;28(2):219-228.
37. Wang Z, Jin H, Xu R, Mei Q, Fan D. Triptolide downregulates Rac1 and the JAK/STAT3 pathway and inhibits colitis-related colon cancer progression. Exp Mol Med. 2009;41(10):717-727.
38. Li Y, de Haar C, Chen M, et al. Disease-related expression of the IL6/ STAT3/SOCS3 signalling pathway in ulcerative colitis and ulcerative colitis-related carcinogenesis. Gut. 2010;59(2):227-235.
39. Oskouian B, Saba J. Sphingosine-1-phosphate metabolism and intestinal tumorigenesis: lipid signaling strikes again. Cell Cycle. 2007;6(5): 522-527.
40. Furuya H, Shimizu Y, Kawamori T. Sphingolipids in cancer. Cancer Metastasis Rev. 2011;30(3-4):567-576.
41. Alvarez SE, Harikumar KB, Hait NC, et al. Sphingosine-1-phosphate is a missing cofactor for the E3 ubiquitin ligase TRAF2. Nature. 2010;465(7301):1084-1088.
42. Hait NC, Allegood J, Maceyka M, et al. Regulation of histone acetylation in the nucleus by sphingosine-1-phosphate. Science. 2009;325(5945):1254-1257.
43. Mandala SM. Sphingosine-1-phosphate phosphatases. Prostaglandins. 2001;64(1-4):143-156.
44. Aguilar A, Saba JD. Truth and consequences of sphingosine-1-phosphate lyase. Adv Biol Regul. 2012;52(1):17-30.
45. Saba JD, Nara F, Bielawska A, Garrett S, Hannun YA. The BST1 gene of Saccharomyces cerevisiae is the sphingosine-1-phosphate lyase. J Biol Chem. 1997;272(42):26087-26090.
46. Oskouian B, Sooriyakumaran P, Borowsky AD, et al. Sphingosine-1-phosphate lyase potentiates apoptosis via p53- and p38-dependent pathways and is down-regulated in colon cancer. Proc Natl Acad Sci U S A. 2006;103(46):17384-17389.
47. Kohno M, Momoi M, Oo ML, et al. Intracellular role for sphingosine kinase 1 in intestinal adenoma cell proliferation. Mol Cell Biol. 2006;26(19):7211-7223.
48. Liang J, Nagahashi M, Kim E Y, et al. Sphingosine-1-phosphate links persistent STAT3 activation, chronic intestinal inflammation, and development of colitis-associated cancer. Cancer Cell. 2013;23(1):107-120.
49. Duan RD. Physiological functions and clinical implications of sphin-golipids in the gut. J Dig Dis. 2011;12(2):60-70.
50. Skieceviciene J, Kiudelis G, Ellinghaus E, et al. Replication study of ulcerative colitis risk loci in a Lithuanian-Latvian case-control sample. Infamm Bowel Dis. 2013;19(11):2349-2355.
51. Matloubian M, Lo CG, Cinamon G, et al. Lymphocyte egress from thymus and peripheral lymphoid organs is dependent on S1P receptor 1. Nature. 2004;427(6972):355-360.
52. Lo CG, Xu Y, Proia RL, Cyster JG. Cyclical modulation of sphingosine-1-phosphate receptor 1 surface expression during lymphocyte recirculation and relationship to lymphoid organ transit. J Exp Med. 2005;201(2):291-301.
53. Schwab SR, Pereira J P, Matloubian M, Xu Y, Huang Y, Cyster JG. Lymphocyte sequestration through S1P lyase inhibition and disruption of S1P gradients. Science. 2005;309(5741):1735-1739.
54. Vogel P, Donoviel MS, Read R, et al. Incomplete inhibition of sphingosine 1-phosphate lyase modulates immune system function yet prevents early lethality and non-lymphoid lesions. PLoS One. 2009;4(1): e4112.
55. Bréart B, Ramos-Perez WD, Mendoza A, et al. Lipid phosphate phosphatase 3 enables effcient thymic egress. J Exp Med. 2011;208(6): 1267-1278.
56. Kappos L, Antel J, Comi G, et al; FTY720 D2201 Study Group. Oral fngolimod (FTY720) for relapsing multiple sclerosis. N Engl J Med. 2006;355(11):1124-1140.
57. Kappos L, Radue EW, O'Connor P, et al; FREEDOMS Study Group. A placebo-controlled trial of oral fngolimod in relapsing multiple sclerosis. N Engl J Med. 2010;362(5):387-401.
58. Cohen JA, Barkhof F, Comi G, et al; TRANSFORMS Study Group. Oral fngolimod or intramuscular interferon for relapsing multiple sclerosis. N Engl J Med. 2010;362(5):402-415.
59. Comi G, O'Connor P, Montalban X, et al; FTY720D2201 Study Group. Phase II study of oral fngolimod (FTY720) in multiple sclerosis: 3 -year results. Mult Scler. 2010;16(2):197-207.
60. Wang F, Okamoto Y, Inoki I, et al. Sphingosine-1-phosphate receptor-2 defciency leads to inhibition of macrophage proinfammatory activities and atherosclerosis in apoE-defcient mice. J Clin Invest. 2010;120(11): 3979-3995.
61. Garris CS, Wu L, Acharya S, et al. Defective sphingosine 1-phosphate receptor 1 (S1P1) phosphorylation exacerbates TH17-mediated autoimmune neuroinfammation. Nat Immunol. 2013;14(11): 1166-1172.
62. Nixon GF. Sphingolipids in inflammation: pathological implications and potential therapeutic targets. Br J Pharmacol. 2009;158(4): 982-993.
63. Duan RD, Nilsson A. Metabolism of sphingolipids in the gut and its relation to inflammation and cancer development. Prog Lipid Res. 2009;48(1):62-72.
64. Soo I, Madsen KL, Tejpar Q, et al. VSL#3 probiotic upregulates intestinal mucosal alkaline sphingomyelinase and reduces inflammation. Can J Gastroenterol. 2008;22(3):237-242.
65. Mazzei JC, Zhou H, Brayfeld B P, Hontecillas R, Bassaganya-Riera J, Schmelz EM. Suppression of intestinal inflammation and inflammation-driven colon cancer in mice by dietary sphingomyelin: importance of peroxisome proliferator-activated receptor γ expression. J Nutr Biochem. 2011;22(12):1160-1171.
66. Deguchi Y, Andoh A, Yagi Y, et al. The S1P receptor modulator FTY720 prevents the development of experimental colitis in mice. Oncol Rep. 2006;16(4):699-703.
67. 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. 2011;6(9):e23933.
68. Mizushima T, Ito T, Kishi D, et al. Therapeutic effects of a new lymphocyte homing reagent FTY720 in interleukin-10 gene-defcient mice with colitis. Infamm Bowel Dis. 2004;10(3):182-192.
69. 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. 2008;324(1):276-283.
70. Fuss IJ, Neurath M, Boirivant M, et al. Disparate CD4+ lamina propria (LP) lymphokine secretion profles in inflammatory bowel disease. Crohn's disease LP cells manifest increased secretion of IFN-gamma, whereas ulcerative colitis LP cells manifest increased secretion of IL-5. J Immunol. 1996;157(3):1261-1270.
71. Strober W, Fuss IJ. Proinflammatory cytokines in the pathogen-esis of inflammatory bowel diseases. Gastroenterology. 2011;140(6): 1756-1767.
72. Fuss IJ, Heller F, Boirivant M, et al. Nonclassical CD1d-restricted NK T cells that produce IL-13 characterize an atypical Th2 response in ulcerative colitis. J Clin Invest. 2004;113(10):1490-1497.
73. Daniel C, Sartory NA, Zahn N, et al. FTY720 ameliorates oxazolone colitis in mice by directly affecting T helper type 2 functions. Mol Immunol. 2007;44(13):3305-3316.
74. 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(4):2458-2468.
75. Snider AJ, Kawamori T, Bradshaw SG, et al. A role for sphingosine kinase 1 in dextran sulfate sodium-induced colitis. FASEB J. 2009;23(1):143-152.
76. Maines LW, Fitzpatrick LR, French KJ, et al. Suppression of ulcerative colitis in mice by orally available inhibitors of sphingosine kinase. Dig Dis Sci. 2008;53(4):997-1012.
77. Borowsky AD, Bandhuvula P, Kumar A, et al. Sphingosine-1-phosphate lyase expression in embryonic and adult murine tissues. Natl Acad Sci USA. 2006;103(46):17384-17389.
78. Oskouian B, Sooriyakumaran P, Borowsky AD, et al. Sphingosine-1-phosphate lyase potentiates apoptosis via p53- and p38-dependent pathways and is down-regulated in colon cancer. J Lipid Res. 2012;53(9):1920-1931.
79. Selhub J, Byun A, Liu Z, Mason JB, Bronson RT, Crott J W. Dietary vitamin B6 intake modulates colonic inflammation in the IL10-/-model of inflammatory bowel disease. J Nutr Biochem. 2013;24(12): 2138-2143.
80. Paugh BS, Bryan L, Paugh S W, et al. Interleukin-1 regulates the expression of sphingosine kinase 1 in glioblastoma cells. J Biol Chem. 2009;284(6):3408-3417.
81. Yamaguchi K, Lantowski A, Dannenberg AJ, Subbaramaiah K. Histone deacetylase inhibitors suppress the induction of c-Jun and its target genes including COX-2. J Biol Chem. 2005;280(38): 32569-32577.
82. Atreya I, Atreya R, Neurath MF. NF-kappaB in inflammatory bowel disease. J Intern Med. 2008;263(6):591-596.
83. Karin M. NF-kappaB as a critical link between inflammation and cancer. Cold Spring Harb Perspect Biol. 2009;1(5):a000141.
84. Xiao W, Hodge DR, Wang L, Yang X, Zhang X, Farrar WL. NF-kappaB activates IL-6 expression through cooperation with c-Jun and IL6-AP1 site, but is independent of its IL6-NFkappaB regulatory site in auto-crine human multiple myeloma cells. Cancer Biol Ther. 2004;3(10): 1007-1017.
85. Brinkmann V. FTY720 (fngolimod) in multiple sclerosis: therapeutic effects in the immune and the central nervous system. Br J Pharmacol. 2009;158(5):1173-1182.
86. Vessey DA, Kelley M, Zhang J, Li L, Tao R, Karliner JS. Dimethylsphingosine and FTY720 inhibit the SK1 form but activate the SK2 form of sphingosine kinase from rat heart. J Biochem Mol Toxicol. 2007;21(5):273-279.
87. 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. 2011;286(21):18633-18640.
88. Vesper H, Schmelz EM, Nikolova-Karakashian MN, Dillehay DL, Lynch DV, Merrill AH Jr. Sphingolipids in food and the emerging importance of sphingolipids to nutrition. J Nutr. 1999;129(7):1239-1250.
89. Thaker AI, Shaker A, Rao MS, Ciorba MA. Modeling colitis-associated cancer with azoxymethane (AOM) and dextran sulfate sodium (DSS). J Vis Exp. 2012;(67).
90. Santiago C, Pagán B, Isidro AA, Appleyard CB. Prolonged chronic inflammation progresses to dysplasia in a novel rat model of colitis-associated colon cancer. Cancer Res. 2007;67(22):10766-10773.
91. Hamiza OO, Rehman MU, Tahir M, et al. Amelioration of 1,2 dimeth-ylhydrazine (DMH) induced colon oxidative stress, inflammation and tumor promotion response by tannic acid in Wistar rats. Asian Pac J Cancer Prev. 2012;13(9):4393-4402.
92. Dillehay DL, Webb SK, Schmelz EM, Merrill AH Jr. Dietary sphingomyelin inhibits 1,2-dimethylhydrazine-induced colon cancer in CF1 mice. J Nutr. 1994;124(5):615-620.
93. Symolon H, Schmelz EM, Dillehay DL, Merrill AH Jr. Dietary soy sphingolipids suppress tumorigenesis and gene expression in 1,2-dimethylhydrazine-treated CF1 mice and ApcMin/+ mice. J Nutr. 2004;134(5):1157-1161.
94. Mazzei JC, Zhou H, Brayfield BP, Hontecillas R, Bassaganya-Riera J, Schmelz EM. Suppression of intestinal inflammation and inflammation-driven colon cancer in mice by dietary sphingomyelin: importance of peroxisome proliferator-activated receptory expression. J Nutr Biochem. 2011;22(12):1160-1171.
95. Fischbeck A, Leucht K, Frey-Wagner I, et al. Sphingomyelin induces cathepsin D-mediated apoptosis in intestinal epithelial cells and increases inflammation in DSS colitis. Gut. 2011;60(1):55-65.
96. Fyrst H, Oskouian B, Bandhuvula P, et al. Natural sphingadienes inhibit Akt-dependent signaling and prevent intestinal tumorigenesis. Cancer Res. 2009;69(24):9457-9464.
97. Kumar A, Pandurangan AK, Lu F, et al. Chemopreventive sphingadienes downregulate Wnt signaling via a PP2A/Akt/GSK3β pathway in colon cancer. Carcinogenesis. 2012;33(9):1726-1735.
98. Montrose DC, Scherl EJ, Bosworth BP, et al. S1P. localizes to the colonic vasculature in ulcerative colitis and maintains blood vessel integrity. J Lipid Res. 2013;54(3):843-851.
99. 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. 2012;80(8): 2712-2723.
100. Samy ET, Meyer CA, Caplazi P, et al. Cutting edge: Modulation of intestinal autoimmunity and IL-2 signaling by sphingosine kinase 2 independent of sphingosine 1-phosphate. J Immunol. 2007;179(9): 5644-5648.