Sphingosine-1-Phosphate Links Persistent STAT3 Activation, Chronic Intestinal Inflammation, and Development of Colitis-Associated Cancer

Cancer Cell

Volumn 23, Issue 1, 2013, Pages 107-120

  Liang, Jie ^a,c   Nagahashi, Masayuki ^a,b   Kim, Eugene Y ^a   Harikumar, Kuzhuvelil B ^a   Yamada, Akimitsu ^a,b   Huang, Wei Ching ^a   Hait, Nitai C ^a   Allegood, Jeremy C ^a   Price, Megan M ^a   Avni, Dorit ^a   Takabe, Kazuaki ^a,b   Kordula, Tomasz ^a   Milstien, Sheldon ^a   Spiegel, Sarah ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^b VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c State Key Laboratory of Cancer Biology   (China)

Author keywords

[No Author keywords available]

Indexed keywords

DEXTRAN SULFATE; FINGOLIMOD; INTERLEUKIN 6; SPHINGOSINE 1 PHOSPHATE; STAT3 PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CARCINOGENESIS; COLITIS; COLITIS ASSOCIATED CANCER; COLON CANCER; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE SEVERITY; ENTERITIS; GENE DELETION; HEMATOPOIETIC STEM CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; ULCERATIVE COLITIS; UPREGULATION; WEIGHT REDUCTION;

MUS;

EID: 84872406787     PISSN: 15356108     EISSN: 18783686     Source Type: Journal    
DOI: 10.1016/j.ccr.2012.11.013     Document Type: Article

References (59)

1. Alvarez S.E., Harikumar K.B., Hait N.C., Allegood J., Strub G.M., Kim E.Y., Maceyka M., Jiang H., Luo C., Kordula T., et al. Sphingosine-1-phosphate is a missing cofactor for the E3 ubiquitin ligase TRAF2. Nature 2010, 465:1084-1088.
2. Becker C., Fantini M.C., Schramm C., Lehr H.A., Wirtz S., Nikolaev A., Burg J., Strand S., Kiesslich R., Huber S., et al. TGF-beta suppresses tumor progression in colon cancer by inhibition of IL-6 trans-signaling. Immunity 2004, 21:491-501.
3. Ben-Neriah Y., Karin M. Inflammation meets cancer, with NF-κB as the matchmaker. Nat. Immunol. 2011, 12:715-723.
4. Billich A., Bornancin F., Dévay P., Mechtcheriakova D., Urtz N., Baumruker T. Phosphorylation of the immunomodulatory drug FTY720 by sphingosine kinases. J. Biol. Chem. 2003, 278:47408-47415.
5. Bollrath J., Phesse T.J., von Burstin V.A., Putoczki T., Bennecke M., Bateman T., Nebelsiek T., Lundgren-May T., Canli O., Schwitalla S., et al. gp130-mediated Stat3 activation in enterocytes regulates cell survival and cell-cycle progression during colitis-associated tumorigenesis. Cancer Cell 2009, 15:91-102.
6. Brinkmann V., Billich A., Baumruker T., Heining P., Schmouder R., Francis G., Aradhye S., Burtin P. Fingolimod (FTY720): discovery and development of an oral drug to treat multiple sclerosis. Nat. Rev. Drug Discov. 2010, 9:883-897.
7. Daniel C., Sartory N.A., Zahn N., Schmidt R., Geisslinger G., Radeke H.H., Stein J.M. FTY720 ameliorates oxazolone colitis in mice by directly affecting T helper type 2 functions. Mol. Immunol. 2007, 44:3305-3316.
8. De Palma C., Meacci E., Perrotta C., Bruni P., Clementi E. Endothelial nitric oxide synthase activation by tumor necrosis factor alpha through neutral sphingomyelinase 2, sphingosine kinase 1, and sphingosine 1 phosphate receptors: a novel pathway relevant to the pathophysiology of endothelium. Arterioscler. Thromb. Vasc. Biol. 2006, 26:99-105.
9. Deguchi Y., Andoh A., Yagi Y., Bamba S., Inatomi O., Tsujikawa T., Fujiyama Y. The S1P receptor modulator FTY720 prevents the development of experimental colitis in mice. Oncol. Rep. 2006, 16:699-703.
10. Deng J., Liu Y., Lee H., Herrmann A., Zhang W., Zhang C., Shen S., Priceman S.J., Kujawski M., Pal S.K., et al. S1PR1-STAT3 signaling is crucial for myeloid cell colonization at future metastatic sites. Cancer Cell 2012, 21:642-654.
11. Deng L., Zhou J.F., Sellers R.S., Li J.F., Nguyen A.V., Wang Y., Orlofsky A., Liu Q., Hume D.A., Pollard J.W., et al. A novel mouse model of inflammatory bowel disease links mammalian target of rapamycin-dependent hyperproliferation of colonic epithelium to inflammation-associated tumorigenesis. Am. J. Pathol. 2010, 176:952-967.
12. Gao P., Smith C.D. Ablation of sphingosine kinase-2 inhibits tumor cell proliferation and migration. Mol. Cancer Res. 2011, 9:1509-1519.
13. Greten F.R., Eckmann L., Greten T.F., Park J.M., Li Z.W., Egan L.J., Kagnoff M.F., Karin M. IKKbeta links inflammation and tumorigenesis in a mouse model of colitis-associated cancer. Cell 2004, 118:285-296.
14. Grivennikov S., Karin E., Terzic J., Mucida D., Yu G.Y., Vallabhapurapu S., Scheller J., Rose-John S., Cheroutre H., Eckmann L., Karin M. IL-6 and Stat3 are required for survival of intestinal epithelial cells and development of colitis-associated cancer. Cancer Cell 2009, 15:103-113.
15. Grivennikov S.I., Greten F.R., Karin M. Immunity, inflammation, and cancer. Cell 2010, 140:883-899.
16. Hait N.C., Allegood J., Maceyka M., Strub G.M., Harikumar K.B., Singh S.K., 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.
17. Karin M. NF-κB as a critical link between inflammation and cancer. Cold Spring Harbor Perspectives in Biology 2009, 1-14. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY. L.M. Staudt, M. Karin (Eds.).
18. Kawamori T., Kaneshiro T., Okumura M., Maalouf S., Uflacker A., Bielawski J., Hannun Y.A., Obeid L.M. Role for sphingosine kinase 1 in colon carcinogenesis. FASEB J. 2009, 23:405-414.
19. Kharel Y., Lee S., Snyder A.H., Sheasley-O'neill S.L., Morris M.A., Setiady Y., Zhu R., Zigler M.A., Burcin T.L., Ley K., et al. Sphingosine kinase 2 is required for modulation of lymphocyte traffic by FTY720. J. Biol. Chem. 2005, 280:36865-36872.
20. Kim S., Keku T.O., Martin C., Galanko J., Woosley J.T., Schroeder J.C., Satia J.A., Halabi S., Sandler R.S. Circulating levels of inflammatory cytokines and risk of colorectal adenomas. Cancer Res. 2008, 68:323-328.
21. Kortylewski M., Kujawski M., Wang T., Wei S., Zhang S., Pilon-Thomas S., Niu G., Kay H., Mulé J., Kerr W.G., et al. Inhibiting Stat3 signaling in the hematopoietic system elicits multicomponent antitumor immunity. Nat. Med. 2005, 11:1314-1321.
22. Lee H., Deng J., Kujawski M., Yang C., Liu Y., Herrmann A., Kortylewski M., Horne D., Somlo G., Forman S., et al. STAT3-induced S1PR1 expression is crucial for persistent STAT3 activation in tumors. Nat. Med. 2010, 16:1421-1428.
23. Li W., Yu C.P., Xia J.T., Zhang L., Weng G.X., Zheng H.Q., Kong Q.L., Hu L.J., Zeng M.S., Zeng Y.X., et al. Sphingosine kinase 1 is associated with gastric cancer progression and poor survival of patients. Clin. Cancer Res. 2009, 15:1393-1399.
24. Li Y., de Haar C., Chen M., Deuring J., Gerrits M.M., Smits R., Xia B., Kuipers E.J., van der Woude C.J. Disease-related expression of the IL6/STAT3/SOCS3 signalling pathway in ulcerative colitis and ulcerative colitis-related carcinogenesis. Gut 2010, 59:227-235.
25. Lim K.G., Tonelli F., Li Z., Lu X., Bittman R., Pyne S., Pyne N.J. 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, 286:18633-18640.
26. Lindström T.M., Mohan A.R., Johnson M.R., Bennett P.R. Histone deacetylase inhibitors exert time-dependent effects on nuclear factor-kappaB but consistently suppress the expression of proinflammatory genes in human myometrial cells. Mol. Pharmacol. 2008, 74:109-121.
27. Liu Y., Deng J., Wang L., Lee H., Armstrong B., Scuto A., Kowolik C., Weiss L.M., Forman S., Yu H. S1PR1 is an effective target to block STAT3 signaling in activated B cell-like diffuse large B-cell lymphoma. Blood 2012, 120:1458-1465.
28. Matsumoto S., Hara T., Mitsuyama K., Yamamoto M., Tsuruta O., Sata M., Scheller J., Rose-John S., Kado S., Takada T. Essential roles of IL-6 trans-signaling in colonic epithelial cells, induced by the IL-6/soluble-IL-6 receptor derived from lamina propria macrophages, on the development of colitis-associated premalignant cancer in a murine model. J. Immunol. 2010, 184:1543-1551.
29. Nagahashi M., Ramachandran S., Kim E.Y., Allegood J.C., Rashid O.M., Yamada A., Zhao R., Milstien S., Zhou H., Spiegel S., Takabe K. Sphingosine-1-phosphate produced by sphingosine kinase 1 promotes breast cancer progression by stimulating angiogenesis and lymphangiogenesis. Cancer Res. 2012, 72:726-735.
30. Oshima M., Dinchuk J.E., Kargman S.L., Oshima H., Hancock B., Kwong E., Trzaskos J.M., Evans J.F., Taketo M.M. Suppression of intestinal polyposis in Apc delta716 knockout mice by inhibition of cyclooxygenase 2 (COX-2). Cell 1996, 87:803-809.
31. Paugh B.S., Bryan L., Paugh S.W., Wilczynska K.M., Alvarez S.M., Singh S.K., Kapitonov D., Rokita H., Wright S., Griswold-Prenner I., et al. Interleukin-1 regulates the expression of sphingosine kinase 1 in glioblastoma cells. J. Biol. Chem. 2009, 284:3408-3417.
32. Paugh S.W., Payne S.G., Barbour S.E., Milstien S., Spiegel S. The immunosuppressant FTY720 is phosphorylated by sphingosine kinase type 2. FEBS Lett. 2003, 554:189-193.
33. Paugh S.W., Paugh B.S., Rahmani M., Kapitonov D., Almenara J.A., Kordula T., Milstien S., Adams J.K., Zipkin R.E., Grant S., Spiegel S. A selective sphingosine kinase 1 inhibitor integrates multiple molecular therapeutic targets in human leukemia. Blood 2008, 112:1382-1391.
34. Pettus B.J., Bielawski J., Porcelli A.M., Reames D.L., Johnson K.R., Morrow J., Chalfant C.E., Obeid L.M., Hannun Y.A. The sphingosine kinase 1/sphingosine-1-phosphate pathway mediates COX-2 induction and PGE2 production in response to TNF-alpha. FASEB J. 2003, 17:1411-1421.
35. Pitson S.M., Moretti P.A., Zebol J.R., Lynn H.E., Xia P., Vadas M.A., Wattenberg B.W. Activation of sphingosine kinase 1 by ERK1/2-mediated phosphorylation. EMBO J. 2003, 22:5491-5500.
36. Popivanova B.K., Kitamura K., Wu Y., Kondo T., Kagaya T., Kaneko S., Oshima M., Fujii C., Mukaida N. Blocking TNF-alpha in mice reduces colorectal carcinogenesis associated with chronic colitis. J. Clin. Invest. 2008, 118:560-570.
37. Pyne N.J., Pyne S. Sphingosine 1-phosphate and cancer. Nat. Rev. Cancer 2010, 10:489-503.
38. Rakhit S., Conway A.M., Tate R., Bower T., Pyne N.J., Pyne S. Sphingosine 1-phosphate stimulation of the p42/p44 mitogen-activated protein kinase pathway in airway smooth muscle: role of endothelial differentiation gene 1, c-Src tyrosine kinase and phosphoinositide 3-kinase. Biochem. J. 1999, 338:643-649.
39. Saleh M., Trinchieri G. Innate immune mechanisms of colitis and colitis-associated colorectal cancer. Nat. Rev. Immunol. 2011, 11:9-20.
40. Samy E.T., Meyer C.A., Caplazi P., Langrish C.L., Lora J.M., Bluethmann H., Peng S.L. Cutting edge: modulation of intestinal autoimmunity and IL-2 signaling by sphingosine kinase 2 independent of sphingosine 1-phosphate. J. Immunol. 2007, 179:5644-5648.
41. Sanna M.G., Wang S.K., Gonzalez-Cabrera P.J., Don A., Marsolais D., Matheu M.P., Wei S.H., Parker I., Jo E., Cheng W.C., et al. Enhancement of capillary leakage and restoration of lymphocyte egress by a chiral S1P1 antagonist in vivo. Nat. Chem. Biol. 2006, 2:434-441.
42. Scherer E.Q., Yang J., Canis M., Reimann K., Ivanov K., Diehl C.D., Backx P.H., Wier W.G., Strieth S., Wangemann P., et al. Tumor necrosis factor-α enhances microvascular tone and reduces blood flow in the cochlea via enhanced sphingosine-1-phosphate signaling. Stroke 2010, 41:2618-2624.
43. Schiechl G., Bauer B., Fuss I., Lang S.A., Moser C., Ruemmele P., Rose-John S., Neurath M.F., Geissler E.K., Schlitt H.J., et al. Tumor development in murine ulcerative colitis depends on MyD88 signaling of colonic F4/80+CD11b(high)Gr1(low) macrophages. J. Clin. Invest. 2011, 121:1692-1708.
44. Sensken S.C., Bode C., Gräler M.H. Accumulation of fingolimod (FTY720) in lymphoid tissues contributes to prolonged efficacy. J. Pharmacol. Exp. Ther. 2009, 328:963-969.
45. Shaner R.L., Allegood J.C., Park H., Wang E., Kelly S., Haynes C.A., Sullards M.C., Merrill A.H. Quantitative analysis of sphingolipids for lipidomics using triple quadrupole and quadrupole linear ion trap mass spectrometers. J. Lipid Res. 2009, 50:1692-1707.
46. Siegmund B., Lehr H.A., Fantuzzi G., Dinarello C.A. IL-1 beta-converting enzyme (caspase-1) in intestinal inflammation. Proc. Natl. Acad. Sci. USA 2001, 98:13249-13254.
47. Snider A.J., Kawamori T., Bradshaw S.G., Orr K.A., Gilkeson G.S., Hannun Y.A., Obeid L.M. A role for sphingosine kinase 1 in dextran sulfate sodium-induced colitis. FASEB J. 2009, 23:143-152.
48. Sobue S., Murakami M., Banno Y., Ito H., Kimura A., Gao S., Furuhata A., Takagi A., Kojima T., Suzuki M., et al. v-Src oncogene product increases sphingosine kinase 1 expression through mRNA stabilization: alteration of AU-rich element-binding proteins. Oncogene 2008, 27:6023-6033.
49. Spiegel S., Milstien S. The outs and the ins of sphingosine-1-phosphate in immunity. Nat. Rev. Immunol. 2011, 11:403-415.
50. Takeda K., Clausen B.E., Kaisho T., Tsujimura T., Terada N., Förster I., Akira S. Enhanced Th1 activity and development of chronic enterocolitis in mice devoid of Stat3 in macrophages and neutrophils. Immunity 1999, 10:39-49.
51. Tonelli F., Lim K.G., Loveridge C., Long J., Pitson S.M., Tigyi G., Bittman R., Pyne S., Pyne N.J. 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. 2010, 22:1536-1542.
52. Ullman T.A., Itzkowitz S.H. Intestinal inflammation and cancer. Gastroenterology 2011, 140:1807-1816.
53. Williams K.L., Fuller C.R., Dieleman L.A., DaCosta C.M., Haldeman K.M., Sartor R.B., Lund P.K. Enhanced survival and mucosal repair after dextran sodium sulfate-induced colitis in transgenic mice that overexpress growth hormone. Gastroenterology 2001, 120:925-937.
54. Wu S., Rhee K.J., Albesiano E., Rabizadeh S., Wu X., Yen H.R., Huso D.L., Brancati F.L., Wick E., McAllister F., et al. A human colonic commensal promotes colon tumorigenesis via activation of T helper type 17 T cell responses. Nat. Med. 2009, 15:1016-1022.
55. Xia P., Gamble J.R., Rye K.A., Wang L., Hii C.S.T., Cockerill P., Khew-Goodall Y., Bert A.G., Barter P.J., Vadas M.A. Tumor necrosis factor-alpha induces adhesion molecule expression through the sphingosine kinase pathway. Proc. Natl. Acad. Sci. USA 1998, 95:14196-14201.
56. Yamaguchi K., Lantowski A., Dannenberg A.J., Subbaramaiah K. Histone deacetylase inhibitors suppress the induction of c-Jun and its target genes including COX-2. J. Biol. Chem. 2005, 280:32569-32577.
57. Yu C.L., Meyer D.J., Campbell G.S., Larner A.C., Carter-Su C., Schwartz J., Jove R. Enhanced DNA-binding activity of a Stat3-related protein in cells transformed by the Src oncoprotein. Science 1995, 269:81-83.
58. Yu H., Pardoll D., Jove R. STATs in cancer inflammation and immunity: a leading role for STAT3. Nat. Rev. Cancer 2009, 9:798-809.
59. Zemann B., Kinzel B., Müller M., Reuschel R., Mechtcheriakova D., Urtz N., Bornancin F., Baumruker T., Billich A. Sphingosine kinase type 2 is essential for lymphopenia induced by the immunomodulatory drug FTY720. Blood 2006, 107:1454-1458.