Revisiting the sphingolipid rheostat: Evolving concepts in cancer therapy

Experimental Cell Research

Volumn 333, Issue 2, 2015, Pages 195-200

  Newton, Jason ^a   Lima, Santiago ^a   Maceyka, Michael ^a   Spiegel, Sarah ^a  

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

Author keywords

Ceramide; Sphingolipid rheostat; Sphingosine kinase; Sphingosine 1 phosphate

Indexed keywords

CERAMIDE; LYASE; PHOSPHATASE; SPHINGOLIPID; SPHINGOSINE 1 PHOSPHATE; SPHINGOSINE 1 PHOSPHATE RECEPTOR; SPHINGOSINE 1 PHOSPHATE TRANSPORTER; SPHINGOSINE KINASE 1; SPHINGOSINE KINASE 2; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; LYSOPHOSPHOLIPID; LYSOPHOSPHOLIPID RECEPTOR; PHOSPHOTRANSFERASE; SPHINGOSINE; SPHINGOSINE 1-PHOSPHATE; SPHINGOSINE KINASE;

CANCER THERAPY; CELL FATE; CELL GROWTH; CELL SURVIVAL; HUMAN; MALIGNANT NEOPLASTIC DISEASE; METABOLITE; MODULATION; NONHUMAN; PRIORITY JOURNAL; REVIEW; SPHINGOLIPID METABOLISM; ANALOGS AND DERIVATIVES; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL TRANSFORMATION; METABOLISM; MOLECULARLY TARGETED THERAPY; NEOPLASMS; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; ANTINEOPLASTIC AGENTS; CELL TRANSFORMATION, NEOPLASTIC; CERAMIDES; HUMANS; LYSOPHOSPHOLIPIDS; MOLECULAR TARGETED THERAPY; NEOPLASMS; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); RECEPTORS, LYSOPHOSPHOLIPID; SIGNAL TRANSDUCTION; SPHINGOSINE;

EID: 84927913180     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2015.02.025     Document Type: Review

References (46)

1. Cuvillier O., Pirianov G., Kleuser B., Vanek P.G., Coso O.A., Gutkind S., Spiegel S. Suppression of ceramide-mediated programmed cell death by sphingosine-1-phosphate. Nature 1996, 381:800-803.
2. Zhang H., Desai N.N., Olivera A., Seki T., Brooker G., Spiegel S. Sphingosine-1-phosphate, a novel lipid, involved in cellular proliferation. J. Cell Biol. 1991, 114:155-167.
3. Obeid L.M., Lindaric C.M., Karolak L.A., Hannun Y.A. Programmed cell death induced by ceramide. Science 1993, 259:1769-1771.
4. Olivera A., Spiegel S. Sphingosine-1-phosphate as a second messenger in cell proliferation induced by PDGF and FCS mitogens. Nature 1993, 365:557-560.
5. Morad S.A., Cabot M.C. Ceramide-orchestrated signalling in cancer cells. Nat. Rev. Cancer 2013, 13:51-65.
6. Abuhusain H.J., Matin A., Qiao Q., Shen H., Kain N., Day B.W., Stringer B.W., Daniels B., Laaksonen M.A., Teo C., McDonald K.L., Don A.S. A metabolic shift favoring sphingosine 1-phosphate at the expense of ceramide controls glioblastoma angiogenesis. J. Biol. Chem. 2013, 288:37355-37364.
7. Lee M.J., Van Brocklyn J.R., Thangada S., Liu C.H., Hand A.R., Menzeleev R., Spiegel S., Hla T. Sphingosine-1-phosphate as a ligand for the G protein-coupled receptor EDG-1. Science 1998, 279:1552-1555.
8. Rosen H., Stevens R.C., Hanson M., Roberts E., Oldstone M.B. Sphingosine-1-phosphate and its receptors: structure, signaling, and influence. Annu. Rev. Biochem. 2013, 82:637-662.
9. Hobson J.P., Rosenfeldt H.M., Barak L.S., Olivera A., Poulton S., Caron M.G., Milstien S., Spiegel S. Role of the sphingosine-1-phosphate receptor EDG-1 in PDGF-induced cell motility. Science 2001, 291:1800-1803.
10. Takabe K., Spiegel S. Export of sphingosine-1-phosphate and cancer progression. J. Lipid Res. 2014, 55:1839-1846.
11. Pyne N.J., Pyne S. Sphingosine 1-phosphate and cancer. Nat. Rev. Cancer 2010, 10:489-503.
12. Taniguchi M., Kitatani K., Kondo T., Hashimoto-Nishimura M., Asano S., Hayashi A., Mitsutake S., Igarashi Y., Umehara H., Takeya H., Kigawa J., Okazaki T. Regulation of autophagy and its associated cell death by "sphingolipid rheostat": reciprocal role of ceramide and sphingosine 1-phosphate in the mammalian target of rapamycin pathway. J. Biol. Chem. 2012, 287:39898-39910.
13. Liang J., Nagahashi M., Kim E.Y., Harikumar K.B., Yamada A., Huang W.C., Hait N.C., Allegood J.C., Price M.M., Avni D., Takabe K., Kordula T., Milstien S., Spiegel S. Sphingosine-1-phosphate links persistent STAT3 activation, chronic intestinal inflammation, and development of colitis-associated cancer. Cancer Cell 2013, 23:107-120.
14. Deng J., Liu Y., Lee H., Herrmann A., Zhang W., Zhang C., Shen S., Priceman S.J., Kujawski M., Pal S.K., Raubitschek A., Hoon D.S., Forman S., Figlin R.A., Liu J., Jove R., Yu H. S1PR1-STAT3 signaling is crucial for myeloid cell colonization at future metastatic sites. Cancer Cell 2012, 21:642-654.
15. 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.
16. 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.
17. Priceman S.J., Shen S., Wang L., Deng J., Yue C., Kujawski M., Yu H. S1PR1 is crucial for accumulation of regulatory T cells in tumors via STAT3. Cell Rep. 2014, 6:992-999.
18. 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., Milstien S., Spiegel S. Sphingosine-1-phosphate is a missing cofactor for the E3 ubiquitin ligase TRAF2. Nature 2010, 465:1084-1088.
19. Xiong Y., Lee H.J., Mariko B., Lu Y.C., Dannenberg A.J., Haka A.S., Maxfield F.R., Camerer E., Proia R.L., Hla T. Sphingosine kinases are not required for inflammatory responses in macrophages. J. Biol. Chem. 2013, 288:32563-32573.
20. 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.
21. Nguyen-Tran D.H., Hait N.C., Sperber H., Qi J., Fischer K., Ieronimakis N., Pantoja M., Hays A., Allegood J., Reyes M., Spiegel S., Ruohola-Baker H. Molecular mechanism of sphingosine-1-phosphate action in Duchenne muscular dystrophy. Dis. Model Mech. 2014, 7:41-54.
22. Hait N.C., Wise L.E., Allegood J.C., O'Brien M., Avni D., Reeves T.M., Knapp P.E., Lu J., Luo C., Miles M.F., Milstien S., Lichtman A.H., Spiegel S. Active, phosphorylated fingolimod inhibits histone deacetylases and facilitates fear extinction memory. Nat. Neurosci. 2014, 17:971-980.
23. Truman J.P., Garcia-Barros M., Obeid L.M., Hannun Y.A. Evolving concepts in cancer therapy through targeting sphingolipid metabolism. Biochim. Biophys. Acta 2014, 1841:1174-1188.
24. Kunkel G.T., Maceyka M., Milstien S., Spiegel S. Targeting the sphingosine-1-phosphate axis in cancer, inflammation and beyond. Nat. Rev. Drug Discov. 2013, 12:688-702.
25. Vadas M., Xia P., McCaughan G., Gamble J. The role of sphingosine kinase 1 in cancer: oncogene or non-oncogene addiction?. Biochim. Biophys. Acta 2008, 1781:442-447.
26. Rex K., Jeffries S., Brown M.L., Carlson T., Coxon A., Fajardo F., Frank B., Gustin D., Kamb A., Kassner P.D., Li S., Li Y., Morgenstern K., Plant M., Quon K., Ruefli-Brasse A., Schmidt J., Swearingen E., Walker N., Wang Z., Watson J.E., Wickramasinghe D., Wong M., Xu G., Wesche H. Sphingosine kinase activity is not required for tumor cell viability. PLoS One 2013, 8:e68328.
27. Schnute M.E., McReynolds M.D., Kasten T., Yates M., Jerome G., Rains J.W., Hall T., Chrencik J., Kraus M., Cronin C.N., Saabye M., Highkin M.K., Broadus R., Ogawa S., Cukyne K., Zawadzke L.E., Peterkin V., Iyanar K., Scholten J.A., Wendling J., Fujiwara H., Nemirovskiy O., Wittwer A.J., Nagiec M.M. Modulation of cellular S1P levels with a novel, potent and specific inhibitor of sphingosine kinase-1. Biochem. J. 2012, 444:79-88.
28. Kharel Y., Mathews T.P., Gellett A.M., Tomsig J.L., Kennedy P.C., Moyer M.L., Macdonald T.L., Lynch K.R. Sphingosine kinase type 1 inhibition reveals rapid turnover of circulating sphingosine 1-phosphate. Biochem. J. 2011, 440:345-353.
29. Loveridge C., Tonelli F., Leclercq T., Lim K.G., Long J.S., Berdyshev E., Tate R.J., Natarajan V., Pitson S.M., Pyne N.J., Pyne S. The sphingosine kinase 1 inhibitor 2-(p-hydroxyanilino)-4-(p-chlorophenyl)thiazole induces proteasomal degradation of sphingosine kinase 1 in mammalian cells. J. Biol. Chem. 2010, 285:38841-38852.
30. Wang Z., Min X., Xiao S.H., Johnstone S., Romanow W., Meininger D., Xu H., Liu J., Dai J., An S., Thibault S., Walker N. Molecular basis of sphingosine kinase 1 substrate recognition and catalysis. Structure 2013, 21:798-809.
31. Lima S., Milstien S., Spiegel S. A real-time high-throughput fluorescence assay for sphingosine kinases. J. Lipid Res. 2014, 55:1525-1530.
32. Mandala S., Hajdu R., Bergstrom J., Quackenbush E., Xie J., Milligan J., Thornton R., Shei G.J., Card D., Keohane C., Rosenbach M., Hale J., Lynch C.L., Rupprecht K., Parsons W., Rosen H. Alteration of lymphocyte trafficking by sphingosine-1-phosphate receptor agonists. Science 2002, 296:346-349.
33. French K.J., Zhuang Y., Maines L.W., Gao P., Wang W., Beljanski V., Upson J.J., Green C.L., Keller S.N., Smith C.D. Pharmacology and antitumor activity of ABC294640, a selective inhibitor of sphingosine kinase-2. J. Pharmacol. Exp. Ther. 2010, 333:129-139.
34. Venkata J.K., An N., Stuart R., Costa L.J., Cai H., Coker W., Song J.H., Gibbs K., Matson T., Garrett-Mayer E., Wan Z., Ogretmen B., Smith C., Kang Y. Inhibition of sphingosine kinase 2 downregulates the expression of c-Myc and Mcl-1 and induces apoptosis in multiple myeloma. Blood 2014, 124:1915-1925.
35. Antoon J.W., White M.D., Meacham W.D., Slaughter E.M., Muir S.E., Elliott S., Rhodes L.V., Ashe H.B., Wiese T.E., Smith C.D., Burow M.E., Beckman B.S. Antiestrogenic effects of the novel sphingosine kinase-2 inhibitor ABC294640. Endocrinology 2010, 151:5124-5135.
36. Kharel Y., Raje M., Gao M., Gellett A.M., Tomsig J.L., Lynch K.R., Santos W.L. Sphingosine kinase type 2 inhibition elevates circulating sphingosine 1-phosphate. Biochem. J. 2012, 447:149-157.
37. Bektas M., Allende M.L., Lee B.G., Chen W., Amar M.J., Remaley A.T., Saba J.D., Proia R.L. Sphingosine 1-phosphate lyase deficiency disrupts lipid homeostasis in liver. J. Biol. Chem. 2010, 285:10880-10889.
38. Aguilar A., Saba J.D. Truth and consequences of sphingosine-1-phosphate lyase. Adv. Biol. Regul. 2012, 52:17-30.
39. Degagne E., Pandurangan A., Bandhuvula P., Kumar A., Eltanawy A., Zhang M., Yoshinaga Y., Nefedov M., de Jong P.J., Fong L.G., Young S.G., Bittman R., Ahmedi Y., Saba J.D. Sphingosine-1-phosphate lyase downregulation promotes colon carcinogenesis through STAT3-activated microRNAs. J. Clin. Investig. 2014, 124:536853-536884.
40. Ihlefeld K., Claas R.F., Koch A., Pfeilschifter J.M., Meyer Zu Heringdorf D. Evidence for a link between histone deacetylation and Ca(2)+ homoeostasis in sphingosine-1-phosphate lyase-deficient fibroblasts. Biochem. J. 2012, 447:457-464.
41. Ihlefeld K., Vienken H., Claas R.F., Blankenbach K., Rudowski A., Ter Braak M., Koch A., Van Veldhoven P.P., Pfeilschifter J., Meyer Zu Heringdorf D. Upregulation of ABC transporters contributes to chemoresistance of sphingosine 1-phosphate lyase-deficient fibroblasts. J. Lipid Res. 2015, 56:60-69.
42. Senkal C.E., Ponnusamy S., Bielawski J., Hannun Y.A., Ogretmen B. Antiapoptotic roles of ceramide-synthase-6-generated C16-ceramide via selective regulation of the ATF6/CHOP arm of ER-stress-response pathways. FASEB J. 2010, 24:296-308.
43. Milstien S., Spiegel S. Targeting sphingosine-1-phosphate: a novel avenue for cancer therapeutics. Cancer Cell 2006, 9:148-150.
44. Huang K., Huang J., Chen C., Hao J., Wang S., Liu P., Huang H. AP-1 regulates sphingosine kinase 1 expression in a positive feedback manner in glomerular mesangial cells exposed to high glucose. Cell Signal. 2014, 26:629-638.
45. ter Braak M., Danneberg K., Lichte K., Liphardt K., Ktistakis N.T., Pitson S.M., Hla T., Jakobs K.H., Meyer zu Heringdorf D. Galpha(q)-mediated plasma membrane translocation of sphingosine kinase-1 and cross-activation of S1P receptors. Biochim. Biophys. Acta 2009, 1791:357-370.
46. Vander Heiden M.G., Cantley L.C., Thompson C.B. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 2009, 324:1029-1033.