A metabolic shift favoring sphingosine 1-phosphate at the expense of ceramide controls glioblastoma angiogenesis

Journal of Biological Chemistry

Volumn 288, Issue 52, 2013, Pages 37355-37364

  Abuhusain, Hazem J ^a   Matin, Azadeh ^b   Qiao, Qiao ^b   Shen, Han ^a   Kain, Nupur ^b   Day, Bryan W ^c   Stringer, Brett W ^c   Daniels, Benjamin ^b   Laaksonen, Maarit A ^b   Teo, Charlie ^d   McDonald, Kerrie L ^b   Don, Anthony S ^a,b  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

^b UNIVERSITY OF NEW SOUTH WALES   (Australia)

^c QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

^d PRINCE OF WALES PRIVATE HOSPITAL   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ENDOTHELIAL CELLS; METABOLITES; SPHINGOSINES;

ANGIOGENESIS; ANGIOGENIC FACTOR; ANTIANGIOGENIC; GLIOBLASTOMA CELLS; GLIOBLASTOMAS; METABOLIC SHIFT; SPHINGOLIPIDS; SPHINGOSINE 1 PHOSPHATES;

ALKANOLAMINES;

CERAMIDE; PHOSPHATASE; PHOSPHOTRANSFERASE INHIBITOR; SPHINGOLIPID; SPHINGOSINE 1 PHOSPHATE; SPHINGOSINE KINASE 1; SPHINGOSINE KINASE 1 INHIBITOR; SPHINGOSINE PHOSPHATE PHOSPHATASE 2; UNCLASSIFIED DRUG; VASCULOTROPIN;

ANTIANGIOGENIC ACTIVITY; ARTICLE; CANCER CONTROL; CANCER GRADING; CELL PROLIFERATION; CELL VIABILITY; CONTROLLED STUDY; ENZYME ACTIVITY; GLIOBLASTOMA; GRAY MATTER; HUMAN; HUMAN CELL; HUMAN TISSUE; LIPID METABOLISM; PRIORITY JOURNAL; PROTEIN CONTENT; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN SECRETION; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION; TUMOR CELL CULTURE;

EID: 84891416141     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.494740     Document Type: Article

References (54)

1. Wen, P. Y., and Kesari, S. (2008) Malignant gliomas in adults. N. Engl. J. Med. 359, 492-507
2. Stupp, R., Hegi, M. E., Mason, W. P., van den Bent, M. J., Taphoorn, M. J., Janzer, R. C., Ludwin, S. K., Allgeier, A., Fisher, B., Belanger, K., Hau, P., Brandes, A. A., Gijtenbeek, J., Marosi, C., Vecht, C. J., Mokhtari, K., Wesseling, P., Villa, S., Eisenhauer, E., Gorlia, T., Weller, M., Lacombe, D., Cairncross, J. G., Mirimanoff, R. O., European Organisation for Research and Treatment of Cancer Brain Tumour and Radiation Oncology Groups, and National Cancer Institute of Canada Clinical Trials Group (2009) Effects of radiotherapy with concomitant and adjuvant temozolomide versus radiotherapy alone on survival in glioblastoma in a randomised phase III study: 5-year analysis of the EORTC-NCIC trial. Lancet Oncol. 10, 459-466
3. Bai, R. Y., Staedtke, V., and Riggins, G. J. (2011) Molecular targeting of glioblastoma. Drug discovery and therapies. Trends Mol. Med. 17, 301-312
4. Lai, A., Tran, A., Nghiemphu, P. L., Pope, W. B., Solis, O. E., Selch, M., Filka, E., Yong, W. H., Mischel, P. S., Liau, L. M., Phuphanich, S., Black, K., Peak, S., Green, R. M., Spier, C. E., Kolevska, T., Polikoff, J., Fehrenbacher, L., Elashoff, R., and Cloughesy, T. (2011) Phase II study of bevacizumab plus temozolomide during and after radiation therapy for patients with newly diagnosed glioblastoma multiforme. J. Clin. Oncol. 29, 142-148
5. Friedman, H. S., Prados, M. D., Wen, P. Y., Mikkelsen, T., Schiff, D., Abrey, L. E., Yung, W. K., Paleologos, N., Nicholas, M. K., Jensen, R., Vredenburgh, J., Huang, J., Zheng, M., and Cloughesy, T. (2009) Bevacizumab alone and in combination with irinotecan in recurrent glioblastoma. J. Clin. Oncol. 27, 4733-4740
6. Hannun, Y. A., and Obeid, L. M. (2008) Principles of bioactive lipid signalling. Lessons from sphingolipids. Nat. Rev. Mol. Cell Biol. 9, 139-150
7. Sentelle, R. D., Senkal, C. E., Jiang, W., Ponnusamy, S., Gencer, S., Selvam, S. P., Ramshesh, V. K., Peterson, Y. K., Lemasters, J. J., Szulc, Z. M., Bielawski, J., and Ogretmen, B. (2012) Ceramide targets autophagosomes to mitochondria and induces lethal mitophagy. Nat. Chem. Biol. 8, 831-838
8. Bieberich, E. (2008) Ceramide signaling in cancer and stem cells. Future Lipidol. 3, 273-300
9. Chalfant, C. E., Szulc, Z., Roddy, P., Bielawska, A., and Hannun, Y. A. (2004) The structural requirements for ceramide activation of serinethreonine protein phosphatases. J. Lipid Res. 45, 496-506
10. Zhang, Y., Yao, B., Delikat, S., Bayoumy, S., Lin, X. H., Basu, S., McGinley, M., Chan-Hui, P. Y., Lichenstein, H., and Kolesnick, R. (1997) Kinase suppressor of Ras is ceramide-activated protein kinase. Cell 89, 63-72
11. Maceyka, M., Harikumar, K. B., Milstien, S., and Spiegel, S. (2012) Sphingosine- 1-phosphate signaling and its role in disease. Trends Cell Biol. 22, 50-60
12. Rosen, H., Gonzalez-Cabrera, P. J., Sanna, M. G., and Brown, S. (2009) Sphingosine 1-phosphate receptor signaling. Annu. Rev. Biochem. 78, 743-768
13. Young, N., and Van Brocklyn, J. R. (2007) Roles of sphingosine-1- phosphate (S1P) receptors in malignant behavior of glioma cells. Differential effects of S1P2 on cell migration and invasiveness. Exp. Cell Res. 313, 1615-1627
14. Young, N., Pearl, D. K., and Van Brocklyn, J. R. (2009) Sphingosine-1- phosphate regulates glioblastoma cell invasiveness through the urokinase plasminogen activator system and CCN1/Cyr61. Mol. Cancer Res. 7, 23-32
15. Xia, P., Gamble, J. R., Wang, L., Pitson, S. M., Moretti, P. A., Wattenberg, B. W., D'Andrea, R. J., and Vadas, M. A. (2000) An oncogenic role of sphingosine kinase. Curr. Biol. 10, 1527-1530
16. Pitson, S. M., Xia, P., Leclercq, T. M., Moretti, P. A., Zebol, J. R., Lynn, H. E., Wattenberg, B. W., and Vadas, M. A. (2005) Phosphorylation- dependent translocation of sphingosine kinase to the plasma membrane drives its oncogenic signalling. J. Exp. Med. 201, 49-54
17. Kawamori, T., Kaneshiro, T., Okumura, M., Maalouf, S., Uflacker, A., Bielawski, J., Hannun, Y. A., and Obeid, L. M. (2009) Role for sphingosine kinase 1 in colon carcinogenesis. FASEB J. 23, 405-414
18. Kohno, M., Momoi, M., Oo, M. L., Paik, J. H., Lee, Y. M., Venkataraman, K., Ai, Y., Ristimaki, A. P., Fyrst, H., Sano, H., Rosenberg, D., Saba, J. D., Proia, R. L., and Hla, T. (2006) Intracellular role for sphingosine kinase 1 in intestinal adenoma cell proliferation. Mol. Cell Biol. 26, 7211-7223
19. French, K. J., Schrecengost, R. S., Lee, B. D., Zhuang, Y., Smith, S. N., Eberly, J. L., Yun, J. K., and Smith, C. D. (2003) Discovery and evaluation of inhibitors of human sphingosine kinase. Cancer Res. 63, 5962-5969
20. Ruckhäberle, E., Rody, A., Engels, K., Gaetje, R., von Minckwitz, G., Schiffmann, S., Grösch, S., Geisslinger, G., Holtrich, U., Karn, T., and Kaufmann, M. (2008) Microarray analysis of altered sphingolipid metabolism reveals prognostic significance of sphingosine kinase 1 in breast cancer. Breast Cancer Res. Treat. 112, 41-52
21. Johnson, K. R., Johnson, K. Y., Crellin, H. G., Ogretmen, B., Boylan, A. M., Harley, R. A., and Obeid, L. M. (2005) Immunohistochemical distribution of sphingosine kinase 1 in normal and tumor lung tissue. J. Histochem. Cytochem. 53, 1159-1166
22. Song, L., Xiong, H., Li, J., Liao, W., Wang, L., Wu, J., and Li, M. (2011) Sphingosine kinase-1 enhances resistance to apoptosis through activation of PI3K/Akt/NF-κB pathway in human non-small cell lung cancer. Clin. Cancer Res. 17, 1839-1849
23. Li, J., Guan, H. Y., Gong, L. Y., Song, L. B., Zhang, N., Wu, J., Yuan, J., Zheng, Y. J., Huang, Z. S., and Li, M. (2008) Clinical significance of sphingosine kinase-1 expression in human astrocytomas progression and overall patient survival. Clin. Cancer Res. 14, 6996-7003
24. Van Brocklyn, J. R., Jackson, C. A., Pearl, D. K., Kotur, M. S., Snyder, P. J., and Prior, T. W. (2005) Sphingosine kinase-1 expression correlates with poor survival of patients with glioblastoma multiforme. Roles of sphingosine kinase isoforms in growth of glioblastoma cell lines. J. Neuropathol. Exp. Neurol. 64, 695-705
25. Wong, J. W., Abuhusain, H. J., McDonald, K. L., and Don, A. S. (2012) MMSAT. Automated quantification of metabolites in selected reaction monitoring experiments. Anal. Chem. 84, 470-474
26. Hejazi, L., Wong, J. W., Cheng, D., Proschogo, N., Ebrahimi, D., Garner, B., and Don, A. S. (2011) Mass and relative elution time profiling. Two-dimensional analysis of sphingolipids in Alzheimer's disease brains. Biochem. J. 438, 165-175
27. Bielawski, J., Szulc, Z. M., Hannun, Y. A., and Bielawska, A. (2006) Simultaneous quantitative analysis of bioactive sphingolipids by high-performance liquid chromatography-tandem mass spectrometry. Methods 39, 82-91
28. Day, B. W., Stringer, B. W., Al-Ejeh, F., Ting, M. J., Wilson, J., Ensbey, K. S., Jamieson, P. R., Bruce, Z. C., Lim, Y. C., Offenhäuser, C., Charmsaz, S., Cooper, L. T., Ellacott, J. K., Harding, A., Leveque, L., Inglis, P., Allan, S., Walker, D. G., Lackmann, M., Osborne, G., Khanna, K. K., Reynolds, B. A., Lickliter, J. D., and Boyd, A. W. (2013) EphA3 maintains tumorigenicity and is a therapeutic target in glioblastoma multiforme. Cancer Cell 23, 238-248
29. Jary, E., Bee, T., Walker, S. R., Chung, S. K., Seo, K. C., Morris, J. C., and Don, A. S. (2010) Elimination of a hydroxyl group in FTY720 dramatically improves the phosphorylation rate. Mol. Pharmacol. 78, 685-692
30. Ades, E. W., Candal, F. J., Swerlick, R. A., George, V. G., Summers, S., Bosse, D. C., and Lawley, T. J. (1992) HMEC-1. Establishment of an immortalized human microvascular endothelial cell line. J. Invest. Dermatol. 99, 683-690
31. Chen, Z., Htay, A., Dos Santos, W., Gillies, G. T., Fillmore, H. L., Sholley, M. M., and Broaddus, W. C. (2009) In vitro angiogenesis by human umbilical vein endothelial cells (HUVEC) induced by three-dimensional coculture with glioblastoma cells. J. Neurooncol. 92, 121-128
32. Ogawa, C., Kihara, A., Gokoh, M., and Igarashi, Y. (2003) Identification and characterization of a novel human sphingosine-1-phosphate phosphohydrolase, hSPP2. J. Biol. Chem. 278, 1268-1272
33. Mizutani, Y., Kihara, A., and Igarashi, Y. (2005) Mammalian Lass6 and its related family members regulate synthesis of specific ceramides. Biochem. J. 390, 263-271
34. Ginkel, C., Hartmann, D., vom Dorp, K., Zlomuzica, A., Farwanah, H., Eckhardt, M., Sandhoff, R., Degen, J., Rabionet, M., Dere, E., Dörmann, P., Sandhoff, K., and Willecke, K. (2012) Ablation of neuronal ceramide synthase 1 in mice decreases ganglioside levels and expression of myelinassociated glycoprotein in oligodendrocytes. J. Biol. Chem. 287, 41888-41902
35. Laviad, E. L., Albee, L., Pankova-Kholmyansky, I., Epstein, S., Park, H., Merrill, A. H., Jr., and Futerman, A. H. (2008) Characterization of ceramide synthase 2. Tissue distribution, substrate specificity, and inhibition by sphingosine 1-phosphate. J. Biol. Chem. 283, 5677-5684
36. Kharel, Y., Mathews, T. P., Gellett, A. M., Tomsig, J. L., Kennedy, P. C., Moyer, M. L., Macdonald, T. L., and Lynch, K. R. (2011) Sphingosine kinase type 1 inhibition reveals rapid turnover of circulating sphingosine 1-phosphate. Biochem. J. 440, 345-353
37. 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., and Nagiec, M. M. (2012) Modulation of cellular S1P levels with a novel, potent and specific inhibitor of sphingosine kinase-1. Biochem. J. 444, 79-88
38. 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., and Wesche, H. (2013) Sphingosine kinase activity is not required for tumor cell viability. PLoS ONE 8, e68328
39. Lee, J., Kotliarova, S., Kotliarov, Y., Li, A., Su, Q., Donin, N. M., Pastorino, S., Purow, B. W., Christopher, N., Zhang, W., Park, J. K., and Fine, H. A. (2006) Tumor stem cells derived from glioblastomas cultured in bFGF and EGF more closely mirror the phenotype and genotype of primary tumors than do serum-cultured cell lines. Cancer Cell 9, 391-403
40. Lavieu, G., Scarlatti, F., Sala, G., Carpentier, S., Levade, T., Ghidoni, R., Botti, J., and Codogno, P. (2006) Regulation of autophagy by sphingosine kinase 1 and its role in cell survival during nutrient starvation. J. Biol. Chem. 281, 8518-8527
41. Nagahashi, M., Ramachandran, S., Kim, E. Y., Allegood, J. C., Rashid, O. M., Yamada, A., Zhao, R., Milstien, S., Zhou, H., Spiegel, S., and Takabe, K. (2012) Sphingosine-1-phosphate produced by sphingosine kinase 1 promotes breast cancer progression by stimulating angiogenesis and lymphangiogenesis. Cancer Res. 72, 726-735
42. Visentin, B., Vekich, J. A., Sibbald, B. J., Cavalli, A. L., Moreno, K. M., Matteo, R. G., Garland, W. A., Lu, Y., Yu, S., Hall, H. S., Kundra, V., Mills, G. B., and Sabbadini, R. A. (2006) Validation of an anti-sphingosine-1- phosphate antibody as a potential therapeutic in reducing growth, invasion, and angiogenesis in multiple tumor lineages. Cancer Cell 9, 225-238
43. Chae, S. S., Paik, J. H., Furneaux, H., and Hla, T. (2004) Requirement for sphingosine 1-phosphate receptor-1 in tumor angiogenesis demonstrated by in vivo RNA interference. J. Clin. Invest. 114, 1082-1089
44. Nakatsu, M. N., and Hughes, C. C. (2008) An optimized three-dimensional in vitro model for the analysis of angiogenesis. Methods Enzymol. 443, 65-82
45. Cuvillier, O., Pirianov, G., Kleuser, B., Vanek, P. G., Coso, O. A., Gutkind, S., and Spiegel, S. (1996) Suppression of ceramide-mediated programmed cell death by sphingosine-1-phosphate. Nature 381, 800-803
46. Sutphen, R., Xu, Y., Wilbanks, G. D., Fiorica, J., Grendys, E. C., Jr., LaPolla, J. P., Arango, H., Hoffman, M. S., Martino, M., Wakeley, K., Griffin, D., Blanco, R. W., Cantor, A. B., Xiao, Y. J., and Krischer, J. P. (2004) Lysophospholipids are potential biomarkers of ovarian cancer. Cancer Epidemiol. Biomark. Prev. 13, 1185-1191
47. Le Stunff, H., Giussani, P., Maceyka, M., Lépine, S., Milstien, S., and Spiegel, S. (2007) Recycling of sphingosine is regulated by the concerted actions of sphingosine-1-phosphate phosphohydrolase 1 and sphingosine kinase 2. J. Biol. Chem. 282, 34372-34380
48. Riboni, L., Campanella, R., Bassi, R., Villani, R., Gaini, S. M., Martinelli-Boneschi, F., Viani, P., and Tettamanti, G. (2002) Ceramide levels are inversely associated with malignant progression of human glial tumors. Glia 39, 105-113
49. Karahatay, S., Thomas, K., Koybasi, S., Senkal, C. E., Elojeimy, S., Liu, X., Bielawski, J., Day, T. A., Gillespie, M. B., Sinha, D., Norris, J. S., Hannun, Y. A., and Ogretmen, B. (2007) Clinical relevance of ceramide metabolism in the pathogenesis of human head and neck squamous cell carcinoma (HNSCC). Attenuation of C(18)-ceramide in HNSCC tumors correlates with lymphovascular invasion and nodal metastasis. Cancer Lett. 256, 101-111
50. Senkal, C. E., Ponnusamy, S., Bielawski, J., Hannun, Y. A., and Ogretmen, B. (2010) Antiapoptotic roles of ceramide-synthase-6-generated C16-ceramide via selective regulation of the ATF6/CHOP arm of ER-stress-response pathways. FASEB J. 24, 296-308
51. Kapitonov, D., Allegood, J. C., Mitchell, C., Hait, N. C., Almenara, J. A., Adams, J. K., Zipkin, R. E., Dent, P., Kordula, T., Milstien, S., and Spiegel, S. (2009) Targeting sphingosine kinase 1 inhibits Akt signaling, induces apoptosis, and suppresses growth of human glioblastoma cells and xenografts. Cancer Res. 69, 6915-6923
52. Endo, K., Igarashi, Y., Nisar, M., Zhou, Q. H., and Hakomori, S. (1991) Cell membrane signaling as target in cancer therapy. Inhibitory effect of N, Ndimethyl and N, N, N-trimethyl sphingosine derivatives on in vitro and in vivo growth of human tumor cells in nude mice. Cancer Res. 51, 1613-1618
53. Pchejetski, D., Golzio, M., Bonhoure, E., Calvet, C., Doumerc, N., Garcia, V., Mazerolles, C., Rischmann, P., Teissié, J., Malavaud, B., and Cuvillier, O. (2005) Sphingosine kinase-1 as a chemotherapy sensor in prostate adenocarcinoma cell and mouse models. Cancer Res. 65, 11667-11675
54. Anelli, V., Gault, C. R., Snider, A. J., and Obeid, L. M. (2010) Role of sphingosine kinase-1 in paracrine/transcellular angiogenesis and lymphangiogenesis in vitro. FASEB J. 24, 2727-2738