DOI QR코드

DOI QR Code

Sphingosine 1-phosphate induces vesicular endothelial growth factor expression in endothelial cells

  • Heo, Kyun (Functional Genomics Branch, Division of Convergence Technology, National Cancer Center) ;
  • Park, Kyung-A (Division of Molecular and Life Science, Pohang University of Science and Technology) ;
  • Kim, Yun-Hee (Molecular Imaging & Therapy Branch, Division of Convergence Technology, National Cancer Center) ;
  • Kim, Sun-Hee (Division of Molecular and Life Science, Pohang University of Science and Technology) ;
  • Oh, Yong-Seok (Division of Molecular and Life Science, Pohang University of Science and Technology) ;
  • Kim, In-Hoo (Molecular Imaging & Therapy Branch, Division of Convergence Technology, National Cancer Center) ;
  • Ryu, Sung-Ho (Division of Molecular and Life Science, Pohang University of Science and Technology) ;
  • Suh, Pann-Ghill (Division of Molecular and Life Science, Pohang University of Science and Technology)
  • Published : 2009.10.31

Abstract

Angiogenesis is essential for tumor growth and vascular endothelial cell growth factor (VEGF) plays a key role in this process. Conversely, sphingosine 1-phosphate (S1P) is a biologically active sphingolipid known to play a key role in cancer progression by regulating endothelial cell proliferation and migration. In this study, the authors found that S1P increases the level of VEGF mRNA in human umbilical vein endothelial cells (HUVECs) and immortalized HUVECs (iHUVECs). Additionally, S1P was found to increase VEGF promoter activity in MS-1 mouse pancreatic islet endothelial cells. Furthermore, a pharmacological inhibitory study revealed that $G_{\alpha i/o}$-mediated phospholipase C, Akt, Erk, and p38 MAPK signaling are involved in this S1P-induced expression of VEGF. A component of AP1 transcription factor is important for S1P-induced VEGF expression. Taken together, these findings suggest that S1P enhances endothelial cell proliferation and migrat ion by upregulating the expression of VEGF mRNA.

Keywords

References

  1. Spiegel, S. and Milstien, S. (2003) Sphingosine-1-phosphate: an enigmatic signalling lipid. Nat. Rev. Mol. Cell. Biol. 4, 397-407 https://doi.org/10.1038/nrm1103
  2. Yatomi, Y., Ohmori, T., Rile, G., Kazama, F., Okamoto, H., Sano, T., Satoh, K., Kume, S., Tigyi, G., Igarashi, Y. and Ozaki, Y.Y. (2001) Sphingosine 1-phosphate: synthesis and release. Prostaglandins Other Lipid Mediat. 64, 107-122 https://doi.org/10.1016/S0090-6980(01)00103-4
  3. Ito, K., Anada, Y., Tani, M., Ikeda, M., Sano, T., Kihara, A. and Igarashi, Y. (2007) Lack of sphingosine 1-phosphatedegrading enzymes in erythrocytes. Biochem. Biophys. Res. Commun. 357, 212-217 https://doi.org/10.1016/j.bbrc.2007.03.123
  4. Hanel, P., Andreani, P. and Graler, M. H. (2007) Erythrocytes store and release sphingosine 1-phosphate in blood. c 21, 1202-1209 https://doi.org/10.1096/fj.06-7433com
  5. Lee, M. J., Thangada, S., Claffey, K. P., Ancellin, N., Liu, C. H., Kluk, M., Volpi, M., Sha’afi, R. I. and Hla, T. (1999) Vascular endothelial cell Adherens Junction assembly and morphogenesis induced by sphingosine-1phosphate. Cell 99, 301-312 https://doi.org/10.1016/S0092-8674(00)81661-X
  6. Lee, M. J., Thangada, S., Paik, J. H., Gopal, S. P., Ancellin, N., Chan, S. S., Wu, M., Morales-Ruiz, M., Sessa, W. C., Alessi, D. and Hla, T. (2001) Akt-mediated phosphorylation of G protein-coupled receptor Edg-1 is required for endothelial cell chemotaxis. Mol. Cell 8, 693-704 https://doi.org/10.1016/S1097-2765(01)00324-0
  7. Lee, M. J., VanBrocklyn, J. R., Thangada, S., Liu, C. H., Hand, A. R., Menzeleev, R., Spiegel, S. and Hla, T. (1998) Sphngosine-1-phosphate as a ligand for the protein-coupled receptor EDG-l. Science 279, 1552-1555 https://doi.org/10.1126/science.279.5356.1552
  8. 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 https://doi.org/10.1016/j.ccr.2006.02.023
  9. 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 https://doi.org/10.1172/JCI200422716
  10. Ferrara, N. (2004) Vascular endothelial growth factor: basic science and clinical progress. Endocr. Rev. 25, 581- 611 https://doi.org/10.1210/er.2003-0027
  11. Mukhopadhyay, D., Zeng, H. and Bhattacharya, R. (2004) Complexity in the vascular permeability factor/vascular endothelial growth factor (VPF/VEGF)-receptors signaling. Mol. Cell. Biochem. 264, 51-61 https://doi.org/10.1023/B:MCBI.0000044374.85095.df
  12. Pages, G. and Pouyssegur, J. (2005) Transcriptional regulation of the vascular endothelial growth factor gene--a concert of activating factors. Cardiovasc. Res. 65, 564- 573 https://doi.org/10.1016/j.cardiores.2004.09.032
  13. Levy, N. S., Chung, S., Furneaux, H. and Levy, A. P. (1998) Hypoxic stabilization of vascular endothelial growth factor mRNA by the RNA-binding protein HuR. J. Biol. Chem. 273. 6417-6423 https://doi.org/10.1074/jbc.273.11.6417
  14. Ellis, L. M. and Hicklin, D. J. (2008) VEGF-targeted therapy: mechanisms of anti-tumour activity. Nat. Rev. Cancer 8, 579-591 https://doi.org/10.1038/nrc2403
  15. Shibuya, M. (2006) Differential roles of vascular endothelial growth factor receptor-1 and receptor-2 in angiogenesis. J. Biochem. Mol. Biol. 39, 469-478 https://doi.org/10.5483/BMBRep.2006.39.5.469
  16. Sanchez, T. and Hla, T. (2004) Structural and functional characteristics of S1P receptors. J. Cell. Biochem. 92, 913-922 https://doi.org/10.1002/jcb.20127
  17. Hu, Y. L., Albanese, C., Pestell, R. G. and Jaffe, R. B. (2003) Dual mechanisms for lysophosphatidic acid stimulation of human ovarian carcinoma cells. J. Natl.Cancer Inst. 95, 733-740 https://doi.org/10.1093/jnci/95.10.733
  18. Kim, J. H., Kim, J. H., Song, W. K., Kim, J. H. and Chun, J. S. (2000) Sphingosine 1-phosphate activates Erk-1/-2 by transactivating epidermal growth factor receptor in rat-2 cells. IUBMB Life 50, 119-124 https://doi.org/10.1080/713803698
  19. Daub, H., Wallasch, C., Lankenau, A., Herrlich, A. and Ullrich, A. (1997) Signal characteristics of G protein-transactivated EGF receptor. EMBO J. 16, 7032-7044 https://doi.org/10.1093/emboj/16.23.7032
  20. Dery, M. A. Michaud, M. D. and Richard, D. E. (2005) Hypoxia-inducible factor 1: regulation by hypoxic and non-hypoxic activators. Int. J. Biochem. Cell Biol. 37, 535-540 https://doi.org/10.1016/j.biocel.2004.08.012
  21. Clifford, R. L., Deacon, K. and Knox, A. J. (2008) Novel regulation of vascular endothelial growth factor-A (VEGF-A) by TGFbeta 1: requirement for smads, beta-catenin and GSK3beta. J. Biol. Chem. 283, 35337-35353 https://doi.org/10.1074/jbc.M803342200
  22. Ristimaki, A., Narko, K., Enholm, B., Joukov, V. and Alitalo, K. (1998) Proinflammatory cytokines regulate expression of the lymphatic endothelial mitogen vascular endothelial growth factor-C. J. Biol. Chem. 273, 8413- 8418 https://doi.org/10.1074/jbc.273.14.8413
  23. Lin, C. I., Chen, C. N., Huang, M. T., Lee, S. J., Lin, C. H., Chang, C. C. and Lee, H. (2008) Lysophosphatidic acid up-regulates vascular endothelial growth factor-C and lymphatic marker expressions in human endothelial cells. Cell. Mol. Life Sci. 65, 2740-2751 https://doi.org/10.1007/s00018-008-8314-9
  24. Ancuta, P., Rao, R., Moses, A., Mehle, A., Shaw, S. K., Luscinskas, W. and Gabuzda, D. (2003) J. Exp. Med. 197, 1701-1707 https://doi.org/10.1084/jem.20022156
  25. Lim, S., Choi, J. W., Kim, H. S., Kim, Y. H., Yea, K., Heo, K., Kim, J. H., Kim, S. H., Song, M., Kim, J. I., Ryu, S. H. and Suh, P. G. (2008) A myristoylated pseudosubstrate peptide of PKC-zeta induces degranulation in HMC-1 cells independently of PKC-zeta activity. Life Sci. 82, 733-740 https://doi.org/10.1016/j.lfs.2008.01.005

Cited by

  1. Sphingosine-1-phosphate modulates expression of vascular endothelial growth factor in human articular chondrocytes: a possible new role in arthritis vol.15, pp.4, 2012, https://doi.org/10.1111/j.1756-185X.2012.01756.x
  2. Increased sphingosine-1-phosphate improves muscle regeneration in acutely injured mdx mice vol.3, pp.1, 2013, https://doi.org/10.1186/2044-5040-3-20
  3. Blocking S1P interaction with S1P1 receptor by a novel competitive S1P1-selective antagonist inhibits angiogenesis vol.419, pp.4, 2012, https://doi.org/10.1016/j.bbrc.2012.02.096
  4. Sphingosine-1-phosphate induces human endothelial VEGF and MMP-2 production via transcription factor ZNF580: Novel insights into angiogenesis vol.395, pp.3, 2010, https://doi.org/10.1016/j.bbrc.2010.04.019
  5. Melatonin prevents deregulation of the sphingosine kinase/sphingosine 1-phosphate signaling pathway in a mouse model of diethylnitrosamine-induced hepatocellular carcinoma vol.62, pp.1, 2017, https://doi.org/10.1111/jpi.12369
  6. Extracellular and intracellular sphingosine-1-phosphate in cancer vol.30, pp.3-4, 2011, https://doi.org/10.1007/s10555-011-9305-0
  7. Sphingosine 1-phosphate: A Potential Molecular Target for Ovarian Cancer Therapy? vol.32, pp.3, 2014, https://doi.org/10.3109/07357907.2013.876646
  8. Regulation of lysophosphatidate signaling by autotaxin and lipid phosphate phosphatases with respect to tumor progression, angiogenesis, metastasis and chemo-resistance vol.93, pp.1, 2011, https://doi.org/10.1016/j.biochi.2010.08.002
  9. Polydatin attenuates AGEs-induced upregulation of fibronectin and ICAM-1 in rat glomerular mesangial cells and db/db diabetic mice kidneys by inhibiting the activation of the SphK1-S1P signaling pathway vol.427, 2016, https://doi.org/10.1016/j.mce.2016.03.003
  10. Roles of Sphingosine-1-Phosphate in Reproduction vol.21, pp.5, 2014, https://doi.org/10.1177/1933719113512534
  11. Lipid phosphate phosphatases and their roles in mammalian physiology and pathology vol.56, pp.11, 2015, https://doi.org/10.1194/jlr.R058362
  12. Identification and characterization of a mirror-image oligonucleotide that binds and neutralizes sphingosine 1-phosphate, a central mediator of angiogenesis vol.462, pp.1, 2014, https://doi.org/10.1042/BJ20131422
  13. ApoA-I induces S1P release from endothelial cells through ABCA1 and SR-BI in a positive feedback manner vol.72, pp.4, 2016, https://doi.org/10.1007/s13105-016-0504-6
  14. Combination of RAD001 (everolimus) and docetaxel reduces prostate and breast cancer cell VEGF production and tumour vascularisation independently of sphingosine-kinase-1 vol.7, pp.1, 2017, https://doi.org/10.1038/s41598-017-03728-3
  15. Concise Review: Pancreatic Cancer and Bone Marrow-Derived Stem Cells vol.5, pp.7, 2016, https://doi.org/10.5966/sctm.2015-0291
  16. α-Tocopheryl phosphate-An activated form of vitamin E important for angiogenesis and vasculogenesis? vol.38, pp.1, 2012, https://doi.org/10.1002/biof.198
  17. Examining the Role of Sphingosine Kinase-2 in the Regulation of Endothelial Cell Barrier Integrity vol.23, pp.3, 2016, https://doi.org/10.1111/micc.12271
  18. Acid ceramidase, an emerging target for anti-cancer and anti-angiogenesis pp.1976-3786, 2019, https://doi.org/10.1007/s12272-019-01114-3