About this Journal Submit a Manuscript Table of Contents
Journal of Oncology
Volume 2010 (2010), Article ID 509329, 10 pages
http://dx.doi.org/10.1155/2010/509329
Research Article

An Active Form of Sphingosine Kinase-1 Is Released in the Extracellular Medium as Component of Membrane Vesicles Shed by Two Human Tumor Cell Lines

1Dipartimento di Biologia Cellulare e dello Sviluppo, Università di Palermo, Viale delle, Scienze ed. 16, 90128 Palermo, Italy
2Dipartimento di Scienze Biochimiche, Università di Firenze, Viale G.B. Morgagni n. 50, 50134 Florence, Italy
3Dipartimento Biopatologia e Metodologie Biomediche, Università di Palermo, Via Divisi 83, 90133 Palermo, Italy
4IAMC-CNR, U.O. Capo Granitola, Mazara del Vallo, 91026 Trapani, Italy

Received 16 November 2009; Accepted 8 March 2010

Academic Editor: Kalpna Gupta

Copyright © 2010 Salvatrice Rigogliuso et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. C. F. Singer, D. Gschwantler-Kaulich, A. Fink-Retter, et al., “Differential gene expression profile in breast cancer-derived stromal fibroblasts,” Breast Cancer Research and Treatment, vol. 110, no. 2, pp. 273–281, 2008. View at Publisher · View at Google Scholar · View at Scopus
  2. G. Poste and G. L. Nicolson, “Arrest and metastasis of blood-borne tumor cells are modified by fusion of plasma membrane vesicles from highly metastatic cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 77, no. 1, pp. 399–403, 1980. View at Scopus
  3. D. D. Taylor, C. G. Taylor, C. G. Jiang, and P. H. Black, “Characterization of plasma membrane shedding from murine melanoma cells,” International Journal of Cancer, vol. 41, no. 4, pp. 629–635, 1988. View at Scopus
  4. A. Ginestra, M. D. La Placa, F. Saladino, D. Cassara, H. Nagase, and M. L. Vittorelli, “The amount and proteolytic content of vesicles shed by human cancer cell lines correlates with their in vitro invasiveness,” Anticancer Research, vol. 18, no. 5, pp. 3433–3437, 1998. View at Scopus
  5. S. Zucker, J. M. Wieman, R. M. Lysik, D. P. Wilkie, N. Ramamurthy, and B. Lane, “Metastatic mouse melanoma cells release collagen-gelatin degrading metalloproteinases as components of shed membrane vesicles,” Biochimica et Biophysica Acta, vol. 924, no. 1, pp. 225–237, 1987. View at Scopus
  6. A. Ginestra, S. Monea, G. Seghezzi, et al., “Urokinase plasminogen activator and gelatinases are associated with membrane vesicles shed by human HT1080 fibrosarcoma cells,” Journal of Biological Chemistry, vol. 272, no. 27, pp. 17216–17222, 1997. View at Publisher · View at Google Scholar · View at Scopus
  7. V. Dolo, A. Ginestra, D. Cassara, et al., “Selective localization of matrix metalloproteinase 9, β1 integrins, and human lymphocyte antigen class I molecules on membrane vesicles shed by 8701-BC breast carcinoma cells,” Cancer Research, vol. 58, no. 19, pp. 4468–4474, 1998. View at Scopus
  8. G. Taraboletti, S. D'Ascenzo, P. Borsotti, R. Giavazzi, A. Pavan, and V. Dolo, “Shedding of the matrix metalloproteinases MMP-2, MMP-9, and MT1-MMP as membrane vesicle-associated components by endothelial cells,” American Journal of Pathology, vol. 160, no. 2, pp. 673–680, 2002. View at Scopus
  9. L. E. Graves, E. V. Ariztia, J. R. Navari, H. J. Matzel, M. S. Stack, and D. A. Fishman, “Proinvasive properties of ovarian cancer ascites-derived membrane vesicles,” Cancer Research, vol. 64, no. 19, pp. 7045–7049, 2004. View at Publisher · View at Google Scholar · View at Scopus
  10. V. Dolo, R. Li, M. Dillinger, et al., “Enrichment and localization of ganglioside GD3 and caveolin-1 in shed tumor cell membrane vesicles,” Biochimica et Biophysica Acta, vol. 1486, no. 2-3, pp. 265–274, 2000. View at Publisher · View at Google Scholar · View at Scopus
  11. P. Alexander, “Escape from immune destruction by the host through shedding of surface antigens: is this a characteristic shared by malignant and embryonic cells?” Cancer Research, vol. 34, no. 8, pp. 2077–2082, 1974. View at Scopus
  12. D. D. Poutsiaka, E. W. Schroder, D. D. Taylor, E. M. Levy, and P. H. Black, “Membrane vesicles shed by murine melanoma cells selectively inhibit the expression of Ia antigen by macrophages,” Journal of Immunology, vol. 134, no. 1, pp. 138–144, 1985. View at Scopus
  13. V. Dolo, E. Adobati, S. Canevari, M. A. Picone, and M. L. Vittorelli, “Membrane vesicles shed into the extracellular medium by human breast carcinoma cells carry tumor-associated surface antigens,” Clinical and Experimental Metastasis, vol. 13, no. 4, pp. 277–286, 1995. View at Publisher · View at Google Scholar · View at Scopus
  14. E. Zuccato, E. J. Blott, O. Holt, et al., “Sorting of Fas ligand to secretory lysosomes is regulated by mono-ubiquitylation and phosphorylation,” Journal of Cell Science, vol. 120, no. 1, pp. 191–199, 2007. View at Publisher · View at Google Scholar · View at Scopus
  15. A. Clayton, J. P. Mitchell, J. Court, M. D. Mason, and Z. Tabi, “Human tumor-derived exosomes selectively impair lymphocyte responses to interleukin-2,” Cancer Research, vol. 67, no. 15, pp. 7458–7466, 2007. View at Publisher · View at Google Scholar · View at Scopus
  16. D. I. Gabrilovich, “Molecular mechanisms and therapeutic reversal of immune suppression in cancer,” Current Cancer Drug Targets, vol. 7, no. 1, p. 1, 2007. View at Scopus
  17. S. Taverna, G. Ghersi, A. Ginestra, et al., “Shedding of membrane vesicles mediates fibroblast growth factor-2 release from cells,” Journal of Biological Chemistry, vol. 278, no. 51, pp. 51911–51919, 2003. View at Publisher · View at Google Scholar · View at Scopus
  18. S. Taverna, S. Rigogliuso, M. Salamone, and M. L. Vittorelli, “Intracellular trafficking of endogenous fibroblast growth factor-2,” FEBS Journal, vol. 275, no. 7, pp. 1579–1592, 2008. View at Publisher · View at Google Scholar · View at Scopus
  19. G. Taraboletti, S. D'Ascenzo, I. Giusti, et al., “Bioavailability of VEGF in tumor-shed vesicles depends on vesicle burst induced by acidic pH,” Neoplasia, vol. 8, no. 2, pp. 96–103, 2006. View at Publisher · View at Google Scholar · View at Scopus
  20. G. Schiera, P. Proia, C. Alberti, M. Mineo, G. Savettieri, and I. Di Liegro, “Neurons produce FGF2 and VEGF and secrete them at least in part by shedding extracellular vesicles,” Journal of Cellular and Molecular Medicine, vol. 11, no. 6, pp. 1384–1394, 2007. View at Publisher · View at Google Scholar · View at Scopus
  21. P. Proia, G. Schiera, M. Mineo, et al., “Astrocytes shed extracellular vesicles that contain fibroblast growth factor-2 and vascular endothelial growth factor,” International Journal of Molecular Medicine, vol. 21, no. 1, pp. 63–67, 2008. View at Scopus
  22. J. Skog, T. Wurdinger, S. van Rijn, et al., “Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers,” Nature Cell Biology, vol. 10, no. 12, pp. 1470–1476, 2008. View at Publisher · View at Google Scholar · View at Scopus
  23. C. W. Kim, H. M. Lee, T. H. Lee, C. Kang, H. K. Kleinman, and Y. S. Gho, “Extracellular membrane vesicles from tumor cells promote angiogenesis via sphingomyelin,” Cancer Research, vol. 62, no. 21, pp. 6312–6317, 2002. View at Scopus
  24. S. Pyne and N. J. Pyne, “Sphingosine 1-phosphate signalling in mammalian cells,” Biochemical Journal, vol. 349, no. 2, pp. 385–402, 2000. View at Publisher · View at Google Scholar · View at Scopus
  25. Y. A. Hannun, “Functions of ceramide in coordinating cellular responses to stress,” Science, vol. 274, no. 5294, pp. 1855–1859, 1996. View at Publisher · View at Google Scholar · View at Scopus
  26. R. N. Kolesnick and M. Kronke, “Regulation of ceramide production and apoptosis,” Annual Review of Physiology, vol. 60, pp. 643–665, 1998. View at Publisher · View at Google Scholar · View at Scopus
  27. M. Ito, N. Okino, M. Tani, S. Mitsutake, and K. Mori, “Molecular evolution of neutral ceramidase: signalling molecule and virulence factor,” Tanpakushitsu Kakusan Koso, vol. 47, pp. 455–462, 2002. View at Scopus
  28. A. Olivera, T. Kohama, Z. Tu, S. Milstien, and S. Spiegel, “Purification and characterization of rat kidney sphingosine kinase,” Journal of Biological Chemistry, vol. 273, no. 20, pp. 12576–12583, 1998. View at Publisher · View at Google Scholar · View at Scopus
  29. T. Kohama, A. Olivera, L. Edsall, M. M. Nagiec, R. Dickson, and S. Spiegel, “Molecular cloning and functional characterization of murine sphingosine kinase,” Journal of Biological Chemistry, vol. 273, no. 37, pp. 23722–23728, 1998. View at Publisher · View at Google Scholar · View at Scopus
  30. H. Liu, M. Sugiura, V. E. Nava, et al., “Molecular cloning and functional characterization of a novel mammalian sphingosine kinase type 2 isoform,” Journal of Biological Chemistry, vol. 275, no. 26, pp. 19513–19520, 2000. View at Publisher · View at Google Scholar · View at Scopus
  31. S. M. Pitson, P. A. B. Moretti, J. R. Zebol, et al., “Activation of sphingosine kinase 1 by ERK1/2-mediated phosphorylation,” EMBO Journal, vol. 22, no. 20, pp. 5491–5500, 2003. View at Publisher · View at Google Scholar · View at Scopus
  32. S. Spiegel and S. Milstien, “Exogenous and intracellularly generated sphingosine 1-phosphate can regulate cellular processes by divergent pathways,” Biochemical Society Transactions, vol. 31, no. 6, pp. 1216–1219, 2003. View at Scopus
  33. S. M. Pitson, P. Xia, T. M. Leclercq, et al., “Phosphorylation-dependent translocation of sphingosine kinase to the plasma membrane drives its oncogenic signalling,” Journal of Experimental Medicine, vol. 201, no. 1, pp. 49–54, 2005. View at Publisher · View at Google Scholar · View at Scopus
  34. N. Ancellin, C. Colmont, J. Su, et al., “Extracellular export of sphingosine kinase-1 enzyme. Sphingosine 1-phosphate generation and the induction of angiogenic vascular maturation,” Journal of Biological Chemistry, vol. 277, no. 8, pp. 6667–6675, 2002. View at Publisher · View at Google Scholar · View at Scopus
  35. M.-J. Lee, S. Thangada, K. P. Claffey, et al., “Vascular endothelial cell adherens junction assembly and morphogenesis induced by sphingosine-1-phosphate,” Cell, vol. 99, no. 3, pp. 301–312, 1999. View at Publisher · View at Google Scholar · View at Scopus
  36. K. Harvey, R. A. Siddiqui, D. Sliva, J. G. N. Garcia, and D. English, “Serum factors involved in human microvascular endothelial cell morphogenesis,” Journal of Laboratory and Clinical Medicine, vol. 140, no. 3, pp. 188–198, 2002. View at Publisher · View at Google Scholar · View at Scopus
  37. S. Minafra, V. Morello, F. Glorioso, et al., “A new cell line (8701-BC) from primary ductal infiltrating carcinoma of human breast,” British Journal of Cancer, vol. 60, no. 2, pp. 185–192, 1989. View at Scopus
  38. V. Dolo, A. Ginestra, G. Ghersi, H. Nagase, and M. L. Vittorelli, “Human breast carcinoma cells cultured in the presence of serum shed membrane vesicles rich in gelatinolytic activities,” Journal of Submicroscopic Cytology and Pathology, vol. 26, no. 2, pp. 173–180, 1994. View at Scopus
  39. S. Mitsutake, M. Tani, N. Okino, et al., “Purification, characterization, molecular cloning, and subcellular distribution of neutral ceramidase of rat kidney,” Journal of Biological Chemistry, vol. 276, no. 28, pp. 26249–26259, 2001. View at Publisher · View at Google Scholar · View at Scopus
  40. K. R. Johnson, K. P. Becker, M. M. Facchinetti, Y. A. Hannun, and L. M. Obeid, “PKC-dependent activation of sphingosine kinase 1 and translocation to the plasma membrane. Extracellular release of sphingosine-1-phosphate induced by phorbol 12-myristate 13-acetate (PMA),” Journal of Biological Chemistry, vol. 277, no. 38, pp. 35257–35262, 2002. View at Publisher · View at Google Scholar · View at Scopus
  41. N. Igarashi, T. Okada, S. Hayashi, T. Fujita, S. Jahangeer, and S.-I. Nakamura, “Sphingosine kinase 2 is a nuclear protein and inhibits DNA synthesis,” Journal of Biological Chemistry, vol. 278, no. 47, pp. 46832–46839, 2003. View at Publisher · View at Google Scholar · View at Scopus
  42. W. L. Monsky, C.-Y. Lin, A. Aoyama, et al., “A potential marker protease of invasiveness, seprase, is localized on invadopodia of human malignant melanoma cells,” Cancer Research, vol. 54, no. 21, pp. 5702–5710, 1994. View at Scopus
  43. A. Olivera, H. M. Rosenfeldt, M. Bektas, et al., “Sphingosine kinase type 1 induces G12/13-mediated stress fiber formation, yet promotes growth and survival independent of G protein-coupled receptors,” Journal of Biological Chemistry, vol. 278, no. 47, pp. 46452–46460, 2003. View at Publisher · View at Google Scholar · View at Scopus
  44. C. Donati, F. Cencetti, C. De Palma, et al., “TGFβ protects mesoangioblasts from apoptosis via sphingosine kinase-1 regulation,” Cellular Signalling, vol. 21, no. 2, pp. 228–236, 2009. View at Publisher · View at Google Scholar · View at Scopus
  45. E. Romiti, E. Meacci, M. Tani, et al., “Neutral/alkaline and acid ceramidase activities are actively released by murine endothelial cells,” Biochemical and Biophysical Research Communications, vol. 275, no. 3, pp. 746–751, 2000. View at Publisher · View at Google Scholar · View at Scopus
  46. Y.-H. Hwang, M. Tani, T. Nakagawa, N. Okino, and M. Ito, “Subcellular localization of human neutral ceramidase expressed in HEK293 cells,” Biochemical and Biophysical Research Communications, vol. 331, no. 1, pp. 37–42, 2005. View at Publisher · View at Google Scholar · View at Scopus
  47. M. Tani, M. Ito, and Y. Igarashi, “Ceramide/sphingosine/sphingosine 1-phosphate metabolism on the cell surface and in the extracellular space,” Cellular Signalling, vol. 19, no. 2, pp. 229–237, 2007. View at Publisher · View at Google Scholar · View at Scopus
  48. M. Tani, N. Okino, K. Mori, T. Tanigawa, H. Izu, and M. Ito, “Molecular cloning of the full-length cDNA encoding mouse neutral ceramidase. A novel but highly conserved gene family of neutral/alkaline ceramidases,” Journal of Biological Chemistry, vol. 275, no. 15, pp. 11229–11234, 2000. View at Publisher · View at Google Scholar · View at Scopus
  49. M. Tani, H. Iida, and M. Ito, “O-glycosylation of mucin-like domain retains the neutral ceramidase on the plasma membranes as a type II integral membrane protein,” Journal of Biological Chemistry, vol. 278, no. 12, pp. 10523–10530, 2003. View at Publisher · View at Google Scholar · View at Scopus
  50. Y. Yoshimura, M. Tani, N. Okino, H. Iida, and M. Ito, “Molecular cloning and functional analysis of zebrafish neutral ceramidase,” Journal of Biological Chemistry, vol. 279, no. 42, pp. 44012–44022, 2004. View at Publisher · View at Google Scholar · View at Scopus
  51. E. Romiti, E. Meacci, C. Donati, et al., “Neutral ceramidase secreted by endothelial cells is released in part associated with caveolin-1,” Archives of Biochemistry and Biophysics, vol. 417, no. 1, pp. 27–33, 2003. View at Publisher · View at Google Scholar · View at Scopus
  52. V. Dolo, S. D'Ascenzo, M. Sorice, et al., “New approaches to the study of sphingolipid enriched membrane domains: the use of electron microscopic autoradiography to reveal metabolically tritium labeled sphingolipids in cell cultures,” Glycoconjugate Journal, vol. 17, no. 3-4, pp. 261–268, 2000. View at Publisher · View at Google Scholar · View at Scopus
  53. I. Prudovsky, A. Mandinova, R. Soldi, et al., “The non-classical export routes: FGF1 and IL-1α point the way,” Journal of Cell Science, vol. 116, no. 24, pp. 4871–4881, 2003. View at Publisher · View at Google Scholar · View at Scopus
  54. R. Soldi, A. Mandinova, K. Venkataraman, et al., “Sphingosine kinase 1 is a critical component of the copper-dependent FGF1 export pathway,” Experimental Cell Research, vol. 313, no. 15, pp. 3308–3318, 2007. View at Publisher · View at Google Scholar · View at Scopus
  55. J. D. Saba and T. Hla, “Point-counterpoint of sphingosine 1-phosphate metabolism,” Circulation Research, vol. 94, no. 6, pp. 724–734, 2004. View at Publisher · View at Google Scholar · View at Scopus
  56. R. Bassi, V. Anelli, P. Giussani, G. Tettamanti, P. Viani, and L. Riboni, “Sphingosine-1-phosphate is released by cerebellar astrocytes in response to bFGF and induces astrocyte proliferation through Gi-protein-coupled receptors,” Glia, vol. 53, no. 6, pp. 621–630, 2006. View at Publisher · View at Google Scholar · View at Scopus
  57. R. V. Stahelin, J. H. Hwang, J.-H. Kim, et al., “The mechanism of membrane targeting of human sphingosine kinase 1,” Journal of Biological Chemistry, vol. 280, no. 52, pp. 43030–43038, 2005. View at Publisher · View at Google Scholar · View at Scopus
  58. H. F. G. Heijnen, A. E. Schiel, R. Fijnheer, H. J. Geuze, and J. J. Sixma, “Activated platelets release two types of membrane vesicles: microvesicles by surface shedding and exosomes derived from exocytosis of multivesicular bodies and α-granules,” Blood, vol. 94, no. 11, pp. 3791–3799, 1999. View at Scopus
  59. A. MacKenzie, H. L. Wilson, E. Kiss-Toth, S. K. Dower, R. A. North, and A. Surprenant, “Rapid secretion of interleukin-1β by microvesicle shedding,” Immunity, vol. 15, no. 5, pp. 825–835, 2001. View at Publisher · View at Google Scholar · View at Scopus
  60. S. Pyne and N. J. Pyne, “Sphingosine 1 phosphate signaling via the endothelial differentation gene family of G protein coupled receptors,” Pharmacology and Therapeutics, pp. 115–131, 2000.
  61. Y. Liu, R. Wada, T. Yamashita, et al., “Edg-1, the G protein-coupled receptor for sphingosine-1-phosphate, is essential for vascular maturation,” Journal of Clinical Investigation, vol. 106, no. 8, pp. 951–961, 2000. View at Scopus