Skip to main content

Advertisement

SpringerLink
Log in

Inflammation and melanoma growth and metastasis: The role of platelet-activating factor (PAF) and its receptor

  • Published:
Cancer and Metastasis Reviews Aims and scope Submit manuscript

Abstract

An inflammatory tumor microenvironment fosters tumor growth, angiogenesis and metastatic progression. Platelet-activating factor (PAF) is an inflammatory biolipid produced from membrane glycerophospholipids. Through the activity of its G-protein coupled receptor, PAF triggers a variety of pathological reactions including tumor neo-angiogenesis. Several groups have demonstrated that inhibiting PAF-PAF receptor pathway at the level of a ligand or receptor results in an effective inhibition of experimental tumor growth and metastasis. In particular, our group has recently demonstrated that PAF receptor antagonists can effectively inhibit the metastatic potential of human melanoma cells in nude mice. Furthermore, we showed that PAF stimulated the phosphorylation of CREB and ATF-1 in metastatic melanoma cells, which resulted in overexpression of MMP-2 and MT1-MMP. Our data indicate that PAF acts as a promoter of melanoma metastasis in vivo. Since only metastatic melanoma cells overexpress CREB/ATF-1, we propose that these cells are better equipped to respond to PAF within the tumor microenvironment when compared to their non-metastatic counterparts.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Balkwill, F., & Mantovani, A. (2001). Inflammation and cancer: back to Virchow? Lancet, 357(9255), 539–45.

    Article  PubMed  CAS  Google Scholar 

  2. Coussens, L. M., & Werb, Z. (2002). Inflammation and cancer. Nature, 420(6917), 860–67.

    Article  PubMed  CAS  Google Scholar 

  3. Mantovani, A. (2005). Cancer: Inflammation by remote control. Nature, 435(7043), 752–53.

    Article  PubMed  CAS  Google Scholar 

  4. Pikarsky, E., Porat, R. M., Stein, I., Abramovitch, R., Amit, S., Kasem, S., et al. (2004). NF-kappaB functions as a tumour promoter in inflammation-associated cancer. Nature, 431(7007), 461–66.

    Article  PubMed  CAS  Google Scholar 

  5. Chen, Y. Q., Liu, B., Tang, D. G., & Honn, K. V. (1992). Fatty acid modulation of tumor cell-platelet-vessel wall interaction. Cancer and Metastasis Reviews, 11(3–), 389–09.

    Article  PubMed  CAS  Google Scholar 

  6. Karpatkin, S., & Pearlstein, E. (1981). Role of platelets in tumor cell metastases. Annals of Internal Medicine, 95(5), 636–41.

    PubMed  CAS  Google Scholar 

  7. Honn, K. V., Tang, D. G., & Crissman, J. D. (1992). Platelets and cancer metastasis: A causal relationship? Cancer and Metastasis Reviews, 11(3–), 325–51.

    Article  PubMed  CAS  Google Scholar 

  8. Nieswandt, B., Hafner, M., Echtenacher, B., & Mannel, D. N. (1999). Lysis of tumor cells by natural killer cells in mice is impeded by platelets. Cancer Research, 59(6), 1295–300.

    PubMed  CAS  Google Scholar 

  9. Pinedo, H. M., Verheul, H. M., D’Amato, R. J., & Folkman, J. (1998). Involvement of platelets in tumour angiogenesis? Lancet, 352(9142), 1775–777.

    Article  PubMed  CAS  Google Scholar 

  10. Robinson, S. C., & Coussens, L. M. (2005). Soluble mediators of inflammation during tumor development. Advances in Cancer Research, 93, 159–87.

    Article  PubMed  CAS  Google Scholar 

  11. Dauer, D. J., Ferraro, B., Song, L., Yu, B., Mora, L., Buettner, R., et al. (2005). Stat3 regulates genes common to both wound healing and cancer. Oncogene, 24(21), 3397–408.

    Article  PubMed  CAS  Google Scholar 

  12. Brown, J. R., & DuBois, R. N. (2004). Cyclooxygenase as a target in lung cancer. Clinical Cancer Research, 10(12 Pt 2), 4266s–269s.

    Article  PubMed  CAS  Google Scholar 

  13. Leslie, M. C., & Bar-Eli, M. (2005). Regulation of gene expression in melanoma: New approaches for treatment. Journal of Cell Biochemistry, 94(1), 25–8.

    Article  CAS  Google Scholar 

  14. Amiri, K. I., & Richmond, A. (2005). Role of nuclear factor-kappa B in melanoma. Cancer and Metastasis Reviews, 24(2), 301–13.

    Article  PubMed  CAS  Google Scholar 

  15. Richmond, A., Balentien, E., Thomas, H. G., Flaggs, G., Barton, D. E., Spiess, J., et al. (1988). Molecular characterization and chromosomal mapping of melanoma growth stimulatory activity, a growth factor structurally related to beta-thromboglobulin. EMBO Journal, 7(7), 2025–033.

    PubMed  CAS  Google Scholar 

  16. Claffey, K. P., Brown, L. F., del Aguila, L. F., Tognazzi, K., Yeo, K. T., Manseau, E. J., et al. (1996). Expression of vascular permeability factor/vascular endothelial growth factor by melanoma cells increases tumor growth, angiogenesis, and experimental metastasis. Cancer Research, 56(1), 172–81.

    PubMed  CAS  Google Scholar 

  17. Tellez, C., McCarty, M., Ruiz, M., & Bar-Eli, M. (2003). Loss of activator protein-2alpha results in overexpression of protease-activated receptor-1 and correlates with the malignant phenotype of human melanoma. Journal of Biological Chemistry, 278(47), 46632–6642.

    Article  PubMed  CAS  Google Scholar 

  18. Tellez, C. S., Davis, D. W., Prieto, V. G., Gershenwald, J. E., Johnson, M. M., McCarty, M. F., et al. (2007). Quantitative analysis of melanocytic tissue array reveals inverse correlation between activator protein-2alpha and protease-activated receptor-1 expression during melanoma progression. Journal of Investigative Dermatology, 127(2), 387–93.

    Article  PubMed  CAS  Google Scholar 

  19. Tellez, C., & Bar-Eli, M. (2003). Role and regulation of the thrombin receptor (PAR-1) in human melanoma. Oncogene, 22(20), 3130–137.

    Article  PubMed  CAS  Google Scholar 

  20. Lorant, D. E., Patel, K. D., McIntyre, T. M., McEver, R. P., Prescott, S. M., & Zimmerman, G. A. (1991). Coexpression of GMP-140 and PAF by endothelium stimulated by histamine or thrombin: A juxtacrine system for adhesion and activation of neutrophils. Journal of Cell Biology, 115(1), 223–34.

    Article  PubMed  CAS  Google Scholar 

  21. Zimmerman, G. A., McIntyre, T. M., Mehra, M., & Prescott, S. M. (1990). Endothelial cell-associated platelet-activating factor: A novel mechanism for signaling intercellular adhesion. Journal of Cell Biology, 110(2), 529–40.

    Article  PubMed  CAS  Google Scholar 

  22. Zimmerman, G. A., McIntyre, T. M., Prescott, S. M., & Stafforini, D. M. (2002) The platelet-activating factor signaling system and its regulators in syndromes of inflammation and thrombosis. Critical Care Medicine, 30(5 Suppl), S294’S301.

    Article  PubMed  CAS  Google Scholar 

  23. Bennett, S. A., & Birnboim, H. C. (1997). Receptor-mediated and protein kinase-dependent growth enhancement of primary human fibroblasts by platelet activating factor. Molecular Carcinogenesis, 20(4), 366–75.

    Article  PubMed  CAS  Google Scholar 

  24. Roth, M., Nauck, M., Yousefi, S., Tamm, M., Blaser, K., Perruchoud, A. P., et al. (1996). Platelet-activating factor exerts mitogenic activity and stimulates expression of interleukin 6 and interleukin 8 in human lung fibroblasts via binding to its functional receptor. Journal of Experimental Medicine, 184(1), 191–01.

    Article  PubMed  CAS  Google Scholar 

  25. Prescott, S. M., Zimmerman, G. A., Stafforini, D. M., & McIntyre, T. M. (2000). Platelet-activating factor and related lipid mediators. Annual Reviews of Biochemical, 69, 419–45.

    Article  CAS  Google Scholar 

  26. Camussi, G., Montrucchio, G., Lupia, E., De Martino, A., Perona, L., Arese, M., et al. (1995). Platelet-activating factor directly stimulates in vitro migration of endothelial cells and promotes in vivo angiogenesis by a heparin-dependent mechanism. Journal of Immunology, 154(12), 6492–501.

    CAS  Google Scholar 

  27. Robert, E. G., & Hunt, J. D. (2001). Lipid messengers as targets for antiangiogenic therapy. Current Pharmaceutical Design, 7(16), 1615–626.

    Article  PubMed  CAS  Google Scholar 

  28. Bussolino, F., Arese, M., Montrucchio, G., Barra, L., Primo, L., Benelli, R., et al. (1995). Platelet activating factor produced in vitro by Kaposi’s sarcoma cells induces and sustains in vivo angiogenesis. Journal of Clinical Investigation, 96(2), 940–52.

    Article  PubMed  CAS  Google Scholar 

  29. Shaw, J. O., Pinckard, R. N., Ferrigni, K. S., McManus, L. M., & Hanahan, D. J. (1981). Activation of human neutrophils with 1-O-hexadecyl/octadecyl-2-acetyl-snglycerol-3-phosphorylcholine (platelet activating factor). Journal of Immunology, 127(3), 1250–255.

    CAS  Google Scholar 

  30. Rola-Pleszczynski, M., Pouliot, C., Turcotte, S., Pignol, B., Braquet, P., & Bouvrette, L. (1988). Immune regulation by platelet-activating factor. I. Induction of suppressor cell activity in human monocytes and CD8+ T cells and of helper cell activity in CD4+ T cells. Journal of Immunology, 140(10), 3547–552.

    CAS  Google Scholar 

  31. Stafforini, D. M., McIntyre, T. M., Zimmerman, G. A., & Prescott, S. M. (2003). Platelet-activating factor, a pleiotrophic mediator of physiological and pathological processes. Critical Reviews in Clinical Laboratory Sciences, 40(6), 643–72.

    Article  PubMed  CAS  Google Scholar 

  32. Travers, J. B. (1999). Oxidative stress can activate the epidermal platelet-activating factor receptor. Journal of Investigative Dermatology, 112(3), 279–83.

    Article  PubMed  CAS  Google Scholar 

  33. Shimizu, T., Mutoh, H., & Kato, S. (1996). Platelet-activating factor receptor. Gene structure and tissue-specific regulation. Advances in Experimental Medicine and Biology, 416, 79–4.

    PubMed  CAS  Google Scholar 

  34. Mutoh, H., Bito, H., Minami, M., Nakamura, M., Honda, Z., Izumi, T., et al. (1993). Two different promoters direct expression of two distinct forms of mRNAs of human platelet-activating factor receptor. FEBS Letters, 322(2), 129–34.

    Article  PubMed  CAS  Google Scholar 

  35. Benveniste, J., Tence, M., Varenne, P., Bidault, J., Boullet, C., & Polonsky, J. (1979). [Semi-synthesis and proposed structure of platelet-activating factor (P.A.F.): PAF-acether an alkyl ether analog of lysophosphatidylcholine]. Comptes Rendus des Seances de Academie Sciences De Roumanie, 289(14), 1037–040.

    CAS  Google Scholar 

  36. Blank, M. L., Snyder, F., Byers, L. W., Brooks, B., & Muirhead, E. E. (1979). Antihypertensive activity of an alkyl ether analog of phosphatidylcholine. Biochemical and Biophysical Research Communications, 90(4), 1194–200.

    Article  PubMed  CAS  Google Scholar 

  37. Demopoulos, C. A., Pinckard, R. N., & Hanahan, D. J. (1979). Platelet-activating factor. Evidence for 1-O-alkyl-2-acetyl-sn-glyceryl-3-phosphorylcholine as the active component (a new class of lipid chemical mediators). Journal of Biological Chemistry, 254(19), 9355–358.

    PubMed  CAS  Google Scholar 

  38. Benveniste, J., Henson, P. M., & Cochrane, C. G. (1972). Leukocyte-dependent histamine release from rabbit platelets. The role of IgE, basophils, and a platelet-activating factor. Journal of Experimental Medicine, 136(6), 1356–377.

    Article  PubMed  CAS  Google Scholar 

  39. Snyder, F. (1995). Platelet-activating factor and its analogs: Metabolic pathways and related intracellular processes. Biochimica Biophysica Acta, 1254(3), 231–49.

    Google Scholar 

  40. Prescott, S. M., Zimmerman, G. A., & McIntyre, T. M. (1990). Platelet-activating factor. Journal of Biological Chemistry, 265(29), 17381–7384.

    PubMed  CAS  Google Scholar 

  41. Serhan, C. N., Haeggstrom, J. Z., & Leslie, C. C. (1996). Lipid mediator networks in cell signaling: Update and impact of cytokines. FASEB Journal, 10(10), 1147–158.

    PubMed  CAS  Google Scholar 

  42. Marathe, G. K., Davies, S. S., Harrison, K. A., Silva, A. R., Murphy, R. C., Castro-Faria-Neto, H., et al. (1999). Inflammatory platelet-activating factor-like phospholipids in oxidized low density lipoproteins are fragmented alkyl phosphatidylcholines. Journal of Biological Chemistry, 274(40), 28395–8404.

    Article  PubMed  CAS  Google Scholar 

  43. Uemura, Y., Lee, T. C., & Snyder, F. (1991). A coenzyme A-independent transacylase is linked to the formation of platelet-activating factor (PAF) by generating the lyso-PAF intermediate in the remodeling pathway. Journal of Biological Chemistry, 266(13), 8268–272.

    PubMed  CAS  Google Scholar 

  44. Montrucchio, G., Alloatti, G., & Camussi, G. (2000). Role of platelet-activating factor in cardiovascular pathophysiology. Physiological Reviews, 80(4), 1669–699.

    PubMed  CAS  Google Scholar 

  45. Blank, M. L., Lee, Y. J., Cress, E. A., & Snyder, F. (1988). Stimulation of the de novo pathway for the biosynthesis of platelet-activating factor (PAF) via cytidylyltransferase activation in cells with minimal endogenous PAF production. Journal of Biological Chemistry, 263(12), 5656–661.

    PubMed  CAS  Google Scholar 

  46. Shindou, H., Hishikawa, D., Nakanishi, H., Harayama, T., Ishii, S., Taguchi, R., et al. (2007). A single enzyme catalyzes both platelet-activating factor production and membrane biogenesis of inflammatory cells. Cloning and characterization of acetyl-CoA:LYSO-PAF acetyltransferase. Journal of Biological Chemistry, 282(9), 6532–539.

    Article  PubMed  CAS  Google Scholar 

  47. Stafforini, D. M., Prescott, S. M., & McIntyre, T. M. (1987). Human plasma platelet-activating factor acetylhydrolase. Purification and properties. Journal of Biological Chemistry, 262(9), 4223–230.

    PubMed  CAS  Google Scholar 

  48. Travers, J. B., Sprecher, H., & Fertel, R. H. (1990). The metabolism of platelet-activating factor in human T-lymphocytes. Biochimica et biophysica acta, 1042(2), 193–97.

    PubMed  CAS  Google Scholar 

  49. Wilcox, R. W., Wykle, R. L., Schmitt, J. D., & Daniel, L. W. (1987). The degradation of platelet-activating factor and related lipids: Susceptibility to phospholipases C and D. Lipids, 22(11), 800–07.

    Article  PubMed  CAS  Google Scholar 

  50. Bito, H., Honda, Z., Nakamura, M., & Shimizu, T. (1994). Cloning, expression and tissue distribution of rat platelet-activating-factor-receptor cDNA. European Journal of Biochemistry, 221(1), 211–18.

    Article  PubMed  CAS  Google Scholar 

  51. Nakamura, M., Honda, Z., Izumi, T., Sakanaka, C., Mutoh, H., Minami, M., et al. (1991). Molecular cloning and expression of platelet-activating factor receptor from human leukocytes. Journal of Biological Chemistry, 266(30), 20400–0405.

    PubMed  CAS  Google Scholar 

  52. Ye, R. D., Prossnitz, E. R., Zou, A. H., and Cochrane, C. G. (1991). Characterization of a human cDNA that encodes a functional receptor for platelet activating factor. Biochemical and Biophysical Research Communications, 180(1), 105–11.

    Article  PubMed  CAS  Google Scholar 

  53. Ishii, S., Nagase, T., & Shimizu, T. (2002). Platelet-activating factor receptor. Prostaglandins Other Lipid Mediators 68–9, 599–09.

    Article  Google Scholar 

  54. Ishii, S., & Shimizu, T. (2000). Platelet-activating factor (PAF) receptor and genetically engineered PAF receptor mutant mice. Progress in Lipid Research, 39(1), 41–2.

    Article  PubMed  CAS  Google Scholar 

  55. Nakamura, M., Honda, Z., Waga, I., Matsumoto, T., Noma, M., & Shimizu, T. (1992). Endotoxin transduces Ca2+ signaling via platelet-activating factor receptor. FEBS Letters, 314(2), 125–29.

    Article  PubMed  CAS  Google Scholar 

  56. Uozumi, N., Kume, K., Nagase, T., Nakatani, N., Ishii, S., Tashiro, F., et al. (1997). Role of cytosolic phospholipase A2 in allergic response and parturition. Nature, 390(6660), 618–22.

    Article  PubMed  CAS  Google Scholar 

  57. Fukunaga, K., Ishii, S., Asano, K., Yokomizo, T., Shiomi, T., Shimizu, T., et al. (2001). Single nucleotide polymorphism of human platelet-activating factor receptor impairs G-protein activation. Journal of Biological Chemistry, 276(46), 43025–3030.

    Article  PubMed  CAS  Google Scholar 

  58. Dupre, D. J., Chen, Z., Le Gouill, C., Theriault, C., Parent, J. L., Rola-Pleszczynski, M., et al. (2003). Trafficking, ubiquitination, and down-regulation of the human platelet-activating factor receptor. Journal of Biological Chemistry, 278(48), 48228–8235.

    Article  PubMed  CAS  Google Scholar 

  59. Ihida, K., Predescu, D., Czekay, R. P., & Palade, G. E. (1999). Platelet activating factor receptor (PAF-R) is found in a large endosomal compartment in human umbilical vein endothelial cells. Journal of Cell Science, 112(Pt 3), 285–95.

    PubMed  CAS  Google Scholar 

  60. Marcheselli, V. L., Rossowska, M. J., Domingo, M. T., Braquet, P., & Bazan, N. G. (1990). Distinct platelet-activating factor binding sites in synaptic endings and in intracellular membranes of rat cerebral cortex. Journal of Biological Chemistry, 265(16), 9140–145.

    PubMed  CAS  Google Scholar 

  61. Marrache, A. M., Gobeil, F., Jr., Bernier, S. G., Stankova, J., Rola-Pleszczynski, M., Choufani, S., et al. (2002). Proinflammatory gene induction by platelet-activating factor mediated via its cognate nuclear receptor. Journal of Immunology, 169(11), 6474–481.

    CAS  Google Scholar 

  62. Zhu, T., Gobeil, F., Vazquez-Tello, A., Leduc, M., Rihakova, L., Bossolasco, M., et al. (2006). Intracrine signaling through lipid mediators and their cognate nuclear G-protein-coupled receptors: A paradigm based on PGE2, PAF, and LPA1 receptors. Canadian Journal of Physiology and Pharmacology, 84(3–), 377–91.

    Article  PubMed  CAS  Google Scholar 

  63. Chao, W., & Olson, M. S. (1993). Platelet-activating factor: Receptors and signal transduction. Biochemical Journal, 292(Pt 3), 617–29.

    PubMed  CAS  Google Scholar 

  64. Franklin, R. A., Mazer, B., Sawami, H., Mills, G. B., Terada, N., Lucas, J. J., et al. (1993). Platelet-activating factor triggers the phosphorylation and activation of MAP-2 kinase and S6 peptide kinase activity in human B cell lines. Journal of Immunology, 151(4), 1802–810.

    CAS  Google Scholar 

  65. Honda, Z., Takano, T., Gotoh, Y., Nishida, E., Ito, K., & Shimizu, T. (1994). Transfected platelet-activating factor receptor activates mitogen-activated protein (MAP) kinase and MAP kinase kinase in Chinese hamster ovary cells. Journal of Biological Chemistry, 269(3), 2307–315.

    PubMed  CAS  Google Scholar 

  66. Marques, S. A., Dy, L. C., Southall, M. D., Yi, Q., Smietana, E., Kapur, R., et al. (2002). The platelet-activating factor receptor activates the extracellular signal-regulated kinase mitogen-activated protein kinase and induces proliferation of epidermal cells through an epidermal growth factor-receptor-dependent pathway. Journal of Pharmacology and Experimental Therapeutics, 300(3), 1026–035.

    Article  PubMed  CAS  Google Scholar 

  67. Landis, M., Yi, Q., Hyatt, A. M., Travers, A. R., Lewis, D. A., & Travers, J. B. (2007). Involvement of P38 MAP kinase in the augmentation of UVB-mediated apoptosis via the epidermal platelet-activating factor receptor. Archives of Dermatological Research, 299, 263–66.

    Google Scholar 

  68. Melnikova, V. O., Mourad-Zeidan, A. A., Lev, D. C., & Bar-Eli, M. (2006). Platelet-activating factor mediates MMP-2 expression and activation via phosphorylation of cAMP-response element-binding protein and contributes to melanoma metastasis. Journal of Biological Chemistry, 281(5), 2911–922.

    Article  PubMed  CAS  Google Scholar 

  69. Nick, J. A., Avdi, N. J., Young, S. K., Knall, C., Gerwins, P., Johnson, G. L., et al. (1997). Common and distinct intracellular signaling pathways in human neutrophils utilized by platelet activating factor and FMLP. Journal of Clinical Investigation, 99(5), 975–86.

    Article  PubMed  CAS  Google Scholar 

  70. Coffer, P. J., Schweizer, R. C., Dubois, G. R., Maikoe, T., Lammers, J. W., & Koenderman, L. (1998). Analysis of signal transduction pathways in human eosinophils activated by chemoattractants and the T-helper 2-derived cytokines interleukin-4 and interleukin-5. Blood, 91(7), 2547–557.

    PubMed  CAS  Google Scholar 

  71. Kravchenko, V. V., Pan, Z., Han, J., Herbert, J. M., Ulevitch, R. J., & Ye, R. D. (1995). Platelet-activating factor induces NF-kappa B activation through a G protein-coupled pathway. Journal of Biological Chemistry, 270(25), 14928–4934.

    Article  PubMed  CAS  Google Scholar 

  72. Deo, D. D., Axelrad, T. W., Robert, E. G., Marcheselli, V., Bazan, N. G., & Hunt, J. D. (2002). Phosphorylation of STAT-3 in response to basic fibroblast growth factor occurs through a mechanism involving platelet-activating factor, JAK-2, and Src in human umbilical vein endothelial cells. Evidence for a dual kinase mechanism. Journal of Biological Chemistry, 277(24), 21237–1245.

    Article  PubMed  CAS  Google Scholar 

  73. Deo, D. D., Bazan, N. G., & Hunt, J. D. (2004). Activation of platelet-activating factor receptor-coupled G alpha q leads to stimulation of Src and focal adhesion kinase via two separate pathways in human umbilical vein endothelial cells. Journal of Biological Chemistry, 279(5), 3497–508.

    Article  PubMed  CAS  Google Scholar 

  74. Kume, K., & Shimizu, T. (1997). Platelet-activating factor (PAF) induces growth stimulation, inhibition, and suppression of oncogenic transformation in NRK cells overexpressing the PAF receptor. Journal of Biological Chemistry, 272(36), 22898–2904.

    Article  PubMed  CAS  Google Scholar 

  75. Axelrad, T. W., Deo, D. D., Ottino, P., Van Kirk, J., Bazan, N. G., Bazan, H. E., et al. (2004). Platelet-activating factor (PAF) induces activation of matrix metalloproteinase 2 activity and vascular endothelial cell invasion and migration. FASEB Journal, 18(3), 568–70.

    PubMed  CAS  Google Scholar 

  76. Ko, H. M., Park, Y. M., Jung, B., Kim, H. A., Choi, J. H., Park, S. J., et al. (2005). Involvement of matrix metalloproteinase-9 in platelet-activating factor-induced angiogenesis. FEBS Letters, 579(11), 2369–375.

    Article  PubMed  CAS  Google Scholar 

  77. Ottino, P., & Bazan, H. E. (2001). Corneal stimulation of MMP-1, -9 and uPA by platelet-activating factor is mediated by cyclooxygenase-2 metabolites. Current Eye Research, 23(2), 77–5.

    Article  PubMed  CAS  Google Scholar 

  78. Ottino, P., He, J., Axelrad, T. W., & Bazan, H. E. (2005). PAF-induced furin and MT1-MMP expression is independent of MMP-2 activation in corneal myofibroblasts. Investigative Ophthalmology and Visual Science, 46(2), 487–96.

    Article  PubMed  Google Scholar 

  79. Sugano, T., Nasu, K., Narahara, H., Kawano, Y., Nishida, Y., & Miyakawa, I. (2000). Platelet-activating factor induces an imbalance between matrix metalloproteinase-1 and tissue inhibitor of metalloproteinases-1 expression in human uterine cervical fibroblasts. Biology of Reproduction, 62(3), 540–46.

    Article  PubMed  CAS  Google Scholar 

  80. Takafuji, S., Ishida, A., Miyakuni, Y., & Nakagawa, T. (2003). Matrix metalloproteinase-9 release from human leukocytes. Journal of Investigational Allergology & Clinical Immunology, 13(1), 50–5.

    CAS  Google Scholar 

  81. Barletta, E., Mugnai, G., & Ruggieri, S. (2002). Platelet activating factor inhibits the expression of matrix metalloproteinases and affects invasiveness and differentiation in a system of human neuroblastoma clones. Biological Chemistry, 383(1), 189–97.

    Article  PubMed  CAS  Google Scholar 

  82. Brizzi, M. F., Battaglia, E., Montrucchio, G., Dentelli, P., Del Sorbo, L., Garbarino, G., et al. (1999) Thrombopoietin stimulates endothelial cell motility and neoangiogenesis by a platelet-activating factor-dependent mechanism. Circulation Research, 84(7), 785–96.

    PubMed  CAS  Google Scholar 

  83. Camussi, G., Montrucchio, G., Lupia, E., Soldi, R., Comoglio, P. M., & Bussolino, F. (1997). Angiogenesis induced in vivo by hepatocyte growth factor is mediated by platelet-activating factor synthesis from macrophages. Journal of Immunology, 158(3), 1302–309.

    CAS  Google Scholar 

  84. Montrucchio, G., Lupia, E., Battaglia, E., Passerini, G., Bussolino, F., Emanuelli, G., et al. (1994). Tumor necrosis factor alpha-induced angiogenesis depends on in situ platelet-activating factor biosynthesis. Journal of Experimental Medicine, 180(1), 377–82.

    Article  PubMed  CAS  Google Scholar 

  85. Montrucchio, G., Lupia, E., de Martino, A., Battaglia, E., Arese, M., Tizzani, A., et al. (1997). Nitric oxide mediates angiogenesis induced in vivo by platelet-activating factor and tumor necrosis factor-alpha. American Journal of Pathology, 151(2), 557–63.

    PubMed  CAS  Google Scholar 

  86. Montrucchio, G., Sapino, A., Bussolati, B., Ghisolfi, G., Rizea-Savu, S., Silvestro, L., et al. (1998). Potential angiogenic role of platelet-activating factor in human breast cancer. American Journal of Pathology, 153(5), 1589–596.

    PubMed  CAS  Google Scholar 

  87. Bussolati, B., Biancone, L., Cassoni, P., Russo, S., Rola-Pleszczynski, M., Montrucchio, G., et al. (2000). PAF produced by human breast cancer cells promotes migration and proliferation of tumor cells and neo-angiogenesis. American Journal of Pathology, 157(5), 1713–725.

    PubMed  CAS  Google Scholar 

  88. Sirois, M. G., & Edelman, E. R. (1997). VEGF effect on vascular permeability is mediated by synthesis of platelet-activating factor. American Journal of Physiology, 272(6 Pt 2), H2746–756.

    PubMed  CAS  Google Scholar 

  89. Rollin, S., Lemieux, C., Maliba, R., Favier, J., Villeneuve, L. R., Allen, B. G., et al. (2004). VEGF-mediated endothelial P-selectin translocation: Role of VEGF receptors and endogenous PAF synthesis. Blood, 103(10), 3789–797.

    Article  PubMed  CAS  Google Scholar 

  90. Maliba, R., Lapointe, S., Neagoe, P. E., Brkovic, A., & Sirois, M. G. (2006). Angiopoietins-1 and -2 are both capable of mediating endothelial PAF synthesis: Intracellular signalling pathways. Cell Signal, 18(11), 1947–957.

    Article  PubMed  CAS  Google Scholar 

  91. Russo, S., Bussolati, B., Deambrosis, I., Mariano, F., & Camussi, G. (2003). Platelet-activating factor mediates CD40-dependent angiogenesis and endothelial-smooth muscle cell interaction. Journal of Immunology, 171(10), 5489–497.

    CAS  Google Scholar 

  92. Seo, K. H., Lee, H. S., Jung, B., Ko, H. M., Choi, J. H., Park, S. J., et al. (2004). Estrogen enhances angiogenesis through a pathway involving platelet-activating factor-mediated nuclear factor-kappaB activation. Cancer Research, 64(18), 6482–488.

    Article  PubMed  CAS  Google Scholar 

  93. Cellai, C., Laurenzana, A., Vannucchi, A. M., Caporale, R., Paglierani, M., Di Lollo, S., et al. (2006). Growth inhibition and differentiation of human breast cancer cells by the PAFR antagonist WEB-2086. British Journal of Cancer, 94(11), 1637–642.

    PubMed  CAS  Google Scholar 

  94. Boccellino, M., Biancone, L., Cantaluppi, V., Ye, R. D., & Camussi, G. (2000). Effect of platelet-activating factor receptor expression on CHO cell motility. Journal of Cellular Physiology, 183(2), 254–64.

    Article  PubMed  CAS  Google Scholar 

  95. Bussolati, B., Russo, S., Deambrosis, I., Cantaluppi, V., Volpe, A., Ferrando, U., et al. (2002). Expression of CD154 on renal cell carcinomas and effect on cell proliferation, motility and platelet-activating factor synthesis. International Journal of Cancer, 100(6), 654–61.

    Article  CAS  Google Scholar 

  96. Denizot, Y., Truffinet, V., Bouvier, S., Gainant, A., Cubertafond, P., & Mathonnet, M. (2004). Elevated plasma phospholipase A2 and platelet-activating factor acetylhydrolase activity in colorectal cancer. Mediators of Inflammation, 13(1), 53–4.

    Article  PubMed  CAS  Google Scholar 

  97. Denizot, Y., Descottes, B., Truffinet, V., Valleix, D., Labrousse, F., & Mathonnet, M. (2005). Platelet-activating factor and liver metastasis of colorectal cancer. International Journal of Cancer, 113(3), 503–05.

    Article  CAS  Google Scholar 

  98. Denizot, Y., Gainant, A., Guglielmi, L., Bouvier, S., Cubertafond, P., & Mathonnet, M. (2003). Tissue concentrations of platelet-activating factor in colorectal carcinoma: Inverse relationships with Dukes–stage of patients. Oncogene, 22(46), 7222–224.

    Article  PubMed  CAS  Google Scholar 

  99. Mathonnet, M., Descottes, B., Valleix, D., Truffinet, V., Labrousse, F., & Denizot, Y. (2006). Platelet-activating factor in cirrhotic liver and hepatocellular carcinoma. World Journal of Gastroenterology, 12(17), 2773–778.

    PubMed  CAS  Google Scholar 

  100. Denizot, Y., Chianea, T., Labrousse, F., Truffinet, V., Delage, M., & Mathonnet, M. (2005). Platelet-activating factor and human thyroid cancer. European Journal of Endocrinology, 153(1), 31–0.

    Article  PubMed  CAS  Google Scholar 

  101. Denizot, Y., De Armas, R., Caire, F., Pommepuy, I., Truffinet, V., & Labrousse, F. (2006). Platelet-activating factor and human meningiomas. Neuropathology & Applied Neurobiology 32(6), 674–78.

    Article  CAS  Google Scholar 

  102. Guglielmi, L., Trimoreau, F., Donnard, M., Jaccard, A., Bordessoule, D., & Denizot, Y. (2003). Presence of membrane platelet-activating factor receptors on B cells of chronic B cell leukaemia patients. Leukemia & Lymphoma, 44(6), 1087–088.

    Article  CAS  Google Scholar 

  103. Kotelevets, L., Noe, V., Bruyneel, E., Myssiakine, E., Chastre, E., Mareel, M., et al. (1998). Inhibition by platelet-activating factor of Src- and hepatocyte growth factor-dependent invasiveness of intestinal and kidney epithelial cells. Phosphatidylinositol 3–kinase is a critical mediator of tumor invasion. Journal of Biological Chemistry, 273(23), 14138–4145.

    Article  PubMed  CAS  Google Scholar 

  104. Kita, Y., Takahashi, T., Uozumi, N., & Shimizu, T. (2005). A multiplex quantitation method for eicosanoids and platelet-activating factor using column-switching reversed-phase liquid chromatography-tandem mass spectrometry. Analytical Biochemistry, 342(1), 134–43.

    Article  PubMed  CAS  Google Scholar 

  105. Im, S. Y., Ko, H. M., Kim, J. W., Lee, H. K., Ha, T. Y., Lee, H. B., et al. (1996). Augmentation of tumor metastasis by platelet-activating factor. Cancer Research, 56(11), 2662–665.

    PubMed  CAS  Google Scholar 

  106. Sato, S., Kume, K., Ito, C., Ishii, S., & Shimizu, T. (1999). Accelerated proliferation of epidermal keratinocytes by the transgenic expression of the platelet-activating factor receptor. Archives of Dermatological Research, 291(11), 614–21.

    Article  PubMed  CAS  Google Scholar 

  107. Ishii, S., Nagase, T., Tashiro, F., Ikuta, K., Sato, S., Waga, I., et al. (1997). Bronchial hyperreactivity, increased endotoxin lethality and melanocytic tumorigenesis in transgenic mice overexpressing platelet-activating factor receptor. EMBO Journal, 16(1), 133–42.

    Article  PubMed  CAS  Google Scholar 

  108. Lee, J. T., & Herlyn, M. (2006). Microenvironmental influences in melanoma progression. Journal of Cellular Biochemistry.

  109. Biancone, L., Cantaluppi, V., Del Sorbo, L., Russo, S., Tjoelker, L. W., & Camussi, G. (2003). Platelet-activating factor inactivation by local expression of platelet-activating factor acetyl-hydrolase modifies tumor vascularization and growth. Clinical Cancer Research, 9(11), 4214–220.

    PubMed  CAS  Google Scholar 

  110. Fallani, A., Calorini, L., Mannini, A., Gabellieri, S., Mugnai, G., and Ruggieri, S. (2006). Platelet-activating factor (PAF) is the effector of IFN gamma-stimulated invasiveness and motility in a B16 melanoma line. Prostaglandins Other Lipid Mediators, 81(3–), 171–77.

    Article  PubMed  CAS  Google Scholar 

  111. Ko, H. M., Kang, J. H., Jung, B., Kim, H. A., Park, S. J., Kim, K. J., et al. (2007). Critical role for matrix metalloproteinase-9 in platelet-activating factor-induced experimental tumor metastasis. International Journal of Cancer, 120(6), 1277–283.

    Article  CAS  Google Scholar 

  112. Mannori, G., Barletta, E., Mugnai, G., & Ruggieri, S. (2000). Interaction of tumor cells with vascular endothelia: Role of platelet-activating factor. Clinical & Experimental Metastasis, 18(1), 89–6.

    Article  CAS  Google Scholar 

  113. Barber, L. A., Spandau, D. F., Rathman, S. C., Murphy, R. C., Johnson, C. A., Kelley, S. W., et al. (1998). Expression of the platelet-activating factor receptor results in enhanced ultraviolet B radiation-induced apoptosis in a human epidermal cell line. Journal of Biological Chemistry, 273(30), 18891–8897.

    Article  PubMed  CAS  Google Scholar 

  114. Sheng, Y., & Birkle, D. L. (1995). Release of platelet activating factor (PAF) and eicosanoids in UVC-irradiated corneal stromal cells. Current Eye Research, 14(5), 341–47.

    Article  PubMed  CAS  Google Scholar 

  115. Calignano, A., Cirino, G., Meli, R., & Persico, P. (1988). Isolation and identification of platelet-activating factor in UV-irradiated guinea pig skin. Journal of Pharmacological Methods, 19(1), 89–1.

    Article  PubMed  CAS  Google Scholar 

  116. Travers, J. B., Huff, J. C., Rola-Pleszczynski, M., Gelfand, E. W., Morelli, J. G., & Murphy, R. C. (1995). Identification of functional platelet-activating factor receptors on human keratinocytes. Journal of Investigative Dermatology, 105(6), 816–23.

    Article  PubMed  CAS  Google Scholar 

  117. Pei, Y., Barber, L. A., Murphy, R. C., Johnson, C. A., Kelley, S. W., Dy, L. C., et al. (1998). Activation of the epidermal platelet-activating factor receptor results in cytokine and cyclooxygenase-2 biosynthesis. Journal of Immunology, 161(4), 1954–961.

    CAS  Google Scholar 

  118. Walterscheid, J. P., Ullrich, S. E., & Nghiem, D. X. (2002). Platelet-activating factor, a molecular sensor for cellular damage, activates systemic immune suppression. Journal of Experimental Medicine, 195(2), 171–79.

    Article  PubMed  CAS  Google Scholar 

  119. De Fabo, E. C., Noonan, F. P., Fears, T., & Merlino, G. (2004). Ultraviolet B but not ultraviolet A radiation initiates melanoma. Cancer Research, 64(18), 6372–376.

    Article  PubMed  Google Scholar 

  120. Noonan, F. P., Recio, J. A., Takayama, H., Duray, P., Anver, M. R., Rush, W. L., et al. (2001). Neonatal sunburn and melanoma in mice. Nature, 413(6853), 271–72.

    Article  PubMed  CAS  Google Scholar 

  121. Marathe, G. K., Johnson, C., Billings, S. D., Southall, M. D., Pei, Y., Spandau, D., et al. (2005). Ultraviolet B radiation generates platelet-activating factor-like phospholipids underlying cutaneous damage. Journal of Biological Chemistry, 280(42), 35448–5457.

    Article  PubMed  CAS  Google Scholar 

  122. Bennett, S. A., Leite, L. C., & Birnboim, H. C. (1993). Platelet activating factor, an endogenous mediator of inflammation, induces phenotypic transformation of rat embryo cells. Carcinogenesis, 14(7), 1289–296.

    Article  PubMed  CAS  Google Scholar 

  123. Behrens, T. W., & Goodwin, J. S. (1990). Control of human T cell proliferation by platelet-activating factor. International Journal of Immunopharmacology, 12(2), 175–84.

    Article  PubMed  CAS  Google Scholar 

  124. Maggi, M., Bonaccorsi, L., Finetti, G., Carloni, V., Muratori, M., Laffi, G., et al. (1994). Platelet-activating factor mediates an autocrine proliferative loop in the endometrial adenocarcinoma cell line HEC-1A. Cancer Research, 54(17), 4777–784.

    PubMed  CAS  Google Scholar 

  125. Rutberg, S. E., Goldstein, I. M., Yang, Y. M., Stackpole, C. W., & Ronai, Z. (1994). Expression and transcriptional activity of AP-1, CRE, and URE binding proteins in B16 mouse melanoma subclones. Molecular Carcinogenesis, 10(2), 82–7.

    Article  PubMed  CAS  Google Scholar 

  126. Bohm, M., Moellmann, G., Cheng, E., Alvarez-Franco, M., Wagner, S., Sassone-Corsi, P., et al. (1995). Identification of p90RSK as the probable CREB-Ser133 kinase in human melanocytes. Cell Growth & Differentiation, 6(3), 291–02.

    CAS  Google Scholar 

  127. Walton, K. M., Rehfuss, R. P., Chrivia, J. C., Lochner, J. E., & Goodman, R. H. (1992). A dominant repressor of cyclic adenosine 3–5–monophosphate (cAMP)-regulated enhancer-binding protein activity inhibits the cAMP-mediated induction of the somatostatin promoter in vivo. Molecular Endocrinology, 6(4), 647–55.

    Article  PubMed  CAS  Google Scholar 

  128. Xie, S., Price, J. E., Luca, M., Jean, D., Ronai, Z., & Bar-Eli, M. (1997). Dominant-negative CREB inhibits tumor growth and metastasis of human melanoma cells. Oncogene, 15(17), 2069–075.

    Article  PubMed  CAS  Google Scholar 

  129. Jean, D., Tellez, C., Huang, S., Davis, D. W., Bruns, C. J., McConkey, D. J., et al. (2000). Inhibition of tumor growth and metastasis of human melanoma by intracellular anti-ATF-1 single chain Fv fragment. Oncogene, 19(22), 2721–730.

    Article  PubMed  CAS  Google Scholar 

  130. Jean, D., Harbison, M., McConkey, D. J., Ronai, Z., & Bar-Eli, M. (1998). CREB and its associated proteins act as survival factors for human melanoma cells. Journal of Biological Chemistry, 273(38), 24884–4890.

    Article  PubMed  CAS  Google Scholar 

  131. Halaban, R., Ghosh, S., & Baird, A. (1987). bFGF is the putative natural growth factor for human melanocytes. In Vitro Cellular & Development Biology, 23(1), 47–2.

    Article  CAS  Google Scholar 

  132. Lev, D. C., Onn, A., Melinkova, V. O., Miller, C., Stone, V., Ruiz, M., et al. (2004). Exposure of melanoma cells to dacarbazine results in enhanced tumor growth and metastasis in vivo. Journal of Clinical Oncology, 22(11), 2092–100.

    Article  PubMed  CAS  Google Scholar 

  133. Lev, D. C., Ruiz, M., Mills, L., McGary, E. C., Price, J. E., & Bar-Eli, M. (2003). Dacarbazine causes transcriptional up-regulation of interleukin 8 and vascular endothelial growth factor in melanoma cells: A possible escape mechanism from chemotherapy. Molecular Cancer Therapeutics, 2(8), 753–63.

    PubMed  CAS  Google Scholar 

  134. Mandic, A., Viktorsson, K., Heiden, T., Hansson, J., & Shoshan, M. C. (2001). The MEK1 inhibitor PD98059 sensitizes C8161 melanoma cells to cisplatin-induced apoptosis. Melanoma Research, 11(1), 11–9.

    Article  PubMed  CAS  Google Scholar 

  135. Huang, S., Mills, L., Mian, B., Tellez, C., McCarty, M., Yang, X. D., et al. (2002). Fully humanized neutralizing antibodies to interleukin-8 (ABX-IL8) inhibit angiogenesis, tumor growth, and metastasis of human melanoma. American Journal of Pathology, 161(1), 125–34.

    PubMed  CAS  Google Scholar 

  136. Darst, M., Al-Hassani, M., Li, T., Yi, Q., Travers, J. M., Lewis, D. A., et al. (2004). Augmentation of chemotherapy-induced cytokine production by expression of the platelet-activating factor receptor in a human epithelial carcinoma cell line. Journal of Immunology, 172(10), 6330–335.

    CAS  Google Scholar 

  137. Southall, M. D., Isenberg, J. S., Nakshatri, H., Yi, Q., Pei, Y., Spandau, D. F., et al. (2001). The platelet-activating factor receptor protects epidermal cells from tumor necrosis factor (TNF) alpha and TNF-related apoptosis-inducing ligand-induced apoptosis through an NF-kappa B-dependent process. Journal of Biological Chemistry, 276(49), 45548–5554.

    Article  PubMed  CAS  Google Scholar 

  138. Li, T., Southall, M. D., Yi, Q., Pei, Y., Lewis, D., Al-Hassani, M., et al. (2003). The epidermal platelet-activating factor receptor augments chemotherapy-induced apoptosis in human carcinoma cell lines. Journal of Biological Chemistry, 278(19), 16614–6621.

    Article  PubMed  CAS  Google Scholar 

  139. Ma, X., & Bazan, H. E. (2001). Platelet-activating factor (PAF) enhances apoptosis induced by ultraviolet radiation in corneal epithelial cells through cytochrome c-caspase activation. Current Eye Research, 23(5), 326–35.

    Article  PubMed  CAS  Google Scholar 

  140. Geromin, D., Bourge, J. F., Soulie, A., Pawliuk, R., Fleet, C., Michel, E., et al. (2004). Glycoprotein 170 induces platelet-activating factor receptor membrane expression and confers tumor cell hypersensitivity to NK-dependent cell lysis. Journal of Immunology, 172(6), 3604–611.

    CAS  Google Scholar 

  141. Thurnher, M., Zelle-Rieser, C., Ramoner, R., Bartsch, G., & Holtl, L. (2001). The disabled dendritic cell. FASEB Journal, 15(6), 1054–061.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Cancer Biology, The University of Texas M. D. Anderson Cancer Center, P.O. Box 173, Houston, TX, 77030, USA

    Vladislava Melnikova & Menashe Bar-Eli

Authors
  1. Vladislava Melnikova
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Menashe Bar-Eli
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Menashe Bar-Eli.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Melnikova, V., Bar-Eli, M. Inflammation and melanoma growth and metastasis: The role of platelet-activating factor (PAF) and its receptor. Cancer Metastasis Rev 26, 359–371 (2007). https://doi.org/10.1007/s10555-007-9092-9

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10555-007-9092-9

Keywords

Search

Navigation