About this Journal Submit a Manuscript Table of Contents
Journal of Biomedicine and Biotechnology
Volume 2012 (2012), Article ID 186710, 10 pages
http://dx.doi.org/10.1155/2012/186710
Research Article

The Serine Protease Plasmin Triggers Expression of the CC-Chemokine Ligand 20 in Dendritic Cells via Akt/NF-κB-Dependent Pathways

Institute of Pharmacology of Natural Products and Clinical Pharmacology, Universitat Ulm, Helmholtzstraβe 20, 89081 Ulm, Germany

Received 16 March 2012; Accepted 1 June 2012

Academic Editor: Lindsey A. Miles

Copyright © 2012 Xuehua Li 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. T. Syrovets and T. Simmet, “Novel aspects and new roles for the serine protease plasmin,” Cellular and Molecular Life Sciences, vol. 61, no. 7-8, pp. 873–885, 2004. View at Publisher · View at Google Scholar · View at Scopus
  2. J. L. Martin-Ventura, V. Nicolas, X. Houard et al., “Biological significance of decreased HSP27 in human atherosclerosis,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 26, no. 6, pp. 1337–1343, 2006. View at Publisher · View at Google Scholar · View at Scopus
  3. A. Leclercq, X. Houard, S. Loyau et al., “Topology of protease activities reflects atherothrombotic plaque complexity,” Atherosclerosis, vol. 191, no. 1, pp. 1–10, 2007. View at Publisher · View at Google Scholar · View at Scopus
  4. J. Le Dall, B. Ho-Tin-Noé, L. Louedec et al., “Immaturity of microvessels in haemorrhagic plaques is associated with proteolytic degradation of angiogenic factors,” Cardiovascular Research, vol. 85, no. 1, pp. 184–193, 2010. View at Publisher · View at Google Scholar · View at Scopus
  5. X. Houard, F. Rouzet, Z. Touat et al., “Topology of the fibrinolytic system within the mural thrombus of human abdominal aortic aneurysms,” Journal of Pathology, vol. 212, no. 1, pp. 20–28, 2007. View at Publisher · View at Google Scholar · View at Scopus
  6. I. Weide, B. Tippler, T. Syrovets, and T. Simmet, “Plasmin is a specific stimulus of the 5-lipoxygenase pathway of human peripheral monocytes,” Thrombosis and Haemostasis, vol. 76, no. 4, pp. 561–568, 1996. View at Scopus
  7. T. Syrovets, B. Tippler, M. Rieks, and T. Simmet, “Plasmin is a potent and specific chemoattractant for human peripheral monocytes acting via a cyclic guanosine monophosphate-dependent pathway,” Blood, vol. 89, no. 12, pp. 4574–4583, 1997. View at Scopus
  8. Q. Li, Y. Laumonnier, T. Syrovets, and T. Simmet, “Plasmin triggers cytokine induction in human monocyte-derived macrophages,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 27, no. 6, pp. 1383–1389, 2007. View at Publisher · View at Google Scholar · View at Scopus
  9. T. Syrovets, M. Jendrach, A. Rohwedder, A. Schüle, and T. Simmet, “Plasmin-induced expression of cytokines and tissue factor in human monocytes involves AP-1 and IKKβ-mediated NF-κB activation,” Blood, vol. 97, no. 12, pp. 3941–3950, 2001. View at Publisher · View at Google Scholar · View at Scopus
  10. R. M. Steinman and H. Hemmi, “Dendritic cells: translating innate to adaptive immunity,” Current Topics in Microbiology and Immunology, vol. 311, pp. 17–58, 2006. View at Scopus
  11. S. Sarkar and D. A. Fox, “Dendritic cells in rheumatoid arthritis,” Frontiers in Bioscience, vol. 10, pp. 656–665, 2005. View at Scopus
  12. E. Galkina and K. Ley, “Immune and inflammatory mechanisms of atherosclerosis,” Annual Review of Immunology, vol. 27, pp. 165–197, 2009. View at Publisher · View at Google Scholar · View at Scopus
  13. O. Soehnlein, M. Drechsler, M. Hristov, and C. Weber, “Functional alterations of myeloid cell subsets in hyperlipidaemia: relevance for atherosclerosis,” Journal of Cellular and Molecular Medicine, vol. 13, no. 11-12, pp. 4293–4303, 2009. View at Publisher · View at Google Scholar · View at Scopus
  14. C. Weber and H. Noels, “Atherosclerosis: current pathogenesis and therapeutic options,” Nature Medicine, vol. 17, no. 11, pp. 1410–1422, 2011.
  15. K. Shortman and S. H. Naik, “Steady-state and inflammatory dendritic-cell development,” Nature Reviews Immunology, vol. 7, no. 1, pp. 19–30, 2007. View at Publisher · View at Google Scholar · View at Scopus
  16. M. Merad and M. G. Manz, “Dendritic cell homeostasis,” Blood, vol. 113, no. 15, pp. 3418–3427, 2009. View at Publisher · View at Google Scholar · View at Scopus
  17. X. Li, T. Syrovets, F. Genze et al., “Plasmin triggers chemotaxis of monocyte-derived dendritic cells through an Akt2-dependent pathway and promotes a T-helper type-1 response,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 30, no. 3, pp. 582–590, 2010. View at Publisher · View at Google Scholar · View at Scopus
  18. R. Bonecchi, E. Galliera, E. M. Borroni, M. M. Corsi, M. Locati, and A. Mantovani, “Chemokines and chemokine receptors: an overview,” Frontiers in Bioscience, vol. 14, no. 2, pp. 540–551, 2009. View at Publisher · View at Google Scholar · View at Scopus
  19. P. Miossec, “Dynamic interactions between T cells and dendritic cells and their derived cytokines/chemokines in the rheumatoid synovium,” Arthritis Research and Therapy, vol. 10, supplement 1, article S2, 2008. View at Publisher · View at Google Scholar · View at Scopus
  20. E. Schutyser, S. Struyf, and J. Van Damme, “The CC chemokine CCL20 and its receptor CCR6,” Cytokine and Growth Factor Reviews, vol. 14, no. 5, pp. 409–426, 2003. View at Publisher · View at Google Scholar · View at Scopus
  21. A. Kaser, O. Ludwiczek, S. Holzmann et al., “Increased expression of CCL20 in human inflammatory bowel disease,” Journal of Clinical Immunology, vol. 24, no. 1, pp. 74–85, 2004. View at Publisher · View at Google Scholar · View at Scopus
  22. I. K. Demedts, K. R. Bracke, G. Van Pottelberge et al., “Accumulation of dendritic cells and increased CCL20 levels in the airways of patients with chronic obstructive pulmonary disease,” American Journal of Respiratory and Critical Care Medicine, vol. 175, no. 10, pp. 998–1005, 2007. View at Publisher · View at Google Scholar · View at Scopus
  23. E. G. Harper, C. Guo, H. Rizzo et al., “Th17 cytokines stimulate CCL20 expression in keratinocytes in vitro and in vivo: implications for psoriasis pathogenesis,” Journal of Investigative Dermatology, vol. 129, no. 9, pp. 2175–2183, 2009. View at Publisher · View at Google Scholar · View at Scopus
  24. K. Beider, M. Abraham, M. Begin et al., “Interaction between CXCR4 and CCL20 pathways regulates tumor growth,” PLoS ONE, vol. 4, no. 4, Article ID e5125, 2009. View at Publisher · View at Google Scholar · View at Scopus
  25. M. Le Borgne, N. Etchart, A. Goubier et al., “Dendritic cells rapidly recruited into epithelial tissues via CCR6/CCL20 are responsible for CD8+ T cell crosspriming in vivo,” Immunity, vol. 24, no. 2, pp. 191–201, 2006. View at Publisher · View at Google Scholar · View at Scopus
  26. M. Vulcano, S. Struyf, P. Scapini et al., “Unique regulation of CCL18 production by maturing dendritic cells,” Journal of Immunology, vol. 170, no. 7, pp. 3843–3849, 2003. View at Scopus
  27. B. Marcet, M. Horckmans, F. Libert, S. Hassid, J. M. Boeynaems, and D. Communi, “Extracellular nucleotides regulate CCL20 release from human primary airway epithelial cells, monocytes and monocyte-derived dendritic cells,” Journal of Cellular Physiology, vol. 211, no. 3, pp. 716–727, 2007. View at Publisher · View at Google Scholar · View at Scopus
  28. D. N. J. Hart, “Dendritic cells: unique leukocyte populations which control the primary immune response,” Blood, vol. 90, no. 9, pp. 3245–3287, 1997. View at Scopus
  29. Y. V. Bobryshev and R. S. A. Lord, “55-kD actin-bundling protein (p55) is a specific marker for identifying vascular dendritic cells,” Journal of Histochemistry and Cytochemistry, vol. 47, no. 11, pp. 1481–1486, 1999. View at Scopus
  30. X. Li, T. Syrovets, S. Paskas, Y. Laumonnier, and T. Simmet, “Mature dendritic cells express functional thrombin receptors triggering chemotaxis and CCL18/pulmonary and activation-regulated chemokine induction,” Journal of Immunology, vol. 181, no. 2, pp. 1215–1223, 2008. View at Scopus
  31. Y. Laumonnier, T. Syrovets, L. Burysek, and T. Simmet, “Identification of the annexin A2 heterotetramer as a receptor for the plasmin-induced signaling in human peripheral monocytes,” Blood, vol. 107, no. 8, pp. 3342–3349, 2006. View at Publisher · View at Google Scholar · View at Scopus
  32. B. Sperandio, B. Regnault, J. Guo et al., “Virulent Shigella flexneri subverts the host innate immune response through manipulation of antimicrobial peptide gene expression,” Journal of Experimental Medicine, vol. 205, no. 5, pp. 1121–1132, 2008. View at Publisher · View at Google Scholar · View at Scopus
  33. N. Katoh, S. Kraft, J. H. M. Weßendorf, and T. Bieber, “The high-affinity IgE receptor (FcεRI) blocks apoptosis in normal human monocytes,” Journal of Clinical Investigation, vol. 105, no. 2, pp. 183–190, 2000. View at Scopus
  34. T. Syrovets, A. Schüle, M. Jendrach, B. Büchele, and T. Simmet, “Ciglitazone inhibits plasmin-induced proinflammatory monocyte activation via modulation of p38 MAP kinase activity,” Thrombosis and Haemostasis, vol. 88, no. 2, pp. 274–281, 2002. View at Scopus
  35. T. Syrovets, J. E. Gschwend, B. Büchele et al., “Inhibition of IκB kinase activity by acetyl-boswellic acids promotes apoptosis in androgen-independent PC-3 prostate cancer cells in vitro and in vivo,” Journal of Biological Chemistry, vol. 280, no. 7, pp. 6170–6180, 2005. View at Publisher · View at Google Scholar · View at Scopus
  36. I. Weide, J. Romisch, and T. Simmet, “Contact activation triggers stimulation of the monocyte 5-lipoxygenase pathway via plasmin,” Blood, vol. 83, no. 7, pp. 1941–1951, 1994. View at Scopus
  37. F. Battaglia, S. Delfino, E. Merello et al., “Hypoxia transcriptionally induces macrophage-inflammatory protein-3α/CCL-20 in primary human mononuclear phagocytes through nuclear factor (NF)-κB,” Journal of Leukocyte Biology, vol. 83, no. 3, pp. 648–662, 2008. View at Publisher · View at Google Scholar · View at Scopus
  38. O. N. Ozes, L. D. Mayo, J. A. Gustin, S. R. Pfeffer, L. M. Pfeffer, and D. B. Donner, “NF-κB activation by tumour necrosis factor requires tie Akt serine-threonine kinase,” Nature, vol. 401, no. 6748, pp. 82–85, 1999. View at Publisher · View at Google Scholar · View at Scopus
  39. N. D. Perkins, “Post-translational modifications regulating the activity and function of the nuclear factor kappa B pathway,” Oncogene, vol. 25, no. 51, pp. 6717–6730, 2006. View at Publisher · View at Google Scholar · View at Scopus
  40. F. Huang, C. Y. Kao, S. Wachi, P. Thai, J. Ryu, and R. Wu, “Requirement for both JAK-mediated PI3K signaling and ACT1/TRAF6/TAK1- dependent NF-κB activation by IL-17A in enhancing cytokine expression in human airway epithelial cells,” Journal of Immunology, vol. 179, no. 10, pp. 6504–6513, 2007. View at Scopus
  41. M. S. Hayden and S. Ghosh, “Shared principles in NF-κB signaling,” Cell, vol. 132, no. 3, pp. 344–362, 2008. View at Publisher · View at Google Scholar · View at Scopus
  42. M. S. Hayden, A. P. West, and S. Ghosh, “NF-κB and the immune response,” Oncogene, vol. 25, no. 51, pp. 6758–6780, 2006. View at Publisher · View at Google Scholar · View at Scopus
  43. L. Burysek, T. Syrovets, and T. Simmet, “The serine protease plasmin triggers expression of MCP-1 and CD40 in human primary monocytes via activation of p38 MAPK and Janus kinase (JAK)/STAT signaling pathways,” Journal of Biological Chemistry, vol. 277, no. 36, pp. 33509–33517, 2002. View at Publisher · View at Google Scholar · View at Scopus
  44. S. Sugita, T. Kohno, K. Yamamoto et al., “Induction of macrophage-inflammatory protein-3α gene expression by TNF-dependent NF-κB activation,” Journal of Immunology, vol. 168, no. 11, pp. 5621–5628, 2002. View at Scopus
  45. C. W. Lindsley, Z. Zhao, W. H. Leister et al., “Allosteric Akt (PKB) inhibitors: discovery and SAR of isozyme selective inhibitors,” Bioorganic and Medicinal Chemistry Letters, vol. 15, no. 3, pp. 761–764, 2005. View at Publisher · View at Google Scholar · View at Scopus
  46. S. P. Davies, H. Reddy, M. Caivano, and P. Cohen, “Specificity and mechanism of action of some commonly used protein kinase inhibitors,” Biochemical Journal, vol. 351, no. 1, pp. 95–105, 2000. View at Publisher · View at Google Scholar · View at Scopus
  47. C. Cuaz-Pérolin, L. Billiet, E. Baugé et al., “Antiinflammatory and antiatherogenic effects of the NF-κB inhibitor acetyl-11-Keto-β-boswellic acid in LPS-challenged ApoE-/- mice,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 28, no. 2, pp. 272–277, 2008. View at Publisher · View at Google Scholar · View at Scopus
  48. T. Syrovets, B. Büchele, C. Krauss, Y. Laumonnier, and T. Simmet, “Acetyl-boswellic acids inhibit lipopolysaccharide-mediated TNF-α induction in monocytes by direct interaction with IκB kinases,” Journal of Immunology, vol. 174, no. 1, pp. 498–506, 2005. View at Scopus
  49. H. Wang, T. Syrovets, D. Kess et al., “Targeting NF-κB with a natural triterpenoid alleviates skin inflammation in a mouse model of psoriasis,” Journal of Immunology, vol. 183, no. 7, pp. 4755–4763, 2009. View at Publisher · View at Google Scholar · View at Scopus
  50. A. P. Kaplan, K. Joseph, Y. Shibayama, S. Reddigari, B. Ghebrehiwet, and M. Silverberg, “The intrinsic coagulation/kinin-forming cascade: assembly in plasma and cell surfaces in inflammation,” Advances in Immunology, vol. 66, pp. 225–272, 1997. View at Scopus
  51. A. H. Schmaier, “Contact activation: a revision,” Thrombosis and Haemostasis, vol. 78, no. 1, pp. 101–107, 1997. View at Scopus
  52. R. W. Colman and A. H. Schmaier, “Contact system: a vascular biology modulator with anticoagulant, profibrinolytic, antiadhesive, and proinflammatory attributes,” Blood, vol. 90, no. 10, pp. 3819–3843, 1997. View at Scopus
  53. A. H. Schmaier and K. R. McCrae, “The plasma kallikrein-kinin system: its evolution from contact activation,” Journal of Thrombosis and Haemostasis, vol. 5, no. 12, pp. 2323–2329, 2007. View at Publisher · View at Google Scholar · View at Scopus
  54. E. Ferrero, K. Vettoretto, A. Bondanza et al., “uPA/uPAR system is active in immature dendritic cells derived from CD14+CD34+ precursors and is down-regulated upon maturation,” Journal of Immunology, vol. 164, no. 2, pp. 712–718, 2000. View at Scopus
  55. C. Y. Kao, F. Huang, Y. Chen et al., “Up-regulation of CC chemokine ligand 20 expression in human airway epithelium by IL-17 through a JAK-independent but MEK/NF-κB-dependent signaling pathway,” Journal of Immunology, vol. 175, no. 10, pp. 6676–6685, 2005. View at Scopus
  56. P. Scapini, C. Laudanna, C. Pinardi, et al., “Neutrophils produce biologically active macrophage inflammatory protein-3a (MIP-3a)/CCL20 and MIP-3β/CCL19,” European Journal of Immunology, vol. 31, no. 7, pp. 1981–1988, 2001.
  57. R. Caruso, D. Fina, I. Peluso et al., “A functional role for interleukin-21 in promoting the synthesis of the T-Cell chemoattractant, MIP-3α, by gut epithelial cells,” Gastroenterology, vol. 132, no. 1, pp. 166–175, 2007. View at Publisher · View at Google Scholar · View at Scopus
  58. P. Dhawan and A. Richmond, “A novel NF-κB-inducing kinase-MAPK signaling pathway up-regulates NF-κB activity in melanoma cells,” Journal of Biological Chemistry, vol. 277, no. 10, pp. 7920–7928, 2002. View at Publisher · View at Google Scholar · View at Scopus
  59. L. Vermeulen, G. De Wilde, S. Notebaert, W. Vanden Berghe, and G. Haegeman, “Regulation of the transcriptional activity of the nuclear factor-κB p65 subunit,” Biochemical Pharmacology, vol. 64, no. 5-6, pp. 963–970, 2002. View at Publisher · View at Google Scholar · View at Scopus
  60. L. V. Madrid, M. W. Mayo, J. Y. Reuther, and A. S. Baldwin, “Akt stimulates the transactivation potential of the RelA/p65 subunit of NF-κB through utilization of the IκB kinase and activation of the mitogen-activated protein kinase p38,” Journal of Biological Chemistry, vol. 276, no. 22, pp. 18934–18940, 2001. View at Publisher · View at Google Scholar · View at Scopus
  61. N. Sizemore, N. Lerner, N. Dombrowski, H. Sakurai, and G. R. Stark, “Distinct roles of the IκB kinase α and β subunits in liberating nuclear factor κB (NF-κB) from IκB and in phosphorylating the p65 subunit of NF-κB,” Journal of Biological Chemistry, vol. 277, no. 6, pp. 3863–3869, 2002. View at Publisher · View at Google Scholar · View at Scopus
  62. S. J. Jeong, C. A. Pise-Masison, M. F. Radonovich, H. U. Park, and J. N. Brady, “Activated AKT regulates NF-κB activation, p53 inhibition and cell survival in HTLV-1-transformed cells,” Oncogene, vol. 24, no. 44, pp. 6719–6728, 2005. View at Publisher · View at Google Scholar · View at Scopus